Bumble bee colony health is diminished in a mesotunnel enclosure planted with a cucurbit monoculture crop

Lexi Gauger; Kathleen Fiske Pulliam; Yuuki Cherian; Mateo Garcia; Benjamin Morrison; David Gonthier

doi:10.26786/1920-7603(2025)859

Authors

Lexi Gauger University of Kentucky https://orcid.org/0009-0006-3510-5971
Kathleen Fiske Pulliam University of Kentucky https://orcid.org/0009-0004-3668-6048
Yuuki Cherian University of Kentucky
Mateo Garcia University of Michigan
Benjamin Morrison University of Kentucky
David Gonthier University of Kentucky

DOI:

https://doi.org/10.26786/1920-7603(2025)859

Keywords:

pollinator health, protective cover agriculture, row covers, bee colony health, pollination management

Abstract

The use of “mesotunnels” (mesh netting pest-exclusion structures) as a sustainable pest management strategy is increasing among organic vegetable growers. However, pollination management presents a challenge in this system, and little is known about how mesotunnels impact pollinator health. This study examines bee colony health in mesotunnels, using commercial Bombus impatiens colonies in cucurbit crop mesotunnels as a relevant model system in a two-year experiment. To assess colony-level health, we combined several variables into “colony health indices” that produce summary values of the somatic (related to pollination service delivery, including number of workers, worker and nest mass, and stored pollen and nectar), reproductive (related to sexual reproduction, including number of immatures, drones, and queen size), and overall colony health (including all variables in somatic and reproductive indices). We found that in 2023 B. impatiens colonies in a cucurbit mesotunnel foraging environment had worse reproductive health and overall health than free-foraging colonies, but performed similarly in their somatic health. In several measurements, colonies from mesotunnels performed similarly to colonies with no foraging access. Our results suggest that commercial colonies in mesotunnel environments are not compromised in their potential to provide crop pollination services, but are compromised in their ability to reproduce and persist year-over-year. Our colony health indices could be adapted to assess the status of reproduction and ecosystem service delivery for social bees.

References

Acharya TP, Welbaum GE, Arancibia RA (2019) Low Tunnels Reduce Irrigation Water Needs and Increase Growth, Yield, and Water-use Efficiency in Brussels Sprouts Production. HortScience 54:470–475. DOI: https://doi.org/10.21273/HORTSCI13568-18

Artz DR, Nault BA (2011) Performance of Apis mellifera, Bombus impatiens, and Peponapis pruinosa (Hymenoptera: Apidae) as pollinators of pumpkin. Journal of Economic Entomology 104:1153–1161. DOI: https://doi.org/10.1603/EC10431

Benke K, and Tomkins B (2017) Future food-production systems: vertical farming and controlled-environment agriculture. Sustainability: Science, Practice and Policy 13:13–26. DOI: https://doi.org/10.1080/15487733.2017.1394054

Birmingham AL, Winston ML (2004) Orientation and drifting behaviour of bumblebees (Hymenoptera: Apidae) in commercial tomato greenhouses. Canadian Journal of Zoology 82:52–59. DOI: https://doi.org/10.1139/z03-201

Brochu KK, van Dyke MT, Milano NJ, Petersen JD, McArt SH, Nault BA, Kessler A, Danforth BN (2020) Pollen defenses negatively impact foraging and fitness in a generalist bee (Bombus impatiens: Apidae). Scientific Reports 10:3112. DOI: https://doi.org/10.1038/s41598-020-58274-2

Calvo-Baltanás V, Vilcinskas A, Brück T, Kloas W, Wilke T, Rufino M, Henkel M, Zorn H, Monje O, Asseng S (2025) The future potential of controlled environment agriculture. PNAS Nexus 4, pgaf078 DOI: https://doi.org/10.1093/pnasnexus/pgaf078

Campbell JW, Bammer M, Bustamante TA, Ellis JD (2019) The Health of Commercial Bombus impatiens (Hymenoptera: Apidae) Colonies After Foraging in Florida Watermelon and Blueberry. Environmental Entomology 48:1197–1202. DOI: https://doi.org/10.1093/ee/nvz081

Chandler D, Cooper E, Prince G (2019) Are there risks to wild European bumble bees from using commercial stocks of domesticated Bombus terrestris for crop pollination? Journal of Apicultural Research 58:665–681. DOI: https://doi.org/10.1080/00218839.2019.1637238

Cheng N, Zhang W, Gleason M (2023) Controlling Pests and Diseases Using Mesotunnels: Understanding Organic Cucurbit Crop Growers’ Preferences and Choices. Cornell University, Ithaca, NY, USA. [online] URL: https://dyson.cornell.edu/wp-content/uploads/sites/5/2023/06/EB_05_2023-VD.pdf

Cowan N, Ferrier L, Spears B, Drewer J, Reay D, Skiba U (2022) CEA Systems: the Means to Achieve Future Food Security and Environmental Sustainability? Frontiers in Sustainable Food Systems 6. DOI: https://doi.org/10.3389/fsufs.2022.891256

Cresswell JE (2017) A demographic approach to evaluating the impact of stressors on bumble bee colonies. Ecological Entomology 42:221–229. DOI: https://doi.org/10.1111/een.12376

Dafni A, Kevan P, Gross CL, Goka K (2010) Bombus terrestris, pollinator, invasive and pest: An assessment of problems associated with its widespread introductions for commercial purposes. Applied Entomology and Zoology 45:101–113. DOI: https://doi.org/10.1303/aez.2010.101

Dance C, Botías C, Goulson D (2017) The combined effects of a monotonous diet and exposure to thiamethoxam on the performance of bumblebee micro-colonies. Ecotoxicology and Environmental Safety 139:194–201. DOI: https://doi.org/10.1016/j.ecoenv.2017.01.041

Díaz-Pérez JC, Bag S, Coolong T, Luo X, Hodges A, Bashyal M, Milner H, Konakalla NC, Pitcher A (2024) Plant Growth, Fruit Yield, and Tomato Leaf Curl Disease of High Tunnel Organic Tomato Affected by Shade Net and Plastic Mulch Color. HortScience 59:323–331. DOI: https://doi.org/10.21273/HORTSCI17516-23

Dohlman EN, Maguire K, Davis WV, Husby M, Bovay J, Weber CE, Lee Y, United States. Department of Agriculture.Economic Research Service (2024) Trends, insights, and future prospects for production in controlled environment agriculture and agrivoltaics systems. Economic Research Service, U.S. Department of Agriculture, Washington, D.C. DOI: https://doi.org/10.32747/2024.8254671.ers

Edge AA, van Nest BN, Johnson JN, Miller SN, Naeger N, Boyd SD, Moore D (2012) Diel nectar secretion rhythm in squash (Cucurbita pepo) and its relation with pollinator activity. Apidologie 43:1–16. DOI: https://doi.org/10.1007/s13592-011-0087-8

Fisher RM, Pomeroy N (1989) Pollination of Greenhouse Muskmelons by Bumble Bees (Hymenoptera: Apidae). Journal of Economic Entomology 82:1061–1066. DOI: https://doi.org/10.1093/jee/82.4.1061

Fiske K (2024) Addressing the Trade-Offs of Pest Protective Row Covers for Integrated Pest Management in Vegetable Production. Theses and Dissertations-Entomology, University of Kentucky, Lexington, KY, USA

Fiske K, Cheng N, Kuesel R, Zhang W, Bessin R, Williams MA, Gonthier D (2024) Row covers limit pests and disease and increase profit in organic acorn squash. Frontiers in Sustainable Food Systems 8. DOI: https://doi.org/10.3389/fsufs.2024.1347924

Gervais A, Fournier V, Bélisle M (2020) Agricultural landscape composition affects the development and life expectancy of colonies of Bombus impatiens. Ecosphere 11:e03142. DOI: https://doi.org/10.1002/ecs2.3142

Goulson D (2010) Bumblebees: behaviour, ecology, and conservation, 2nd edn. Oxford University Press Inc., New York, NY. DOI: https://doi.org/10.1093/oso/9780199553068.001.0001

Guerra-Sanz JM (2008) Crop Pollination in Greenhouses. In: Bee Pollination in Agricultural Ecosystems. Oxford University Press, USA

Hass AL, Brachmann L, Batáry P, Clough Y, Behling H, Tscharntke T (2019) Maize-dominated landscapes reduce bumblebee colony growth through pollen diversity loss. Journal of Applied Ecology 56:294–304. DOI: https://doi.org/10.1111/1365-2664.13296

Hulse RA, Van Oystaeyen A, Carnell JD, Beckett D, Grey WG, Goulson D, Wackers F, Hughes WOH (2025) The effects of diet enhancement on the health of commercial bumblebee colonies. Apidologie 56,6. DOI: https://doi.org/10.1007/s13592-024-01132-1

Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out-compete their native conspecifics? Journal of Applied Ecology 43:940–948. DOI: https://doi.org/10.1111/j.1365-2664.2006.01199.x

Jones J, Rader R (2022) Pollinator nutrition and its role in merging the dual objectives of pollinator health and optimal crop production. Philosophical Transactions of the Royal Society B: Biological Sciences 377:20210170. DOI: https://doi.org/10.1098/rstb.2021.0170

Kendall LK, Evans LJ, Gee M, Smith TJ, Gagic V, Lobaton JD, Hall MA, Jones J, Kirkland L, Saunders ME, Sonter C, Cutting BT, Parks S, Hogendoorn K, Spurr C, Gracie A, Simpson M, Rader R (2021) The effect of protective covers on pollinator health and pollination service delivery. Agriculture, Ecosystems & Environment 319:107556. DOI: https://doi.org/10.1016/j.agee.2021.107556

Klatt BK, Nilsson L, Smith HG (2020) Annual flowers strips benefit bumble bee colony growth and reproduction. Biological Conservation 252:108814. DOI: https://doi.org/10.1016/j.biocon.2020.108814

Kleijn D, Winfree R, Bartomeus I, Carvalheiro LG, Henry M, Isaacs R, Klein A-M, Kremen C, M’Gonigle LK, Rader R, Ricketts TH, Williams NM, Lee Adamson N, Ascher JS, Báldi A, Batáry P, Benjamin F, Biesmeijer JC, Blitzer EJ, Bommarco R, Brand MR, Bretagnolle V, Button L, Cariveau DP, Chifflet R, Colville JF, Danforth BN, Elle E, Garratt MPD, Herzog F, Holzschuh A, Howlett BG, Jauker F, Jha S, Knop E, Krewenka KM, Le Féon V, Mandelik Y, May EA, Park MG, Pisanty G, Reemer M, Riedinger V, Rollin O, Rundlöf M, Sardiñas HS, Scheper J, Sciligo AR, Smith HG, Steffan-Dewenter I, Thorp R, Tscharntke T, Verhulst J, Viana BF, Vaissière BE, Veldtman R, Ward KL, Westphal C, Potts SG (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nature Communications 6:7414. DOI: https://doi.org/10.1038/ncomms8414

Knapp JL, Becher MA, Rankin CC, Twiston-Davies G, Osborne JL (2019) Bombus terrestris in a mass-flowering pollinator-dependent crop: A mutualistic relationship? Ecology and Evolution 9:609–618. DOI: https://doi.org/10.1002/ece3.4784

Knapp JL, Osborne JL (2019) Cucurbits as a model system for crop pollination management. Journal of Pollination Ecology 25(9), 89-102. DOI: https://doi.org/10.26786/1920-7603(2019)535

Lefebvre D, Pierre J (2006) Hive weight as an indicator of bumblebee colony growth. Journal of Apicultural Research 45(4), 217–218. DOI: https://doi.org/10.1080/00218839.2006.11101351

Lenth RV (2025) emmeans: Estimated Marginal Means, aka Least-Squares Means. [online] URL: https://rvlenth.github.io/emmeans/

Leza M, Watrous KM, Bratu J, Woodard SH (2018) Effects of neonicotinoid insecticide exposure and monofloral diet on nest-founding bumblebee queens. Proceedings of the Royal Society B: Biological Sciences 285:20180761. DOI: https://doi.org/10.1098/rspb.2018.0761

López-Uribe MM, Ricigliano VA, Simone-Finstrom M (2020) Defining Pollinator Health: A Holistic Approach Based on Ecological, Genetic, and Physiological Factors. Annual Review of Animal Biosciences 8:269–294. DOI: https://doi.org/10.1146/annurev-animal-020518-115045

Mallinger RE, Franco JG, Prischmann-Voldseth DA, Prasifka JR (2019) Annual cover crops for managed and wild bees: Optimal plant mixtures depend on pollinator enhancement goals. Agriculture, Ecosystems & Environment 273:107–116. DOI: https://doi.org/10.1016/j.agee.2018.12.006

Martin CD, Fountain MT, Brown MJF (2021) The potential for parasite spill-back from commercial bumblebee colonies: a neglected threat to wild bees? Journal of Insect Conservation 25:531–539. DOI: https://doi.org/10.1007/s10841-021-00322-x

McGrady CM, Strange JP, López-Uribe MM, Fleischer SJ (2021) Wild bumble bee colony abundance, scaled by field size, predicts pollination services. Ecosphere 12:e03735. DOI: https://doi.org/10.1002/ecs2.3735

McMinn-Sauder HBG, Colin T, Gaines Day HR, Quinlan G, Smart A, Meikle WG, Johnson RM, Sponsler DB (2024) Next-generation colony weight monitoring: a review and prospectus. Apidologie 55:13. DOI: https://doi.org/10.1007/s13592-023-01050-8

Miller O, Hale C, Richardson L, Sossa D, Iverson A, McArt S, Poveda K, Grab H (2023) Commercial Bombus impatiens colonies function as ecological traps for wild queens. Journal of Applied Ecology 60:592–600. DOI: https://doi.org/10.1111/1365-2664.14353

Moerman R, Vanderplanck M, Fournier D, Jacquemart A-L, Michez D (2017) Pollen nutrients better explain bumblebee colony development than pollen diversity. Insect Conservation and Diversity 10:171–179. DOI: https://doi.org/10.1111/icad.12213

Mphande K, Badilla-Arias S, Cheng N, González-Acuña JF, Nair A, Zhang W, Gleason ML (2024) Evaluating Pollination and Weed Control Strategies under Mesotunnel Systems for Organic Muskmelon Production in Iowa. HortTechnology 34:265–279. DOI: https://doi.org/10.21273/HORTTECH05379-23

Nair A, Ngouajio M (2010) Integrating Rowcovers and Soil Amendments for Organic Cucumber Production: Implications on Crop Growth, Yield, and Microclimate. HortScience 45:566–574. DOI: https://doi.org/10.21273/HORTSCI.45.4.566

Natupol Excel | Bumblebee Hives | Pollination Koppert Biological Systems, Inc. [online] URL: https://www.koppert.ca/natupol-excel/ (accessed 11 September 2025).

Nelson HM, González-Acuña JF, Nair A, Cheng N, Mphande K, Badilla-Arias S, Zhang W, Gleason ML (2023) Comparison of Row Cover Systems for Pest Management in Organic Muskmelon in Iowa. HortTechnology 33:103–110. DOI: https://doi.org/10.21273/HORTTECH05096-22

Parmentier L, Meeus I, Cheroutre L, Mommaerts V, Louwye S, Smagghe G (2014) Commercial bumblebee hives to assess an anthropogenic environment for pollinator support: a case study in the region of Ghent (Belgium). Environmental Monitoring and Assessment 186:2357–2367. DOI: https://doi.org/10.1007/s10661-013-3543-2

Pethybridge S, Damann K, Murphy S, Diggins KR, Gleason ML (2024) Optimizing organic muskmelon production by integrating mesotunnel row covers, inter-bed weed management, and pollination strategies. Renewable Agriculture and Food Systems 39:e31. DOI: https://doi.org/10.1017/S1742170524000309

Peto BR, Costa CP, Moore ME, Woodard SH (2025) Social control of egg-laying in independently nest-founding bumble bee queens. BMC Ecology and Evolution 25:30. DOI: https://doi.org/10.1186/s12862-025-02364-0

R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. [online] URL: https://www.R-project.org/

Raven PH, Wagner DL (2021) Agricultural intensification and climate change are rapidly decreasing insect biodiversity. Proceedings of the National Academy of Sciences 118:e2002548117. DOI: https://doi.org/10.1073/pnas.2002548117

Requier F, Jowanowitsch KK, Kallnik K, Steffan-Dewenter I (2020) Limitation of complementary resources affects colony growth, foraging behavior, and reproduction in bumble bees. Ecology 101:e02946. DOI: https://doi.org/10.1002/ecy.2946

Roger N, Michez D, Wattiez R, Sheridan C, Vanderplanck M (2017) Diet effects on bumblebee health. Journal of Insect Physiology 96:128–133. DOI: https://doi.org/10.1016/j.jinsphys.2016.11.002

Roldán-Serrano AS, Guerra-Sanz JM (2005) Reward attractions of zucchini flowers (Cucurbita pepo L.) to bumblebees (Bombus terrestris L.). European Journal of Horticultural Science:23–28. DOI: https://doi.org/10.1079/ejhs.2005/27627

Rotheray EL, Osborne JL, Goulson D (2017) Quantifying the food requirements and effects of food stress on bumble bee colony development. Journal of Apicultural Research 56:288–299. DOI: https://doi.org/10.1080/00218839.2017.1307712

Sachman-Ruiz B, Narváez-Padilla V, Reynaud E (2015) Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central México. Biological Invasions 17:2043–2053. DOI: https://doi.org/10.1007/s10530-015-0859-6

Settele J, Bishop J, Potts SG (2016) Climate change impacts on pollination. Nature Plants 2:1–3. DOI: https://doi.org/10.1038/nplants.2016.92

Sideman B (2017) 4 - Row Covers. In: Orzolek MD (ed) A Guide to the Manufacture, Performance, and Potential of Plastics in Agriculture. Elsevier, pp 61–77. DOI: https://doi.org/10.1016/B978-0-08-102170-5.00004-X

Skidmore A, Wilson N, Williams M, Bessin R (2019) Integrating Rowcovers and Strip Tillage for Pest Management in Summer Squash and Muskmelon Production. HortTechnology 29:923–932. DOI: https://doi.org/10.21273/HORTTECH04221-18

Straub F, Birkenbach M, Leonhardt SD, Ruedenauer FA, Kuppler J, Wilfert L, Ayasse M (2023) Land-use-associated stressors interact to reduce bumblebee health at the individual and colony level. Proceedings of the Royal Society B: Biological Sciences 290:20231322. DOI: https://doi.org/10.1098/rspb.2023.1322

Thorp RW (2003) Bumble Bees (Hymenoptera: Apidae): Commercial Use and Environmental Concerns. In: For Nonnative Crops, Whence Pollinators of the Future? Entomological Society of America, p 21. [online] URL: https://bioone.org/ebooks/thomas-say-proceedings/For-Nonnative-Crops-Whence-Pollinators-of-the-Future/5/Chapter-2--Bumble-Bees-Hymenoptera--Apidae--Commercial/10.4182/ZSGH5376.2003.21 (accessed 18 December 2023). DOI: https://doi.org/10.4182/ZSGH5376.2003.21

Tillman J, Nair A, Gleason M, Batzer J (2015) Evaluating Strip Tillage and Rowcover Use in Organic and Conventional Muskmelon Production. HortTechnology 25:487–495. DOI: https://doi.org/10.21273/HORTTECH.25.4.487

Toni HC, Djossa ,Bruno Agossou, Ayenan ,Mathieu Anatole Tele, and Teka O (2021) Tomato (Solanum lycopersicum) pollinators and their effect on fruit set and quality. The Journal of Horticultural Science and Biotechnology 96:1–13. DOI: https://doi.org/10.1080/14620316.2020.1773937

Treanore ED, Vaudo AD, Grozinger CM, Fleischer SJ (2019) Examining the nutritional value and effects of different floral resources in pumpkin agroecosystems on Bombus impatiens worker physiology. Apidologie 50:542–552. DOI: https://doi.org/10.1007/s13592-019-00668-x

Vaidya C, Fisher K, Vandermeer J (2018) Colony Development and Reproductive Success of Bumblebees in an Urban Gradient. Sustainability 10:1936. DOI: https://doi.org/10.3390/su10061936

Wei T, Simko V (2024) R package “corrplot”: Visualization of a Correlation Matrix. [online] URL: https://github.com/taiyun/corrplot

Whittington R, Winston ML (2003) Are bumble bee colonies in tomato greenhouses obtaining adequate nutrition? The Canadian Entomologist 135:883–892. DOI: https://doi.org/10.4039/n02-121

Zhao X, Jiang J, Pang Z, Ma W, Jiang Y, Fu Y, Liu Y (2024) Tracking Existing Factors Directly Affecting the Reproduction of Bumblebees: Current Knowledge. Insects 15:654. DOI: https://doi.org/10.3390/insects15090654