Fungicide effects on natural enemies are frequently focused on predatory mites

Copper hydroxide is the active ingredient in the pesticide marketed under the trade name Kocide 3000, and mancozeb is the active ingredient in the pesticide Manzate Pro-Stick. They are used to control both bacterial and fungal pathogens in numerous crops, including citrus, conifers, vegetables, tree crops, cereals, and small fruits. In high-value tree crops, they are used in combination to control pathogens such as apple scab, pear scab, fire blight, and powdery mildew . A mixture of copper hydroxide and mancozeb caused significantly high mortality in the predatory mite G. occidentalis, but at a concentration that was twice the maximum label rate. The same study found that, even at a diluted concentration, , exposing females to the pesticide mixture did not affect hatch rates, but, once hatched, the larvae had a higher mortality . On the other hand, a different predatory mite, Amblyseius cucumeris , appears to be compatible with copper hydroxide, in that exposure only causes high mortality at levels 10 times the recommended field rate. Copper hydroxide also had no significant effect on mortality or fecundity on the predatory mite Euseius victoriensis , whereas mancozeb significantly lowered mortality as well as fecundity, with no females laying eggs after treatment . With respect to parasitoids, copper hydroxide has shown little to no toxicity on the predator of citrus leafminer, Ageniaspis citricolaor Tamarixia radiata , a parasitoid of the Asian citrus psyllid . Mancozeb applications, suspected as the cause of low parasitism rates in Indonesian crops,hydroponic bucket demonstrated no toxicity to four different parasitoid species: Hemiptarsenus varicornis , Opius sp., Gronotoma micromorpha, and Diglyphus isaea.

These results suggest that the effects of copper hydroxide and mancozeb vary for different species, and their compatibility with natural enemies cannot be generalized. Lambda-cyhalothrin is a broad spectrum pyrethroid. One of its trade names is Warrior II, approved for use in a wide variety of crops, such as alfalfa, cereal crops, vegetables, tree nuts, tree fruits, cotton, and tobacco. In high-value tree crops, it is used to control many different pests: apple aphid, walnut aphid, codling moth, pear psylla, leafrollers, leafhoppers, and ants. This active ingredient is highly toxic to bees via direct application or residues on vegetation, and should not be applied when either crops or weeds are in bloom. Lambda-cyhalothrin is also highly toxic to aquatic organisms and wildlife, and areas subject to pesticide drift or runoff are considered hazardous . Lambda cyhalothrin has also demonstrated toxic effects on several natural enemies. The predatory mite, G. occidentalis, experienced 96% mortality at the full field rate. Even at 0.1x the full field rate, it was highly toxic to G. occidentalis, causing 76% mortality . In order to test for resistance, one study topically exposed 28 different populations of ladybird beetles to lambda cyhalothrin. However, the majority of populations tested displayed an LD50 below the maximum recommended field rate, including all populations of Coleomegilla maculata, Cycloneda sanguinea, Harmonia axyridis, and 6 of 8 H. convergens populations . Lamba-cyhalothrin is also toxic to both the larvae and adults of two green lacewing species, C. carnea and C. johnsoni . Additionally, it is highly toxic to the parasitoid, Diadegma insulare , which parasitizes diamondback moth, a major pest of brassica crops. Moreover, D. insulare can distinguish between host larvae fed on lambda-cyhalothrin treated plants versus non-treated plants, indicating a change in host preference .

Novaluron is an insect growth regulator, marketed under the trade name Rimon. It is approved for use in crops such as brassica, berries, potatoes, pome fruit, and stone fruit. In pear and apple orchards, it is used to control pear psylla, leafrollers, and codling moth. Its mode of action is to disrupt cuticle formation and deposition during molting. Although novaluron is not a conventional insecticide, it still may have non-target effects on beneficial insects, such as pollinators. For instance, exposure to novaluron may interfere with the development of honey bee larvae. Therefore, its application may not be compatible with beneficial insects when crops are in bloom. In addition, it has demonstrated toxicity to fish and aquatic organisms . Novaluron appears to have variable toxicity on several natural enemies. It demonstrated a low toxicity to O. insidiosus and Chrysoperla rufilabris , both of which are natural enemies in blueberry production . However, when exposed to novaluron residue aged 7 days, nearly 50% of H. convergens displayed acute effects, meaning they were either killed or knocked down. For G. occidentalis, an important predatory mite in apple orchards, novaluron is moderately toxic. Though it did not significantly reduce fertility, it caused reductions in fecundity as well as fertility . It has also demonstrated toxicity to green lacewing larvae, none of which survive to the adult life stage after treatment . Moreover, though it did not impact fecundity, it significantly reduced fertility and egg viability. Podisus maculiventris , a predator of the potato beetle, is susceptible through both direct contact and residual exposure . Additionally, when fed treated prey, 5th instar larvae were unable molt in to adults. Despite its impacts on survivor ship and reproduction, novaluron is still seen as a better alternative to pesticides with greater acute toxicity. For instance, when compared to brassica crops treated with broad spectrum pesticides , novaluron treated crops had higher yields and higher rates of parasitism in the pestiferous diamondback moth .

Spinetoram is chemical derived from the soil bacterium Saccharopolyspora spinosa. It is used as the active ingredient in an insecticide, marketed under the trade name Delegate, which is used to control foliage damaging pests such as leafminers, psyllids, and lepidopterous larvae. It is approved for use in a number of crops, including bananas and plantains, bushberries, hops, citrus, pome fruits, tree fruits, and tree nuts. In pome fruits, it is used to suppress populations of apple maggot, pear psylla, thrips, light brown apple moth and codling moth. In addition to targeting pests, spinetoram is toxic to bees exposed to treated crops, either though foraging on pollen-shedding or nectar producing plant parts. Delegate is recommended for use in integrated pest management programs and is advertised as being compatible with natural enemies, such as ladybird beetles, lacewings, assassin bugs, and spiders . Spinetoram has been demonstrated to be highly toxic to natural enemies and pollinators. For instance, T. triozae is a key parasitoid of the tomato psyllid, Bactericera cockerelli . T. triozae experiences 100% percent mortality when exposed to spinetoram via surface residue,stackable planters even when residue is aged as much as 15 days . Moreover, ingestion of spinetoram resulted in 100% mortality within a period of 12 hours. Additionally, spinetoram is highly toxic to eggs and larvae of the predatory mite G. occidentalis. It also caused 100% mortality in adult females after 72 h of exposure . Spinetoram is also toxic to pollinators via ingestion of treated sugar water, and it may cause mortality through exposure to either dry or wet residue. It is highly toxic to worker bees, and induces 100% mortality in bumble bees when applied at recommended field rates . Moreover, Neochrysocharis formosaand Ganaspidium nigrimanushave demonstrated susceptibility to spinetoram . These natural enemies are important parasitoids of Liriomyza trifolii , a major pest of vegetable and ornamental crops worldwide. Furthermore, spinetoram consistently lowers survival of both parasitoid species when exposed by direct application, residue, or ingestion. Sulfur is commonly used as both a fungicide and acaricide. Known as dry flowable sulfur or wettable sulfur, it is a dry powder that may be mixed with water and used as a foliar spray. It is the active ingredient in the pesticide marketed under the trade name Kumulus, which is used in an extensive variety of crops: ornamentals, turf, alfalfa, brassica, citrus, berries, cotton, hay, tree fruits, peanuts. In apple and pear orchards, sulfur is used to control plant pathogens, such as powdery mildew and scab, and pests, such as the two spotted mite and the red spider mite . It is also ranked as having variable impacts on natural enemies in tree fruits, ranging from low toxicity to aphid parasitoids to high toxicity on the western predatory mite, G. occidentalis . In apple orchards, G. occidentalis is a predator of tetranychid mites, such as the two spotted spider mite and the European red mite . Sulfur residue demonstrated a low toxicity to G. occidentalis adult females, and it had no effect on prey consumption. However, sulfur may have variable toxicity depending on the life stage of natural enemies, because the same study found that sulfur residue was highly toxic to larvae . It has also been shown to affect populations of another predatory mite, Iphiseiodes zuluagai , which preys on the coffee pest Oligonychus ilicis . The recommended field concentration caused approximately 60% mortality of I. zuluagai and decreased reproduction in adult females . Psyllobora vigintimaculatais a mycophagous coccinellid that may reduce the severity of the plant pathogen powdery mildew fungi. Additionally, sulfur was toxic when applied directly to P. vigintimaculata, resulting in 100% mortality within 24 h of exposure . Furthermore, when applied in commercial vineyards, sulfur reduced the density of P. vigintimaculata. Sulfur has also shown to affect multiple life stages of the predatory mired bug, D. brevis, causing acute toxicity in both nymphs and adults .

Exposure also decreased survival of nymphs to the adult life stage , fertility in adult females, and egg viability. Three main routes of exposure have been addressed in the literature: topical, residual, and oral. It is well known that natural enemy susceptibility to pesticide varies depending on exposure route . In a field setting, it is possible for natural enemies to be exposed to pesticide through all three aforementioned routes: topical exposure from direct spraying, residual exposure from a treated plant surface, and/or oral exposure from ingestion of a treated food source . Therefore, to more accurately assess the effects of pesticide exposure on natural enemies, it is necessary to examine multiple routes of exposure. There are several different methods for assessing the effects of pesticides on natural enemies . One route of exposure for assessing pesticide toxicity is to directly expose organisms via topical application. A common tool for topically applying pesticide is through the use of a Potter Spray Tower, which sprays a specific volume of the pesticide solution over a specified surface area . For instance, topical application via a Potter Spray Tower was used to assess the effects of buprofezin, an insect growth regulator that inhibits chitin synthesis, on several general predators, including H. axyridis, Stethorus punctum picipes , Orius tristicolor , Geocoris pallens, and Geocoris punctipes. In addition to direct spraying, there are other methods of topical application. For instance, to measure the effects of several conventional and biorational insecticides on the eggs of the generalist predator Chrysoperla externa , eggs were directly dipped into maximum field rate solutions for 25-s . While topical applications are a factor to consider when assessing pesticide risk, in a field setting, natural enemies are more likely to encounter pesticide via a combination of routes, including residual and oral exposure.Another approach is to measure pesticide toxicity via residual exposure, whereby a substrate is treated with a given pesticide, and the organism is then exposed to the treated substrate. For example, several pesticides frequently used in peach orchards were tested for their effects on the lacewing predator C. carnea using a Potter Spray Tower to apply residues to glass plates, and the predators were then exposed to the dried residue . Additionally, a Cornelis spray chamber was used to coat the sides of glass cages, to which the predatory stinkbug Picromerus bidenswas then added . Another study used a leaf dip bio-assay, in which pesticide residue was formed by dipping green bean leaves into pesticide solution for 5-s. In this manner, reduced-risk pesticides were then tested on multiple natural enemies: O. insidiosus, Amblyseius swirskii , and Eretmocerus eremicus. While most studies are based on fresh dried residues of pesticides, an equally important, but less commonly studied aspect of residues as a route of exposure for natural enemies is their persistence in the field . Several studies have begun to examine how the age of pesticide residue impacts natural enemies .