We present and discuss studies supporting this hypothesis

These insecticides have outstanding efficacy in crop protection against a number of pest invertebrates , especially piercing–sucking insect herbivores . However, neonicotinoids have limited efficacy against lepidopteran and coleopteran pests . Advantages associated with systemic insecticides over nonsystemic insecticides include: 1) reduced sensitivity to spray coverage and canopy penetration , as the active ingredient translocates within and among plant tissues, 2) high water solubility and xylem mobility of the active ingredients , 3) continuous plant protection for an extended period of time without repeated applications , and 4) protection from direct insect herbivore damage and reduced indirect crop damage by pathogens they transmit . Due to these advantages, systemic insecticides, including neonicotinoids, have been widely adopted across a diverse range of food production systems worldwide since the 1990s . Considering the versatility and widespread adoption, pests evolving physiological and behavioral resistance to systemic insecticides should be a concern to global food security.In this opinion-based article,hydroponic grow kit we hypothesize that drought will increase the likelihood of pests evolving behavioral resistance to systemic insecticides.

Moreover, we predict that climate change will increase the likelihood of severe drought events in many agricultural regions and adversely affect the uptake and vascular flow in crop plants treated with systemic insecticides. If so, this may lead to nonuniform distribution of the active ingredient in plant tissues. Under this scenario, pests that can sense and avoid acquisition of lethal dosages of systemic insecticides within crop plants will have a selective advantage.In addition, we wish to highlight the possible effect of drought on the performance of systemic insecticides as a justification for more research into the many ways environmental factors can affect, directly and indirectly, both the performance of insecticides and the risk of target insect pests developing resistance.In 1936, a study showed that levels of aphid infestation in wheat plants were negatively associated with soil content of selenium . This discovery led to experiments with selenium uptake from soils as a systemic insecticide, giving rise to a new method of insecticide applications . In modern crop protection, systemic insecticides are applied to crops in four ways: 1) coating seeds surface prior to planting , 2) spraying of crop foliage or soil, 3) soil drenching after crop emergence, and 4) the addition of the insecticide to starter solutions used at transplanting . Seed treatment and soil applications are the two preferred methods, representing  60% of neonicotinoid insecticide applications worldwide . Seed coating is the primary method for delivering neonicotinoid insecticides to agricultural crops throughout the world . This method is considered a “safe” alternative to conventionally applied insecticides, because seed coating minimizes drift of pesticides to nontarget surfaces and organisms .

In addition, seed coating significantly decreases the amount of insecticide applied to a crop field area compared with conventional spray methods . Neonicotinoid insecticides and fipronil currently account for approximately one-third of the world insecticide market . Their success is due to high efficacy in arthropod pest management, flexibility of application method, and extended residual effect . The neonicotinoid class of insecticides is applied to a wide range of agricultural and horticultural crops, including cotton, maize, potato, and oil seed rape .Absorption and translocation of systemic insecticides are linked to physical and chemical characteristics of the insecticides’ octanol water partition coefficient and dissociation constant . Once absorbed by crop roots, a high water solubility increases the likelihood of uniform distribution and bio-availability of the active ingredients within plant tissues . Typically, the xylem transport system is responsible for translocation of systemic insecticides , but some systemic insecticides can also move within the phloem, or both . Radiolabeled imidacloprid has been observed moving toward leaf tips and margins after foliar applications . However, predicting the translocation of insecticides in treated plants is difficult due to variable plant morphology, physiology, and chemical properties of the specific compounds. Generally, translocation occurs faster in younger stems and leaf tissues , but abiotic factors, such as weather conditions and soil properties, may affect the uniformity of systemic insecticide distribution among plant tissues . Abiotic factors, including light intensity , temperature , relative humidity, and wind, influence water transpiration from leaves, thus influencing movement of systemic insecticides in the vascular tissues.

Depending on environmental conditions, a plant may direct water to certain parts of the plant, which will influence the uniformity of systemic insecticide distribution . Additionally, the uptake of a systemic insecticide is affected by the rate of transpiration of water leaving the plant . This was demonstrated through drench tests, which determined that systemic insecticides require specific amounts of water to be most efficacious .Insecticide resistance was first reported over 100 yr ago . Since then, there have been 11,254 separate records of 546 pest species evolving resistance to 331 insecticidal compounds . Most of these records refer to “metabolic” or “target-specific” insecticide resistance, which are driven by genetic and physiological selection pressures . In addition to target-specific insecticide resistance, “behavioral insecticide resistance” has been reported in >30 species of insects for >40 yr . Insect pests expressing behavioral insecticide resistance avoid contact with or ingestion of a lethal dose of an insecticide, thereby increasing their survivorship . There are a variety of behavioral resistance strategies of pests, and a few are briefly described below. Reduced leaf tissues penetration by piercing–sucking insects has been shown to function as a resistance mechanism to many different insecticides , because it reduces the insecticide acquisition rate . For example, the adult tea mosquito bug Helopel.This theivora demonstrated avoidance of multiple insecticidal compounds . When exposed to insecticide-treated plants, the tea mosquito bug also shifts its oviposition behavior away from tea shoots, where the insecticide is believed to have the highest concentration . Like the tea mosquito bug, diamondback moth Plutella xylostella L. populations have exhibited behavioral avoidance through oviposition site selection . In a different study, diamondback moths larvae and ovipositing females of two diamondback moths strains expressed different behavioral responses when offered cabbage leaves with and without insecticide treatments . The latter study showed a clear and positive relationship between the level of physiological susceptibility to the insecticides by diamondback moth strains and each strain’s level of avoidance to the insecticide-treated cabbage leaves . In addition, insecticide resistance behavior led to the decline in performance of glucose-based attractants for control of German cockroaches Blatella germanica L. in restaurants and food warehouses in the late 1980s and early 1990s . While high selection pressure favored cockroaches avoiding the attractants,4x8ft rolling benches there was a significant fitness cost to German cockroaches of being glucose averse . When studying behavioral insecticide resistance, it is a fundamental assumption that arthropod pests can somehow sense the presence of pesticides and therefore adjust their feeding and oviposition behavior to avoid contact with the lethal active ingredient. The specific mechanisms responsible for such ability to sense the presence of pesticides are not well described, and that may be considered a weakness of the hypothesis discussed in this article. However, it is well-established that evolution has led to strong selection pressures on arthropod populations regarding both their selection of both host and oviposition plants. And a large body of research has been published on the evolution and nonrandom host selection by arthropods. We are therefore arguing that some of the basic traits used by arthropods to optimize their selection of feeding and oviposition sites may also enable them to avoid plant tissues with high concentrations of pesticides. Even though not directly linked to the discussion of main hypothesis in this article, we wish to highlight the importance of studying the many ways environmental factors can affect, directly and indirectly, both the performance of insecticides and the risk of target insect pests developing resistance.Climate change is already predicted to cause significant challenges to agriculture and pest management strategies. Using current greenhouse gas emission scenarios, increases to global temperatures and changes to regional patterns of precipitation and humidity have been predicted , and a likely scenario is more frequent and also more severe drought conditions .

An important body of research has demonstrated that elevation of CO2 concentration in the atmosphere, as a consequence of climate change, may enhance the effectiveness of Bacillus thuringiensis toxins that are applied as foliar applications . The authors demonstrated that the combination of Bt toxins and elevated atmospheric CO2 concentration led to a reduced nitrogen concentration in leaves, so that herbivorous insects had to consume more leaf material in order to acquire enough nitrogen, and that increased their ingestion of Bt toxins. However, regarding expression of Bt toxins in genetically modified crops, elevated atmospheric CO2 concentration appears to reduce the toxin expression , which supports the argument articulated in this article that climate change may adversely affect the performance of systemic insecticides. We are unaware of similar reports detailing any of the possible effects of climate change on the performance of non-Bt systemic insecticides. However, it seems reasonable to speculate that climate change, through its effect on ambient temperature, humidity, and accessible soil water, will affect the rate of transport in the plant’s vascular system . If so, this may lead to a reduction in both uptake and vascular flow of systemic insecticide. This phenomenon represents a serious threat to global food security, as most insect pest management is still based on insecticide applications. Several agricultural systems already demonstrate evolved behavioral resistance, which could be exacerbated by drought. Significant differences in Colorado potato beetle Leptinotarsa decemlineata larval mortality and development among vertical leaf positions provide evidence that the concentration of imidacloprid and its metabolites were unevenly distributed in the potato foliage 8–14 wk post planting . Olson et al. indicated that the concentration of imidacloprid was lowest in the younger tissues of the upper leaves and highest in the older, lower leaves. While these leaves act as toxic barriers to susceptible Colorado potato beetles, beetles could easily develop behavioral resistance that would allow the insects to preferentially feed on the lower insecticide concentrations in the upper canopy. Therefore, the risk of behavioral resistance increases in this system, if the younger upper leaves receive a lower concentration of systemic insecticide . Similarly in sugar beet, the concentration of imidacloprid was six times higher in lower leaves compared with the upper leaves 49 d after application . A similarly nonuniform distribution pattern was noticed with the carbofuran in Douglas firs , which documented decreasing concentrations of the chemical from the roots to the upper part of the tree. These examples highlight nonuniform systemic insecticide distribution within treated plants, and such within-plant gradients may be exacerbated under the effects of climate change. Another significant factor which may lead to an increase in behavioral resistance within a pest population is the unequal amount of insecticide between neighbor plants receiving the same treatments. This can be caused by variable amounts of water available in the soil, a situation likely to occur under drought. Higher quantities of soil moisture favor water uptake, and consequently insecticide uptake . Castle et al. observed little difference in imidacloprid concentration between lower and upper sections of citrus trees, but found significant variation among the trees. Variability in the uptake of insecticide for these trees could be explained through different soil moisture contests, with optimal irrigated plants in the field able to incorporate more product than suboptimally irrigated plants. This situation is exacerbated during a drought, creating an opportune situation for populations of pest insects to develop behavioral resistance . In conclusion, as we prepare for the effects of climate change and predicted increases in frequency and severity of droughts, food production systems face a wide range of direct and indirect challenges. Climate change will, both directly and indirectly, affect crop maintenance, occurrence of invasive species, and existing pest management practices. Compared to the different types of physiological resistance, behavioral insecticide resistance mechanisms have received considerably less research attention . In this article, we discussed potential effects of climate change on the performance of systemic insecticides, and we argue that more research is needed to thoroughly study the likelihood and potential impact of the following scenarios: 1) drought suppression of systemic insecticide uptake and vascular flow rates, 2) the distribution and concentration of systemic insecticide within plant organs , 3) target insect pests developing the ability to sense and avoid leaf tissues with high concentrations of systemic insecticides , and 4) behavioral resistance becoming more widespread as consequence of climate change.