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A mechanistic framework for studying indirect effects of large vertebrate herbivores on pollinators

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Abstract

Globally, large herbivores (e.g., cattle, elk) graze over 2.6 billion hectares of land. These lands can also be used to conserve pollinators that rely on similar resources, specifically diverse plant communities. Pollinator conservation will benefit from management in lands that are used for livestock grazing and wildlife conservation. However, maximizing ecosystem services provided in these areas is often nuanced and difficult. To improve our ability to support multiple ecosystem services in grazing lands, we reviewed published literature to investigate the mechanisms of indirect effects of large herbivores on pollinators via their resources (food plants, nesting sites). We used a framework from previous research on indirect effects of insect herbivores to explore and interpret how plant responses mediate large herbivore effects on pollinators through three mechanistic categories: resource abundance and availability, plant appearance, and plant chemistry. Using the broader conceptual model, we conducted a targeted literature review that found ~ 95% of studies investigating pollinators and large herbivores focused on resource abundance and availability. Consequently, more research is necessary to understand how large herbivores impact pollinators through multiple mechanisms. Future research could also test responses with both large herbivores and insect herbivores to determine their combined ecological consequences. This research will provide insights for managing large herbivores and pollinators simultaneously, while connecting concepts of pollinator ecology and grazing ecology. Filling research gaps on the mechanisms of indirect effects of large herbivores on pollinators will ultimately improve management of multiple ecosystem services and our ability to conserve declining pollinator species.

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References

  • Adler LS (2000) Alkaloid uptake increases fitness in a hemiparasitic plant via reduced herbivory and increased pollination. Am Nat 156:92–99

    Article  PubMed  Google Scholar 

  • Adler LS, Karban R, Strauss SY (2001) Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecol 82:2032–2044

    Article  Google Scholar 

  • Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  • Bailey DW, Mosley J, Estell RE, Cibils AF, Horney M, Hendrickson JR, Walker JW, Launchbaugh KL, Burritt EA (2019) Synthesis paper: targeted livestock grazing: prescription for healthy rangelands. Rangel Ecol Manag 72:865–877

    Article  Google Scholar 

  • Batáry P, Baldi A, Saropataki M, Kohler F, Verhulst J, Knop E, Herzog F, Kleijn D (2010) Effect of conservation management on bees and insect-pollinated grassland plant communities in three European countries. Agric Ecosyst Environ 136:35–39

    Article  Google Scholar 

  • Black SH, Shepherd M, Vaughan M (2011) Rangeland management for pollinators. Rangelands 33:9–13. https://doi.org/10.2111/1551-501X-33.3.9

    Article  Google Scholar 

  • Branson DH, Haferkamp MA (2014) Insect herbivory and vertebrate grazing impact food limitation and grasshopper populations during a severe outbreak. Ecol Entomol 39:371–381

    Article  Google Scholar 

  • Briske DD (1996) Strategies of plant survival in grazed systems: a functional interpretation. In: Hodgson J, Illius AW (eds) The ecology and management of grazing systems. CAB International, pp 37–67

    Google Scholar 

  • Brody AK, Irwin RE (2012) When resources don’t rescue: flowering phenology and species interactions affect compensation to herbivory in Ipomopsis aggregata. Oikos 121:1424–1434

    Article  Google Scholar 

  • Bruinsma M, Lucas-Barbosa D, ten Broeke CJM, van Dam NM, van Beek TA, Dicke M, van Loon JJA (2014) Folivory affects composition of nectar, floral odor and modifies pollinator behavior. J Chem Ecol 40:39–49

    Article  CAS  PubMed  Google Scholar 

  • Buckles BJ, Harmon-Threatt AN (2019) Bee diversity in tallgrass prairies affected by management and its effects on above- and below-ground resources. J Appl Ecol 56:2443–2453

    Article  Google Scholar 

  • Bultman TL, McNeill MR, Krueger K, De Nicolo G, Popay AJ, Hume DE, Mace WJ, Fletcher LR, Koh YM, Sullivan TJ (2018) Complex interactions among sheep, insects, grass, and fungi in a simple New Zealand grazing system. J Chem Ecol 44:957–964

    Article  CAS  PubMed  Google Scholar 

  • Burkle LA, Irwin RE (2009) The effects of nutrient addition on floral characters and pollination in two subalpine plants, Ipomopsis aggregata and Linum lewisii. Plant Ecol 203:83–98

    Article  Google Scholar 

  • Burkle LA, Irwin RE (2010) Beyond biomass: measuring the effects of community-level nitrogen enrichment on floral traits, pollinator visitation and plant reproduction. J Ecol 98:705–717

    Article  Google Scholar 

  • Cardel Y (2004) Linking herbivory and pollination: costs and selection implications in Centrosema virginianum Bentham (Fabaceae: Papilionoideae). MS Thesis, Florida International University, USA. Institutional Repository.

  • Carvell C (2002) Habitat use and conservation of bumblebees (Bombus spp.) under different grassland management regimes. Biol Conserv 103:33–49

    Article  Google Scholar 

  • Chi K, Molano-Flores B (2015) Degradation of habitat disrupts plant-pollinator interactions for a rare self-compatible plant. Plant Ecol 216:1275–1283

    Article  Google Scholar 

  • Cole LJ, Brocklehurst S, Robertson D, Harrison W, McCracken DI (2017) Exploring the interactions between resource availability and the utilisation of semi-natural habitats by insect pollinators in an intensive agricultural landscape. Agric Ecosyst Environ 246:157–167

    Article  Google Scholar 

  • Coughenour MB (1985) Graminoid responses to grazing by large herbivores: adaptations, exaptations, and interacting processes. Ann Missouri Bot Gar 72:852–863

    Article  Google Scholar 

  • Cozzolino S, Fineschi S, Litto M, Scopece G, Trunschke J, Schiestl FP (2015) Herbivory increases fruit set in Silene latifolia: a consequence of induced pollinator-attracting floral volatiles? J Chem Ecol 41:622–630

    Article  CAS  PubMed  Google Scholar 

  • Cutter J, Geaumont B, McGranahan D, Harmon J, Limb R, Schauer C, Hovick T (2021) Cattle and sheep differentially alter floral resources and the native bee communities in working landscapes. Ecol Appl 31:e02406. https://doi.org/10.1002/eap.2406

    Article  PubMed  Google Scholar 

  • Davidson KE, Fowler MS, Skov MW, Forman D, Alison J, Botham M, Beaumont N, Griffin JN (2020) Grazing reduces bee abundance and diversity in saltmarshes by suppressing flowering of key plant species. Agric Ecosyst Environ 291:106760. https://doi.org/10.1016/j.agee.2019.106760

    Article  Google Scholar 

  • de Paz M, Raffaele E (2013) Cattle change plant reproductive phenology, promoting community changes in a post-fire Nothofagus forest in northern Patagonia, Argentina. J Plant Ecol 6:459–467

    Article  Google Scholar 

  • DeBano SJ, Roof SM, Rowland MM, Smith LA (2016) Diet overlap of mammalian herbivores and native bees: implications for managing co-occurring grazers and pollinators. Nat Areas J 36:458–477

    Article  Google Scholar 

  • Ehrlén J, Kack S, Agren J (2002) Pollen limitation, seed predation and scape length in Primula farinosa. Oikos 97:45–51

    Article  Google Scholar 

  • Enkhtur K, Pfeiffer M, Lkhagva A, Boldgiv B (2017) Response of moths (Lepidoptera: Heterocera) to livestock grazing in Mongolian rangelands. Ecol Indic 72:667–674

    Article  Google Scholar 

  • Filazzola A, Brown C, Dettlaff MA, Batbaatar A, Grenke J, Bao T, Heida IP, Cahill JF (2020) The effects of livestock grazing on biodiversity are multi-trophic: a meta-analysis. Ecol Lett 23:1298–1309

    Article  PubMed  Google Scholar 

  • Fisher KE, Hellmich RL, Bradbury SP (2020) Estimates of common milkweed (Asclepias syriaca) utilization by monarch larvae (Danaus plexippus) and the significance of larval movement. J Insect Conserv 24:297–307

    Article  Google Scholar 

  • Gámez-Virués S, Perovic DJ, Gossner MM, Borsching C, Bluthgen N, de Jong H, Simons NK, Klein AM, Krauss J, Maier G, Scherber C, Steckel J, Rothenwohrer C, Steffan-Dewenter I, Weiner CN, Weisser W, Werner M, Tscharntke T, Westphal C (2015) Landscape simplification filters species traits and drives biotic homogenization. Nat Commun 6:8568

    Article  PubMed  Google Scholar 

  • Gegear RJ, Manson JS, Thomson JD (2007) Ecological context influences pollinator deterrence by alkaloids in floral nectar. Ecol Lett 10:375–382

    Article  PubMed  Google Scholar 

  • Haas SM, Lortie CJ (2020) A systematic review of the direct and indirect effects of herbivory on plant reproduction mediated by pollination. PeerJ 8:e9049

    Article  PubMed  PubMed Central  Google Scholar 

  • Hallett LM, Stein C, Suding KN (2017) Functional diversity increases ecological stability in a grazed grassland. Oecologia 183:831–840

    Article  PubMed  Google Scholar 

  • Hanberry BB, DeBano SJ, Kaye TN, Rowland MM, Hartway CR, Shorrock D (2020) Pollinators of the great plains: disturbances, stressors, management, and research needs. Rangel Ecol Manag 78:220–234. https://doi.org/10.1016/j.rama.2020.08.006

    Article  Google Scholar 

  • Hatfield RG, LeBuhn G (2007) Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera:Apidae), in montane meadows. Biol Conserv 139:150–158

    Article  Google Scholar 

  • Henderson BB, Gerber PJ, Hilinski TE, Falcucci A, Ojima DS, Salvatore M, Conant RT (2015) Greenhouse gas mitigation potential of the world’s grazing lands: modeling soil carbon and nitrogen fluxes of mitigation practices. Agric Ecosyst Environ 207:91–100

    Article  CAS  Google Scholar 

  • Hendrickson J, Olson B (2006) Understanding plant response to grazing. In: Launchbaugh K (ed) Targeted grazing: a natural approach to vegetation management and landscape enhancement. Vancouver, pp 32–39.

  • Hopfenmüller S, Holzschuh A, Steffan-Dewenter I (2020) Effects of grazing intensity, habitat area and connectivity on snail-shell nesting bees. Biol Conserv 242:108406. https://doi.org/10.1016/j.biocon.2020.108406

    Article  Google Scholar 

  • Irwin RE, Cook D, Richardson LL, Manson JS, Gardner DR (2014) Secondary compounds in floral rewards of toxic rangeland plants: impacts on pollinators. J Agric Food Chem 62:7335–7344

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen DJ, Raguso RA (2018) Lingering effects of herbivory and plant defenses on pollinators. Curr Biol 28:R1164–R1169

    Article  CAS  PubMed  Google Scholar 

  • Jamieson MA, Burkle LA, Manson JS, Runyon JB, Trowbridge AM, Zientek J (2017) Global change effects on plant-insect interactions: the role of phytochemistry. Curr Opin Insect Sci 23:70–80

    Article  PubMed  Google Scholar 

  • Johansson V, Kindvall O, Askling J, Franzen M (2019) Intense grazing of calcareous grasslands has negative consequences for the threatened marsh fritillary butterfly. Biol Conserv 239:108280. https://doi.org/10.1016/j.biocon.2019.108280

    Article  Google Scholar 

  • Joubert-van der Merwe L, Pryke JS, Samways MJ (2019) Well-managed grassland heterogeneity promotes butterfly conservation in a corridor network. J Environ Manag 238:382–395

    Article  CAS  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Kessler A, Halitschke R (2009) Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Funct Ecol 23:901–912

    Article  Google Scholar 

  • Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecol 92:1769–1780

    Article  Google Scholar 

  • Kimoto C, DeBano SJ, Thorp RW, Taylor RV, Schmalz H, DelCurto T, Johnson T, Kennedy PL, Rao S (2012) Short-term responses of native bees to livestock and implications for managing ecosystem services in grasslands. Ecosphere 3:1–19. https://doi.org/10.1890/ES12-00118.1

    Article  Google Scholar 

  • Koutsoukis C, Akrida-Demertzi K, Demertzis PG, Roukos C, Voidarou C, Kandrelis S (2016) The variation of crude protein and total fat of the main grassland plants, in various stages of growth, in “Kostilata” subalpine grassland in Theodoriana, Arta, Greece. Ekin J Crop Breed Genet 2:69–75

    Google Scholar 

  • Kral KC, Limb RF, Harmon JP, Hovick TJ (2017) Arthropods and fire: Previous research shaping future conservation. Rangel Ecol Manag 70:589–598

    Article  Google Scholar 

  • Kral KC, Hovick TJ, Limb RF, Harmon JP (2018) Multi-scale considerations for grassland butterfly conservation in agroecosystems. Biol Conserv 226:196–204

    Article  Google Scholar 

  • Kral-O’Brien KC, Limb RF, Hovick TJ, Harmon JP (2019) Compositional shifts in forb and butterfly communities associated with Kentucky bluegrass invasions. Rangel Ecol Manag 72:301–309

    Article  Google Scholar 

  • Lázaro A, Tscheulin T, Devalez J, Nakas G, Stefanaki A, Hanlidou E, Petanidou T (2016) Moderation is best: effects of grazing intensity on plant-flower visitor networks in Mediterranean communities. Ecol Appl 26:796–807

    Article  PubMed  Google Scholar 

  • Lev-Yadun S, Ne’eman G (2012) Does bee or wasp mimicry by orchid flowers also deter herbivores? Arthropod-Plant Interact 6:327–332

    Article  Google Scholar 

  • Lockwood JA, Schell SP (1995) Outbreak dynamics of rangeland grasshoppers (Orthoptera: Acrididae) in the western Plains ecoregion: eruptive, gradient, both, or neither? J Orth Res 4:35–48

    Article  Google Scholar 

  • Lucas-Barbosa D, van Loon JJA, Dicke M (2011) The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647–1654

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Coppock DL (2012) Perceptions of Utah ranchers toward carbon sequestration: policy implications for US rangelands. J Environ Manag 111:78–86

    Article  Google Scholar 

  • Manson JS, Thomson JD (2009) Post-ingestive effects of nectar alkaloids depend on dominance status of bumblebees. Ecol Entomol 34:421–426

    Article  Google Scholar 

  • Manson JS, Cook D, Gardner DR, Irwin RE (2013) Dose-dependent effects of nectar alkaloids in a montane plant-pollinator community. J Ecol 101:1604–1612

    Article  CAS  Google Scholar 

  • Massey FP, Hartley SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Ani Ecol 78:281–291

    Article  Google Scholar 

  • Massey FP, Ennos AR, Hartley SE (2007) Herbivore specific induction of silica-based plant defences. Oecologia 152:677–683

    Article  PubMed  Google Scholar 

  • McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365

    Article  PubMed  Google Scholar 

  • Meindl GA, Bain DJ, Ashman TL (2013) Edaphic factors and plant-insect interactions: direct and indirect effects of serpentine soil on florivores and pollinators. Oecologia 173:1355–1366

    Article  PubMed  Google Scholar 

  • Mitchell SR, DeBano SJ, Rowland MM, Burrows S (2021) Feed the bees and shade the streams: riparian shrubs planted for restoration provide forage for native bees. Restor Ecol 30:e13525. https://doi.org/10.1111/rec.13525

    Article  Google Scholar 

  • Moranz RA, Fuhlendorf SD, Engle DM (2014) Making sense of a prairie butterfly paradox: the effects of grazing, time since fire, and sampling period on regal fritillary abundance. Biol Conserv 173:32–41

    Article  Google Scholar 

  • Moreira X, Castagneyrol B, Abdala-Roberts L, Traveset A (2019) A meta-analysis of herbivore effects on plant attractiveness to pollinators. Ecology 100:e02707

    Article  PubMed  Google Scholar 

  • Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecol 81:30–40

    Google Scholar 

  • Nolte S, Esselink P, Bakker JP (2013) Flower production of Aster tripolium is affected by behavioral differences in livestock species and stocking densities: the role of activity and selectivity. Ecol Res 28:821–831

    Article  Google Scholar 

  • Nyoka SE (2010) Can restoration management improve habitat for insect pollinators in ponderosa pine forests of the American southwest? Ecol Res 28:280–290

    Article  Google Scholar 

  • Öckinger E, Smith HG (2007) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59

    Article  Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: Herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105

    Article  Google Scholar 

  • Olson BE, Wallander RT, Fay PK (1997) Intensive cattle grazing of oxeye daisy (Chrysanthemum leucanthemum). Weed Technol 11:176–181

    Article  Google Scholar 

  • Porensky LM, Augstine DJ, Derner JD, Wilmer H, Lipke MN, Fernández-Giménez ME, Briske DD, CARM Stakeholder Group (2021) Collaborative adaptive rangeland management, multipaddock rotational grazing, and the story of the regrazed grass plant. Rangeland Ecol Manage 78:127–141

    Article  Google Scholar 

  • Potts SG, Vulliamy B, Dafni A, Ne’eman G, O’Toole C, Roberts S, Willmer P (2003) Response of plant-pollinator communities to fire: changes in diversity, abundance and floral reward structure. Oikos 101:103–112

    Article  Google Scholar 

  • Roininen H, Price PW, Bryant JP (1997) Response of galling insects to natural browsing by mammals in Alaska. Oikos 80:481–486

    Article  Google Scholar 

  • Rusman Q, Poelman EH, Nowrin F, Polder G, Lucas-Barbosa D (2019) Floral plasticity: herbivore-species-specific-induced changes in flower traits with contrasting effects on pollinator visitation. Plant Cell Environ 42:1882–1896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schtickzelle N, Turlure C, Baguette M (2007) Grazing management impacts on the viability of the threatened bog fritillary butterfly Proclossiana eunomia. Biol Conserv 136:651–660

    Article  Google Scholar 

  • Searle KR, Shipley LA (2008) The comparative feeding behaviour of large browsing and grazing herbivores. In: Herbert HT, Gordon IJ (eds) The ecology of browsing and grazing. Springer, pp 117–148

    Chapter  Google Scholar 

  • Senapathi D, Biesmeijer JC, Breeze TD, Kleijn D, Potts SG, Carvalheiro LG (2015) Pollinator conservation - the difference between managing for pollination services and preserving pollinator diversity. Curr Opin Insect Sci 12:93–101

    Article  Google Scholar 

  • Shapira T, Henkin Z, Dag A, Mandelik Y (2020) Rangeland sharing by cattle and bees: moderate grazing does not impair bee communities and resource availability. Ecol Appl 30:e02066

    Article  PubMed  Google Scholar 

  • Sjödin NE, Bengtsson J, Ekbom B (2008) The influence of grazing intensity and landscape composition on the diversity and abundance of flower-visiting insects. J Appl Ecol 45:763–772

    Article  Google Scholar 

  • Smallidge PJ, Leopold DJ (1997) Vegetation management for the maintenance and conservation of butterfly habitats in temperate human-dominated landscapes. Landsc Urban Plan 38:259–280

    Article  Google Scholar 

  • Sobhy IS, Miyake A, Shinya T, Galis I (2017) Oral secretions affect HIPVs induced by generalist (Mythimna loreyi) and specialist (Parnara guttata) herbivores in rice. J Chem Ecol 43:929–943

    Article  CAS  PubMed  Google Scholar 

  • Solga MJ, Harmon JP, Ganguli AC (2014) Timing is everything: an overview of phenological changes to plants and their pollinators. Nat Areas J 34:227–234

    Article  Google Scholar 

  • Stevenson PC, Nicolson SW, Wright GA (2017) Plant secondary metabolites in nectar: impacts on pollinators and ecological functions. Funct Ecol 31:65–75

    Article  Google Scholar 

  • Strauss SY, Conner JK, Rush SL (1996) Foliar herbivory affects floral characters and plant attractiveness to pollinators: Implications for male and female plant fitness. Am Nat 147:1098–1107

    Article  Google Scholar 

  • Swengel AB (2001) A literature review of insect responses to fire, compared to other conservation managements of open habitat. Biodivers Conserv 10:1141–1169

    Article  Google Scholar 

  • Tadey M (2015) Indirect effects of grazing intensity on pollinators and floral visitation. Ecol Entomol 40:451–460

    Article  Google Scholar 

  • Thapa-Magar KB, Davis TS, Kondratieff B (2020) Livestock grazing is associated with seasonal reduction in pollinator biodiversity and functional dispersion but cheatgrass invasion is not: variation in bee assemblages in a multi-use shortgrass prairie. PLoS ONE 15:e0237484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomann M, Ehrlen J, Agren J (2018) Grazers affect selection on inflorescence height both directly and indirectly and effects change over time. Ecol 99:2167–2175

    Article  Google Scholar 

  • van Noordwijk CGE, Flierman DE, Remke E, WallisDeVries MF, Berg MP (2012) Impact of grazing management on hibernating caterpillars of the butterfly Melitaea cinxia in calcareous grasslands. J Insect Conserv 16:909–920

    Article  Google Scholar 

  • Vanbergen AJ, Baude M, Biesmeijer JC, Britton NF, Brown MJF, Brown M, Bryden J, Budge GE, Bull JC, Carvell C, Challinor AJ, Connolly CN, Evans DJ, Feil EJ, Garratt MP, Greco MK, Heard MS, Jansen VAA, Keeling MJ, Kunis WE, Marris GC, Memmott J, Murray JT, Nicolson SW, Osborne JL, Paxton RJ, Pirk CWW, Polce C, Potts SG, Priest NK, Raine NE, Roberts S, Ryabov EV, Shafir S, Shirley MDF, Simpson SJ, Stevenson PC, Stone GN, Termansen M, Wright GA, Insect Pollinators I (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259

    Article  Google Scholar 

  • Vázquez DP, Simberloff D (2004) Indirect effects of an introduced ungulate on pollination and plant reproduction. Ecol Monogr 74:281–308

    Article  Google Scholar 

  • Vulliamy B, Potts SG, Willmer PG (2006) The effects of cattle grazing on plant-pollinator communities in a fragmented Mediterranean landscape. Oikos 114:529–543

    Article  Google Scholar 

  • Welti EAR, Joern A (2018) Fire and grazing modulate the structure and resistance of plant-floral visitor networks in a tallgrass prairie. Oecologia 186:517–528

    Article  PubMed  Google Scholar 

  • Wheatall L, Nuttle T, Yerger E (2013) Indirect effects of pandemic deer overabundance inferred from caterpillar-host relations. Conserv Biol 27:1107–1116

    Article  PubMed  Google Scholar 

  • Wilkerson ML, Roche LM, Young TP (2013) Indirect effects of domestic and wild herbivores on butterflies in an African savanna. Ecol Evol 3:3672–3682

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshihara Y, Chimeddorj B, Buuueibaatar B, Lhaquasuren B, Takatsuki S (2008) Effects of livestock grazing on pollination on a steppe in eastern Mongolia. Biol Conserv 141:2376–2386

    Article  Google Scholar 

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Funding

This work was supported by the North Dakota State University Agricultural Experiment Station.

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  1. School of Natural Resource Sciences, North Dakota State University, Fargo, ND, USA

    Katherine C. Kral-O’Brien, Bethany Roberton, Torre J. Hovick & Jason P. Harmon

  2. New Mexico State University, Las Cruces, NM, USA

    Cameron A. Duquette

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  1. Katherine C. Kral-O’Brien
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  2. Bethany Roberton
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  3. Cameron A. Duquette
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The literature search and first draft of the manuscript was written by KK-O’B. The conceptualization of the manuscript was developed by JH. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Katherine C. Kral-O’Brien.

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Kral-O’Brien, K.C., Roberton, B., Duquette, C.A. et al. A mechanistic framework for studying indirect effects of large vertebrate herbivores on pollinators. Arthropod-Plant Interactions 17, 263–274 (2023). https://doi.org/10.1007/s11829-023-09964-x

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