Previously, I have written articles on the compatibility of alternative pesticides, primarily insecticides and miticides, with biological control agents or natural enemies such as parasitoids and predators. In general, natural enemies tend to be more susceptible to insecticides and miticides than insect and mite pests. However, fungicides are applied routinely in greenhouses to control both aboveground and belowground fungal pathogens. So how compatible are fungicides with natural enemies?
Although fungicides may not be directly or immediately harmful to a specific natural enemy, there may be indirect or sublethal effects, such as delayed development of the prey and natural enemy, delayed adult emergence of the natural enemy or decreased natural enemy survival. There is, in general, less information on the direct (immediate) and indirect (sublethal) effects of fungicides on natural enemies.
In fact, both the Koppert and BioBest Side Effects Manual/Guide contain minimal information on the effects of fungicides on many natural enemies compared to insecticides and miticides. In addition, many studies have involved natural enemies that are typically found in field or fruit crop production systems.
When using biological control agents in greenhouse production systems, it is important that fungicide applications not directly or indirectly harm natural enemies in order to avoid disrupting the success of biological control programs.
In general, older fungicides tend to be harmful to most natural enemies, which may be associated with these fungicides having a broad mode of action. Sublethal concentrations of fungicides may affect the fecundity or fertility of natural enemy females by either directly reducing oviposition or decreasing percent egg hatch. For example, mancozeb (Protect T/O) reduces egg-hatch of Amblyseius andersonii eggs. However, mancozeb displays no indirect effects on females and does not impact offspring or young in regards to growth rate and mortality. Mancozeb has been shown to reduce the parasitism rate of the caterpillar parasitoid, Trichogramma cacoeciae by 100 percent. Both mancozeb and thiophanate-methyl (Cleary’s 3336 or Fungo) are directly harmful to the predatory mite, Typhlodromus pyri. Applications of thiophanate-methyl may also result in sublethal effects such as sterilizing T. pyri females. Additionally, mixtures of mancozeb or thiophanate-methyl with the insecticide chlorpyrifos (Dursban or DuraGuard) are more directly toxic to the predatory mite than when these pesticides are applied separately.
Although no longer commercially available, benomyl (Benlate) is toxic to the immature and adult stages of several predatory mites including Amblyseius fallacis and Metaseiulus occidentalis. Predatory mites exposed to benomyl applications tend to have higher adult mortality and decreased female reproductive capacity or fecundity. Furthermore, predatory mites are negatively affected when consuming prey that contains benomyl residues. The fungicides, vinclozolin (Ornalin) and iprodione (Chipco 26019) have been shown to be directly harmful to the first and second instar larvae of the coccinellid, Adalia bipunctata. Maneb, which is an old fungicide and no longer registered for use in greenhouses, is extremely toxic to the parasitoid Microplitis croceipes; however, maneb is not adversely harmful to the commonly used twospotted spider mite (Tetranychus urticae) predatory mite (Phytoseiulus persimilis).
The newer fungicides are typically less toxic to natural enemies, which may be associated with their site-specific mode of action. For example, the demethylation-inhibiting (DMI) fungicides triflumazole (Terraguard) and myclobutanil (Eagle), and the strobilurin fungicide trifloxystrobin (Compass) are not harmful to the twospotted spider mite predator, Galendromus occidentalis. None of the fungicides exhibited any direct or sublethal effects. For example, the fungicides did not affect egg hatch, female fecundity rate or increase immature or adult mortality compared to the untreated checks. The fungicides triadimefon (Strike) and fenarimol (Rubigan) have been shown to control diseases without harming predatory mites, which avoids disrupting the biological control of twospotted spider mite.
In The Lab
In our research, we have demonstrated under laboratory conditions that the fungicides fosetyl-Al (Aliette) and mefenoxam (Subdue Maxx), which are typically applied as a drench to control root rot pathogens such as Pythium spp. and Phytophthora spp., are compatible with the soil-predatory mite Stratiolaelaps scimitus (=”Hypoaspis miles”) since neither fungicide negatively affected the development of the protonymph stage and reproduction of adult females.
Although not directly harmful to natural enemies, fungicides may have repellent activity that may deter natural enemies from locating insect or mite hosts or inhibit foraging behavior, which will affect the ability of natural enemies to regulate insect and mite pests.
It is important to note that most studies associated with evaluating the effects of fungicides on natural enemies are conducted under laboratory evaluations in which the natural enemies are enclosed in Petri dishes exposed to fungicide treatments (either wet or dry residues). These evaluations tend to over-estimate the effects of fungicides compared to those effects observed in the field since the laboratory tests are designed to represent a worst case situation. If the fungicides are not harmful under laboratory conditions then in all likelihood they will not be harmful when used in greenhouses. In order to avoid any harmful effects to natural enemies, it is best to make releases several days following a fungicide application. However, fungicide applications may still decrease host quality, which may indirectly increase parasitoid or predator mortality. For example, parasitoid females may not deposit eggs in unsuitable hosts and predators may avoid consuming hosts that are not a viable food source.
Any differences in natural enemy susceptibility to fungicides may be due to a number of factors including whether the natural enemy is a parasitoid or predator, species of natural enemy, life stage (e.g. egg, larva, pupa and adult) sensitivity, application rate used, timing of application and mode of action of the fungicide. All these factors are complex primarily due to the different interactions that may occur among the aforementioned factors and the variability in natural enemy sensitivity. Furthermore, any harmful effects from fungicide applications may not be associated with the active ingredient, but may be due to the inert ingredients, such as carriers or surfactants. Fungicides applied as a drench to the growing medium may negate any negative effects to natural enemies residing on aboveground plant parts (e.g. leaves and stems).
The compatibility of natural enemies with fungicides is highly variable. Interactions may be associated with the type of fungicide, whether the natural enemy is a parasitoid or predator, and the stage of development. More research is needed to assess the potential compatibility of commercially available natural enemies with fungicides in order to avoid disrupting successful biological control programs.