Abstract
Landscape structure and local floral resources can modulate bee diversity and ecological interactions in agroecosystems. Theory predicts that, at different spatial scales, both factors may interact and influence assemblage patterns and interactions simultaneously, ultimately affecting the provision of ecosystem services. We investigated how habitat heterogeneity at different spatial scales influenced the assemblage of tomato flower-visiting bees in organic cropped areas in the Cerrado biome, Brazil, from 2019 to 2020. We also evaluated the structure and stability of the interaction network among tomatoes, non-crop plants, and bees. We found that landscape heterogeneity can benefit and serve as a source of bee species when natural vegetation remnants are not highly fragmented in the landscape. Non-crop plants increase the permeability of agroecosystems to bees by providing additional and diverse floral resources. The interaction network between non-crop plants and bees was found to be modular and robust, suggesting spatial habitat partitioning among the bee species. The presence of non-crop plants plays a central role in preventing bee species loss in the cropped areas by locally maintaining the stability of the interaction network.
Implications for insect conservation
Factors operating at multiple spatial scales determine species occurrence in the landscape, but local interactions with non-crop plants dictate habitat permeability to species. Such factors should be considered when designing strategies to make tropical agroecosystems more permeable and functional to bee biodiversity and the pollination services they provide.
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References
Albrecht M, Kleijn D, Williams NM, Tschumi M, Blaauw BR, Bommarco R et al (2020) The effectiveness of flower strips and hedgerows on pest control, pollination services and crop yield: a quantitative synthesis. Ecol Lett 23:1488–1498. https://doi.org/10.1111/ele.13576
Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178. https://doi.org/10.1016/j.envsoft.2010.08.003
Alvarenga AS, Silveira FA, dos Santos Júnior JE, de Novais SMA, Quesada M, de Siqueira NF (2020) Vegetation composition and structure determine wild bee communities in a tropical dry forest. J Insect Conserv 24:487–498. https://doi.org/10.1007/s10841-020-00231-5
Aranda R, Graciolli G (2013) First report of Exomalopsis fulvofasciata (Hymenoptera: Anthophoridae) as host of two Timulla species (Hymenoptera: Mutillidae). Biota Neotrop 13:382–384. https://doi.org/10.1590/S1676-06032013000400033
Argueta-Guzmán M, Golubov J, Cano-Santana Z, Ayala R (2022) The role of seasonality and disturbance in bee-plant interactions in semi-arid communities of the southern Chihuahuan desert. Insect Conserv Divers 1:12. https://doi.org/10.1111/icad.12572
Baaren J, Candolin U (2018) Plasticity in a changing world: behavioural responses to human perturbations. Curr Opin Insect Sci 27:21–25. https://doi.org/10.1016/j.cois.2018.02.003
Benjamin FE, Reilly JR, Winfree R (2014) Pollinator body size mediates the scale at which land use drives crop pollination services. J Appl Ecol 51:440–449. https://doi.org/10.1111/1365-2664.12198
BPBES/REBIP (2019) Relatório temático sobre Polinização, Polinizadores e Produção de Alimentos no Brasil. Editora Cubo, São Carlos, Brazil. http://doi.editoracubo.com.br/https://doi.org/10.4322/978-85-60064-83-0
Bretagnolle V, Gaba S (2015) Weeds for bees? A review. Agron Sustain Dev 35:891–909. https://doi.org/10.1007/s13593-015-0302-5
Brosi BJ, Daily GC, Shih TM, Oviedo F, Durán G (2008) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45:773–783. https://doi.org/10.1111/j.1365-2664.2007.01412.x
Carvalheiro LG, Veldtman R, Shenkute AG, Tesfay GB, Pirk CWW, Donaldson JS, Nicolson SW (2011) Natural and within-farmland biodiversity enhances crop productivity. Ecol Lett 14:251–259. https://doi.org/10.1111/j.1461-0248.2010.01579.x
Carvalho DM, Presley SJ, Santos GMM (2014) Niche overlap and network specialization of flower-visiting bees in an agricultural system. Neotrop Entomol 43:489–499. https://doi.org/10.1007/s13744-014-0239-4
Corcoran D, Ávila-Thieme MI, Valdovinos FS, Navarrete SA, Marquet PA(2019) Network Extinction, v0. 1.1. https://www.rdocumentation.org/packages/NetworkExtinction/versions/0.1.1
Crawley MJ (2012) The R book. John Wiley & Sons, Chichester, UK
Dainese M, Martin EA, Aizen MA, Albrecht M, Bartomeus I, Bommarco R, Steffan-Dewenter I (2019) A global synthesis reveals biodiversity-mediated benefits for crop production. Sci Adv 5:eaax0121. https://doi.org/10.1126/sciadv.aax0121
Dallas T, Cornelius E (2015) Co-extinction in a host-parasite network: identifying key hosts for network stability. Sci Rep 5:1–10. https://doi.org/10.1038/srep13185
Deprá MS, Delaqua G, Carla G, Freitas L, Gaglianone MC (2014) Pollination deficit in open-field tomato crops (Solanum lycopersicum L., Solanaceae) in Rio de Janeiro state, Southeast Brazil. J Pollinat Ecol 12:1–8. https://doi.org/10.26786/1920-7603(2014)7
Diekötter T, Haynes KJ, Mazeffa D, Crist TO (2007) Direct and indirect effects of habitat area and matrix composition on species interactions among flower-visiting insects. Oikos 116:1588–1598. https://doi.org/10.1111/j.0030-1299.2007.15963.x
Dormann CF, Strauss R (2014) A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol 5:90–98. https://doi.org/10.1111/2041-210X.12139
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. Interaction 1:8–11
Dunne JA, Williams RJ (2009) Cascading Extinctions and Community Collapse in Model Food Webs. Philos Trans R Soc B 364:1711–1723. https://doi.org/10.1098/rstb.2008.0219
Escobedo-Kenefic N, Landaverde-González P, Theodorou P, Cardona E, Dardón MJ, Martínez O Domínguez CA (2020) Disentangling the effects of local resources, landscape heterogeneity and climatic seasonality on bee diversity and plant-pollinator networks in tropical highlands. Oecologia 194:333–344. https://doi.org/10.1007/s00442-020-04715-8
Estrada E (2007) Characterization of topological keystone species local, global and “meso-scale” centralities in food webs. Ecol Complex 4:48–57. https://doi.org/10.1016/j.ecocom.2007.02.018
FAO - Food and Agriculture Organization of the United Nations (2021) Food and Agriculture Data. http://www.fao.org/faostat/en/?#data/. Accessed February 2021
Fisher K, Gonthier DJ, Ennis KK, Perfecto I (2017) Floral resource availability from groundcover promotes bee abundance in coffee agroecosystems. Ecol Appl 27:1815–1826. https://doi.org/10.1002/eap.1568
Franceschinelli EV, Elias MA, Bergamini LL, Silva-Neto CM, Sujii ER (2017) Influence of landscape context on the abundance of native bee pollinators in tomato crops in Central Brazil. J Insect Conserv 21:715–726. https://doi.org/10.1007/s10841-017-0015-y
Freeman LC (1979) Centrality in social networks conceptual clarification. Soc Netw 1:215–239. https://doi.org/10.1016/0378-8733(78)90021-7
Gaglianone MC, Campos LAO, Campos MJO, Franceschinelli E, Deprá MS, Silva PN, Montagnana PC, Hautequestt AP, Moraes MCM(2015) Plano de manejo para os polinizadores do tomateiro. Fundo Brasileiro para a Biodiversidade (Funbio), Rio de Janeiro, v.23
Garibaldi LA, Aizen MA, Klein AM, Cunningham SA, Harder LD (2011) Global growth and stability of agricultural yield decrease with pollinator dependence. Proc Natl Acad Sci USA 108:5909–5914. https://doi.org/10.1073/pnas.1012431108
Garibaldi LA, Carvalheiro LG, Leonhardt SD, Aizen MA, Blaauw BR, Isaacs R, Winfree R (2014) From research to action: enhancing crop yield through wild pollinators. Front Ecol Environ 12:439–447. https://doi.org/10.1890/130330
Garibaldi LA, Pérez-Méndez N, Cordeiro GD, Hughes A, Orr M, Alves‐dos‐Santos I, Viana BF (2021) Negative impacts of dominance on bee communities: Does the influence of invasive honey bees differ from native bees? Ecology 102:e03526. https://doi.org/10.1002/ecy.3526
Gaston K (2000) Global patterns in biodiversity. Nature 405:220–227. https://doi.org/10.1038/35012228
Gergel SE, Turner MG (2017) Learning landscape ecology: a practical guide to concepts and techniques. Springer, Berlin
Gibbs J (2017) Notes on the nests of Augochloropsis metallica fulgida and Megachile mucida in central Michigan (Hymenoptera: Halictidae, Megachilidae). Gt Lakes Entomol 50:4
Gibson RH, Nelson IL, Hopkins GW, Hamlett BJ, Memmott J (2006) Pollinator webs, plant communities and the conservation of rare plants: arable weeds as a case study. J Appl Ecol 43:246–257. https://doi.org/10.1111/j.1365-2664.2006.01130.x
González-Chaves A, Jaffé R, Metzger JP, de Kleinert MP A (2020) Forest proximity rather than local forest cover affects bee diversity and coffee pollination services. Landsc Ecol 35:1841–1855. https://doi.org/10.1007/s10980-020-01061-1
Grass I, Jauker B, Steffan-Dewenter I, Tscharntke T, Jauker F (2018) Past and potential future effects of habitat fragmentation on structure and stability of plant-pollinator and host-parasitoid networks. Nat Ecol Evol 2:1408–1417. https://doi.org/10.1038/s41559-018-0631-2
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
Gutiérrez-Chacón C, Valderrama-A C, Klein AM (2020) Biological corridors as important habitat structures for maintaining bees in a tropical fragmented landscape. J Insect Conserv 24:187–197. https://doi.org/10.1007/s10841-019-00205-2
Hadley AS, Betts MG (2012) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev 87:526–544. https://doi.org/10.1111/j.1469-185x.2011.00205.x
Hansen K, Sritongchuay T, Bumrungsri S, Simmons BI, Strange N, Dalsgaard B (2020) Landscape-level effects of forest on pollinators and fruit set of guava (Psidium guajava L.) in orchards across southern Thailand. Diversity 12:259. https://doi.org/10.3390/d12060259
Hass AL, Kormann UG, Tscharntke T, Clough Y, Baillod AB, Sirami C, Batáry P (2018) Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe. Proc R Soc B: Biol Sci 285:20172242. https://doi.org/10.1098/rspb.2017.2242
Hipólito J, Boscolo D, Viana BF (2018) Landscape and crop management strategies to conserve pollination services and increase yields in tropical coffee farms. Agric Ecosyst Environ 256:218–225. https://doi.org/10.1016/j.agee.2017.09.038
Holzschuh A, Steffan-Dewenter I, Tscharntke T (2008) Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 117:354–361. https://doi.org/10.1111/j.2007.0030-1299.16303.x
Hung KLJ, Kingston JM, Lee A, Holway DA, Kohn JR (2019) Non-native honey bees disproportionately dominate the most abundant floral resources in a biodiversity hotspot. Proc R Soc B 286:20182901. https://doi.org/10.1098/rspb.2018.2901
Jauker F, Diekötter T, Schwarzbach F, Wolters V (2009) Pollinator dispersal in an agricultural matrix: opposing responses of wild bees and hoverflies to landscape structure and distance from main habitat. Landsc Ecol 24:547–555. https://doi.org/10.1007/s10980-009-9331-2
Jordán F, Liu W, Davis AD (2006) Topological keystone species: measures of positional importance in food webs. Oikos 112:535–546. https://doi.org/10.1111/j.0030-1299.2006.13724.x
Jung ML (2016) LecoS - A python plugin for automated landscape ecology analysis. Ecol Inf 31:18–21. https://doi.org/10.1016/j.ecoinf.2015.11.006
Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol Lett 13:442–452. https://doi.org/10.1111/j.1461-0248.2009.01437.x
Kaiser-Bunbury CN, Vazquez DP, Stang M, Ghazoul J (2014) Determinants of the microstructure of plant–pollinator networks. Ecology 95:3314–3324. https://doi.org/10.1890/14-0024.1
Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R, Bommarco R et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. https://doi.org/10.1111/ele.12082
Klink CA, Machado RB (2005) Conservation of the Brazilian cerrado. Conserv Biol 19:707–713. https://doi.org/10.1111/j.1523-1739.2005.00702.x
Krebs CJ (1999) Ecological methodology. Addison Wesley Longman Menlo Park, USA
Laha S, Chatterjee S, Das A, Smith B, Basu P (2020) Exploring the importance of floral resources and functional trait compatibility for maintaining bee fauna in tropical agricultural landscapes. J Insect Conserv 24:431–443. https://link.springer.com/article/https://doi.org/10.1007/s10841-020-00225-3
Landaverde-González P, Quezada‐Euán JJG, Theodorou P, Murray TE, Husemann M, Ayala R, Paxton RJ (2017) Sweat bees on hot chillies: Provision of pollination services by native bees in traditional slash‐and‐burn agriculture in the Yucatán Peninsula of tropical Mexico. J Appl Ecol 54:1814–1824. https://doi.org/10.1111/1365-2664.12860
Landaverde-González P, Enríquez E, Núñez-Farfán J (2021) The effect of landscape on Cucurbita pepo-pollinator interaction networks varies depending on plants’ genetic diversity. Arthropod-Plant Interact 15:917–928. https://doi.org/10.1007/s11829-021-09872-y
Lautenbach S, Seppelt R, Liebscher J, Dormann CF (2012) Spatial and temporal trends of global pollination benefit. PLoS ONE 7:e35954. https://doi.org/10.1371/journal.pone.0035954
Lowenstein DM, Matteson KC, Minor ES (2019) Evaluating the dependence of urban pollinators on ornamental, non-native, and ‘weedy’ floral resources. Urban Ecosyst 22:293–302. https://doi.org/10.1007/s11252-018-0817-z
Maccagnani B, Veromann E, Ferrari R, Boriani L, Boecking O (2020) Agroecosystem Design Supports the Activity of Pollinator Networks. In: Smagghe G, Boecking O, Maccagnani B, Mänd M, Kevan P (eds) Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops. Springer, Cham, pp 1–17
Machado ACP, Barônio GJ, de Oliveira FF, Garcia CT, Rech AR (2021) Does a coffee plantation host potential pollinators when it is not flowering? Bee distribution in an agricultural landscape with high biological diversity in the Brazilian Campo Rupestre. J Sci Food Agric 101:2345–2354
MEA – Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: synthesis. Island Press, Washington, DC
Michener CD (2000) The bees of the world. The Johns Hopkins University Press, Baltimore
Montagnana PC, Alves RS, Garófalo CA, Ribeiro MC (2021) Landscape heterogeneity and forest cover shape cavity-nesting hymenopteran communities in a multi-scale perspective. Basic Appl Ecol 56:239–249. https://doi.org/10.1016/j.baae.2021.08.004
Nicholson CC, Koh I, Richardson LL, Beauchemin A, Ricketts TH (2017) Farm and landscape factors interact to affect the supply of pollination services. Agric Ecosyst Environ 250:113–122. https://doi.org/10.1016/j.agee.2017.08.030
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci USA 104:19891–19896. https://doi.org/10.1073/pnas.0706375104
Oliveira-Filho AT, Ratter JA (2002) Vegetation Physiognomies and Woody Flora of the Cerrado Biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil. Columbia University Press, pp 91–120
Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229. https://doi.org/10.1038/nature20588
QGIS Development Team (2020) QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org Accessed February 2021
Quinto J, Marcos-García M, Diaz-Castelazo C, Rico-Gray V, Brustel H, Galante E, Mico E (2012) Breaking down complex saproxylic communities: understanding sub-networks structure and implications to network robustness. PLoS ONE 7:e45062. https://doi.org/10.1371/journal.pone.0045062
R Core Team (2018) R: A Language and Environment for Statistical Computing. Version 3.5.2. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Raderschall CA, Bommarco R, Lindström SA, Lundin O (2021) Landscape crop diversity and semi-natural habitat affect crop pollinators, pollination benefit and yield. Agric Ecosyst Environ 306:107189. https://doi.org/10.1016/j.agee.2020.107189
Raw A (2007) A riqueza de espécies e aspectos zoogeográficos nos cerrados. Brasil. Ministério do Meio Ambiente Secretaria de Biodiversidade e Florestas (ed) Biodiversidade do Cerrado e Pantanal: áreas e ações prioritárias para conservação. Brasília, Brazil, pp 173–189
Renauld M, Hutchinson A, Loeb G, Poveda K, Connelly H (2016) Landscape simplification constrains adult size in a native ground-nesting bee. PLoS ONE 11:e0150946. https://doi.org/10.1371/journal.pone.0150946
Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conserv Biol 18:1262–1271. https://doi.org/10.1111/j.1523-1739.2004.00227.x
Sano EE, Rodrigues AA, Martins ES, Bettiol GM, Bustamante MM, Bezerra AS, Couto AF Jr, Vasconcelos V, Schüler J, Bolfe EL (2019) Cerrado ecoregions: A spatial framework to assess and prioritize Brazilian savanna environmental diversity for conservation. J Environ Manag 232:818–828. https://doi.org/10.1016/j.jenvman.2018.11.108
Saturni FT, Jaffe R, Metzger JP (2016) Landscape structure influences bee community and coffee pollination at different spatial scales. Agric Ecosyst Environ 235:1–12. https://doi.org/10.1016/j.agee.2016.10.008
Saunders ME, Rader R (2019) Network modularity influences plant reproduction in a mosaic tropical agroecosystem. Proc R Soc B 286:20190296. https://doi.org/10.1098/rspb.2019.0296
Sawyer D, Mesquita B, Coutinho B, Almeida FD, Figueiredo I, Lamas I, Pereira LE, Pinto LP, Pires MO, Kasecker T (2018) Ecosystem Profile: Cerrado Biodiversity Hotspot: Full Report. Supernova, Brasília, Brazil
Schleuning M, Fründ J, Klein AM, Abrahamczyk S, Alarcón R, Albrecht M, Blüthgen N (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Curr Biol 22:1925–1931. https://doi.org/10.1016/j.cub.2012.08.015
Silva-Neto CM, Lima FG, Gonçalves BB, Bergamini L, Bergamini BAR, Elias MAS, Franceschinelli EV (2013) Native bees pollinate tomato flowers and increase fruit production. J Pollinat Ecol 11:41–45. https://doi.org/10.26786/1920-7603(2013)4
Silveira FA, Melo GA, Almeida EA (2002) Abelhas brasileiras: sistemática e identificação. Ministério do Meio Ambiente, Fundação Araucária, Belo Horizonte, Brazil
Sonne J, Vizentin-Bugoni J, Maruyama PK, Araujo AC, Chávez-González E, Coelho AG, Dalsgaard B (2020) Ecological mechanisms explaining interactions within plant hummingbird networks: morphological matching increases towards lower latitudes. Proc R Soc B 287:20192873. https://doi.org/10.1098/rspb.2019.2873
Souza C, Maruyama PK, Aoki C, Sigrist MR, Raizer J, Gross CL, Araujo AC (2018) Temporal variation in plant-pollinator networks from seasonal tropical environments: higher specialization when resources are scarce. J Ecol 106:2409–2420. https://doi.org/10.1111/1365-2745.12978
Souza CMZ, Shimbo J, Rosa MR, Oliveira SW (2020) Reconstructing three decades of land use and land cover changes in brazilian biomes with landsat archive and earth engine. Remote Sens 12:2735. https://doi.org/10.3390/rs12172735
Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432. https://doi.org/10.1890/0012-9658(2002)083[1421:SDEOLC]2.0.CO;2
Sutter L, Jeanneret P, Bartual AM, Bocci G, Albrecht M (2017) Enhancing plant diversity in agricultural landscapes promotes both rare bees and dominant crop-pollinating bees through complementary increase in key floral resources. J Appl Ecol 54:1856–1864. https://doi.org/10.1111/1365-2664.12907
Sutter L, Albrecht M, Jeanneret P (2018) Landscape greening and local creation of wildflower strips and hedgerows promote multiple ecosystem services. J Appl Ecol 55:612–620. https://doi.org/10.1111/1365-2664.12977
Togni PHB, Venzon M, Lagôa ACG, Sujii ER (2019a) Brazilian legislation leaning towards fast registration of biological control agents to benefit organic agriculture. Neotrop Entomol 48:175–185. https://doi.org/10.1007/s13744-019-00675-8
Togni PHB, Venzon M, Souza LM, Sousa AATC, Harterreiten-Souza ÉS, Pires CSS, Sujii ER (2019b) Dynamics of predatory and herbivorous insects at the farm scale: the role of cropped and noncropped habitats. Agric For Entomol 21:351–362. https://doi.org/10.1111/afe.12337
Togni PHB, Harterreiten-Souza ÉS, Novaes DR, Sujii ER (2021) Spatial dynamic and spillover of the polyphagous pest Bemisia tabaci is influenced by differences in farmland habitats on tropical organic farms. Agric Ecosyst Environ 320:107610. https://doi.org/10.1016/j.agee.2021.107610
Tonhasca A, Blackmer JL, Albuquerque GS (2002) Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic Forest. Biotropica 34:416–422. https://doi.org/10.1111/j.1744-7429.2002.tb00555.x
Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Westphal C (2012) Landscape moderation of biodiversity patterns and processes-eight hypotheses. Biol Rev 87:661–685. https://doi.org/10.1111/j.1469-185X.2011.00216.x
Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Ann Rev Ecol Evol Syst 48:25–48. https://doi.org/10.1146/annurev-ecolsys-110316-022821
Vergara CH, Badano EI (2009) Pollinator diversity increases fruit production in Mexican coffee plantations: The importance of rustic management systems. Agric Ecosyst Environ 129:117–123. https://doi.org/10.1016/j.agee.2008.08.001
Vizentin-Bugoni J, Maruyama PK, Souza CS, Ollerton J, Rech AR, Sazima M (2018) Plant‐pollinator networks in the tropics: A review. In: Dáttilo W, Rico‐Gray V (eds) Ecological networks in the tropics. Springer, Cham, Netherlands, pp 73–91
Watts S, Dormann CF, Martín González AM, Ollerton J (2016) The influence of floral traits on specialization and modularity of plant–pollinator networks in a biodiversity hotspot in the Peruvian Andes. Ann Bot 118:415–429. https://doi.org/10.1093/aob/mcw114
Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149:289–300. https://doi.org/10.1111/j.0030-1299.2007.15963.x
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. J Appl Ecol 45:793–802. https://doi.org/10.1111/j.1365-2664.2007.01418.x
Wu P, Dai P, Wang M, Feng S, Olhnuud A, Xu H, Liu Y (2021) Improving habitat quality at the local and landscape scales increases wild bee assemblages and associated pollination services in apple orchards in China. Front Ecol Evol 9:67. https://doi.org/10.3389/fevo.2021.621469
Zurbuchen A, Landert L et al (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143:669–676. https://doi.org/10.1016/j.biocon.2009.12.003
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The authors are grateful to all farm owners who kindly allowed us to conduct this study on their lands. We acknowledge EMATER-DF for their support in finding farms for sampling.
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The present study was carried out with support by the ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq) and the ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - PROEX)’ through scholarships and research grants. C.S.S. Pires received financial support from the CNPq / A.B.E.L.H.A. / IBAMA / MCTIC (Process 400555/2018-2) project and Fundação de Apoio a Pesquisa do Distrito Federal (FAPDF) (Process 00193. 0000054/2019-37).
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RMA, PHBT, CSSP, and ERS: conceived and designed the study. RMA, LSS, EMR, and GMT: collected data. RMA and NFC: analyzed the data under the supervision of PHBT. RMA: led the manuscript writing. All authors contributed critically to the first draft and approved the final version of the manuscript.
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Assunção, R.M., Camargo, N.F., Souza, L.S. et al. Landscape conservation and local interactions with non-crop plants aid in structuring bee assemblages in organic tropical agroecosystems. J Insect Conserv 26, 933–945 (2022). https://doi.org/10.1007/s10841-022-00438-8
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DOI: https://doi.org/10.1007/s10841-022-00438-8