Honeydew as a newly described route of insecticide exposure to beneficial insects

Beneficial insects provide vital ecosystem services including pollination, biological control of pests and weeds, nutrient cycling and providing food sources to higher trophic levels in the food web (Resh and Cardé, 2009). These ecosystem services are of such importance that their annual value has been estimated to be at least $57 billion, only in the United States (Losey and Vaughan, 2006). Here, we will focus on two of the main groups of beneficial insects: biological control agents of agricultural pests and pollinators. Biological control is the use of a population of one living organism to reduce the population of another organism (van Lenteren et al., 2017). Insects that are currently used in biological control comprise parasitic wasps and predators. Biological control can be subdivided in four categories. I) Natural biological control is an ecosystem service whereby pest populations are reduced by naturally occurring beneficial organisms. Humans do not interfere in this type of biological control. Nonetheless, this is the most valuable type of biological control to agriculture in economic terms, with an annual estimated value of $4.49 billion, or $417 per ha and year, only in the United States (Costanza et al., 1998; Losey and Vaughan, 2006; van Lenteren et al., 2017). II) Conservation biological control consists of enhancing the performance of naturally occurring biological control agents by conserving their resources and reducing the pesticide-induced mortality of biological control agents (Holland et al., 2016; van Lenteren et al., 2017). III) Classical biological control consists of the introduction, in an area where a pest is invasive, of a biological control agent collected from the area where the pest is native (van Lenteren et al., 2017). Classical biological control often results in enormous economic benefits due to a permanent pest population reduction (Cock et al., 2010; van Lenteren et al., 2017). For instance, the African citrus psyllid, Trioza erytreae (Del Guercio) (Hemiptera: Triozidae), is a vector of the citrus greening or huanglongbing (HLB) disease. This pest has recently invaded the Iberian Peninsula and Canary Islands. In order to reduce its population levels, a classical biological control program has been successfully implemented with the introduction of the South African parasitoid Tamarixia dryi (Waterson) (Hymenoptera: Eulophidae) (Urbaneja-Bernat et al., 2020a, 2019). IV) Augmentative biological control consists of mass-rearing and releasing large numbers of living organisms for pest control. In 2015, augmentative biological control was applied on more than 30 million ha worldwide with a market value of $1.7 billion (van Lenteren et al., 2017).