A screening-level assessment of the pollinator-attractiveness of ornamental nursery stock using a honey bee foraging assay.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
21 01 2020
21 01 2020
Historique:
received:
11
07
2019
accepted:
06
01
2020
entrez:
23
1
2020
pubmed:
23
1
2020
medline:
25
11
2020
Statut:
epublish
Résumé
In urban and suburban landscapes characterized by extensive designed greenspaces, the support of pollinator communities hinges significantly on floral resources provided by ornamental plants. The attractiveness of ornamental plants to pollinators, however, cannot be presumed, and some studies suggest that a majority of ornamental plant varieties receive little or no pollinator visitation. Here, we harness the sampling power of the western honey bee, a generalist pollinator whose diet breadth overlaps substantially with that of other pollinators, to survey the utilization of ornamental plants grown at three commercial nurseries in Connecticut, USA. Using a combination of DNA metabarcoding and microscopy, we identify, to genus-level, pollen samples from honey bee colonies placed within each nursery, and we compare our results with nursery plant inventories to identify the subset of cultivated genera that were visited during pollen foraging. Samples were collected weekly from May to September, encompassing the majority of the growing season. Our findings show that some plant genera known to be cultivated as ornamentals in our system, particularly ornamental trees and shrubs (e.g. Hydrangea, Rosa, Spiraea, Syringa, Viburnum), functioned as major pollen sources, but the majority of plants inventoried at our nurseries provided little or no pollen to honey bees. These results are in agreement with a growing body of literature highlighting the special importance of woody plants as resources for flower-visiting insects. We encourage further exploration of the genera highlighted in our data as potential components of pollinator-friendly ornamental greenspace.
Identifiants
pubmed: 31965017
doi: 10.1038/s41598-020-57858-2
pii: 10.1038/s41598-020-57858-2
pmc: PMC6972849
doi:
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
831Références
Quigley, M. F. Potemkin gardens: Biodiversity in small designed landscapes. In Urban Ecology: Patterns, Processes, and Applications (ed. Niemelä, J.) 85–91 (Oxford University Press, 2011).
Bascompte, J. & Jordano, P. Plant-Animal Mutualistic Networks: The Architecture of Biodiversity. Annu. Rev. Ecol. Evol. Syst. 38, 567–593 (2007).
doi: 10.1146/annurev.ecolsys.38.091206.095818
IPBES. The Assessment Report on Pollinators, Pollination and Food Production. ((IPBES) Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, 2016).
Roulston, T. H. & Goodell, K. The role of resources and risks in regulating wild bee populations. Annu. Rev. Entomol. 56, 293–312 (2011).
doi: 10.1146/annurev-ento-120709-144802
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).
doi: 10.1126/science.1255957
Hall, D. M. et al. The city as a refuge for insect pollinators. Conserv. Biol. 31, 24–29 (2017).
doi: 10.1111/cobi.12840
Baldock, K. C. R. et al. A systems approach reveals urban pollinator hotspots and conservation opportunities. Nat. Ecol. Evol. 3, 363–373 (2019).
doi: 10.1038/s41559-018-0769-y
Ornamental Crops (ed. J. Van Huylenbroeck). (Springer, 2018).
Corbet, S. A. et al. Native or Exotic? Double or Single? Evaluating Plants for Pollinator-friendly Gardens. Ann. Bot. 87, 219–232 (2001).
doi: 10.1006/anbo.2000.1322
Comba, L. et al. Garden Flowers: Insect Visits and the Floral Reward of Horticulturally-modfied Variants. Ann. Bot. 83, 73–86 (1999).
doi: 10.1006/anbo.1998.0798
Garbuzov, M., Alton, K. & Ratnieks, F. L. W. Most ornamental plants on sale in garden centres are unattractive to flower-visiting insects. PeerJ 5, e3066 (2017).
doi: 10.7717/peerj.3066
Garbuzov, M. & Ratnieks, F. L. W. Using the British National Collection of Asters to Compare the Attractiveness of 228 Varieties to Flower-Visiting Insects. Environ. Entomol. 44, 638–646 (2015).
doi: 10.1093/ee/nvv037
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, 700–705 (2015).
doi: 10.1111/1744-7917.12162
Garbuzov, M. & Ratnieks, F. L. W. Quantifying variation among garden plants in attractiveness to bees and other flower-visiting insects. Funct. Ecol. 28, 364–374 (2014).
doi: 10.1111/1365-2435.12178
Lowenstein, D. M., Matteson, K. C. & Minor, E. S. Evaluating the dependence of urban pollinators on ornamental, non-native, and ‘weedy’ floral resources. Urban Ecosyst. 22, 293–302 (2019).
doi: 10.1007/s11252-018-0817-z
Goulson, D. Effects of Introduced Bees on Native Ecosystems. Annu. Rev. Ecol. Evol. Syst. 34, 1–26 (2003).
doi: 10.1146/annurev.ecolsys.34.011802.132355
National Plant Data Team. PLANTS database. (USDA-NRCS, 2019).
Couvillon, M. J., Schürch, R. & Ratnieks, F. L. W. Waggle Dance Distances as Integrative Indicators of Seasonal Foraging Challenges. PLoS One 9, e93495 (2014).
doi: 10.1371/journal.pone.0093495
Ayers, G. S. & Harman, J. R. Bee forage of North America and the potential for planting for bees. The Hive and the Honey Bee 437–493 (1992).
Mach, B. M. & Potter, D. A. Quantifying bee assemblages and attractiveness of flowering woody landscape plants for urban pollinator conservation. PLoS One 13, e0208428 (2018).
doi: 10.1371/journal.pone.0208428
Donkersley, P. et al. Nutritional composition of honey bee food stores vary with floral composition. Oecologia 185, 749–761 (2017).
doi: 10.1007/s00442-017-3968-3
Richardson, R. T. et al. Application of ITS2 Metabarcoding to Determine the Provenance of Pollen Collected by Honey Bees in an Agroecosystem. Appl. Plant Sci. 3, 1400066 (2015).
doi: 10.3732/apps.1400066
Odoux, J.-F. et al. Territorial biodiversity and consequences on physico-chemical characteristics of pollen collected by honey bee colonies. Apidologie 43, 561–575 (2012).
doi: 10.1007/s13592-012-0125-1
Donkersley, P. Trees for bees. Agric. Ecosyst. Environ. 270-271, 79–83 (2019).
doi: 10.1016/j.agee.2018.10.024
King, M. J. & Buchmann, S. L. Bumble bee-initiated vibration release mechanism of rhododendron pollen. Am. J. Bot. 82, 1407–1411 (1995).
doi: 10.1002/j.1537-2197.1995.tb12677.x
Schneider, E. L. & Chaney, T. The floral biology of Nymphaea. Southwest. Nat. 26, 159–165 (1981).
doi: 10.2307/3671112
Nicolson, S. W. Water homeostasis in bees, with the emphasis on sociality. J. Exp. Biol. 212, 429–434 (2009).
doi: 10.1242/jeb.022343
Bryant, V. M. & Jones, G. D. The r‐values of honey: Pollen coefficients. Palynology 25, 11–28 (2001).
Leonhardt, S. D. & Blüthgen, N. The same, but different: pollen foraging in honeybee and bumblebee colonies. Apidologie 43, 449–464 (2012).
doi: 10.1007/s13592-011-0112-y
Heeger, F. et al. Long-read DNA metabarcoding of ribosomal RNA in the analysis of fungi from aquatic environments. Mol. Ecol. Resour. 18, 1500–1514 (2018).
doi: 10.1111/1755-0998.12937
Crampton-Platt, A., Yu, D. W., Zhou, X. & Vogler, A. P. Mitochondrial metagenomics: letting the genes out of the bottle. Gigascience 5, 15 (2016).
doi: 10.1186/s13742-016-0120-y
Smart, M. D. et al. A Comparison of Honey Bee-Collected Pollen From Working Agricultural Lands Using Light Microscopy and ITS Metabarcoding. Environ. Entomol., https://doi.org/10.1093/ee/nvw159 (2017).
Keller, A. et al. Evaluating multiplexed next-generation sequencing as a method in palynology for mixed pollen samples. Plant Biol. 17, 558–566 (2015).
doi: 10.1111/plb.12251
Richardson, R. T. et al. Quantitative multi-locus metabarcoding and waggle dance interpretation reveal honey bee spring foraging patterns in Midwest agroecosystems. Mol. Ecol., https://doi.org/10.1111/mec.14975 (2018).
doi: 10.1111/mec.14975
Rosenzweig, M. L. W-win Ecology: How the Earth’s Species Can Survive in the Midst of Human Enterprise. (Oxford University Press, 2003).
Tallamy, D. W. Bringing Nature Home: How You Can Sustain Wildlife with Native Plants, Updated and Expanded. (Timber Press, 2009).
Miller, J. R. Biodiversity conservation and the extinction of experience. Trends Ecol. Evol. 20, 430–434 (2005).
doi: 10.1016/j.tree.2005.05.013
Stoner, K. A., Cowles, R. S., Nurse, A. & Eitzer, B. D. Tracking Pesticide Residues to a Plant Genus Using Palynology in Pollen Trapped from Honey Bees (Hymenoptera: Apidae) at Ornamental Plant Nurseries. Environ. Entomol. 48, 351–362 (2019).
doi: 10.1093/ee/nvz007
Sickel, W. et al. Increased efficiency in identifying mixed pollen samples by meta-barcoding with a dual-indexing approach. BMC Ecol. 15, 20 (2015).
doi: 10.1186/s12898-015-0051-y
Cheng, T. et al. Barcoding the kingdom Plantae: new PCR primers for ITS regions of plants with improved universality and specificity. Mol. Ecol. Resour. 16, 138–149 (2016).
doi: 10.1111/1755-0998.12438
Berry, D., Ben Mahfoudh, K., Wagner, M. & Loy, A. Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification. Appl. Environ. Microbiol. 77, 7846–7849 (2011).
doi: 10.1128/AEM.05220-11
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. & Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol, https://doi.org/10.1128/AEM.01043-13 (2013).
doi: 10.1128/AEM.01043-13
Sherril-Mix, S. taxonomizr: Functions to Work with NCBI Accessions and Taxonomy. R package version 0.5.3, https://CRAN.R-project.org/package=taxonomizr (2019).
Richardson, R. T., Sponsler, D. B., McMinn-Sauder, H. & Johnson, R. M. MetaCurator: A hidden Markov model-based toolkit for extracting and curating sequences from taxonomically-informative genetic markers. bioRxiv 672782, https://doi.org/10.1101/672782 (2019).
Eddy, S. R. Accelerated Profile HMM Searches. PLoS Comput. Biol. 7, e1002195 (2011).
doi: 10.1371/journal.pcbi.1002195
Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).
doi: 10.7717/peerj.2584
Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, (614–620 (2014).
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL, https://www.R-project.org/ (2019).
Faegri, K., Kaland, P. E. & Krzywinski, K. Textbook of pollen analysis. (John Wiley & Sons Ltd., 1989).
Crompton, C. W., Wojtas, W. A. & Others. Pollen grains of Canadian honey plants. (Agriculture Canada and Canada Communication Group-Publishing, 1993).
McAndrews, J. H., Berti, A. A. & Norris, G. Key to the Quaternary pollen and spores of the Great Lakes region. (Royal Ontario Museum, Toronto, 1973).
O’Rourke, M. K. & Buchmann, S. L. Standardized Analytical Techniques for Bee-Collected Pollen. Environ. Entomol. 20, 507–513 (1991).
doi: 10.1093/ee/20.2.507