Resistance to clothianidin reduces the efficacy of SumiShield® 50WG, a neonicotinoid formulation for indoor residual spraying, againstAnopheles gambiae

Abstract

Background: New active ingredients, mostly repurposed from the agricultural sector, are gradually being introduced into malaria vector control programs. Prior to scaling up novel insecticides, it is vital to assess if their use in agriculture has already selected mosquito populations with reduced susceptibility in some areas. The aim of the present study was to determine if the use of neonicotinoids in agricultural pest management could drive resistance to clothianidin - a neonicotinoid recently prequalified by WHO for indoor residual spraying. Methods: We carried out intensive sampling of Anopheles gambiae, An. coluzzii and Culex sp. larvae from a large suburban farm and from 4 surrounding locations belonging to the rural and urban ecosystems of Yaounde, Cameroon. Using WHO tube tests and CDC bottle bioassays, we tested the recommended diagnostic doses of clothianidin against field-collected populations using two laboratory strains as susceptible controls. We exposed adult mosquitoes to the insecticide for 1 h and monitored mortality rates for seven consecutive days. Results: An. coluzzii and Culex sp. mosquitoes were fully susceptible to clothianidin reaching 100% mortality by day 3. By contrast, An. gambiae populations revealed heterogeneous profiles ranging from susceptibility to strong resistance. Populations from the suburban farm, where neonicotinoids are routinely used, displayed the lowest mortality rate (46.5 % ± 5.65) and were capable of surviving 5X and 10X the diagnostic dose of clothianidin. When clothianidin was tested in combination with the synergist piperonyl butoxide, mortality of resistant populations increased from 46.5 % to 92.7 % implying that Cytochrome P450 enzymes play an integral role in the genetic mechanism underlying clothianidin resistance in An. gambiae. Conclusions: These findings show that small clusters of resistance to clothianidin may exist around farmlands where agricultural neonicotinoids are being used. Patches of intensive agriculture should be particularly monitored in indoor residual spraying target areas.

Neonicotinoid and pyrethroid combination: A tool to manage insecticide resistance in malaria vectors? Insights from experimental evolution

“…In such context, the large-scale implementation of Fludora® Fusion for vector control might lead to the rapid selection of these resistance alleles leading to a decreased efficacy of this novel formulation, particularly if pyrethroid resistance alleles are also present. Such hypothesis is supported by a recent study suggesting the presence of neonicotinoid resistance alleles in Anopheles coluzzi populations neighboring agriculture areas [26,27].…”

“…Because the operational advantage of this novel product essentially stands on the association of two active ingredients with distinct modes of action, our controlled selection experiment compared resistance dynamics to each insecticide separately and to their combination. As neonicotinoid resistance alleles may already be circulating in mosquito populations indirectly exposed to neonicotinoids used in agriculture [26,27], a field-derived An. gambiae line originating from the agricultural area of Tiassalé, Côte d'Ivoire was used as a parental line selection.…”

“…For each gene the following conditions were compared: Tiassalé-S unexposed (Tiassalé-S); Clothia-R unexposed (Clothia-R); Clothia-R surviving clothianidin exposure (Clothia-R surv); Clothia-R exposed to the P450 inhibitor piperonyl butoxide PBO (Clothia-R PBO+); Clothia-R pre-exposed to PBO and surviving clothianidin exposure (Clothia-R PBO+ surv). PBO exposure consisted in exposing batches of 25 mosquitoes to 4% PBO for 1h in glass bottles as described in [74]. Clothianidin exposure consisted in exposing batches of 25 mosquitoes for 1h to the same dose of clothianidin used for selection (0.45 µg/mL).…”

Effect of wall type, delayed mortality and mosquito age on the residual efficacy of a clothianidin-based indoor residual spray formulation (SumiShield™ 50WG) in southern Mozambique

“…Adequate insecticide resistance management remains critical, as resistance to most approved IRS insecticides has been documented in sub-Saharan Africa[51,52,57] and there are only five approved chemical classes of IRS insecticides. Worryingly, resistance to SumiShield TM 50WG's active ingredient, clothianidin, has been detected in Cameroon[58], which means that proper resistance monitoring, cross-border insecticide resistance management initiatives, and alternative non-insecticidal tools[59] are urgently needed in Mozambique. doi: https://doi.org/10.1101/2020.08.06.239509.…”

Effect of Neonicotinoid Exposure on the Life History Traits and Susceptibility to Plasmodium Infection on the Major Avian Malaria Vector Culex pipiens (Diptera: Culicidae)

“…The impact of pesticide exposure may, as observed in several invertebrate species, impact development, notably by disrupting the midgut structure [26], immunity [27][28][29], and survivorship [10,26] of mosquitoes, which could ultimately modify their vectorial capacity. Moreover, the sublethal concentration of pesticides found in aquatic environments can select for insecticide resistance in invertebrate vectors [30][31][32], and therefore negatively impact vector control strategies.…”