[en] The availability of pollen in urban-rural landscapes is an essential factor that influences the population dynamics of insect pollinators. The amount and diversity of pollen play a pivotal role in the foraging ecology of pollinators for their growth and health, but investigations on the spatio-temporal patterns of foraged plants remain rare, especially in cities as neo - ecosystems. Here, we explored the temporal foraging habits of a highly pollinator (Apis mellifera L.) in Tokyo, including different landscape classes from rural to urban areas. Mixed-pollen samples in each month and each location (N = 17) were analysed using DNA meta-barcoding to identify plants visited by honeybees. The results showed that the landscape class (rural, suburban and urban areas) explains spatial variations in pollen source-plant composition foraged by honeybees, but not in taxa richness. Furthermore, pollen diversity and pollen source-plant composition showed a strong seasonal dependence. A higher plant richness and foraged woody taxa was found to occur in spring, which was mainly dominated by the genera Prunus and Acer. In summer and autumn, the genera Trifolium and Plantago of the herbaceous stratum were the most visited plants. The Fabaceae, Rosaceae, Brassicaceae, Plantaginaceae, and Onagraceae plant families were the most frequently observed in all combined samples. The present study contributes to a deeper understanding of the foraging ecology of A. mellifera colonies across urban-rural gradient surrounding mega-cities such as Tokyo.
Disciplines :
Entomology & pest control
Author, co-author :
Noël, Grégoire ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs
Mestrez, Arnaud; Functional and Evolutionary Entomology – Gembloux Agro-Bio Tech (University of Liège), Gembloux, Belgium
Lejeune, Philippe ; Université de Liège - ULiège > TERRA Research Centre > Gestion des ressources forestières et des milieux naturels
Francis, Frédéric ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
Kawai, Junko; Graduate School of Global and Transdisciplinary Studies, Chiba University, Inage-ku, Japan
Miwa, Masayuki; Center for Environment, Health and Field Sciences, Chiba University, Kashiwa, Japan
Uehara, Koichi; Graduate School of Global and Transdisciplinary Studies, Chiba University, Inage-ku, Japan
Nagase, Ayako; Graduate School of Global and Transdisciplinary Studies, Chiba University, Inage-ku, Japan
Language :
English
Title :
Pollen meta-barcoding reveals different community structures of foraged plants by honeybees (Apis mellifera L.) along space-time gradient in Japan
The sequencing data have been deposited with links to BioProject accession number PRJNA74415 in the NCBI BioProject database ( https://www.ncbi.nlm.nih.gov/bioproject/ ). This work was supported by JSPS KAKENHI, Japan (grant number 18KK0121 ) and the Yamada Research Grant , Japan. The pollen was provided by following beekeepers in Japan: Ryuta Aikyo, Sayuri Aoki, Shinta Hegizono, Honami Kawabe, Tamaki Maruhashi, Haruko Nagae, Emi Nobunaga, Nobuyuki Okada, Takumi Sakou, Yuichi Shibasaki, Yosuke Toyomasu, Misa Uchino, and Tomoyuki Yuzurihara.The sequencing data have been deposited with links to BioProject accession number PRJNA74415 in the NCBI BioProject database (https://www.ncbi.nlm.nih.gov/bioproject/). This work was supported by JSPS KAKENHI, Japan (grant number 18KK0121) and the Yamada Research Grant, Japan. The pollen was provided by following beekeepers in Japan: Ryuta Aikyo, Sayuri Aoki, Shinta Hegizono, Honami Kawabe, Tamaki Maruhashi, Haruko Nagae, Emi Nobunaga, Nobuyuki Okada, Takumi Sakou, Yuichi Shibasaki, Yosuke Toyomasu, Misa Uchino, and Tomoyuki Yuzurihara.
Ahrné, K., Bengtsson, J., Elmqvist, T., Bumble bees (Bombus spp) along a gradient of increasing urbanization. PLoS One, 4, 2009, e5574, 10.1371/journal.pone.0005574.
Alaux, C., Ducloz, F., Crauser, D., Le Conte, Y., Diet effects on honeybee immunocompetence. Biol. Lett. 6 (2010), 562–565, 10.1098/rsbl.2009.0986.
Alaux, C., Allier, F., Decourtye, A., Odoux, J.-F., Tamic, T., Chabirand, M., Delestra, E., Decugis, F., Le Conte, Y., Henry, M., A ‘Landscape physiology’ approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats. Sci. Rep., 7, 2017, 40568, 10.1038/srep40568.
Anderson, M.J., A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26 (2001), 32–46, 10.1111/j.1442-9993.2001.01070.pp.x.
Appelhans, T., Detsch, F., Reudenbach, C., Woellauer, S., 2019. mapview: Interactive Viewing of Spatial Data in R.
Avni, D., Dag, A., Shafir, S., Pollen sources for honeybees in Israel: Source, periods of shortage, and influence on population growth. Isr. J. Plant Sci. 57 (2009), 263–275, 10.1560/IJPS.57.3.263.
Avni, D., Hendriksma, H.P., Dag, A., Uni, Z., Shafir, S., Nutritional aspects of honey bee-collected pollen and constraints on colony development in the eastern Mediterranean. J. Insect Physiol. 69 (2014), 65–73, 10.1016/j.jinsphys.2014.07.001.
Baguette, M., Blanchet, S., Legrand, D., Stevens, V.M., Turlure, C., Individual dispersal, landscape connectivity and ecological networks. Biol. Rev. 88 (2012), 310–326, 10.1111/brv.12000.
Baldock, K.C.R., Opportunities and threats for pollinator conservation in global towns and cities. Curr. Opin. Insect Sci. 38 (2020), 63–71, 10.1016/j.cois.2020.01.006.
Baldock, K.C.R., Goddard, M.A., Hicks, D.M., Kunin, E., Mitschunas, N., Osgathorpe, L.M., Potts, S.G., Robertson, K.M., Scott, A.V., Stone, G.N., Vaughan, I.P., Memmott, J., Where is the UK ’ s pollinator biodiversity ? The importance of urban areas for flower- visiting insects. Proc. R. Soc. Biol. Sci., 282, 2015, 20142849 https://doi.org/10.1098.
Barascou, L., Sene, D., Barraud, A., Michez, D., Lefebvre, V., Medrzycki, P., Di Prisco, G., Strobl, V., Yañez, O., Neumann, P., Le Conte, Y., Alaux, C., Pollen nutrition fosters honeybee tolerance to pesticides. R. Soc. Open Sci., 8, 2021, 10.1098/rsos.210818.
Bastin, L., Thomas, C.D., The distribution of plant species in urban vegetation fragments. Landsc. Ecol. 14 (1999), 493–507.
Bell, K.L., De Vere, N., Keller, A., Richardson, R.T., Gous, A., Burgess, K.S., Brosi, B.J., Pollen DNA barcoding: Current applications and future prospects. Genome 59 (2016), 629–640, 10.1139/gen-2015-0200.
Bell, K.L., Fowler, J., Burgess, K.S., Dobbs, E.K., Gruenewald, D., Lawley, B., Morozumi, C., Brosi, B.J., Applying pollen DNA metabarcoding to the study of plant–pollinator interactions. Appl. Plant Sci., 5, 2017, 1600124, 10.3732/apps.1600124.
Bell, K.L., Petit, R.A., Cutler, A., Dobbs, E.K., Macpherson, J.M., Read, T.D., Burgess, K.S., Brosi, B.J., Comparing whole-genome shotgun sequencing and DNA metabarcoding approaches for species identification and quantification of pollen species mixtures. Ecol. Evol. 11 (2021), 16082–16098, 10.1002/ece3.8281.
Benson, D.A., Cavanaugh, M., Clark, K., Karsch-mizrachi, I., Lipman, D.J., Ostell, J., Sayers, E.W., GenBank 41 (2013), 36–42, 10.1093/nar/gks1195.
Bolyen, E., Rideout, J.R., Dillon, M.R., Bokulich, N.A., Abnet, C.C., Al-Ghalith, G.A., Alexander, H., Alm, E.J., Arumugam, M., Asnicar, F., Bai, Y., Bisanz, J.E., Bittinger, K., Brejnrod, A., Brislawn, C.J., Brown, C.T., Callahan, B.J., Caraballo-Rodríguez, A.M., Chase, J., Cope, E.K., Da Silva, R., Diener, C., Dorrestein, P.C., Douglas, G.M., Durall, D.M., Duvallet, C., Edwardson, C.F., Ernst, M., Estaki, M., Fouquier, J., Gauglitz, J.M., Gibbons, S.M., Gibson, D.L., Gonzalez, A., Gorlick, K., Guo, J., Hillmann, B., Holmes, S., Holste, H., Huttenhower, C., Huttley, G.A., Janssen, S., Jarmusch, A.K., Jiang, L., Kaehler, B.D., Kang, K., Bin, Keefe, C.R., Keim, P., Kelley, S.T., Knights, D., Koester, I., Kosciolek, T., Kreps, J., Langille, M.G.I., Lee, J., Ley, R., Liu, Y.-X., Loftfield, E., Lozupone, C., Maher, M., Marotz, C., Martin, B.D., McDonald, D., McIver, L.J., Melnik, A.V., Metcalf, J.L., Morgan, S.C., Morton, J.T., Naimey, A.T., Navas-Molina, J.A., Nothias, L.F., Orchanian, S.B., Pearson, T., Peoples, S.L., Petras, D., Preuss, M.L., Pruesse, E., Rasmussen, L.B., Rivers, A., Robeson, M.S., Rosenthal, P., Segata, N., Shaffer, M., Shiffer, A., Sinha, R., Song, S.J., Spear, J.R., Swafford, A.D., Thompson, L.R., Torres, P.J., Trinh, P., Tripathi, A., Turnbaugh, P.J., Ul-Hasan, S., van der Hooft, J.J.J., Vargas, F., Vázquez-Baeza, Y., Vogtmann, E., von Hippel, M., Walters, W., Wan, Y., Wang, M., Warren, J., Weber, K.C., Williamson, C.H.D., Willis, A.D., Xu, Z.Z., Zaneveld, J.R., Zhang, Y., Zhu, Q., Knight, R., Caporaso, J.G., Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37 (2019), 852–857, 10.1038/s41587-019-0209-9.
Brodschneider, R., Gratzer, K., Kalcher-Sommersguter, E., Heigl, H., Auer, W., Moosbeckhofer, R., Crailsheim, K., A citizen science supported study on seasonal diversity and monoflorality of pollen collected by honey bees in Austria. Sci. Rep., 9, 2019, 16633, 10.1038/s41598-019-53016-5.
Brooks, M.E., Kristensen, K., van Benthem, K.J., Magnusson, A., Berg, C.W., Nielsen, A., Skaug, H.J., Maechler, M., Bolker, B.M., {glmmTMB} Balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R. J. 9 (2017), 378–400.
Chen, B., Jin, Y., Brown, P., An enhanced bloom index for quantifying floral phenology using multi-scale remote sensing observations. ISPRS J. Photogramm. Remote Sens. 156 (2019), 108–120, 10.1016/j.isprsjprs.2019.08.006.
Chen, J.K., 1989. Systematic and evolutionary biology studies on chinese Sagittaria. Wuhan University Press.
Cheng, T., Xu, C., Lei, L., Li, C., Zhang, Y., Zhou, S., Barcoding the kingdom Plantae: New PCR primers for ITS regions of plants with improved universality and specificity. Mol. Ecol. Resour. 16 (2016), 138–149, 10.1111/1755-0998.12438.
Cho, Y., Lee, D., ‘Love honey, hate honey bees’: reviving biophilia of elementary school students through environmental education program. Environ. Educ. Res. 24 (2018), 445–460, 10.1080/13504622.2017.1279277.
Concepción, E.D., Moretti, M., Altermatt, F., Nobis, M.P., Obrist, M.K., Impacts of urbanisation on biodiversity: The role of species mobility, degree of specialisation and spatial scale. Oikos 124 (2015), 1571–1582, 10.1111/oik.02166.
Cornman, R.S., Otto, C.R.V., Iwanowicz, D., Pettis, J.S., Taxonomic characterization of honey bee (Apis mellifera) pollen foraging based on non-overlapping paired-end sequencing of nuclear ribosomal loci. PLoS One, 10, 2015, 10.1371/journal.pone.0145365 e0145365–e0145365.
Critchley, C.N.R., Fowbert, J.A., Wright, B., Dynamics of species-rich upland hay meadows over 15 years and their relation with agricultural management practices. Appl. Veg. Sci. 10 (2007), 307–314, 10.1111/j.1654-109X.2007.tb00429.x.
Danner, N., Molitor, A.M., Schiele, S., Härtel, S., Steffan-Dewenter, I., Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecol. Appl. 26 (2016), 1920–1929, 10.1890/15-1840.1.
Danner, N., Keller, A., Ha, S., Steffan-dewenter, I., Honey bee foraging ecology: Season but not landscape diversity shapes the amount and diversity of collected pollen. PLoS One 12 (2017), 9–12, 10.1371/journal.pone.0183716.
De França Alves, R., De Assis Ribeiro DosSantos, F., Plant sources for bee pollen load production in Sergipe, northeast Brazil. Palynology 38 (2014), 90–100, 10.1080/01916122.2013.846280.
De Vere, N., Jones, L.E., Gilmore, T., Moscrop, J., Lowe, A., Smith, D., Hegarty, M.J., Creer, S., Ford, C.R., Using DNA metabarcoding to investigate honey bee foraging reveals limited flower use despite high floral availability. Sci. Rep. 7 (2017), 1–10, 10.1038/srep42838.
Decourtye, A., Mader, E., Desneux, N., Landscape enhancement of floral resources for honey bees in agro-ecosystems. Apidologie 41 (2010), 264–277, 10.1051/apido/2010024.
Delaplane, K.S., Steen, J.Van Der, Guzman-Novoa, E., Standard methods for estimating strength parameters of Apis mellifera colonies. J. Apic. Res. 52 (2013), 1–12, 10.3896/IBRA.1.52.1.03.
Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A., Kretzschmar, A., Suchail, S., Brunet, J.L., Alaux, C., Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter. PLoS One, 8, 2013, 10.1371/journal.pone.0072016 (e72016–e72016).
Di Pasquale, G., Alaux, C., Le Conte, Y., Odoux, J.-F., Pioz, M., Vaissière, B.E., Belzunces, L.P., Decourtye, A., Variations in the availability of pollen resources affect honey bee health. PLoS One, 11, 2016, e0162818, 10.1371/journal.pone.0162818.
Doherty, T.S., Driscoll, D.A., Coupling movement and landscape ecology for animal conservation in production landscapes. Proc. R. Soc. B Biol. Sci., 285, 2018, 20172272, 10.1098/rspb.2017.2272.
Donaldson-Matasci, M.C., Dornhaus, A., How habitat affects the benefits of communication in collectively foraging honey bees. Behav. Ecol. Sociobiol. 66 (2012), 583–592, 10.1007/s00265-011-1306-z.
Donkersley, P., Rhodes, G., Pickup, R.W., Jones, K.C., Power, E.F., Wright, G.A., Wilson, K., Nutritional composition of honey bee food stores vary with floral composition. Oecologia 185 (2017), 749–761, 10.1007/s00442-017-3968-3.
Dormann, C.F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., Marquéz, J.R.G., Gruber, B., Lafourcade, B., Leitão, P.J., Münkemüller, T., McClean, C., Osborne, P.E., Reineking, B., Schröder, B., Skidmore, A.K., Zurell, D., Lautenbach, S., Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36 (2013), 27–46, 10.1111/j.1600-0587.2012.07348.x.
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (2011), 2194–2200, 10.1093/bioinformatics/btr381.
E-Vojtkó, A., de Bello, F., Durka, W., Kühn, I., Götzenberger, L., The neglected importance of floral traits in trait-based plant community assembly. J. Veg. Sci. 31 (2020), 529–539, 10.1111/jvs.12877.
Fornoff, F., Klein, A.M., Hartig, F., Benadi, G., Venjakob, C., Schaefer, H.Martin, Ebeling, A., Functional flower traits and their diversity drive pollinator visitation. Oikos 126 (2017), 1020–1030, 10.1111/oik.03869.
Fortel, L., Henry, M., Guilbaud, L., Guirao, A.L., Kuhlmann, M., Mouret, H., Rollin, O., Vaissière, B.E., Decreasing abundance, increasing diversity and changing structure of the wild bee community (Hymenoptera: Anthophila) along an urbanization gradient. PLoS One, 9, 2014, e104679, 10.1371/journal.pone.0104679.
von Frisch, K., Tanzsprache und Orientierung der Bienen, Tanzsprache und Orientierung der Bienen. 1965, Springer Berlin Heidelberg, Berlin, Heidelberg 〈https://doi.org/10.1007/978-3-642-94916-6〉.
Galimberti, A., De Mattia, F., Bruni, I., Scaccabarozzi, D., Sandionigi, A., Barbuto, M., Casiraghi, M., Labra, M., A DNA barcoding approach to characterize pollen collected by honeybees. PLoS One, 9, 2014, e109363.
Garbuzov, M., Ratnieks, F.L.W., Quantifying variation among garden plants in attractiveness to bees and other flower-visiting insects. Funct. Ecol. 28 (2014), 364–374, 10.1111/1365-2435.12178.
Garbuzov, M., Samuelson, E.E.W., Ratnieks, F.L.W., Survey of insect visitation of ornamental flowers in Southover Grange garden, Lewes, UK. Insect Sci. 22 (2015), 700–705, 10.1111/1744-7917.12162.
Garbuzov, M., Schürch, R., Ratnieks, F.L.W., Eating locally: dance decoding demonstrates that urban honey bees in Brighton, UK, forage mainly in the surrounding urban area. Urban Ecosyst. 18 (2015), 411–418, 10.1007/s11252-014-0403-y.
Geslin, B., Gauzens, B., Baude, M., Dajoz, I., Fontaine, C., Henry, M., Ropars, L., Rollin, O., Thébault, E., Vereecken, N.J., Massively introduced managed species and their consequences for plant–pollinator interactions. Adv. Ecol. Res. 57 (2017), 1–53, 10.1016/j.talanta.2011.11.033.
Grueber, C.E., Nakagawa, S., Laws, R.J., Jameson, I.G., Multimodel inference in ecology and evolution: challenges and solutions. J. Evol. Biol. 24 (2011), 699–711, 10.1111/j.1420-9101.2010.02210.x.
Hadley, A.S., Betts, M.G., The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol. Rev. 87 (2012), 526–544, 10.1111/j.1469-185X.2011.00205.x.
Hall, D.M., Camilo, G.R., Tonietto, R.K., Smith, D.H., Ollerton, J., Ahrné, K., Arduser, M., Ascher, J.S., Baldock, K.C.R., Fowler, R., Frankie, G., Goulson, D., Gunnarsson, B., Hanley, M.E., Jackson, J.I., Langellotto, G., Lowenstein, D., Minor, E.S., Philpott, S.M., Potts, S.G., Sirohi, M.H., Spevak, E.M., Stone, G.N., Threlfall, C.G., The city as a refuge for insect pollinators. Conserv. Biol., 2016, 10.1111/cobi.12840.
Hashim, H., Abd Latif, Z., Adnan, N.A., Urban vegetation classification with NDVI threshold value method with very high resolution (VHR) Pleiades imagery. Int. Arch. Photogramm. Remote Sens. Spat. Inf. Sci. - ISPRS Arch. 42 (2019), 237–240, 10.5194/isprs-archives-XLII-4-W16-237-2019.
Hawkins, J., De Vere, N., Griffith, A., Ford, C.R., Allainguillaume, J., Hegarty, M.J., Baillie, L., Adams-Groom, B., Using DNA metabarcoding to identify the floral composition of honey: A new tool for investigating honey bee foraging preferences. –e0134735 PLoS One, 10, 2015, e0134735, 10.1371/journal.pone.0134735.
Hervé, M., 2020. RVAideMemoire: Testing and plotting procedures for biostatistics.
Hesselbarth, M.H.K., Sciaini, M., With, K.A., Wiegand, K., Nowosad, J., Landscapemetrics: an open-source R tool to calculate landscape metrics. Ecography 42 (2019), 1648–1657.
Hijmans, R.J., van Etten, J., Sumner, M., Cheng, J., Baston, D., Bevan, A., Bivand, R., Busetto, L., Canty, M., Forrest, D., Ghosh, A., Golicher, D., Gray, J., Greenberg, J.A., Hiemstra, P., Hingee, K., Geosciences, I. for M.A., Karney, C., Mattiuzzi, M., Mosher, S., Nowosad, J., Pebesma, E., Perpinan Lamigueiro, O., Racine, E.B., Rowlingson, B., Shortridge, A., Venables, B., Wueest, R., 2020. raster: Geographic data analysis and modeling.
Joshi, N., Fass, J., 2011. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files.
Kaškoniene, V., Venskutonis, P.R., Floral markers in honey of various botanical and geographic origins: a review. Compr. Rev. Food Sci. Food Saf. 9 (2010), 620–634, 10.1111/j.1541-4337.2010.00130.x.
Kassambara, A., Fabian, M., 2020. factoextra: Extract and visualize the results of multivariate data analyses.
Kimura, K., Yoshiyama, M., Saiou, K., Nirasawa, K., Ishizaka, M., Examination of mass honey bee death at the entrance to hives in a paddy rice production district in Japan: The influence of insecticides sprayed on nearby rice fields. J. Apic. Res. 53 (2014), 599–606, 10.3896/IBRA.1.53.5.12.
Kodinariya, T.M., Makwana, P.R., Review on determining number of cluster in k-means clustering. Int. J. Adv. Res. Comput. Sci. Manag. Stud. 1 (2013), 90–95.
Kraaijeveld, K., de Weger, L.A., Ventayol García, M., Buermans, H., Frank, J., Hiemstra, P.S., den Dunnen, J.T., Efficient and sensitive identification and quantification of airborne pollen using next-generation DNA sequencing. Mol. Ecol. Resour. 15 (2014), 8–16, 10.1111/1755-0998.12288.
Lau, P., Bryant, V., Ellis, J.D., Huang, Z.Y., Sullivan, J., Schmehl, D.R., Cabrera, A.R., Rangel, J., Seasonal variation of pollen collected by honey bees (Apis mellifera) in developed areas across four regions in the United States. PLoS One, 14, 2019, e0217294, 10.1371/journal.pone.0217294.
Legendre, P., Interpreting the replacement and richness difference components of beta diversity. Glob. Ecol. Biogeogr. 23 (2014), 1324–1334, 10.1111/geb.12207.
Librán-Embid, F., Klaus, F., Tscharntke, T., Grass, I., Unmanned aerial vehicles for biodiversity-friendly agricultural landscapes - a systematic review. Sci. Total Environ., 732, 2020, 139204, 10.1016/j.scitotenv.2020.139204.
Lindén, A., Mäntyniemi, S., Using negative binomial distribution to model overdispersion in ecological count data. Ecology 92 (2011), 1414–1421, 10.2307/23035094.
Lindsay, J.B., Whitebox GAT: a case study in geomorphometric analysis. Comput. Geosci. 95 (2016), 75–84, 10.1016/j.cageo.2016.07.003.
Liolios, V., Tananaki, C., Dimou, M., Kanelis, D., Goras, G., Karazafiris, E., Thrasyvoulou, A., Clasificación del polen de las plantas melíferas en función de su aportación de proteínas para las abejas de la miel. J. Apic. Res. 54 (2015), 582–592, 10.1080/00218839.2016.1173353.
Lucek, K., Galli, A., Gurten, S., Hohmann, N., Maccagni, A., Patsiou, T., Willi, Y., Metabarcoding of honey to assess differences in plant-pollinator interactions between urban and non-urban sites. Apidologie 50 (2019), 317–329, 10.1007/s13592-019-00646-3.
MacDonald, P.L., Gardner, R.C., Type I error rate comparisons of post hoc procedures for I × J chi-square tables. Educ. Psychol. Meas. 60 (2000), 735–754, 10.1177/00131640021970871.
Maeda, M., Takahashi, J., 2017. Investigation of foraging plants using analysis of honey DNA: Analysis of multifloral honey and honeydew, in: Poster Session, Bee Summit in Tsukuba (Japan).
Magoč, T., Salzberg, S.L., FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27 (2011), 2957–2963, 10.1093/bioinformatics/btr507.
Mahmood, R., Asad, S., Sarwar, G., Ahmad, W., Qadir, Z.A., Balouch, A., Rafque, M.K., Pollen collection and pollen foraging behaviour of honeybees (Apis mellifera) during different time intervals from brassica campestris L. Pak. J. Zool. 49 (2017), 733–736, 10.17582/journal.pjz/2017.49.2.sc4.
Martinez Arbizu, P., 2020. pairwiseAdonis: Pairwise multilevel comparison using adonis.
Masamura, N., Kikuchi, R., Nagatomi, Y., Developments of an identification method for foreign substances of plant origin using ITS 1 Region. Bunseki Kagaku 63 (2014), 245–253, 10.2116/bunsekikagaku.63.245.
Miller, G.J., Morris, J.T., Wang, C., Estimating aboveground biomass and its spatial distribution in coastal wetlands utilizing planet multispectral imagery. Remote Sens, 11, 2019, 2020, 10.3390/rs11172020.
Muratet, A., Fontaine, B., Contrasting impacts of pesticides on butterflies and bumblebees in private gardens in France. Biol. Conserv. 182 (2015), 148–154, 10.1016/j.biocon.2014.11.045.
Ohe, W., von der, Persano Oddo, L., Piana, M.L., Morlot, M., Martin, P., Harmonized methods of melissopalynology. Apidologie 35 (2004), 18–25, 10.1051/apido.
Oksanen, J., Blanchet Michael, F.G.F., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E., Wagner, H., 2019. vegan: Community Ecology Package.
Pardee, G.L., Philpott, S.M., Native plants are the bee's knees: local and landscape predictors of bee richness and abundance in backyard gardens. Urban Ecosyst. 17 (2014), 641–659, 10.1007/s11252-014-0349-0.
Park, B., Nieh, J.C., Seasonal trends in honey bee pollen foraging revealed through DNA barcoding of bee-collected pollen. Insectes Soc. 64 (2017), 425–437, 10.1007/s00040-017-0565-8.
Planet Core Team, 2020. Planet application program interface: In space for life on earth. [WWW Document]. URL 〈https://www.planet.com/markets/education-and-research/〉.
Plant, R.E., Spatial Data Analysis in Ecology and Agriculture Using R. 2012, CRC Press, Boca Raton.
Pornon, A., Escaravage, N., Burrus, M., Holota, H., Khimoun, A., Mariette, J., Pellizzari, C., Iribar, A., Etienne, R., Taberlet, P., Vidal, M., Winterton, P., Zinger, L., Andalo, C., Using metabarcoding to reveal and quantify plant-pollinator interactions. Sci. Rep., 6, 2016, 27282, 10.1038/srep27282.
Pritt, M., Chern, G., 2017. Satellite image classification with deep learning, in: IEEE Applied Imagery Pattern Recognition Workshop. pp. 1–7. 〈https://doi.org/10.1109/AIPR.2017.8457969〉.
R Core Team, 2020. R: A language and environment for statistical computing.
Rahl, M., Microscopic identification and purity determination of pollen grains. Methods Mol. Med. 138 (2008), 263–269, 10.1007/978-1-59745-366-0_22.
Requier, F., Odoux, J.F., Tamic, T., Moreau, N., Henry, M., Decourtye, A., Bretagnolle, V., Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol. Appl. 25 (2015), 881–890, 10.1890/14-1011.1.
Richards, S.A., Dealing with overdispersed count data in applied ecology. J. Appl. Ecol. 45 (2008), 218–227.
Richardson, R.T., Lin, C.-H., Sponsler, D.B., Quijia, J.O., Goodell, K., Johnson, R.M., Application of ITS2 metabarcoding to determine the provenance of pollen collected by honey bees in an agroecosystem. Appl. Plant Sci. 3 (2015), 1–6, 10.3732/apps.1400066.
Richardson, R.T., Lin, C., Quijia, J.O., Riusech, N.S., Goodell, K., Johnson, R.M., Rank-based characterization of pollen assemblages collected by honey bees using a multi-locus metabarcoding approach. Appl. Plant Sci., 3, 2015, 1500043, 10.3732/apps.1500043.
Richardson, R.T., Eaton, T.D., Lin, C.H., Cherry, G., Johnson, R.M., Sponsler, D.B., Application of plant metabarcoding to identify diverse honeybee pollen forage along an urban–agricultural gradient. Mol. Ecol. 30 (2021), 310–323, 10.1111/mec.15704.
Ropars, L., Dajoz, I., Fontaine, C., Muratet, A., Geslin, B., Wild pollinator activity negatively related to honey bee colony densities in urban context. PLoS One, 14, 2019, e0222316, 10.1371/journal.pone.0222316.
Roskov, Y., Ower, G., Orrell, T., Nicolson, D., Bailly, N., Kirk, P.M., Bourgoin, T., DeWalt, R.E., Decock, W., Nieukerken, E. van, Zarucchi, J., Penev, L., 2019. Species 2000 & ITIS catalogue of life, 2019 annual checklist [WWW Document]. URL 〈http://www.catalogueoflife.org/annual-checklist/2019〉.
Sánchez-Bayo, F., Wyckhuys, K.A.G., Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 232 (2019), 8–27, 10.1016/j.biocon.2019.01.020.
Saunders, M.E., Insect pollinators collect pollen from wind-pollinated plants: implications for pollination ecology and sustainable agriculture. Insect Conserv. Divers. 11 (2018), 13–31, 10.1111/icad.12243.
Saura, S., Pascual-Hortal, L., A new habitat availability index to integrate connectivity in landscape conservation planning: comparison with existing indices and application to a case study. Landsc. Urban Plan. 83 (2007), 91–103, 10.1016/j.landurbplan.2007.03.005.
Seeley, T.D., The Wisdom of the Hive, Illustrate. ed. 1995, Harvard University Press.
Shannon, C.E., A mathematical theory of communication. Bell Syst. Tech. J. 27 (1948), 623–656, 10.1002/j.1538-7305.1948.tb00917.x.
Sickel, W., Ankenbrand, M.J., Grimmer, G., Holzschuh, A., Härtel, S., Lanzen, J., Increased efficiency in identifying mixed pollen samples by meta ‑ barcoding with a dual ‑ indexing approach. BMC Ecol. 15 (2015), 1–9, 10.1186/s12898-015-0051-y.
Smart, M.D., Cornman, R.S., Iwanowicz, D.D., McDermott-Kubeczko, M., Pettis, J.S., Spivak, M.S., Otto, C.R.V., A comparison of honey bee-collected pollen from working agricultural lands using light microscopy and its metabarcoding. Environ. Entomol. 46 (2017), 38–49, 10.1093/ee/nvw159.
Spanowicz, A.G., Jaeger, J.A.G., Measuring landscape connectivity: On the importance of within-patch connectivity. Landsc. Ecol. 34 (2019), 2261–2278, 10.1007/s10980-019-00881-0.
Sponsler, D.B., Shump, D., Richardson, R.T., Grozinger, C.M., Characterizing the floral resources of a North American metropolis using a honey bee foraging assay. Ecosphere, 11, 2020, 10.1002/ecs2.3102.
Steffan-Dewenter, I., Kuhn, A., Honeybee foraging in differentially structured landscapes. Proc. R. Soc. B Biol. Sci. 270 (2003), 569–575, 10.1098/rspb.2002.2292.
Strickland, J.S., 2014. Predictive analytics using R. Lulu Inc.
Tanaka, K., Nozaki, A., Nakadai, H., Shiwa, Y., Shimizu-Kadota, M., Using pollen DNA metabarcoding to profile nectar sources of urban beekeeping in Kōtō-ku, Tokyo. BMC Res. Notes 13 (2020), 1–6, 10.1186/s13104-020-05361-2.
Taufik, A., Syed Ahmad, S.S., Azmi, E.F., Classification of landsat 8 satellite data using unsupervised methods. J. Telecommun. Electron. Comput. Eng. 8 (2016), 37–40.
Theodorou, P., Radzevičiūtė, R., Lentendu, G., Kahnt, B., Husemann, M., Bleidorn, C., Settele, J., Schweiger, O., Grosse, I., Wubet, T., Murray, T.E., Paxton, R.J., Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nat. Commun. 11 (2020), 1–13, 10.1038/s41467-020-14496-6.
Threlfall, C.G., Walker, K., Williams, N.S.G., Hahs, A.K., Mata, L., Stork, N., Livesley, S.J., The conservation value of urban green space habitats for Australian native bee communities. Biol. Conserv. 187 (2015), 240–248, 10.1016/j.biocon.2015.05.003.
Urbanowicz, C., Muñiz, P.A., McArt, S.H., Honey bees and wild pollinators differ in their preference for and use of introduced floral resources. Ecol. Evol. 10 (2020), 6741–6751, 10.1002/ece3.6417.
Visscher, P.K., Seeley, T.D., Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63 (1982), 1790–1801, 10.2307/1940121.
Wenzel, A., Grass, I., Belavadi, V.V., Tscharntke, T., How urbanization is driving pollinator diversity and pollination – A systematic review. Biol. Conserv., 241, 2020, 108321, 10.1016/j.biocon.2019.108321.
Wickham, H., ggplot2: Elegant Graphics for Data analysis. 2016, Springer-Verlag, New York.
Wilde, J., Bratkowski, J., Siuda, M., Pollen collection by 3 subspecies of honeybee Apis mellifera L. Acta Biol. Univ. Daugavp. 3 (2003), 101–106.
Williams, N.M., Cariveau, D., Winfree, R., Kremen, C., Bees in disturbed habitats use, but do not prefer, alien plants. Basic Appl. Ecol. 12 (2011), 332–341, 10.1016/j.baae.2010.11.008.
Xue, J., Su, B., Significant remote sensing vegetation indices: a review of developments and applications. J. Sens. 2017 (2017), 1–17, 10.1155/2017/1353691.
Yonekura, K., Kajita, T., 2007. Japanese botanical name-scientific name index YList [WWW Document].
