Using bumblebees to disseminate biocontrol agents in strawberry cultivation

From Triple Performance
Damage caused by Botrytis cinerea on a strawberry

In crops of strawberries, it is possible to use the antagonist fungus Gliocladium catenulatum as a biocontrol agent to fight against Botrytis cinerea and to disseminate it onto flowers via the use of bumblebees.

Context

The grey mold caused by Botrytis cinerea is one of the most important threats to crops of strawberries. Conventional strawberry cultivation requires 3 to 8 fungicide treatments per season. Currently, in organic farming, strawberry growers have no effective control means against this pathogen which becomes resistant and causes heavy agricultural losses. In conventional farming, grey mold causes losses of between 10 to 35% of the harvest despite 3 to 8 fungicide treatments per season [1] [2]. There are some prevention methods already commonly used in agriculture [3].

Some current prevention methods against Botrytis cinerea

  • Remove infected parts of the plant: Collecting and removing infected parts of the plant can slow the spread of the disease.
  • Improve air circulation around plants: Space plants widely and prune leaves so that adequate airflow can speed up drying of vegetation.
  • Choose the right location: Plant strawberries in full sun and ensure the planting area is cleared of weeds. This will help improve airflow around the plants, making them less humid and thus less easily infected.
  • Avoid spring applications of nitrogen fertilizer: High levels of nitrogen promote excessive leaf growth and surfaces available for infection.
  • Harvest regularly: Remove and discard rotten or severely damaged fruits throughout the season.
  • Choose a good cultivar: Select cultivars that produce smaller leaves such as "Allstar", "Earliglow" or "Jewel".
Symptoms of Botrytis cinerea infections in strawberry. A) Senescent flower with B. cinerea mycelium growth. B) Advanced stage floral infection. C and D) Fruit infections at different stages. E and F) Fruit rot [2]

Protecting strawberries with a biocontrol agent

Infection by B. cinerea occurs mainly during flowering, after which the pathogen can remain inactive for a long period and cause fruit rot before or after harvest [4].   Protecting flowers is therefore considered a key strategy in fighting grey mold[5].

Bumblebee used in the Flying Doctors system foraging on a strawberry flower

To precisely control the disease, it is possible to use bumblebees (Bombus terrestris) as a vector to carry the antagonist fungus Gliocladium catenulatum J1446 (Prestop® 4B) to flowers using the Flying Doctors system [5].


The antagonistic effect of G. catenulatum is based on competition with pathogenic fungi. By colonizing the flower surface faster than B. cinerea, it deprives it of living space and nutrients. It thus prevents infection by inhibiting the pathogen [6]. It can be compared to a hyperparasite [7].

The Flying Doctors system

The Flying Doctors system consists of a bumblebee hive with an integrated product dispenser. Bumblebees leaving the hive pass through the dispenser filled with Prestop® 4B and their hairs become loaded with the biocontrol product safe for the health of these insects.  

A European project named BICOPOLL has proven the effectiveness and rapidly increased the dissemination of this technology to fight against Botrytis cinerea [8][9].

Effectiveness

Prestop® 4B is mainly used preventively in greenhouse crops of strawberries and raspberries, but it can also be used in the field.. The concept has proven effective on a wide range of crops, such as strawberries, raspberries, pears, apples, blueberries, cherries and even grapes [8][9].

The effectiveness of the device on Prestop® Mix has been evaluated both in greenhouse and field [6].


It has been shown that hives with Gliocladium catenulatum (biocontrol agent) were as effective in protecting strawberry crops from grey mold as conventional fungicides [10]. Under high disease pressure, Flying Doctors reduced the infected plant area by 50% on average, a result comparable to conventional fungicides. Under low disease pressure, biological control achieved a reduction in grey mold affected areas of 68.4% on average, which was superior to fungicide sprays. [11] [5][12][13]

Results of Flying Doctors protection effectiveness against grey mold caused by B. cinerea. The following treatments were compared to test the impact of G. catenulatum vectored by bumblebees: untreated control, conventional chemical spray (fungicide), Flying Doctors (Biocontrol), conventional spray with G. catenulatum (Fungicide + biocontrol) [11].
Graph showing the increase in strawberry shelf life after harvest using Flying Doctors technology. The Flying Doctors treatment with Prestop® 4B is compared to a conventional spray scheme [6].

Moreover, the use of the Flying Doctors device has resulted in yield increases of up to 50% [8][9]. The shelf life of strawberries after harvest is also extended when grey mold is controlled from flowering [6].   This resulted in more durable control with healthier strawberries and fewer residues [5] [14] .  

The Flying Doctors technique provides precise, continuous and targeted biocontrol, thus ensuring good protection against B. cinerea.

Materials

  • Flying Doctors hive (Hive or multi-Hive) [6][7]
  • Dispenser [6][7]
  • Pollinator agent, in this case the terrestrial bumblebee (Bombus terrestris)
  • Active biocontrol agent, here Prestop® 4B (contains 1x10^8 cfu/g of G. catenulatum J 1446). In France, the product is available in a 100 g aluminum sachet [6].

Estimated doses and costs

  • 2 applications per week of 5-10g of Prestop® 4B per hive, corresponding to 500-800g of product per hectare over a 1-month period [7][15].
  • In greenhouses, estimated costs are 150 euros per Flying Doctors hive including the biocontrol agent [7][15].
  • Outdoors, estimated costs are 300 euros per hive [7][15].
  • Costs depend on the size of the field and the type of crop to be treated. Although honeybee hives can still be rented, bumblebee hives are now also available on the market through companies such as BioBest and Koppert.
Description and diagram of a Flying Doctors hive and its internal distribution system [7].


Method

To fully benefit from the Flying Doctors technique, it is recommended that organic berry and fruit producers:

  • Hire beekeepers.
  • Manage vegetation inside and around the target crop to support pollinators activity [1].


The complete usage method is available on the website Biobest Flying Doctors [6][7]. It is necessary to:

  • Set up the Flying Doctors hive and wait 30 minutes before opening.
  • The product must be distributed evenly in the Flying Doctors system dispenser and reloaded/replaced every 3 to 4 days or sooner if the product is depleted.
  • STORAGE: Unopened packages of Prestop® 4B can be stored for one year if kept in dry and cool conditions (below +8 ºC), and for two weeks at room temperature. Once opened, carefully reseal and keep in a cool place for up to one month.

In Finland, it is estimated that this technique is implemented on more than 500 hectares of strawberry crops (15% of the strawberry growing area) [1].

Differences in quantities of pesticides and products used between conventional and organic farming (BVT or Flying Doctors).

An example of application in France

La Framboiseraie is a family business growing small fruits for 35 years in Haute-Savoie. The company’s manager has been committed to an eco-responsible approach for more than 10 years, favoring biological methods over synthetic pesticides for his crops.

A collaboration started with BIOBEST in 2010 and has continued to this day. Besides integrated pest management deployed over the entire protected area, since 2019 he has integrated the unique and innovative Flying Doctors system combined with Prestop® 4B.

According to the manager, this solution is a real success because it works much better than synthetic references: it allows him to make no treatments against B. cinerea with ultimately better results than before, without fungicide residues and without disrupting the integrated control in place. A boon in a context where restrictions on pesticide residues in France and also in Switzerland (the marketing country for his production) are significant. However, according to La Framboiseraie, as this technique is still recent, the application costs of Flying Doctors are higher than conventional fungicide application.

Implementation

Spatial scale

  • Position the hive so that the flight hole faces Southeast [7].
  • In greenhouse: between 7 to 10 normal Flying Doctors hives per hectare [7][15].
  • Outdoors: Multi-hive Flying Doctors containing 3 large bumblebee colonies per hive are more appropriate. Between 5 to 8 hives per hectare are needed [10][7].

The effectiveness and impact of the Flying Doctors technique can be improved by good hive management (size, number, location) and vegetation management around crops [8][9].

Photos of a Flying Doctors hive in a greenhouse (A) and a Multi-Hive outdoors (B).

Environmental scale

  • Terrestrial bumblebees work optimally between 8°C and 35°C [6][7].
  • The biocontrol agent (G. catenulatum) is more effective at temperatures ranging from 15 to 25 °C and relative humidity between 60 and 80 %. At temperatures above 42 °C, the fungus, spores and mycelium are not viable [6][7] .

Results show that crop protection is equal or superior to that provided by a full chemical fungicide program, under the same weather conditions and over a wider geographical area [1].

Temporal scale

  • Open hives in the early morning. Never open them in the afternoon [6][7].
  • Prestop® 4B must be used from the start of the flowering period [6][7] .
  • For hives and multi-hives (Multi-Hive), pollination lasts 6 to 10 weeks and they are equipped with a feeding system safe for bumblebees [6] [7].

Chemical pesticides are generally sprayed early in the morning or late in the evening when bumblebees are inside the hive. Consequently, this technique is compatible with chemical treatments such as insecticides or fungicides and can be used in an integrated pest management program [1].

The list of compatible active substances is given below:

Table of fungicides and insecticides compatible with the use of Flying Doctors. [6] [7]

Regulations

  • The application of Prestop® 4B by pollinating bumblebees (product placed in hive dispensers) is authorized to fight grey mold in strawberry and raspberry crops since 2013 in Belgium, since 2015 in the Netherlands and since 2016 in France (Marketing Authorization, no. 2150847, under greenhouses and tunnels) [16].
  • Local legislation may impose restrictions regarding the use of terrestrial bumblebees in fields and greenhouses [6][7].

Sales and Alternatives

The Flying Doctors system with Prestop® 4B is sold directly by Biobest France but the company also offers alternatives such as Verdera B4. Other companies also sell equally effective alternatives like LALLEMAND PLANT CARE and Verdera (Prestop® Mix)[16]. The Canadian company BVT (Bee Vectoring Technologies) is also expected to enter the European market within a few years with the product BVT-CR-7.

Indeed, other biocontrol agents than Gliocladium catenulatum are currently under trial and development such as Trichoderma harzianum or Beauveria bassiana.

Additional information

The Flying Doctors technology won the 1st TROPHY ENVIRONMENT CATEGORY (Innovations that improve farmers' quality of life and the image of their profession) in 2016 and the 1st GOLD PRIZE - SIVAL COMPETITION (best innovations in equipment, products and services for all productions of plants) in 2017.

For more information regarding advantages/disadvantages, economic, environmental, social criteria and some testimonials on the use of pollinators in biocontrol, see the article « Use of pollinators as vectors of biocontrol agents ».


Cette page a été rédigée en partenariat avec Msc Boost




Appendices

Contribue à

S'applique aux cultures suivantes

Défavorise les bioagresseurs suivants


Sources

  1. 1.0 1.1 1.2 1.3 1.4 Hokkanen, H. M. T., Menzler-Hokkanen, I. & Lahdenpera, M.-L. Managing Bees for Delivering Biological Control Agents and Improved Pollination in Berry and Fruit Cultivation. SAR 4, 89 (2015).
  2. 2.0 2.1 Petrasch, S., Knapp, S. J., van Kan, J. A. L. & Blanco‐Ulate, B. Grey mould of strawberry, a devastating disease caused by the ubiquitous necrotrophic fungal pathogen Botrytis cinerea. Molecular Plant Pathology 20, 877–892 (2019).
  3. https://www.missouribotanicalgarden.org/gardens-gardening/your-garden/help-for-the-home-gardener/advice-tips-resources/pests-and-problems/diseases/fruit-spots/gray-mold-of-strawberry.aspx
  4. Blanco, C., de Santos, B. los & Romero, F. Relationship between Concentrations of Botrytis Cinerea Conidia in Air, Environmental Conditions, and the Incidence of Grey Mould in Strawberry Flowers and Fruits. Eur J Plant Pathol 114, 415–425 (2006).
  5. 5.0 5.1 5.2 5.3 Stoffels, K., Wäckers, F. & Baets, W. Control of Botrytis cinerea in strawberries with Gliocladium catenulatum vectored by bumblebees. 9.
  6. 6.00 6.01 6.02 6.03 6.04 6.05 6.06 6.07 6.08 6.09 6.10 6.11 6.12 6.13 6.14 https://www.biobestgroup.com/fr/actualites/flying-doctors%C2%AE-et-prestop%C2%AE-4b-en-framboises-%3A-pollinisation-et-lutte-biologique-contre-le-botrytis
  7. 7.00 7.01 7.02 7.03 7.04 7.05 7.06 7.07 7.08 7.09 7.10 7.11 7.12 7.13 7.14 7.15 7.16 7.17 https://www.biobestgroup.com/fr/biobest/produits/la-pollinisation-par-les-bourdons-4458/ruches-de-bourdons-7130/flying-doctors-hive-%28b-t-%29-4836/
  8. 8.0 8.1 8.2 8.3 https://projects.au.dk/co2results/conclusions-and-recommendations/bicopoll/
  9. 9.0 9.1 9.2 9.3 https://mahekeskus.emu.ee/en/projects/bicopoll/
  10. 10.0 10.1 Reeh, K. W. Commercial Bumble Bees as Vectors of the Microbial Antagonist Clonostachys rosea for Management of Botrytis Blight in Wild Blueberry (Vaccinium angustifolium). 99.
  11. 11.0 11.1 https://quoidansmonassiette.fr/bicopoll-project-culture-fraise-bio-abeilles-remplacer-pesticides-alternatives/
  12. Jane, M. M., Mary, W. G., Rebecca, K. & Sheila, O. Managed bees as pollinators and vectors of bio control agent against grey mold disease in strawberry plantations. Afr. J. Agric. Res. 16, 1674–1680 (2020).
  13. Macedo, J. et al. The Potential of Bee Vectoring on Coffee in Brazil. in Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops (eds. Smagghe, G., Boecking, O., Maccagnani, B., Mänd, M. & Kevan, P. G.) 165–181 (Springer International Publishing, 2020). doi:10.1007/978-3-030-18917-4_10.
  14. Pozo, M. I., Vendeville, J., Mommaerts, V. & Wackers, F. Flying Doctors for a Better Quality in Fruit Production. in Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops (eds. Smagghe, G., Boecking, O., Maccagnani, B., Mänd, M. & Kevan, P. G
  15. 15.0 15.1 15.2 15.3 Using pollinators to apply a biofungicide (Prestop 4B) against grey mold of strawberry, Liette Lambert, 2017.
  16. 16.0 16.1 https://www.beevt.com/industry-news/articles/01042021-bee-vectoring-technologies-delivers-patented-organic-pesticides-with-some-help-from-the-hive