Distinct pollinator communities persist among co-flowering specialty crops in Indiana

Authors

DOI:

https://doi.org/10.26786/1920-7603(2024)808

Keywords:

bee communities, pan traps, pollinator diversity, wild bees, pollinator observations

Abstract

Diverse bee communities pollinate fruits and vegetables, and the composition of these communities has been described for many specialty crops in major production regions. However, pollinator communities in landscapes dominated by agronomic crops may differ in species composition and the contribution of wild bees. With over 4 million ha of maize and soybean, Indiana presents a novel landscape to compare pollinator communities among specialty crops that differ in their use of managed bees and bloom phenology, with potential implications for the composition of wild bee communities and their contributions to flower visitation. We sampled pollinator communities with flower observations and pan traps in spring-blooming apples and blueberries and summer-blooming tomatoes and watermelons, allowing us to compare communities between specialty crops with overlapping and distinct bloom times. Apples, blueberries, and watermelons were stocked with honey bees, and watermelons additionally had managed bumble bees. Across two years of sampling, we observed 1,651 flower visits by 13 taxa, collected 1,967 bees, and identified 84 taxa from collected specimens. Apples and blueberries hosted the richest pollinator communities (34 and 51 taxa, respectively) followed by watermelons (22 taxa), and tomatoes (19 taxa). While 70% of flower visits in apples and blueberries were attributed to honey bees, wild bees accounted for 82% and 99% of flower visits in watermelons and tomatoes, respectively. Our results indicate that distinct pollinator communities persist among co-flowering specialty crops in a landscape dominated by maize and soybean production and underscore the contribution of wild bees for specialty crop pollination, particularly in watermelons and tomatoes.

References

Arbizu MP (2017) pairwiseAdonis: Pairwise Multilevel Comparison using Adonis. R package version 0.4.1.

Bloom EH, Wood TJ, Hung K-LJ, Ternest JJ, Ingwell LL, Goodell K, Kaplan I, Szendrei Z (2021) Synergism between local- and landscape-level pesticides reduces wild bee floral visitation in pollinator-dependent crops. Journal of Applied Ecology 58:1187–1198. https://doi.org/10.1111/1365-2664.13871

Boyer KJ, Fragoso FP, Dieterich Mabin ME, Brunet J (2020) Netting and pan traps fail to identify the pollinator guild of an agricultural crop. Scientific Reports 10:13819. https://doi.org/10.1038/s41598-020-70518-9

Calderone NW (2012) Insect pollinated crops, insect pollinators and us agriculture: trend analysis of aggregate data for the period 1992–2009. PLOS ONE 7:e37235. https://doi.org/10.1371/journal.pone.0037235

Campbell JW, Stanley-Stahr C, Bammer M, Daniels JC, Ellis JD (2019) Contribution of bees and other pollinators to watermelon (Citrullus lanatus Thunb.) pollination. Journal of Apicultural Research 58:597–603. https://doi.org/10.1080/00218839.2019.1614271

Carrasco L, Papeş M, Lochner EN, Ruiz BC, Williams AG, Wiggins GJ (2021) Potential regional declines in species richness of tomato pollinators in North America under climate change. Ecological Applications 31 https://doi.org/10.1002/eap.2259

Cooley H, Vallejo-Marín M (2021) Buzz-pollinated crops: a global review and meta-analysis of the effects of supplemental bee pollination in tomato. Journal of economic entomology 114:505–519. https://doi.org/10.1093/jee/toab009

Delaplane KS, Mayer DF (2000) Crop pollination by bees. Crop pollination by bees. [online] URL: https://www.cabdirect.org/cabdirect/abstract/2000070 9824 (accessed 27 March 2023).

Duelli P, Obrist M (2003) Regional biodiversity in an agricultural landscape: The contribution of seminatural habitat islands. Basic and Applied Ecology 4:129–138. https://doi.org/10.1078/1439-1791-00140

Eeraerts M, DeVetter LW, Batáry P, Ternest JJ, Mallinger R, Arrington M, Benjamin FE, Blaauw BR, Campbell JW, Cavigliasso P, Daniels JC, de Groot GA, Ellis JD, Gibbs J, Goldstein L, Hoffman GD, Kleijn D, Melathopoulos A, Miller SZ, Montero-Castaño A, Naranjo SM, Nicholson CC, Perkins JA, Rao S, Raine NE, Reilly JR, Ricketts TH, Rogers E, Isaacs R (2023) Synthesis of highbush blueberry pollination research reveals region-specific differences in the contributions of honeybees and wild bees. Journal of Applied Ecology 60. https://doi.org/10.1111/1365-2664.14516

Eilers EJ, Kremen C, Greenleaf SS, Garber AK, Klein A-M (2011) Contribution of pollinator-mediated crops to nutrients in the human food supply. PLOS ONE 6:e21363. https://doi.org/10.1371/journal.pone.0021363

Garibaldi LA, Sáez A, Aizen MA, Fijen T, Bartomeus I (2020) Crop pollination management needs flower-visitor monitoring and target values. Journal of Applied Ecology 57:664–670. https://doi.org/10.1111/1365-2664.13574

Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhöffer JH, Greenleaf SS, Holzschuh A, Isaacs R, Krewenka K, Mandelik Y, Mayfield MM, Morandin LA, Potts SG, Ricketts TH, Szentgyörgyi H, Viana BF, Westphal C, Winfree R, Klein AM (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters 14:1062–1072. https://doi.org/10.1111/j.1461-0248.2011.01669.x

Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 340:1608–1611. https://doi.org/10.1126/science.1230200

Gibbs J, Elle E, Bobiwash K, Haapalainen T, Isaacs R (2016) Contrasting pollinators and pollination in native and non-native regions of highbush blueberry production. PLoS ONE 11 https://doi.org/10.1371/journal.pone.0158937

Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. https://doi.org/10.1126/science.1255957

Greenleaf SS, Kremen C (2006) Wild bee species increase tomato production and respond differently to surrounding land use in Northern California. Biological Conservation 133:81–87. https://doi.org/10.1016/J.BIOCON.2006.05.025

Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. https://doi.org/10.1007/s00442-007-0752-9

Grundel R, Jean RP, Frohnapple KJ, Gibbs J, Glowacki GA, Pavlovic NB (2011) A Survey of Bees (Hymenoptera: Apoidea) of the Indiana Dunes and Northwest Indiana, USA. Journal of the Kansas Entomological Society 84:105–138. https://doi.org/10.2317/JKES101027.1

Heneberg P, Bogusch P (2014) To enrich or not to enrich? Are there any benefits of using multiple colors of pan traps when sampling aculeate Hymenoptera? Journal of Insect Conservation 18:1123–1136. https://doi.org/10.1007/s10841-014-9723-8

Jean, Robert P. (2010) Studies of Bee Diversity in Indiana: The Influence of Collection Methods on Species Captures, and a State Checklist Based on Museum Collection. Indiana State University

Julier HE, Roulston TH (2009) Wild Bee Abundance and Pollination Service in Cultivated Pumpkins: Farm Management, Nesting Behavior and Landscape Effects. Journal of Economic Entomology 102:563–573. https://doi.org/10.1603/029.102.0214

Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R, Bommarco R, Brittain C, Burley AL, Cariveau D, Carvalheiro LG, Chacoff NP, Cunningham SA, Danforth BN, Dudenhöffer J, Elle E, Gaines HR, Garibaldi LA, Gratton C, Holzschuh A, Isaacs R, Javorek SK, Jha S, Klein AM, Krewenka K, Mandelik Y, Mayfield MM, Morandin L, Neame LA, Otieno M, Park M, Potts SG, Rundlöf M, Saez A, Steffan‐Dewenter I, Taki H, Viana BF, Westphal C, Wilson JK, Greenleaf SS, Kremen C (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems Anderson M (ed). Ecology Letters 16:584–599. https://doi.org/10.1111/ele.12082

King MJ, Buchmann SL (2003) Floral sonication by bees: mesosomal vibration by Bombus and Xylocopa, but not Apis (Hymenoptera: Apidae), ejects pollen from poricidal anthers. Journal of the Kansas Entomological Society 76:295–305.

Klein A-M, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2006) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274:303–313. https://doi.org/10.1098/rspb.2006.3721

Kline O, Phan NT, Porras MF, Chavana J, Little CZ, Stemet L, Acharya RS, Biddinger DJ, Reddy GVP, Rajotte EG, Joshi NK (2023) Biology, genetic diversity, and conservation of wild bees in tree fruit orchards. Biology 12:31. https://doi.org/10.3390/biology12010031

Kratschmer S, Pachinger B, Schwantzer M, Paredes D, Guernion M, Burel F, Nicolai A, Strauss P, Bauer T, Kriechbaum M, Zaller JG, Winter S (2018) Tillage intensity or landscape features: What matters most for wild bee diversity in vineyards? Agriculture, Ecosystems & Environment 266:142–152. https://doi.org/10.1016/j.agee.2018.07.018

Lázaro A, Nielsen A, Totland Ø (2010) Factors related to the inter-annual variation in plants’ pollination generalization levels within a community. Oikos 119:825–834. https://doi.org/10.1111/j.1600-0706.2009.18017.x

Leach A, Kaplan I (2022) Prioritizing pollinators over pests: wild bees are more important than beetle damage for watermelon yield. Proceedings of the Royal Society B: Biological Sciences 289:20221279. https://doi.org/10.1098/rspb.2022.1279

Leach A, Pecenka J, Kaplan I (2022) Does IPPM bear fruit? Evaluating reduced-risk insecticide programmes on pests, pollinators and marketable yield. Journal of Applied Ecology 59:2993–3002. https://doi.org/10.1111/1365-2664.14294

Lundin O, Rundlöf M, Jonsson M, Bommarco R, Williams NM (2021) Integrated pest and pollinator management – expanding the concept. Frontiers in Ecology and the Environment 19:283–291. https://doi.org/10.1002/fee.2325

Main AR, Webb EB, Goyne KW, Mengel D (2019) Field-level characteristics influence wild bee functional guilds on public lands managed for conservation. Global Ecology and Conservation 17:e00598. https://doi.org/10.1016/j.gecco.2019.e00598

Mallinger R, Ternest JJ, Naranjo SM (2021) Blueberry Yields Increase With Bee Visitation Rates, but Bee Visitation Rates are not Consistently Predicted by Colony Stocking Densities Strange J (ed). Journal of Economic Entomology 114:1441–1451. https://doi.org/10.1093/jee/toab111

Millard J, Outhwaite CL, Kinnersley R, Freeman R, Gregory RD, Adedoja O, Gavini S, Kioko E, Kuhlmann M, Ollerton J, Ren Z-X, Newbold T (2021) Global effects of land-use intensity on local pollinator biodiversity. Nature Communications 12:2902. https://doi.org/10.1038/s41467-021-23228-3

NASS (2017) 2017 Census of Agriculture. [online] URL: www.nass.usda.gov/AgCensus

Nooten SS, Odanaka K, Rehan SM (2020) Characterization of wild bee communities in apple and blueberry orchards. Agricultural and Forest Entomology 22:157–168. https://doi.org/10.1111/afe.12370

Ogilvie JE, Forrest JR (2017) Interactions between bee foraging and floral resource phenology shape bee populations and communities. Current Opinion in Insect Science 21:75–82. https://doi.org/10.1016/j.cois.2017.05.015

Ogilvie JE, Griffin SR, Gezon ZJ, Inouye BD, Underwood N, Inouye DW, Irwin RE (2017) Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology. Ecology Letters 20:1507–1515. https://doi.org/10.1111/ele.12854

Page ML, Nicholson CC, Brennan RM, Britzman AT, Greer J, Hemberger J, Kahl H, Müller U, Peng Y, Rosenberger NM, Stuligross C, Wang L, Yang LH, Williams NM (2021) A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors. American Journal of Botany 108:2196–2207. https://doi.org/10.1002/ajb2.1764

Pecenka JR, Ingwell LL, Foster RE, Krupke CH, Kaplan I (2021) IPM reduces insecticide applications by 95% while maintaining or enhancing crop yields through wild pollinator conservation. PNAS 118 https://doi.org/10.1073/pnas.2108429118

Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007

Prendergast KS, Menz M, Dixon KW, Bateman PW (2020) The relative performance of sampling methods for native bees: an empirical test and review of the literature. Ecosphere 11. https://doi.org/10.1002/ecs2.3076

Rader R, Bartomeus I, Garibaldi LA, Garratt MPD, Howlett BG, Winfree R, Cunningham SA, Mayfield MM, Arthur AD, Andersson GKS, Bommarco R, Brittain C, Carvalheiro LG, Chacoff NP, Entling MH, Foully B, Freitas BM, Gemmill-Herren B, Ghazoul J, Griffin SR, Gross CL, Herbertsson L, Herzog F, Hipólito J, Jaggar S, Jauker F, Klein AM, Kleijn D, Krishnan S, Lemos CQ, Lindström SAM, Mandelik Y, Monteiro VM, Nelson W, Nilsson L, Pattemore DE, Pereira NDO, Pisanty G, Potts SG, Reemer M, Rundlöf M, Sheffield CS, Scheper J, Schüepp C, Smith HG, Stanley DA, Stout JC, Szentgyörgyi H, Taki H, Vergara CH, Viana BF, Woyciechowski M (2016) Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Sciences of the United States of America 113:146–151. https://doi.org/10.1073/pnas.1517092112

Reilly JR, Artz DR, Biddinger D, Bobiwash K, Boyle NK, Brittain C, Brokaw J, Campbell JW, Daniels J, Elle E, Ellis JD, Fleischer SJ, Gibbs J, Gillespie RL, Gundersen KB, Gut L, Hoffman G, Joshi N, Lundin O, Mason K, McGrady CM, Peterson SS, Pitts-Singer TL, Rao S, Rothwell N, Rowe L, Ward KL, Williams NM, Wilson JK, Isaacs R, Winfree R (2020) Crop production in the USA is frequently limited by a lack of pollinators. Proceedings of the Royal Society B: Biological Sciences 287:20200922. https://doi.org/10.1098/rspb.2020.0922

Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng’ A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecology Letters 11:499–515. https://doi.org/10.1111/j.1461-0248.2008.01157.x

Roulston TH, Smith SA, Brewster AL (2007) A Comparison of Pan Trap and Intensive Net Sampling Techniques for Documenting a Bee (Hymenoptera: Apiformes) Fauna. Journal of the Kansas Entomological Society 80:179–181. https://doi.org/10.2317/0022-8567(2007)80[179:ACOPTA]2.0.CO;2

St. Clair AL, Zhang G, Dolezal AG, O’Neal ME, Toth AL (2020) Diversified Farming in a Monoculture Landscape: Effects on Honey Bee Health and Wild Bee Communities. Environmental Entomology 49:753–764. https://doi.org/10.1093/ee/nvaa031

Toni HC, Djossa BA, Ayenan MAT, Teka O (2020) Tomato (Solanum lycopersicum) pollinators and their effect on fruit set and quality. Journal of Horticultural Science and Biotechnology:1–13. https://doi.org/10.1080/14620316.2020.1773937

Tschanz P, Vogel S, Walter A, Keller T, Albrecht M (2023) Nesting of ground-nesting bees in arable fields is not associated with tillage system per se, but with distance to field edge, crop cover, soil and landscape context. Journal of Applied Ecology 60:158–169. https://doi.org/10.1111/1365-2664.14317

Tuell JK, Ascher JS, Isaacs R (2009) Wild bees (Hymenoptera: Apoidea: Anthophila) of the Michigan highbush blueberry agroecosystem. Annals of the Entomological Society of America 102:275–287. https://doi.org/10.1603/008.102.0209

Ullmann KS, Meisner MH, Williams NM (2016) Impact of tillage on the crop pollinating, ground-nesting bee, Peponapis pruinosa in California. Agriculture, Ecosystems & Environment 232:240–246. https://doi.org/10.1016/j.agee.2016.08.002

Vaissière BE, Freitas BM, Gemmill-Herren B (2011) Protocol to detect and assess pollination deficits in crops. FAO, Rome

Watson JC, Wolf AT, Ascher JS (2011) Forested landscapes promote richness and abundance of native bees (Hymenoptera: Apoidea: Anthophila) in Wisconsin apple orchards. Environmental Entomology 40:621–632. https://doi.org/10.1603/EN10231

Williams N, Minckley R, Silveira F (2001) Variation in Native Bee Faunas and its Implications for Detecting Community Changes. Conservation Ecology 5. https://doi.org/10.5751/ES-00259-050107

Winfree R, Williams NM, Gaines H, Ascher JS, Kremen C (2008) Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. Journal of Applied Ecology 45:793–802. https://doi.org/10.1111/j.1365-2664.2007.01418.x

Published

2024-10-20

How to Cite

Eleanor Stroh, Ashley Leach, Zeus Mateos-Fierro, & Ian Kaplan. (2024). Distinct pollinator communities persist among co-flowering specialty crops in Indiana. Journal of Pollination Ecology, 36, 269–283. https://doi.org/10.26786/1920-7603(2024)808

Issue

Section

Early View

Similar Articles

1 2 3 4 5 6 7 8 9 10 > >> 

You may also start an advanced similarity search for this article.