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Food in a row: urban trees offer valuable floral resources to pollinating insects

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Abstract

Urbanization affects the availability and diversity of floral resources (pollen and/or nectar) for wild pollinating insects. For example, urban green areas are characterized by an abundance of ornamental plant species. Increasingly, trees are planted to improve the aesthetics of urban streets and parks. These urban trees might offer important floral resources to pollinating insects. To examine the suitability of urban trees as resources for pollinating insects, we investigated the chemical composition of pollen and nectar as well as the amount of nectar produced by the nine major insect-pollinated tree species planted in cities of Western Europe, namely Acer pseudoplatanus, Aesculus carnea, A. hippocastanum, Robinia pseudoacacia, Tilia cordata, T. x euchlora, T. x europaea, T. platyphyllos and T. tomentosa. The analyses revealed that globally the Tilia trees provide pollen with lower contents of polypeptides, amino acids and phytosterols compared with the other species. Urban tree flowers offer abundant nectar with relatively high sugar contents (0.16–1.28 mg/flower); sucrose was the predominant sugar in all nectars. The investigated tree species could therefore be considered in future city plantings.

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References

  • Acar C, Acar H, Eroğlu E (2007) Evaluation of ornamental plant resources to urban biodiversity and cultural changing: A case study of residential landscapes in Trabzon city (Turkey). Build Environ 42:218–229

    Article  Google Scholar 

  • Ahrné K, Bengtsson J, Elmqvist T (2009) Bumble bees (Bombus spp) along a gradient of increasing urbanization. PLoS One 4:e5574

    Article  PubMed  PubMed Central  Google Scholar 

  • Alton K, Ratnieks F (2013) To bee or not to bee. Biologist 60:12–15

    Google Scholar 

  • Anderson GJ (1976) The pollination biology of Tilia. Am J Bot 63:1203–1212

    Article  Google Scholar 

  • Baldock KCR, Goddard MA, Hicks DM, et al. (2015) Where is the UK’s pollinator biodiversity? the importance of urban areas for flower-visiting insects. Proc R Soc London B: Biol Sci 282:2014–2849

    Article  Google Scholar 

  • Banaszak-Cibicka W, Żmihorski M (2012) Wild bees along an urban gradient: winners and losers. J Insect Conserv 16:331–343

    Article  Google Scholar 

  • Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ (2011) Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS One 6:e23459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batra SWT (1985) Red maple (Acer rubrum L.), an important early spring food resource for honey bees and other insects. J Kansas Entomol Soc 58:169–172

    Google Scholar 

  • Baude M, Kunin WE, Boatman ND, Conyers S, Davies N, Gillespie MA, Morton RD, Smart SM, Memmott JL (2016) Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530:85–88. doi:10.1038/nature16532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruxelles Environnement (2003) Rapport de synthèse sur l’état de l’environnement en Région de Bruxelles-Capitale - Edition 2002, Bruxelles

  • Burke JM, Wyatt R, dePamphilis CW, Arnold ML (2000) Nectar characteristics of interspecific hybrids and their parents in Aesculus (Hippocastanaceae) and Iris (Iridaceae). J Torrey Bot Soc 127:200–206

    Article  Google Scholar 

  • Cawoy V, Jonard M, Mayer C, Jacquemart A-L (2012) Do abundance and proximity of the alien Impatiens glandulifera affect pollination and reproductive success of two sympatric co-flowering native species? J Poll Ecol 10:130–139

    Google Scholar 

  • Cierjacks A, Kowarik I, Joshi J, Hempel S, Ristow M, von der Lippe M, Weber E (2013) Biological flora of the British Isles: Robinia pseudoacacia. J Ecol 101:1623–1640

    Article  Google Scholar 

  • Cnaani J, Thomson JD, Papaj DR (2006) Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112:278–285

    Article  Google Scholar 

  • Collins J, Kinzig A, Grimm N, Fagan W, Hope D, Wu J, Borer E (2000) A new urban ecology. Am Sci 88:416–425

    Article  Google Scholar 

  • Comba L, Corbet SA, Barron A, Bird A, Collinge S, Miyazaki N, Powell M (1999a) Garden flowers: insect visits and the floral reward of horticulturally-modified variants. Ann Bot 83:73–86

    Article  Google Scholar 

  • Comba L, Corbet SA, Hunt L, Warren B (1999b) Flowers, nectar and insect visits: evaluating British plant species for pollinator-friendly gardens. Ann Bot 83:369–383

    Article  Google Scholar 

  • Corbet SA (2003) Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34:1–10

    Article  CAS  Google Scholar 

  • Corbet SA, Bee J, Dasmahapatra K, Gale S, Gorringe E, La Ferla B, Moorhouse T, Trevail A, Van Bergen Y, Vorontsova M (2001) Native or exotic? Double or single? evaluating plants for pollinator-friendly gardens. Ann Bot 87:219–232

    Article  Google Scholar 

  • Couvillon MJ, Schürch R, Ratnieks FLW (2014) Waggle dance distances as integrative indicators of seasonal foraging challenges. PLoS One 9:e93495

    Article  PubMed  PubMed Central  Google Scholar 

  • Crane E (1977) Dead bees under lime trees. Bee World 58:129–130

    Article  Google Scholar 

  • Dafni A, Kevan PG, Husband BC (eds) (2005) Practical pollination biology. Enviroquest, Cambridge, Ontario, Canada

    Google Scholar 

  • Detzel A, Wink M (1993) Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:8–18

    Article  CAS  Google Scholar 

  • Dicks LV, Baude M, Roberts SPM, Phillips J, Green M, Carvell C (2015) How much flower-rich habitat is enough for wild pollinators? Answering a key policy question with incomplete knowledge. Ecol Entomol 40:22–35

    Article  PubMed  PubMed Central  Google Scholar 

  • Eckhardt M, Haider M, Dorn S, Müller A (2014) Pollen mixing in pollen generalist solitary bees: a possible strategy to complement or mitigate unfavourable pollen properties? J Anim Ecol 83:588–597

    Article  PubMed  Google Scholar 

  • Everaars J, Strohbach MW, Gruber B, Dormann CF (2011) Microsite conditions dominate habitat selection of the red mason bee (Osmia bicornis, Hymenoptera: Megachilidae) in an urban environment: A case study from Leipzig, Germany. Landsc Urban Plan 103:15–23

    Article  Google Scholar 

  • Frankie GW, Thorp RW, Schindler M, Hernandez J, Ertter B, Rizzardi M (2005) Ecological patterns of bees and their host ornamental flowers in two Northern California cities. J Kansas Entomol Soc 78:227–246

    Article  Google Scholar 

  • Garbuzov M, Ratnieks FLW (2014) Quantifying variation among garden plants in attractiveness to bees and other flower-visiting insects. Funct Ecol 28:364–374

    Article  Google Scholar 

  • Génissel A, Aupinel P, Bressac C, Tasei JN, Chevrier C (2002) Influence of pollen origin on performance of Bombus terrestris micro-colonies. Entomol Exper Applic 104:329–336

    Article  Google Scholar 

  • Gonzalez-Teuber M, Heil M (2009) Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Pl Signal Behav 4:809–813

    Article  CAS  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • Goulson D (2009) Bumble bees: behaviour, ecology, and conservation, 2nd edn. Oxford University Press, USA

    Google Scholar 

  • Goulson D, Darvill B (2004) Niche overlap and diet breadth in bumblebees. are rare species more specialized in their choice of flowers? Apidologie 35:55–63

    Article  Google Scholar 

  • Goulson D, Hughes W, Derwent L, Stout J (2002) Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130:267–273

    Article  Google Scholar 

  • Goulson D, Sparrow KR (2008) Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size. J Insect Conserv 13:177–181

    Article  Google Scholar 

  • Gunnarsson B, Federsel LM (2014) Bumble bees in the city: abundance, species richness and diversity in two urban habitats. J Insect Conserv 18:1185–1191

    Article  Google Scholar 

  • Haaland C, Gyllin M (2010) Butterflies and bumblebees in greenways and sown wildflower strips in Southern Sweden. J Insect Conserv 14:125–132

    Article  Google Scholar 

  • Hanley ME, Awbi AJ, Franco M (2014) Going native? flower use by bumblebees in English urban gardens. Ann Bot 113:799–806

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanley ME, Franco M, Pichon S, Darvill B, Goulson D (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct Ecol 22:592–598

    Article  Google Scholar 

  • Harmon-Threatt AN, Kremen C (2015) Bumble bees selectively use native and exotic species to maintain nutritional intake across highly variable and invaded local floral resource pools. Ecol Entomol 40:471–478

    Article  Google Scholar 

  • Hernandez J, Frankie G, Thorp R (2009) Ecology of urban bees: a review of current knowledge and directions for future study. Cities and the Environment 2:2–15

    Article  Google Scholar 

  • Hunter MR, Hunter MD (2008) Designing for conservation of insects in the built environment. Insect Conserv Div 1:189–196

    Google Scholar 

  • Janson EM, Grebenok RJ, Behmer ST, Abbot P (2009) Same host-plant, different sterols: variation in sterol metabolism in an insect herbivore community. J Chem Ecol 35:1309–1319

    Article  CAS  PubMed  Google Scholar 

  • Kaluza BF, Wallace H, Heard TA, Klein AM, Leonhardt SD (2016) Urban gardens promote bee foraging over natural habitats and plantations. Ecol Evol 6:1304–1316

  • Käpylä M (1978) Amount and type of nectar sugar in some wild flowers in Finland. Ann Bot Fenn 15:85–88

    Google Scholar 

  • Kevan PG (1990) How large bees, Bombus and Xylocopa (Apoidea Hymenoptera) forage on trees: optimality and patterns of movement in temperate and tropical climates. Ethol Ecol Evol 2:233–242

    Article  Google Scholar 

  • Kitaoka TK, Nieh JC (2009) Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav Ecol Sociobiol 63:625–625

    Article  Google Scholar 

  • Krasenbrink A, Popp M, Denker B (1994) Nektarzusammensetzung von Tilia tomentosa (Moench) und anderen Lindenarten/−hybriden. Z. Okologie und Naturschutz 3:237–242

    Google Scholar 

  • Lambinon J, Verloove F (2012) Nouvelle Flore de Belgique, du Grand-Duché de Luxembourg, du Nord de la France et des régions voisines, 6th edn. Meise, Belgium

    Google Scholar 

  • Macior LW (1978) Pollination ecology of vernal Angiosperms. Oikos 30:452–460

    Article  Google Scholar 

  • Matteson KC, Langellotto GA (2010) Determinates of inner city butterfly and bee species richness. Urban Ecosyst 13:333–347

    Article  Google Scholar 

  • McFrederick QS, Le Buhn G (2006) Are urban parks refuges for bumble bees Bombus spp. (Hymenoptera: Apidae)? Biol Conserv 129:372–382

    Article  Google Scholar 

  • McKinney ML (2008) Effects of urbanization on species richness: A review of plants and animals. Urban Ecosyst 11:161–176

    Article  Google Scholar 

  • Moquet L, Mayer C, Michez D, Wathelet B, Jacquemart AL (2015) Early spring floral foraging resources for pollinators in wet heathlands in Belgium. J Insect Conserv 19:837–848

    Article  Google Scholar 

  • Naef R, Jaquier A, Velluz A, Bachofen B (2004) Fron the linden flower to linden honey - volatile constituents of linden nectar, and extract of bee-stomach and ripe honey. Chem Biodivers 1:1870–1879

    Article  CAS  PubMed  Google Scholar 

  • Nicolson SW (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr Zool 46:197–204

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2013). Vegan: community ecology package. R package version 2.0–9.http://CRAN.R-project.org/package=vegan. Accessed: 2014 July 20

  • Pauleit S, Jones N, Garcia-Martin G, Garcia-Valdecantos JL, Rivière LM, Vidal-Beaudet L, Bodson M, Randrup T (2002) Tree establishment practice in towns and cities – results from a European survey. Urban For Urban Green 1:83–96

    Article  Google Scholar 

  • Pawelek J, Frankie G, Thorp R, Przybylski M (2009) Modification of a community garden to attract native bee pollinators in urban San Luis Obispo, California. Cities and the Environment 2:7–21

    Article  Google Scholar 

  • Pawlikowski T (2010) Pollination activity of bees (Apoidea: Apiformes) visiting the flowers of Tilia cordata Mill. and Tilia tomentosa Moench in an urban environment. J Apic Sci 54:73–79

    Google Scholar 

  • Percival MS (1961) Types of nectar in Angiosperms. New Phytol 60:235–281

    Article  Google Scholar 

  • Pigott C (2012) Lime-trees and basswoods: a biological monograph of the genus Tilia. Cambridge Univ Press, Cambridge, UK

    Book  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Potts SG, Roberts S, Dean R, Marris G, Brown M, Jones R, Neumann P, Settele J (2010b) Declines of managed honey bees and beekeepers in Europe. J Apic Res 49:134–136

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org

  • Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209

    Article  CAS  Google Scholar 

  • Salisbury A, Armitage J, Bostock H, Perry J, Tatchell M, Thompson K (2015) Enhancing gardens as habitats for flower-visiting aerial insects (pollinators): should we plant native or exotic species? J Appl Ecol 52:1156–1164

    Article  CAS  Google Scholar 

  • Sedivy C, Müller A, Dorn S (2011) Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: evidence for physiological adaptations to digest pollen. Funct Ecol 25:718–725

    Article  Google Scholar 

  • Singaravelan N, Inbar M, Ne’eman G, Distl M, Wink M (2006) The effects of nectar-nicotine on colony fitness of caged honeybees. J Chem Ecol 32:49–59

    Article  CAS  PubMed  Google Scholar 

  • Sirohi MH, Jackson J, Edwards M, Ollerton J (2015) Diversity and abundance of solitary and primitively eusocial bees in an urban centre: a case study from Northampton (England). J Insect Conserv 19:487–500

    Article  Google Scholar 

  • Sjöman H, Gunnarsson A, Pauleit S, Bothmer R (2012a) Selection approach of urban trees for inner-city environments: learning from nature. Arboricult Urban For 38:194–204

    Google Scholar 

  • Sjöman H, Östberg J, Bühler O (2012b) Diversity and distribution of the urban tree population in ten major Nordic cities. Urban For Urban Green 11:31–39

    Article  Google Scholar 

  • Somme L, Vanderplanck M, Michez D, Lombaerde I, Moerman R, Wathelet B, Wattiez R, Lognay G, Jacquemart AL (2015) Pollen and nectar quality drive the major and minor floral choices of bumble bees. Apidologie 46:92–106

    Article  Google Scholar 

  • Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542

    Article  CAS  PubMed  Google Scholar 

  • Tasei JN, Aupinel P (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumble bee workers (Bombus terrestris, Hymenoptera: Apidae). Apidologie 39:397–409

    Article  CAS  Google Scholar 

  • Tedeschini E, Rodriguez-Rajo FJ, Caramiello R, Jato V, Frenguelli G (2006) The influence of climate changes in Platanus spp. pollination in Spain and Italy. Grana 45:222–229

    Article  Google Scholar 

  • Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85:458–470

    Article  Google Scholar 

  • Vanderplanck M, Leroy B, Wathelet B, Wattiez R, Michez D (2014a) Standardized protocol to evaluate pollen polypeptides as bee food source. Apidologie 45:192–204

    Article  CAS  Google Scholar 

  • Vanderplanck M, Michez D, Vancraenenbroeck S, Lognay G (2011) Micro-quantitative method for analysis of sterol levels in honeybees and their pollen loads. Anal Lett 44:1807–1820

    Article  CAS  Google Scholar 

  • Vanderplanck M, Moerman R, Rasmont P, Lognay G, Wathelet B, Wattiez R, Michez D (2014b) How does pollen chemistry impact development and feeding behaviour of polylectic bees? PLoS One 9:e86209

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Curr Opin Insect Sci 10:133–141

    Article  Google Scholar 

  • Vervoort A, Cawoy V, Jacquemart AL (2011) Comparative reproductive biology in co-occurring invasive and native Impatiens species. Int J Plant Sci 172:366–377

    Article  Google Scholar 

  • Villette C, Berna A, Compagnon V, Schaller H (2015) Plant sterol diversity in pollen from Angiosperms. Lipids 50:749–760

    Article  CAS  PubMed  Google Scholar 

  • Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, USA

    Google Scholar 

  • Weiner CN, Hilpert A, Werner M, Linsenmair KE, Blüthgen N (2010) Pollen amino acids and flower specialisation in solitary bees. Apidologie 41:476–487

    Article  Google Scholar 

  • Weryszko-Chmielewska E, Tietze M, Michońska M (2012) Ecological features of the flowers of Aesculus hippocastanum L. and characteristics of Aesculus L. pollen seasons under the conditions of Central-Eastern Poland. Acta Agrobot 65:61–68

    Article  Google Scholar 

  • Williams IH, Carreck N, Little DJ (1993) Nectar sources for honey bees and the movement of honey bee colonies for crop pollination and honey production in England. Bee World 74:160–175

    Article  Google Scholar 

  • Winfree R, Aguilar R, Vázquez DP, Le Buhn G, Aizen MA (2009) A Meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076

    Article  PubMed  Google Scholar 

  • Wojcik VA, Frankie GW, Thorp RW, Hernandez JL (2008) Seasonality in bees and their floral resource plants at a constructed urban bee habitat in Berkeley, California. J Kansas Entomol Soc 81:15–28

    Article  Google Scholar 

  • Wykes GR (1952) An investigation of the sugars present in the nectar of flowers of various species. New Phytol 51:210–215

    Article  Google Scholar 

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Acknowledgments

We thank D. Geerinck, V. Decoux (Bruxelles Mobilité), S. Kempeneers (Bruxelles Environnement) and M. Wollast (ApisBruoc’Sella) for site identification. We are grateful to N. Roger, C. Buyens, and I. Van de Vreken for technical assistance, L. C. Kouonon for field assistance, R. Wattiez (Proteomics and Biochemistry of Proteins, University of Mons) and Bernard Wathelet (Industrial Biological Chemistry Unit, University of Liège) for granting access to their lab, and M. Warnier (Centre Apicole de Recherche et d’Information, Louvain-la-Neuve) for nectar analyses. We thank A. Valster and N. R. Hoffmann (Plant Editors cooperative) for language improvement, and two anonymous reviewers for their valuable comments on a previous version of the manuscript. MV holds a “Chargé de Recherches” fellowship (Fonds National de la Recherche Scientifique, Belgium). This work was supported by Innoviris, Brussels (contract BB2B 2012-2-15, post-doc grant for L.C. Kouonon).

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  1. Earth and Life Institute, Research Group Genetics, Reproduction, Populations, Université catholique de Louvain, Croix du Sud 2, Box L7 05 14, 1348, Louvain-la-Neuve, Belgium

    Laurent Somme, Laura Moquet, Muriel Quinet & Anne-Laure Jacquemart

  2. Laboratory of Zoology, Research Institute of Biosciences, Université de Mons, Place du Parc 23, 7000, Mons, Belgium

    Maryse Vanderplanck & Denis Michez

  3. Laboratory of Analytical Chemistry, Gembloux Agro-Bio Tech, Université de Liège, Passage des Déportés 2, 5030, Gembloux, Belgium

    Georges Lognay

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  1. Laurent Somme
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  2. Laura Moquet
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Somme, L., Moquet, L., Quinet, M. et al. Food in a row: urban trees offer valuable floral resources to pollinating insects. Urban Ecosyst 19, 1149–1161 (2016). https://doi.org/10.1007/s11252-016-0555-z

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