Rearing Neoseiulus cucumeris and Amblyseius swirskii (Mesostigmata: Phytoseiidae) on non-target species reduces their predation efficacy on target species

1 Introduction

In 2021, strawberry (Fragaria x ananassa Rosaceae) production in Florida was valued at approximately US $399 million dollars (Hudson 2022), making the state the second largest producer of strawberries in the USA and the highest producer of winter strawberries (Guan et al. 2016). Similar to other crops grown in the state, strawberries face various arthropod pests such as phytophagous thrips (Thysanoptera: Thripidae), particularly Frankliniella occidentalis Pergande and Scirtothrips dorsalis Hood (Lahiri and Panthi 2020; Lahiri et al. 2022; Panthi and Renkema 2020; Renkema et al. 2020). In addition, spider mites (Trombidiformes: Tetranychidae), especially Tetranychus urticae Koch commonly known as twospotted spider mites, are frequently found damaging strawberries (Lahiri et al. 2022; Nyoike and Liburd 2013; Zhou et al. 2023). During the strawberry season, it is common to find numerous fields experiencing simultaneous infestations of S. dorsalis and T. urticae (Lahiri 2023).

Management of these pests has centered around the use of insecticides and miticides, however there is growing evidence that these pests have already developed resistance to these compounds (Kaur and Lahiri 2022; Kaur et al. 2023; Lahiri and Panthi 2020; Lahiri et al. 2024). Twospotted spider mites have been reported to already exhibit resistance to a variety of miticides used in their management (Van Leeuwen et al. 2010). In addition to development of resistance, chemical management of these pests can have unintended effects on beneficial insects found in strawberry such as Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) and Chrysoperla sinica (Tjeder) (Neuroptera: Chrysopidae) used in aphid management (Bommarco et al. 2011; Liu et al. 2016) and predatory mites released for S. dorsalis and T. urticae management (Busuulwa et al. 2024). Furthermore, the environmental fate of these insecticides has continuously raised concern as their increased persistence in soils could have implications for human health (Adeyinka et al. 2023; Hasnaki et al. 2023).

Over the years, considerable attention has been given to the use of biological control agents in managing various strawberry pests, both in the greenhouse and in the field. Currently, augmentative biological control is gaining popularity as an alternative to chemical control in strawberry pest management (Lahiri et al. 2022). Special attention has been given to predatory mites in the Phytoseiidae family due to their capacity to prey on many phytophagous mites and different thrips species (Cock et al. 2010).

For example, the specialist predatory mite Phytoseiulus persimilis Athias-Henriot (Mesostigmata: Phytoseiidae) has been used successfully in managing T. urticae populations both in greenhouses and fields (Cloyd et al. 2006; Raworth 2001; Rhodes and Liburd 2006). Similarly, commercially available generalist predators such as Neoseiulus cucumeris Oudemans, Amblyseius swirskii (Athias-Henriot), and Neoseiulus californicus McGregor (all Mesostigmata: Phytoseiidae) have been used to control a variety of soft bodied arthropod pests such as western flower thrips (F. occidentalis), common blossom thrips Frankliniella schultzei Trybom (Thysanoptera: Thripidae), broad mites Polyphagotarsonemus latus (Banks) (Trombidiformes: Tarsonemidae), and twospotted spider mites on various crops (Arthurs et al. 2009; Rhodes and Liburd 2006).

The unique ability of these generalist predatory mites to feed not only on insects and mites, but also on pollen has contributed to their wide adaptation for use in many biological control programs (McMurtry et al. 2013). Given that strawberries in Florida experience simultaneous infestation from both S. dorsalis and T. urticae (Lahiri et al. 2022), using a specialist predatory mite such as P. persimilis would not be effective in managing both pests. Therefore, reliance on the generalist predatory mites, A. swirskii and N. cucumeris for management of both S. dorsalis and T. urticae has become prevalent (Lahiri and Yambisa 2021). This is because both A. swirskii and N. cucumeris have been found to be effective in feeding on both pests (Buitenhuis et al. 2015; Dalir et al. 2021; Easterbrook et al. 2001). Although N. californicus is a generalist, it has been shown to have a higher affinity for T. urticae, compared to thrips (Blackwood et al. 2001; Cloyd et al. 2006; McMurtry et al. 2013), therefore limiting its use in strawberries for management of S. dorsalis and T. urticae simultaneous infestations.

Given that A. swirskii and N. cucumeris control a wide variety of soft bodied arthropod pests (McMurtry et al. 2013), improving their predation efficacies has become an important aspect of biocontrol. The most common approach for achieving this has been through predator behavioral modifications resulting from early life exposure of the predatory mites to pests (Schausberger et al. 2021). Schausberger et al. (2010) showed that N. californicus and A. swirskii posed the ability to not only learn to prey on a new food source but also imprint on prey that they experienced early in life. The exposure of generalist predatory mites to a variety of potential prey, early on in life, permits them to learn to recognize and feed on the prey more efficiently in their adulthood (Rahmani et al. 2009; Reichert et al. 2017; Schausberger et al. 2021, 2010; Seiter and Schausberger 2015). This comes as a result of positive modulation of trophic top-down cascades where learned predators become more efficient, thus facilitating high optimization of large-scale augmentative biocontrol (Schausberger et al. 2021; Seiter and Schausberger 2016).

Nonetheless, commercially available generalist predatory mites especially N. californicus, N. cucumeris, and A. swirskii are mass reared using factitious prey, such as the flour mite Acarus siro L. (Acari: Acaridae), the dried fruit mite Carpoglyphus lactis L. (Acari: Carpoglyphidae) (Nguyen et al. 2013), and Thyreophagus entomophagus Laboulbène (Acari: Acaridae) (Fidgett and Stinson 2008). Furthermore, commercial producers do not include protocols that allow predatory mites to readjust to their new target prey and environment. Therefore, this creates the need to understand the predation capability of commercially available generalist predatory mites before their release and how long it would take them to learn new prey in order to provide a baseline of expectations which may have vital implications for integrated pest management practices.

It is important to mention that previous research on this topic has centered around the exposure of prey-naïve and prey-experienced predators to the same prey species (Reichert et al. 2017; Schausberger et al. 2021, 2018; Schausberger and Peneder 2017; Seiter and Schausberger 2016, 2015). Therefore, the objective of this study was to compare the predation capability of commercially available N. cucumeris and A. swirskii feeding on known prey (Acarus spp.) and various stages of T. urticae (unfamiliar prey) in the context of strawberry production. We hypothesize that commercially available N. cucumeris and A. swirskii will possess low predation capacity on T. urticae due to prey unfamiliarity.

2 Materials and methods

3 Results

Our analysis showed that there was an effect of prey type (χ² = 432.42, df = 3, P < 0.001) and duration (χ² = 703.36, df = 3, P < 0.001) on the proportion of prey consumed by both predators. Nonetheless, there was no effect of predator species on prey consumption (χ² = 2.401, df = 1, P = 0.12). The effect of trial was also not significant (χ² = 0.58, df = 1, P = 0.45), and, as a result, trial was subsequently removed from the model. On the other hand, the interaction of prey type with species of predatory mite was significant (χ² = 117.51, df = 3, P < 0.001). Similarly, the interaction of prey type (treatment) with duration (χ² = 75.99, df = 9, P < 0.001) and predatory mite species with time (χ² = 12.75, df = 3, P = 0.0052) were significant. In addition, the three-way interaction of prey type (treatment) with species of predatory mites and time was significant (χ² = 24.54, df = 9, P = 0.0035).

On average, the proportion of pooled prey consumption across both predatory mite species and time was higher when the prey was Acarus spp. (familiar prey control) compared to the other three prey items (Table 2). No statistical differences were observed between pooled average consumption of nymphs (38.8 % CI: 35.41–42.34 %) nor adults (36.9 % CI: 33.60–40.43 %). At the species level, consumption of prey varied depending on the type of prey (Figure 1). In both predatory mite species, the proportion of Acarus spp. (familiar prey “control”) consumed was higher than any other prey (A. swirskii (69.7 % CI: 65.5–73.6 %) and N. cucumeris (88.2 % CI: 85.8–90.3 %), followed by T. urticae eggs (A. swirskii (52.0 % CI: 47.4–56.6 %) and N. cucumeris (57.6 % CI: 52.7–62.4 %), nymphs (A. swirskii (38.1 % CI: 33.8–42.6 %) and N. cucumeris (35.9 % CI: 31.4–40.6 %), and adults (A. swirskii (48.9 % CI: 44.3–53.5 %) and N. cucumeris (29.7 % CI: 25.7–34.1 %)). However, in N. cucumeris there was no difference in consumption between nymphs (35.8 % CI: 31.40–40.60 %) and adults (29.7 % CI: 25.7–34.1 %). On the contrary, in A. swirskii significantly higher consumption of adults (48.9 % CI: 44.2–53.4 %) was observed compared to nymphs (38.1 % CI: 33.80–42.60 %).

Figure 1:

Proportion of egg, nymph and adult Tetranychus urticae and adult Acarus spp. (control) consumed by each species of predatory mite (Neoseiulus cucumeris and Amblyseius swirskii) averaged across time. Proportions of prey consumed that differ based on linear contrasts (Tukey P < 0.05) are differentiated by having different letters.

Overall, when we compared prey consumption for adult T. urticae (unfamiliar prey) and adult Acarus spp. (familiar prey control), we observed that the proportion of prey consumed by both A. swirskii and N. cucumeris increased over time (Figure 2). However, the rate of increase in prey consumption was higher for familiar prey compared to unfamiliar prey. Additionally, when provided with adult T. urticae as prey, we observed a difference in prey consumption between the two predators. The proportion of prey consumed at all time intervals was higher for A. swirskii compared to N. cucumeris. Conversely, when Acarus spp. was provided as a food source, the opposite trend was observed in that prey consumption was higher for N. cucumeris compared to A. swirskii, with the exception that there were no differences in the proportion of Acarus spp. consumed by both predatory mite species at 48 h of observation (Figure 2).

Figure 2:

Consumption of adult Tetranychus urticae and adult Acarus spp. (control) by Neoseiulus cucumeris and Amblyseius swirskii at different time points. *Comparisons that are significantly different (Tukey P < 0.05).

4 Discussion

Our results indicate that prey familiarity is important in determining predation efficacy of A. swirskii and N. cucumeris feeding on T. urticae. In both predatory mites, prey consumption was higher when prey was familiar (control) compared to unfamiliar prey. Both A. swirskii and N. cucumeris showed higher consumption of T. urticae eggs compared to nymphs and adults. Nonetheless, in both predatory mite species, we observed an increase in the proportion of prey consumed with time (Figure 2). Higher consumption of familiar prey (Acarus spp.) by both species of predatory mites can be attributed to food imprinting, a phenomenon common in many groups of insects such as predatory mites and parasitoids (Ishii and Shimada 2012; Schausberger et al. 2010; Schausberger et al. 2018). This phenomenon is vital for the survival of many predatory insect species given that it allows predators to effectively adjust to not only qualitative, but also quantitative variations in food availability, which directly improves their survival (Immelmann 1975).

Given that commercially available predatory mites are in most cases mass reared on food sources different from the target prey, our study shows that this is disadvantageous given that it results in low predator efficacies. To address this, we suggest that commercial producers of predatory mites modify rearing techniques to allow for exposure of their predators to various cues of target pests to allow them to learn these prey species early on in life (Rahmani et al. 2009; Reichert et al. 2017; Seiter and Schausberger 2016). This could be done by rearing predatory mites on a variety of potential prey species to be targeted upon augmentative releases or dissemination of artificial herbivore-induced plant volatiles corresponding to a particular pest into rearing arenas. Use of synthetic herbivore-induced plant volatiles in priming biological control agents has been widely studied (Vet and Dicke 1992) and successfully used to improve efficacy of some biological control agents such as parasitoids (Hare and Morgan 1997). This would be advantageous in that it would lead to increased predation and numerical response of predatory mites, therefore improving their efficacy (Rahmani et al. 2009; Schausberger et al. 2021). For instance, it was shown that early life exposure of the predatory mite N. californicus to F. occidentalis resulted in higher predation rates (Schausberger et al. 2021). Similarly, early exposure of A. swirskii to kairomones emanating from F. occidentalis lead to an increase in predation of F. occidentalis by A. swirskii (Schausberger et al. 2020).

On the other hand, we observed high consumption of T. urticae eggs by both predatory mites compared to other T. urticae life stages (Figure 1). Egg preference by predators has been reported in many oligophagous spider mite specialists including P. persimilis, Neoseiulus fallacis (Garman), Phytoseiulus macropilis (Banks), and Neoseiulus longispinosus (Evans) (Blackwood et al. 2001). Similarly, the phytoseiid mite, Amblyseius largoensis Muma, preferred to feed on eggs of the red palm mite Raoiella indica Hirst (Trombidiformes: Tenuipalpidae) in comparison to its other life stages (Carrillo and Peña 2012). This can be attributed to the fact that eggs are of more nutritional value to predators than nymphs and adults of T. urticae (McMurtry and Rodriquez 1987; Xiao et al. 2013). In addition, other factors such as reduced time of prey attack and nutrient digestion may explain the observed trend (Soleymani et al. 2016). It has been demonstrated that some phytoseiid mites such as A. swirskii, prefer feeding on prey of smaller size (Nomikou et al. 2003). Our results contradict this previous finding, as we observed a higher proportion of adults consumed by A. swirskii compared to nymphs. This discrepancy could potentially be attributed to the lower number of adults (5) provided in our study compared to the number of nymphs (10) presented. Prey size affecting predator prey choice was further demonstrated in citrus, where various phytoseiid mites were observed consuming T. urticae eggs more than other life stages (Grafton-Cardwell et al. 1997).

Overall, the proportion of unfamiliar prey consumed by both predatory mites increased over time (Figure 2). We attributed this increase in predation to the fact that the predators had learned to recognize the provided prey as a potential food source (Schausberger et al. 2021, 2010; Schausberger and Peneder 2017). However, it should be noted that the efficacy of using A. swirskii and N. cucumeris in the field to manage T. urticae can be affected by the webbing produced by T. urticae, given that these two predators cannot easily escape getting entangled in these webs (Shimoda et al. 2010). A. swirskii consumed higher proportions of T. urticae adults compared to N. cucumeris. This is because, A. swirskii females are usually more aggressive while feeding compared to other generalist phytoseiid mites (Calvo et al. 2015; Wimmer et al. 2008). Our results, in addition, show that with familiar prey (control), both predatory mite species were able to consume 50 % of prey provided in 12 h. Besides T. urticae eggs, where 50 % consumption occurred at approximately 24 h, 36–48 h were required for 50 % of the T. urticae adults and nymphs to be consumed. This finding has great implications at the field level as it suggests that strawberry growers utilizing these predatory mites ought to refrain from the using any management practice that would be detrimental to predatory mites for a period of at least 48 h. This approach would potentially allow predatory mites to rapidly adjust to their new environment with less stress, allowing for rapid establishment of predator populations. This, in turn, could improve the efficacy of these biocontrol agents leading to season-long suppression of S. dorsalis in strawberry fields, and potentially eliminating the need for multiple releases of predatory mites.