Sub-lethal effects of spinetoram application interacts with temperature in complex ways to influence respiratory metabolism, life history and macronutrient composition in false codling moth (Thaumatotibia leucotreta)

The false codling moth (FCM) (Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae)) is a pest of economic importance on several crops in South Africa, including citrus, pomegranates, prickly pears, apricots and avocados, and is native to sub-Saharan Africa (EPPO, 2020). In South Africa, efforts to control FCM include the use of biological control agents (such as parasitoids, entomopathogenic nematodes (EPN’s), entomopathogenic fungi (EPF’s) and viruses), mating disruption, the sterile insect technique (SIT) and insecticide applications with these techniques most often employed in conjunction as part of an integrated pest management programme (IPM) (Carpenter et al., 2007). Several insecticides have been used in the control of FCM in South Africa, including triflumuron and teflubenzuron (chitin synthesis inhibitors that inhibits growth and oviposition), the novel insecticides chlorantraniliprole (ryanodine receptor modulator) and methoxyfenozide (ecdysone receptor agonists) (both effective against eggs and larvae), cypermethrin (sodium channel modulators, effective on larvae) and spinetoram (nicotinic acetylcholine receptor (nAChR) allosteric modulators, a nervous system disruptor effective on all life stages) (Adom et al., 2020). Insecticides with new modes of action like spinetoram are often used in rotation with other insecticides to decrease the chance of insecticide resistance development, the latter of which has previously been documented for triflumuron in FCM in South Africa (Hofmeyr et al., 1998).

The efficacy of insecticides on an insect can be influenced by several biotic and abiotic factors. These factors can influence the susceptibility of an insect to become insecticide resistant (Müller, 2018). Biotic factors include behavioural and physiological adjustments to exposure, interactions with other living creatures (entomopathogenic nematodes, parasitoids, fungi) and the type of food consumed (Guedes et al., 2016), whilst abiotic factors include environmental conditions such as ambient temperature, solar radiation, and moisture availability (Vassilakos and Athanassiou, 2013). Temperature has been shown to interact with compounds such as contaminants and insecticides (Kim et al., 2015, Mahdjoub et al., 2020). For example, high temperatures were found to work synergistically with ivermectin (an anti-parasitic drug for livestock) to drastically reduce the survival of offspring in the yellow dung fly (González-Tokman et al., 2022). Additionally, several species exhibit increased or decreased tolerance to insecticides depending on the temperature experienced during exposure (Amarasekare and Edelson, 2004, Boina and D., Onagbola, E.O., Salyani, M. and Stelinski, L.L. , 2009). For example, organophosphates and neonicotinoids have shown lower toxicity against Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) at lower temperatures, while pyrethroids and spinosyns were equally effective at all temperatures (Saeed et al., 2018). However, in Ostrinia nubilalis (Hubner) (Lepidoptera: Crambidae) the toxicity of spinosyns decreased as temperatures increased (Musser and Shelton, 2005). Therefore, it is important to determine the influence of the temperature experienced during pesticide exposure on the pesticide efficacy.

There is also an additional layer of complexity to environmental effects on pesticides since many insects adjust physiologically and behaviourally across seasons through phenotypic plasticity (Whitman and Agrawal, 2009). Classic examples include overwintering diapause (e.g. versus direct development), summer aestivation, diverse polyphenisms or polymorphisms changing morphology, flight ability or coloration, or alterations of climate stress resistance (Whitman and Agrawal, 2009). Metabolic rates, for example, can also be up- or down-regulated to cope with seasonal stress variation (Chown and Gaston, 1999, Storey and Storey, 2004, Storey, 2005, Van Dievel et al., 2017) and these may, in turn, interact with animal activity patterns (Chown and Gaston, 1999). This is seldom accounted for in tests of pesticide efficacy, but it is reasonable to presume that if activity and/or metabolism is adjusted in response to changing ambient thermal conditions, then pesticide efficacy will likely be influenced. An increase in environmental temperature leads to an increased metabolic rate, with roughly a doubling in rate with a 10°C increase in temperature, which could increase the rate of tissue and cellular uptake of a pesticide. Thus, making a number of simplifying assumptions, increasing the metabolic rate of the insect may enhance the toxicity of the pesticide (Hallman and Brooks, 2015, Meng et al., 2020, Meng et al., 2022). On the other hand, increasing temperature may accelerate the natural chemical breakdown of the toxic pesticide resulting in less potent target effects, unless the molecular structure is particularly robust to such perturbations, possibly resulting in higher survival rates at warmer temperatures. These results can however change in response to exposure to a range of different temperatures for different durations (Sgro et al., 2016).

Spinetoram is a semi-synthetic spinosyn mixture (spinosyn J and spinosyn L) obtained through making chemical modifications to a mixture consisting of natural spinosyns, which are derived from insecticidal secondary metabolites produced by the soil-dwelling bacteria, Saccharopolyspora spinosa (Mertz and Yao) (Bacteria: Actinobacteridae) (Dripps et al., 2011). It acts through contact and ingestion (with ingestion being more effective) and acts on the insect nervous system at a unique site of the nicotinic acetylcholine receptor causing overexcitement in the insect nervous system, leading to involuntary muscle action, tremors, paralysis, and subsequently, death (Dripps et al., 2011; Galm et al., 2016). The lethal effects of spinetoram are well documented in several species (Sparks et al., 2008, Vassilakos et al., 2012) including FCM (Nepgen et al., 2018). Recently, however there has been an increase in studies on the sub-lethal effects of spinetoram on lepidopteran species including cotton bollworm (Helicoverpa armigera Hübner (Lepidoptera: Noctuidae)), diamondback moth (Plutella xylostella Linnaeus (Lepidoptera: Plutellidae)), fall armyworm (Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)) and the cotton leafworm (Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae)), with these studies showing that a sub-lethal dose of spinetoram has a negative impact on the development and reproduction of the target species (Wei et al., 2018, Ismail, 2020, Gao et al., 2021, Tamilselvan et al., 2021). To our knowledge, however, no studies have examined the sub-lethal effects of spinetoram in FCM.

The sub-lethal effects of an insecticide on the target pest are important as the breakdown of applied insecticides in the field will invariably lead to many individuals being exposed to sub-lethal concentrations of the substance (Guedes et al., 2016, Guedes et al., 2017). Several studies have shown that sub-lethal exposure to an insecticide has detrimental effects on insects leading to physiological impairment in the survivors, including increased development time, decreased fecundity, decreased emergence rate and changes in metabolic rate which can increase the level of control of the target species by negatively impacting crucial insect activities (Wang et al., 2009, Tomé et al., 2014, Karise and Mänd, 2015, De França et al., 2017, Xiao et al., 2017). These physiological responses to insecticide exposure can include protective responses in which the production of detoxification enzymes is favoured to allow survival at the expense of other functions, such as reproduction or growth and body size, and which can form the basis for insecticide resistance (Guedes et al., 2016, Katagi and Tanaka, 2016, Guedes et al., 2017). Thus, information on sub-lethal effects of an insecticide on a pest species can inform pest management decisions, possibly limiting the overuse of insecticides (Wei et al., 2018).

The ways in which FCM responds phenotypically to changes in temperature and how this influences pesticide efficacy is not well established (but see some work on their metabolic responses to fluctuating thermal regimes (Boardman et al., 2013)). In this study we therefore aimed to determine i) whether the efficacy of spinetoram on FCM varies with changes in ambient temperature during exposure to the pesticide, and also ii) if thermal history might modulate such metabolic responses which would point to one of the two major mechanisms outlined above (Fig. 1; increasing vs decreasing efficacy of spinetoram with warming conditions). Here we investigated the effect of a combination of a sub-lethal dose of spinetoram and thermal acclimation at two acute temperatures (22°C and 28°C) during larval development and measured a suite of traits including pupal metabolic rate, life history responses, and adult body composition of FCM to gain insight into likely effects of changing weather in the field. As mentioned above, the efficacy of an insecticide can be influenced by the physiology of the pest (such as metabolic rate), the temperature experienced by FCM during exposure and the environmental temperature (Fig. 1). Being exposed to higher temperatures could increase the metabolic rate of FCM which could increase the efficacy of the insecticide, however higher environmental temperatures could also lead to a breakdown of the insecticide in the field which would decrease its efficacy. Additionally, a combination of these temperature effects could lead to no difference in mortality in the pest population (Fig. 1).

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