Supplementary material


Frontiers in Ecology and Evolution


Artificial intelligence-aided meta-analysis of toxicological assessment of agrochemicals in bees



Rodrigo Cupertino Bernardes1; Lorena Lisbetd Botina1; Renan dos Santos Araújo1*; Raul Narciso Carvalho Guedes1; Gustavo Ferreira Martins2; Maria Augusta Pereira Lima3


1Departamento de Entomologia. Universidade Federal de Viçosa. Viçosa, Minas Gerais, Brazil.

2Departamento de Biologia Geral. Universidade Federal de Viçosa. Viçosa, Minas Gerais, Brazil.

3Departamento de Biologia Animal. Universidade Federal de Viçosa. Viçosa, Minas Gerais, Brazil.


*Correspondence: R.S. Araújo E-mail:


Table S1.

Summary of the categorization of variables sampled in the systematic review on toxicological assessment of agrochemicals in pollinators.

   
Variables   
   
Description   
   
Agrochemical_use   
   
Agrochemicals were categorized   according to its role in crops. For instance: Insecticides are   compounds used against insect pests; Herbicides are compounds used   against weed control; Mixtures are when there was a mixture of two or   more compounds with different types of use.   
   
Agrochemical_groups   
   
Based on IRAC MoA Classification   Version 9.4, March 2020, using the table column “Sub-group”   
   
Active_ingredient   
   
The principal component of the   formulation or only ingredient activate. Based on IRAC MoA Classification   Version 9.4, March 2020, using the table column “exemplifying Active   Ingredient”   
   
Synthetic_or_natural   
   
When the primary origin of the   compound is biological or natural (i.e., the chemical structure of the   molecule has not been synthetically modified).   
   
Pollinator_order;   Pollinator_family; Pollinator_subfamily; Pollinator_tribe; Specie   
   
The pollinators were identified   according to the taxonomic order, family, subfamily, tribe, and specie. The   taxonomy of bee groups was based on: J. S. Moure, 2012. Apini Latreille,   1802. In Moure, J. S., Urban, D. & Melo, G. A. R. (Orgs). Catalogue of   Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version.   Available at http://www.moure.cria.org.br/catalogue. Accessed Dec/29/2021   
   
Experimental_set_up   
   
The level of social organization   of the pollinators in which the study was performed.
   
Colony: exposition of the pollinator in   colony with queen laying eggs;
   
Microcolony: exposition of a group of bee   workers (usually between 4 and 12bees) isolated in a queenless environment   and the workers laying eggs;
   
Individual: exposition in the individual or small   bee group without queen and work laying egg.
   
   
   
Development_stage   
   
Stages of post-embryonic development   of pollinators: Adult and immature (larva, pupa or nymph)   
   
Sex_caste   
   
Social pollinator with caste differentiation   (i.e., worker, queen, and drone)   
   
Stressor_association   
   
When the study evaluated the   toxicity of some agrochemicals associated with some other stressors: virus,   bacteria, mite, protozoa, fungi, and environmental (temperature, humidity and   availability of food resources)     
   
Study_system   
   
Lab, field, and Semi-field   (greenhouse)   
   
Application   
   
How the agrochemical was applied   to pollinators.
   
Oral: ingested the agrochemical   (e.g., ingestion of food contaminated with agrochemical); topical: application   directly on the pollinator body, usually on the thorax; contact: application   by spray, pulverize or pot treated were the pollinator has contact.   
   
Exposure   
   
Acute: Regardless of the type of   application (oral, topical or contact), acute exposure was considered when   the agrochemical was administered for a short period of time, and, usually,   only once. We considered acute exposure when the duration of exposure   represented less than 10% of the life span of the studied pollinator.
   

   
Chronical: Regardless of the type   of application (oral, topical or contact), chronic exposure was considered   when the agrochemical was administered repeatedly for a period of time   greater than 10% of the lifetime of the studied pollinator.   
   
Response_variables   
   
Response variables quantified in   studies.
   

   
Survival: lethal effect measurement   considering both the survival over time and the mortality of individuals   after exposure;
   

   
Behavior: flight, foraging,   locomotion, defensive response, number of visits, buzzing, repellence, pollination   activity, learning, and Memory;
   

   
Feeding: generally, amount of food   ingest;
   

   
Gene expression: molecular biology   with specific genes, RT-PCR, genetic diversity, microsatellite markers,   expression of antioxidant genes, expression of immune system related gene   transcripts, HSP genes, genes Lipid metabolism, DNA damage, DNA metalation;
   

   
Metabolism: enzyme activity, ATP,   hemolymph carbohydrates, oxidative stress; Bioenergy; hibernation, Thorax temperature,   Mitochondrial function;
   

   
Reproduction: caste   differentiation, new number of eggs, number of larvae, number of broods, sperm   viability, population size, brood area, richness;
   

   
Morphology: histology, Internal   morphology (gut, brain, hypopharyngeal glands, ovary, spermatheca, mushroom   bodies, immunocytochemistry, reactive oxygen species, caspase-3, antennal   lobes, optic lobes), morphometric measurements from external morphology (shape   body, head width, intertegular span, and wing asymmetry).
   

   
Agrochemical residue: residues in   pollen, wax, and honey, but necessarily it must evaluate the bee’s body   treated; biomarkers (residues of heavy metals in pollinator body).
   

   
Biomass: body or colony mass.
   

   
Immunity: Infestation/infection (by   virus, mites, fungi, bacteria), encapsulation, hemocytes, immunocompetence,   heart rate, antimicrobial activity.
   

   
Physiology: respiration, neuronal   activity, thermoregulation, receptors, rhianodine.
   

   
Microbiota: metagenomics,   microbiome, gut bactéria, gut microbiota
   

   
Omics: genomic, proteomic,   metabolomic, transcriptome   

Table S2.

Database built after selection and inclusion of data in meta-analysis on toxicological assessment of agrochemicals in bees.