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Non-native plants are a seasonal pollen source for native honeybees in suburban ecosystems

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Abstract

In urban and suburban ecosystems, biodiversity can depend on various non-native plant species, including crop plants, garden plants and weeds. Non-native plants may help to maintain biodiversity by providing a source of forage for pollinators in these ecosystems. However, the contribution of plants in urban and agricultural areas to ecosystem services has often been underestimated in biodiversity assessments. In this study, we investigated the pollen sources of native honeybees (Apis cerana) in an arboretum containing native trees and urban and agricultural plants in a suburban landscape. We surveyed the flowering tree species planted inside the arboretum, which were potential pollen sources. The number of potential pollen-source species of native trees peaked in June and July and decreased after August. We collected A. cerana pollen balls every month and identified plant species of pollen in the collected pollen balls using DNA barcoding. In total, we identified 29 plant species from A. cerana pollen balls. The probability of A. cerana using pollen from urban and agricultural plants was higher in July and August than in June. A. cerana collected pollen forages from native tree species (53%), but also gathered pollen from crop plants (13%), garden trees (19%) and native and non-native weeds (14%); the predominant pollen sources in September and October were the garden tree Ulmus parvifolia and the non-native weed Solidago altissima. We found that native honeybees used plants from a variety of habitats including non-native plants to compensate for apparent seasonal shortages of native tree sources in suburban ecosystems. Our results highlight the importance of assessments of both positive and negative roles of non-native plants in urbanized ecosystems to improve biodiversity conservation.

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References

  • Alvarez ME, Cushman JH (2002) Community-level consequences of a plant invasion: effects on three habitats in coastal California. Ecol Appl 12:1434–1444

    Article  Google Scholar 

  • Aronne G, Giovanetti M, Guarracino MR, de Micco V (2012) Foraging rules of flower selection applied by colonies of Apis mellifera: ranking and associations of floral sources. Funct Ecol 26:1186–1196

    Article  Google Scholar 

  • Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM, Potts SG, Robertson KM, Scott AV, Stone GN, Vaughan IP, Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. P Roy Soc Lond Bio 282:20142849. https://doi.org/10.1098/rspb.2014.2849

    Article  Google Scholar 

  • BBOP (2012) Biodiversity offset design handbook. BBOP, Washington, D.C.

    Google Scholar 

  • Bjerknes AL, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference. Springer, New York

    Google Scholar 

  • Capotorti G, Del Vico E, Lattanzi E, Tilia A, Celesti-Grapow L (2013) Exploring biodiversity in a metropolitan area in the Mediterranean region: the urban and suburban flora of Rome (Italy). Plant Biosyst 147:174–185

    Article  Google Scholar 

  • CBOL Plant Working Group (2009) A DNA barcode for land plants. Proc Natl Acad Sci U S A 106:12794–12797

    Article  Google Scholar 

  • D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Evol Syst 23:63–87

    Article  Google Scholar 

  • Danner N, Härtel S, Steffan-Dewenter I (2014) Maize pollen foraging by honey bees in relation to crop area and landscape context. Basic Appl Ecol 15:677–684

    Article  Google Scholar 

  • Dassonville N, Vanderhoeven S, Vanparys V, Hayez M, Gruber W, Meerts P (2008) Impacts of alien invasive plants on soil nutrients are correlated with initial site conditions in NW Europe. Oecologia 157:131–140

    Article  Google Scholar 

  • DSE (2004) Vegetation quality assessment manual: guidelines for applying the habitat hectares scoring method. ver. 1.3. Victorian Government Department of Sustainability and Environment, Melbourne, 68 pp.

  • Dyer F (1991) Dance dialects and foraging range in three Asian honey bee species. Behav Ecol Sociobiol 28:227–233

    Article  Google Scholar 

  • Etterson JR, Delf DE, Craig TP, Ando Y, Ohgushi T (2008) Parallel patterns of clinal variation in Solidago altissima in its native range in Central USA and its invasive range in Japan. Botany 86:91–97

    Article  Google Scholar 

  • Fortel L, Henry M, Guilbaud L, Guirao AL, Kuhlmann M, Mouret H, Rollin O, Vaissière BE (2014) Decreasing abundance, increasing diversity and changing structure of the wild bee community (hymenoptera: Anthophila) along an urbanization gradient. PLoS One 9:e104679

    Article  Google Scholar 

  • Foster G, Bennett J, Sparks T (2017) An assessment of bumblebee (Bombus spp.) land use and floral preference in UK gardens and allotments cultivated for food. Urban Ecosyst 20:425–434

    Article  Google Scholar 

  • French K, Major R, Hely K (2005) Use of native and exotic garden plants by suburban nectarivorous birds. Biol Conserv 121:545–559

    Article  Google Scholar 

  • Fujiki T, Miyoshi N, Kimura H (2016) Pollen flora of Japan, 2nd edn. Hokkaido University Press, Sapporo (in Japanese)

    Google Scholar 

  • Fujiwara A, Washitani I (2017) Dependence of Asian honeybee on deciduous woody plants for pollen resource during spring to midsummer in northern Japan. Entomol Sci 20:96–99

    Article  Google Scholar 

  • Fujiwara A, Nishihiro J, Washitani I (2014) Evaluating ecosystem services of the Japanese honeybee, Apis cerana japonica, in a satoyama landscape: flower use and colony development. Jpn J Conserv Ecol 19:39–51 (In Japanese)

    Google Scholar 

  • Galimberti A, De Mattia F, Bruni I et al (2014) A DNA barcoding approach to characterize pollen collected by honeybees. PLoS One 9:e109363

    Article  Google Scholar 

  • Geslin B, Le Féon V, Folschweiller M, Flacher F, Carmignac D, Motard E, Perret S, Dajoz I (2016) The proportion of impervious surfaces at the landscape scale structures wild bee assemblages in a densely populated region. Ecol Evol 6:6599–6615

    Article  Google Scholar 

  • Goddard MA, Dougill AJ, Benton TG (2010) Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol 25:90–98

    Article  Google Scholar 

  • Gross CL, Gorrell L, Macdonald MJ, Fatemi M (2010) Honeybees facilitate the invasion of Phyla canescens (Verbenaceae) in Australia – no bees, no seed! Weed Res 50:364–372

    Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    Article  Google Scholar 

  • Hopwood JL (2008) The contribution of roadside grassland restorations to native bee conservation. Biol Conserv 141:2632–2640

    Article  Google Scholar 

  • Ikin K, Knight E, Lindenmayer DB, Fischer J, Manning AD (2013) The influence of native versus exotic streetscape vegetation on the spatial distribution of birds in suburbs and reserves. Divers Distrib 19:294–306

    Article  Google Scholar 

  • Japan Beekeepers Association (JBA) (2005) The honeybee plants of Japan. Japan Beekeepers Association, Tokyo (in Japanese)

    Google Scholar 

  • Kaiser-Bunbury CN, Mougal J, Whittington AE, Valentin T, Gabriel R, Olesen JM, Blüthgen N (2017) Ecosystem restoration strengthens pollination network resilience and function. Nature 542:223–227

    Article  CAS  Google Scholar 

  • Kajzer-Bonk J, Szpiłyk D, Woyciechowski M (2016) Invasive goldenrods affect abundance and diversity of grassland ant communities (Hymenoptera: Formicidae). J Insect Conserv 20:99–105

    Article  Google Scholar 

  • Kareiva P, Watts S, McDonald R, Boucher T (2007) Domesticated nature: shaping landscapes and ecosystems for human welfare. Science 316:1866–1869

    Article  CAS  Google Scholar 

  • Kawarasaki S, Hori Y (2001) Flowering phenology of understory herbaceous species in a cool temperate deciduous forest in Ogawa forest reserve, Central Japan. J Plant Res 114:19–23

    Article  Google Scholar 

  • Keller I, Fluri P, Imdorf A (2005a) Pollen nutrition and colony development in honey bees: part 1. Bee World 86:3–10

    Article  Google Scholar 

  • Keller I, Fluri P, Imdorf A (2005b) Pollen nutrition and colony development in honey bees: part II. Bee World 86:27–34

    Article  Google Scholar 

  • Kikuti H, Chishima T, Okamoto M, Tohgo R (1994) List of tree species planted in the arboreta of Forestry and Forest Products Research Institute (Headquarters) (1978–1990). Bull For Pros Res Inst 368:109–205

    Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond Ser B Biol Sci 274:303–313

    Article  Google Scholar 

  • Lambdon PW, Pyšek P, Basnou C et al (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80:101–149

    Google Scholar 

  • Lin BB, Philpott SM, Jha S (2015) The future of urban agriculture and biodiversity-ecosystem services: challenges and next steps. Basic Appl Ecol 16:189–201

    Article  Google Scholar 

  • Mattila HR, Otis GW (2007) Dwindling pollen resources trigger the transition to broodless populations of long-lived honeybees each autumn. Ecol Entomol 32:496–505

    Article  Google Scholar 

  • Nagamitsu T, Inoue T (1999) Differences in pollen sources of Apis cerana and Apis mellifera at a primary beech forest in Central Japan. J Apic Res 38:71–78

    Article  Google Scholar 

  • Nagamitsu T, Yasuda M, Saito-Morooka F, Inoue MN, Nishiyama M, Goka K, Sugiura S, Maeto K, Okabe K, Taki H (2016) Genetic structure and potential environmental determinants of local genetic diversity in Japanese honeybees (Apis cerana japonica). PLoS One 11:1–15

    Article  Google Scholar 

  • Nakamura J (1980a) Diagnostic characters of pollen gains of Japan, II. Special publications from the Osaka Museum of Natural History 12:1–157 (in Japanese)

    Google Scholar 

  • Nakamura J (1980b) Diagnostic characters of pollen gains of Japan, I. Special publications from the Osaka Museum of Natural History 13:1–91 (in Japanese)

    Google Scholar 

  • Nishikawa T, Okazaki K, Uchino T, Arakawa K, Nagamine T (1999) A molecular phylogeny of Lilium in the internal transcribed spacer region of nuclear ribosomal DNA. J Mol Evol 49:238–249

    Article  CAS  Google Scholar 

  • Osada N, Sugiura S, Kawamura K, Cho M, Takeda H (2003) Community-level flowering phenology and fruit set: comparative study of 25 woody species in a secondary forest in Japan. Ecol Res 18:711–723

    Article  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  Google Scholar 

  • Putra RE, Nakamura K (2016) Foraging ecology of a local wild bee community in an abandoned Satoyama system in Kanazawa, Central Japan. Entomol Res 39:99–106

    Article  Google Scholar 

  • Pyšek P, Pergl J, Essl F, Lenzner B, Dawson W, Kreft H, Weigelt P, Winter M, Kartesz J, Nishino M, Antonova LA, Barcelona JF, Cabesaz FJ, Cárdenas D, Cárdenas-Toro J, Castaño N, Chacón E, Chatelain C, Dullinger S, Ebel AL, Figueiredo E, Fuentes N, Genovesi P, Groom QJ, Henderson L, Inderjit, Kupriyanov A, Masciadri S, Maurel N, Meerman J, Morozova O, Moser D, Nickrent D, Nowak PM, Pagad S, Patzelt A, Pelser PB, Seebens H, Shu WS, Thomas J, Velayos M, Weber E, Wieringa JJ, Baptiste MP, Kleunen M (2017) Naturalized alien flora of the world: species diversity, taxonomic and phylogenetic patterns, geographic distribution and global hotspots of plant invasion. Preslia 89:203–274

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Regan HM, Davis FW, Andelman SJ, Widyanata A, Freese M (2007) Comprehensive criteria for biodiversity evaluation in conservation planning. Biodivers Conserv 16:2715–2728

    Article  Google Scholar 

  • Richards AJ (2001) Does low biodiversity resulting from modern agricultural practice affect crop pollination and yield? Ann Bot 88:165–172

    Article  Google Scholar 

  • Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196:383–396

    Article  Google Scholar 

  • Ruffner ME (2012) Ecosystem function differs between Old World bluestem invaded and native coastal prairie in South Texas. Biol Invasions 14:1483–1500

    Article  Google Scholar 

  • Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer Science & Business Media, Berlin, Heidelberg

    Book  Google Scholar 

  • Sasaki M (2010) Bee’s eye view of flowering plants: nectar- and pollen-source plants and related honeybee products. Kaiyusha, Tokyo (in Japanese)

    Google Scholar 

  • Schlaepfer MA, Sax D, Olden JD (2011) The potential conservation value of non-native species. Conserv Biol 25:428–437

    Article  Google Scholar 

  • Seeley TD, Visscher PK (1985) Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecol Entomol 10:81–88

    Article  Google Scholar 

  • Smith RM, Thompson K, Hodgson JG, Warren PH, Gaston KJ (2006) Urban domestic gardens (IX): composition and richness of the vascular plant flora and implications for native biodiversity. Biol Conserv 129:312–322

    Article  Google Scholar 

  • Song XY, Yao YF, Yang WD (2012) Pollen analysis of natural honeys from the central region of Shanxi, North China. PLoS One 7:e49545

    Article  CAS  Google Scholar 

  • Stout JC, Morales CL (2009) Ecological impacts of invasive alien species on bees. Apidologie 40:388–409

    Article  Google Scholar 

  • Suryanarayana M, Rao GM, Singh T (1992) Studies on pollen sources for Apis cerana Fabr and Apis mellifera L bees at Muzaffarpur, Bihar, India. Apidologie 23:33–46

    Article  Google Scholar 

  • Taki H, Okabe K, Yamaura Y, Matsuura T, Sueyoshi M, Makino S, Maeto K (2010) Effects of landscape metrics on Apis and non-Apis pollinators and seed set in common buckwheat. Basic Appl Ecol 11:594–602

    Article  Google Scholar 

  • Taki H, Yamaura Y, Okabe K, Maeto K (2011) Plantation vs. natural forest: Matrix quality determines pollinator abundance in crop fields. Sci Rep 1. https://doi.org/10.1038/srep00132

  • Taki H, Ikeda H, Nagamitsu T, Yasuda M, Sugiura S, Maeto K, Okabe K (2017) Stable nitrogen and carbon isotope ratios in wild native honeybees: the influence of land use and climate. Biodivers Conserv 26:3157–3166

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis ver. 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Tokuoka Y, Ohigashi K, Nakagoshi N (2011) Limitations on tree seedling establishment across ecotones between abandoned fields and adjacent broad-leaved forests in eastern Japan. Plant Ecol 212:923–944

    Article  Google Scholar 

  • Ushio M, Yamasaki E, Takasu H, Nagano AJ, Fujinaga S, Honjo MN, Ikemoto M, Sakai S, Kudoh H (2015) Microbial communities on flower surfaces act as signatures of pollinator visitation. Sci Rep 5. https://doi.org/10.1038/srep08695

  • Visscher PK, Seeley TD (1982) Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63:1790–1801

    Article  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Wania A, Kühn I, Klotz S (2006) Plant richness patterns in agricultural and urban landscapes in Central Germany: spatial gradients of species richness. Landsc Urban Plan 75:97–110

    Article  Google Scholar 

  • Weber E (1998) The dynamics of plant invasions: a case study of three exotic goldenrod species (Solidago L.) in Europe. J Biogeogr 25:147–154

    Article  Google Scholar 

  • Westphal C, Steffan-Dewenter I, Tscharntke T (2003) Mass flowering crops enhance pollinator densities at a landscape scale. Ecol Lett 6:961–965

    Article  Google Scholar 

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Acknowledgements

We are grateful to Dr. T. Masaki for providing the flora list of the FFPRI arboretum. We also thank Dr. A. Nikkeshi for his advice on pollen observation methods, and Dr. T. F. Koyanagi for her advice on GIS analysis. This work received financial support from the Environment Research and Technology Development Fund (1-1401 and 5-1407).

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Author notes

  1. Asuka Koyama

    Present address: Institute for Sustainable Agro-ecosystem Services, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1, Midori-cho, Nishi-Tokyo, Tokyo, 188-0002, Japan

  2. Mika Yasuda

    Present address: BirdLife International Tokyo, 1-13-1 Kakigara-cho, Nihonbashi, Tokyo, 103-0014, Japan

  3. Natsumi Kanzaki

    Present address: Kansai Research Center, Forestry and Forest Products Research Institute, Fushimi, Kyoto, 612-0855, Japan

  4. Tatsuya Ide

    Present address: National Museum of Nature and Science, 4-1-1Amakubo, Tsukuba, Ibaraki, 305-0005, Japan

Authors and Affiliations

  1. Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki, 305-8687, Japan

    Asuka Koyama, Hisatomo Taki, Mika Yasuda, Natsumi Kanzaki, Tatsuya Ide & Kimiko Okabe

  2. Institute for Agro-Environmental Sciences, NARO, 3-1-3 Kannondai, Tsukuba, Ibaraki, 305-8604, Japan

    Chika Egawa

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  1. Asuka Koyama
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Appendices

Appendix 1

Table 3 Effects of pesticides on A. cerana pollen-foraging behavior
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Appendix 2

Table 4 List of flowering tree species planted in the Forestry and Forest Products Research Institute arboretum
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Koyama, A., Egawa, C., Taki, H. et al. Non-native plants are a seasonal pollen source for native honeybees in suburban ecosystems. Urban Ecosyst 21, 1113–1122 (2018). https://doi.org/10.1007/s11252-018-0793-3

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