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Photo Tarryn Anne Goble

by Tarryn Anne Goble

Innovation Project Director


Content

1 - It’s a jungle in there – the complex greenhouse

2 - The IOBC toxicity classification system

3 - How LALGUARD M52 OD targets thrips & spider mites without harming beneficial allies

4 - We need kilograms of harvest not kilograms of natural enemies

5 - References

1 - It’s a jungle in there – the complex greenhouse

We often think of modern greenhouses as simple and sterile ecosystems with low biodiversity – the arctic circle to be sensationalistic. But greenhouses accommodate complex artificial communities of multiple pests and natural enemies – a jungle of complex interactions1. This complexity differs by crop because they have different susceptibilities to pests and may not be suitable for all natural enemies. Take sweet pepper for instance – a crop that has multiple pests (thrips, whitefly, aphids, and spider mites) and can have as many as eight plus different highly specialized parasitoids and generalist insect predators released for pest control (Fig 1.).

 

Fig 1. Artificial insect community in sweet pepper of the most used natural enemies of key pests. The generalist predators are bugs from the genus Orius (O. sp.), the mirid bug Macrolophus pygmaeus (M. p.) and generalist phytoseiid predatory mites (g). Specialist enemies of aphids are parasitoids: Aphidius (A. sp.), the predatory midge Aphidoletes aphidimyza (A.a.) and the syrphid Episyrphus balteatus (E.b.). Parasitoids are commonly attacked by several species of hyperparasitoids (h). The specialist predator of spider mites Phytoseiulus persimilis (P.p.). The main whitefly species in sweet pepper is Bemisia tabaci, which can be controlled by specialist whitefly parasitoids from the genus Eretmocerus (E. sp.). SOURCE: Messelink et al. 2013.

 

Despite the success of natural enemies in high-value greenhouse crops, there are still many cases where arthropod natural enemies are not used due to high costs or low efficacy14. Western flower thrips, Frankliniella occidentalis (WFT) (Fig 2.) for example, can be controlled effectively by phytoseiid predatory mites in sweet pepper which provides pollen and nectar, but not in many ornamental plants lacking these supplemental food resources2. In such scenarios, microbials have potential as a complementary measure in biological control programs. These natural enemies (I include microbials here) not only interact with the pests they control but also have complex interactions with each other – some positive, neutral or negative1.

Fig 2. Western flower thrips (Frankliniella occidentalis). Photo: Matthew Bertone

The pirate bug, Orius spp. act as intraguild predators of phytoseiid mites, predatory midge, and aphid parasitoids1 and the biological control of aphids can be seriously disrupted by hyper predation by the predatory mite Amblyseius swirskii on the predatory midge, Aphidoletes aphidimyza3. Likewise, fungal based microbials (LALGUARD M52 OD) can have negative impacts on the natural enemies (predatory mites) of WFT under laboratory conditions (<30% mortality) but overall increased biological control effects are observed when both agents are applied in the greenhouse4. Application of additional control agents (I include microbials here) should, ideally, complement or support these persistent communities of natural enemies. It’s an expensive business for growers to invest in natural enemies – they don’t come cheap! An estimated cost for all biological control agents in an IPM program ranges between €1.5 – 2 per m2 (Sterk pers comm). So, the conservation of natural enemies in IPM programs is a key goal and it’s important to select ‘low risk,’ selective pesticides with a lower level of persistence. Making sure their investments don’t go the way of the dinosaurs compels growers to ask tough questions about microbial compatibility. “Why, if LALGUARD M52 OD is a broad-spectrum bioinsecticide, is it considered compatible with natural enemies that themselves could become infected?”

2 - The IOBC toxicity classification system

Before we start – it is important to understand how compatibility between natural enemies and pesticides is measured. The International Organization of Biological and Integrated Control (IOBC-WPRS Working Group) published a database (https://iobc-wprs.org/ip-tools/) aimed at compiling information on the effects of synthetic insecticides and natural compounds on natural enemies (e.g. predators and parasitoids) of crop pests, to assist growers in choosing compatible, low risk pesticides, thereby creating a harmonized international standard. It is largely based on the IOBC’s ‘Pesticide Side Effect Database’- employing a tiered approach to categorize pesticides into four classes depending on the mortality level (%) they induce and/or reductions in life history performance in natural enemies5,6. The guidelines are based on the release of natural enemies on residues in laboratory trials – a worst case scenario.

Table 1: IOBC system for classifying adverse effects by pesticides at their recommended dose rates on natural enemies.

 

2.1 – The evolution of the IOBC toxicity system – introduction of the predator/prey or parasitoid/host ratio

Unfortunately – like all good intentions – the simplicity of the IOBC’s toxicity classification system was met with some criticism, for example: what was the practical relevance of worst-case scenario laboratory trials? What was the difference between 74% mortality (Class 3 – moderately toxic) and 76% mortality (Class 4 – harmful) for a semi-field or field trial? Or how to interpret the classes? For example: can a Class 3 compound be used and if so, when? Also, the adoption of the IOBC’s rating system brought with it a clash between the experimental results and feedback from horticulture. There were examples of false positive/negative results, causes of mortality due to prey/host scarcity and differences in conclusions based of beneficial release methods and timings5,6.

To accommodate the complexity of nature that doesn’t quite seem to fit inside a neat little box, and to make the integration of pesticides into IPM programs a little more practical, companies, like IPM Impact7 have taken the IOBC’s classification system’s and evolved it further. This brought about the introduction of a fifth class “the eradicant” – dum dum dum dah – compounds which cause 98-100% mortality -causing natural enemies to be eliminated and cannot be included in IPM programs (Table 1)5. Since IPM focuses on decreasing pests in a crop, the efficacy of the pesticide also needs to be considered and new formulae to calculate the predator/prey or parasitism/host ratio = (IOBC Toxicity Class) x (reversed Efficacy Class) was introduced5.

This considers both pesticidal toxicity to the natural enemy but also the efficacy of the pesticide against the target pest. The efficacy class of the pesticide is calculated as pest mortality (%) but reversed where: 1 for > 80% efficacy, 2 for 60-80% efficacy, 3 for 40-60%, 4 for 20-40% efficacy, and 5 for <20% efficacy. Lallemand Plan Care has been progressively collecting data from undertaken with LALGUARD M52 OD  by IPM Impact and could integrate the IOBC toxicity rating and the predator/prey or parasitism/host ratio to assess IPM compatibility with natural enemies (Table 2). We see that ultimately, the product is compatible with natural enemies and can be integrated into IPM programs. This is not surprising, as a suite of literature describes this compatibility well, provided the appropriate release timings are respected15.

Table 2: Integrated Pest Management compatibility of LALGUARD M52 OD (at 1.25L/ha) with various thrips natural enemies highlighting the IOBC toxicity class and the integration of the predator/prey ratio.

3 - How LALGUARD M52 OD targets thrips & spider mites without harming beneficial allies

3.1 Western flower thrips

In the greenhouse world, western flower thrips (WFT) pose a daunting challenge. Their ability to damage crops and spread viruses demands efficient integrated pest management (IPM), especially with EU legislation tightening on chemical insecticides. In the battle against thrips, key allies emerge – predatory foliar and soil mites like Amblyseius swirskii, Neoseiulus cucumeris, Amblyseius andersoni, Amblydromalus limonicus, Macrocheles robustulus, Gaeolaelaps aculeifer and Stratiolaelaps scimitus, alongside generalist predators like Orius spp., notably the predatory anthocorid bug8.

These relentless hunters target thrips at every stage, maintaining balance and safeguarding crops with precision. LALGUARD M52 OD was found to have minimal impact on beneficial predatory mites, N. cucumeris and A. swirskii, with mortality levels below 30% (IOBC toxicity class 2) and observations indicated compatibility and overall increased effects when both biological control agents were applied in the greenhouse4. Also, when the soil-dwelling predatory mite, G. aculeifer was exposed to M. brunneum F52 there were no mortality effects nor effects on longevity and fecundity9. Soil dwelling natural enemies, rove beetles and predatory mites exposed for 12 days to LALGUARD M52 GR reacted differently to the product but in container studies the efficacy against WFT was significantly improved when the predators and fungi were combined, achieving >90% thrips mortality, compared to each used separately16.

 

Orius spp. (Fig. 3), play a crucial role in controlling thrips and spider mites. However, they’re not invulnerable. Exposure to M. brunnuem F52 can make Orius spp. susceptible to fungal infections, earning them a “moderately toxic” (class 3) or “slightly toxic” (class 2) rating in the IOBC classification system depending on species. Yet, strategic behaviors that Orius spp. have like detection, spatial avoidance, and selective predation can mitigate this susceptibility.

Fig 3. Genus Orius spp. Photo: Bufface

Orius albidipennis, for instance, demonstrated an ability to detect and avoid patches treated with M. brunneum13. Moreover, feeding and predation rates remained unaffected when preying on Metarhizium-treated thrips13. Combinations of soil applied Metarhizium and early release of O. laevigatus (targeting L1 larvae) can be a successful and reliable biocontrol strategy for WFT and even result in additive biological control17. Some authors assessed commercial entomopathogenic fungi applied every week for a month in a Mediterranean strawberry greenhouse where Orius spp. and thrips were naturally established – no negative effects were seen in Orius spp. populations with the fungal bioinsecticides18. It was concluded that fungal biopesticides might be useful at the beginning of spring when winter temperatures induce diapause in Orius spp. but thrips con­tinues to reproduce through winter18. Biopesticides may also be useful as corrective tools when pest outbreaks occur.

3.2 Two spotted spider mites

Likewise, two-spotted spider mites are pervasive pest of protected crops, many chemical acaricides fail to control them because resistance develops quickly due to their short generation time and high fecundity. Predatory mites P. persimilis, N. californicus and predatory pirate bugs Orius spp. are important natural enemies of two-spotted spider mites. We also know that LALGUARD M52 OD is efficient against two-spotted spider mites – so how is it possible that we can achieve compatibility?

Beneficial insects and mites have a repertoire of physiological and behaviors that safeguard them against fungal infections. Research suggests that the intrinsic immunity of adult two-spotted spider mites is weaker, and they were more susceptible to M. brunneum F52 infection than predatory mites P. persimilis and N. californicus when exposed to the same spore concentration10. Also-predatory mites’ natural resistance to fungal infection (differences in cuticle proteins and fatty acids),11 grooming behavior12 and strong aversion behaviour12 to fungal sprayed leaves help maintain their population despite fungal exposure – immunity and behaviors that are not observed in two spotted spider mites.

4 - We need kilograms of harvest not kilograms of natural enemies

While growers are spending considerable amounts of money establishing natural enemies in greenhouse crops and while it’s important to conserve this investment by conducting compatibility studies to find low risk insecticides to compliment natural enemy efficacy – it’s critical to maintain some perspective. Its sounds spectacular to have many beneficial insects in a crop but remember these natural enemies only build up populations by feeding on the pest, so it also means that there are a lot of pests and thus severe crop damage. One might happily observe hundreds of Aphidius sp. mummies in sweet pepper atop black leaves dauntingly covered in sooty mold from the honeydew of Myzus persicae. To quote IPM Impact, “we don’t need kilograms of beneficial organisms in our crop, we need kilograms of quality harvest.” Afterall, the main aim of crop production is to achieve both high quantity and quality yields.

All this to say that it might be easy for a grower to quickly dismiss adding microbial pesticides to biological control programs because they may reduce natural enemies , but the sheer complexity of these artificial greenhouse ecosystems means that all sorts of interactions are going on and it’s difficult to point fingers at simply one component. The best way to approach this is first to consider the type of crop – not all crops are susceptible to the same pests and not all natural enemies are suitable, effective enough, available to purchase, or simply too expensive for the crop. Microbials in this case represents a complementary strategy but their application against the pests should not disrupt populations of natural enemies, thus careful consideration should be given to the timing and repeat number of microbial applications used. Growers will continuously monitor the effectiveness of microbial pesticides and their impact on natural enemy populations. If necessary, adjust the application timing to optimize pest control while preserving their beneficial organism investment. If the pest affects yields and successful biocontrol is achieved overall, some negative side effects on natural enemies can be tolerated.

5 - References

  1. Messelink, G., Sabelis, M., & Janssen, A. (2012). Generalist predators, food web complexities and biological pest control in greenhouse crops. 10.5772/30835.
  2. Messelink, G. J., et al. (2014). Approaches to conserving natural enemy populations in greenhouse crops: Current methods and future prospects. Biocontrol, 59, 377–393.
  3. Messelink, G., Bloemhard, C., Sabelis, M., & Janssen, A. (2013). Biological control of aphids in the presence of thrips and their enemies. BioControl, 58, 45–55.
  4. Saito, T., & Brownbridge, M. (2018). Compatibility of foliage-dwelling predatory mites and mycoinsecticides, and their combined efficacy against WFT Frankliniella occidentalis. Journal of Pest Science, 91.
  5. Sterk, G., Hanegraaf, J., Hennen, P., & Kolokytha, P. Reconsidering the IOBC Toxicity Classification System: Problems and incompatibilities arising from its use. Introduction of the Predator/Prey or Parasitoid/Host ratio as a new, more realistic Classification System. [Online]. Available: https://iobc-wprs.org/product/reconsidering-the-iobc-toxicity-classification-system-problems-and-incompatibilities-arising-from-its-use-introduction-of-the-predator-prey-or-parasitoid-host-ratio-as-a-new-more-realistic-classifi/
  6. Hassan, S. A. (1998). The initiative of the IOBC/WPRS Working Group on Pesticides and Beneficial Organisms. In P. T. Haskell & P. McEwen (Eds.), Ecotoxicol. Springer.
  7. IPM Impact. Retrieved from https://www.ipmimpact.com/
  8. Mouden, S., Facun, K., Klinkhamer, P., & Leiss, K. (2017). Integrated pest management in WFT: Past, present and future. Pest Management Science, 73. 10.1002/ps.4531.
  9. De Azevedo, A. G. C., Eilenberg, J., Steinwender, B. M., & Sigsgaard, L. (2019). Non-target effects of Metarhizium brunneum (BIPESCO 5/F 52) in soil show that this fungus varies between being compatible with, or moderately harmful to, four predatory arthropods. Biological Control, 131, 18–24.
  10. Dogan, Y. O., Hazir, S., Yildiz, A., Butt, T. M., & Cakmak, I. (2017). Evaluation of entomopathogenic fungi for the control of Tetranychus urticae (Acari: Tetranychidae) and the effect of Metarhizium brunneum on the predatory mites (Acari: Phytoseiidae). Biological Control, 111, 6–12.
  11. Wu, S., Xie, H., Li, M., Xu, X., & Lei, Z. (2016). Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite species. Experimental and Applied Acarology, 70(4), 421–435.
  12. Wu, S., Xing, Z., Sun, W., Xu, X., Meng, R., & Lei, Z. (2018). Effects of Beauveria bassiana on predation and behavior of the predatory mite Phytoseiulus persimilis. Journal of Invertebrate Pathology, 153, 51–56.
  13. Pourian, H.-R., Talaei-Hassanloui, R., Kosari, A. A., & Ashouri, A. (2011). Effects of Metarhizium anisopliae on searching, feeding and predation by Orius albidipennis (Hem., Anthocoridae) on Thrips tabaci (Thy., Thripidae) larvae. Biocontrol Science and Technology, 21(1), 15–21.
  14. Gonzalez, F., Tkaczuk, C., Dinu, M. M., Fiedler, Ż., Vidal, S., Zchori-Fein, E., & Messelink, G. J. (2016). New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops. Journal of Pest Science, 89, 295–311.
  15. Koller, J.; Sutter, L.; Gonthier, J.; Collatz, J.; Norgrove, L. (2023) Entomopathogens and Parasitoids. Allied in Biocontrol: A Systematic Review. Pathogens. 12, 957.
  16. Saito, T; Brownbridge, M. (2016) Compatibility of soil-dwelling predators and microbial agents and their efficacy in controlling soil-dwelling stages of WFT Frankliniella occidentalis. Biological Control, 92, 92-100.
  17. Otieno, J.A., Pallmann, P. & Poehling, HM. (2017) Additive and synergistic interactions amongst Orius laevigatus(Heteroptera: Anthocoridae), entomopathogens and azadirachtin for controlling WFT (Thysanoptera: Thripidae). BioControl, 62, 85–95.
  18. Bonsignore, C. & Vacante, Vincenzo. (2012). Influences of Botanical Pesticides and Biological Agents on Orius Laevigatus – Frankliniella Occidentalis Dynamics Under Greenhouse Conditions. Journal of Plant Protection Research. 52. 15-23.

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