Here, we demonstrated that B. amnigenus adults voraciously preyed upon mosquito larvae, especially when the prey was at higher densities. Such findings reinforce previous reports that indicates backswimmers as promising biological agents to prey upon and control mosquito larvae population of different species (Shaalan and Canyon 2009; Gutiérrez et al. 2017a; Eba et al. 2021). Here, we also demonstrated that pyriproxyfen was more toxic to A. aegypti larvae than to backswimmers. Interestingly, our results revealed that the abilities of adult backswimmers to prey upon mosquito larvae were unaffected by pyriproxyfen exposure, even at concentrations as high as 100 µg a.i./L, which is a 10-fold higher concentration of pyriproxyfen than recommended for larvicidal field applications. Even though some studies have shown the potential of mosquito larvae to encounter their predator in artificial and natural environments (Shaalan and Canyon 2009; Sivagnaname 2009; Kweka et al. 2011; Eba et al. 2021), it is worth noting that we used A. aegypti larvae focusing on a prey/predator association model to test our hypothesis. Thus, such scenario might not necessarily reflect the real interactions in the aquatic ecosystems.
Although the insecticide selectivity has recently been investigated in different aquatic invertebrate species (Ser and Cetin 2015; Gutiérrez et al. 2016; Santos et al. 2018; Valbon et al. 2018; Reegan et al. 2020), it remained unclear whether pyriproxyfen could impact the survival and predatory abilities of backswimmers. Our results demonstrated differential susceptibilities to pyriproxyfen between the mosquito larvae and backswimmer adults, which can be explained in different ways. Firstly, given that the primary mode of action of pyriproxyfen is disrupting the insect endocrine system, maintaining the insect in an immature state until their death or reducing the number of emerged adults (Sullivan and Goh 2008; Ginjupalli and Baldwin 2013), it is reasonable to consider that the pyriproxyfen binding site receptors are more promptly available in the second instar mosquito larvae than backswimmer adults. Indeed, in a recent investigation we could show that low pyriproxyfen concentration (i.e., 2.5 µg a.i./L) reduced the survival and predatory abilities of nymphs of the water bug Belostoma anurum (Hemiptera: Belostomatidae), a naturally occurring mosquito control agent in the Neotropical region (Valbon et al. 2019a, 2021).
Our findings may not suffice to rule out the possibility that B. amnigenus higher tolerance to pyriproxyfen by having differential molecular interactions between pyriproxyfen and their receptor site receptors. However, the results described here are sufficient to suggest that backswimmers tolerance likely reflects their physiological status and life stage as demonstrate to other predator-prey relationships. For instance, differences in the properties of the cuticle (e.g., thickness and binding proteins) (Wood et al., 2010) and insecticide metabolism by detoxifying enzymes (e.g., cytochrome P450 monooxygenases, glutathione-S-transferase, and general esterases) of backswimmers and mosquito larvae could also contribute to explain the pyriproxyfen selectivity as described for other aquatic insects (Liu 2015; Valbon et al. 2019b).
Because backswimmers are cosmopolitan predators and are among the first insects to colonize freshwater habitats (Giller and McNeill 1981), they are constantly prone to reach insecticide-contaminated ecosystems in both artificial and natural water reservoirs. However, as notonectid adults are well-flight insects (i.e., semi-aquatic organisms), these organisms can easily evade contaminated habitats migrating to more favorable environments (Briers and Warren 2000; McCauley and Rowe 2010). Our results for the survival abilities of B. amnigenus under such scenario, i.e., facing a 24h pyriproxyfen exposure and placed under non-contaminated environment, revealed that backswimmers did not show any difference in their survival abilities when compared to those pyriproxyfen-unexposed predators.
Recent studies have reported that mosquito larvicides can impair key behavioral parameters in aquatic predators, such as locomotion and prey catching, leading to unsuccessful foraging (Gutiérrez et al. 2017b; Valbon et al. 2018; Lajmanovich et al. 2019). Interestingly, at low and intermediate prey densities, backswimmers that were previously exposed to pyriproxyfen preyed on a higher number of mosquito larvae than unexposed insects (i.e., soon after pyriproxyfen exposure). A similar foraging pattern has been reported in a coexisting backswimmer, Buenoa tarsalis, when sublethally exposed to Bacillus thuringiensis var israelensis (Bti) toxins-based larvicide (Gutiérrez et al. 2017a), suggesting that backswimmers may share hormetic-like responses (i.e., when an unexpected beneficial effect occur in individuals facing non-lethal stresses, (Guedes et al. 2017)) in insecticide-contaminated environments. However, as we found no alteration in the total number of larvae preyed upon by backswimmers exposed to sublethal levels of pyriproxyfen, at both mosquito larval densities, further studies are required before drawing firm conclusions. At the highest prey density, we found that backswimmers exposed to high pyriproxyfen concentrations (150 µg a.i./L, a concentration 15-fold higher than that recommended for field application) preyed upon significantly fewer mosquito larvae than unexposed predators.