Abstract
Recent declines in the abundance and diversity of wild bee species have made it important to understand how introduced species such as honey bees contribute to pollinating native plants. In this study, we decoded the waggle dances of Apis mellifera pollen foragers and used DNA barcoding of bee-collected pollen over 17 months to characterize spatio-temporal patterns in recruitment behavior and dietary breadth in a diverse yet fragmented Mediterranean scrub environment. Foragers danced for small, nearby patches of pollen resources during the cool dormant season but danced for 1.6–2.7-fold more distant and more widely dispersed resources during the hot dry season, a time of seasonal drought and floral dearth. Individual foragers collected pollen from a wide variety of species, but colonies focused recruitment on a small subset of common species in flower during each season: 2.7, 6.3, and 10% of all species in bloom during the dormant, growth, and dry seasons, respectively. Pollen foragers danced almost exclusively for cold-adapted native species during the dormant season, equally for native and non-native plants during the short growth season, and primarily for non-native ornamental species during the dry season. Our results suggest that honey bee recruitment behavior and dietary breadth may be influenced by seasonal changes in pollen resources. Furthermore, they indicate that honey bees may be useful in pollinating common native plants, and that non-native ornamental species can provide a major source of colony protein during a seasonal dearth of flowering native species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ackerly DD (2009) Evolution, origin and age of lineages in the Californian and Mediterranean floras. J Biogeogr 36(7):1221–1233. doi:10.1111/J.1365-2699.2009.02097.X
Aebil A, Vaissiere BE, vanEngelsdorp D, Delaplane KS, Roubik DW, Neumann P et al (2012) Back to the future: apis versus non-Apis pollination—a response to Ollerton. Trend Ecol Evol 27(3):142–143. doi:10.1016/j.tree.2011.11.017
Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9(8):968–980. doi:10.1111/J.1461-0248.2006.00927.X
Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19(11):915–918. doi:10.1016/j.cub.2009.03.071
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6(2):396–403. doi:10.1371/Journal.Pbio.0060031
Baddley A, Turner R (2005) spatstat: an R package for analyzing spatial point patterns. J Stat Softw 12(6):1–42
Balfour NJ, Fensome KA, Samuelson EEW, Ratnieks FLW (2015) Following the dance: ground survey of flowers and flower-visiting insects in a summer foraging hotspot identified via honey bee waggle dance decoding. Agric Ecosys Environ 213:265–271. doi:10.1016/j.agee.2015.08.007
Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100(16):9383–9387. doi:10.1073/pnas.1633576100
Baum KA, Rubink WL, Coulson RN, Bryant VM (2004) Pollen selection by feral honey bee (Hymenoptera: Apidae) colonies in a coastal prairie landscape. Environ Entomol 33(3):727–739
Beekman M, Bin Lew J (2008) Foraging in honey bees—when does it pay to dance? Behav Ecol 19(2):255–262. doi:10.1093/Beheco/Arm117
Beekman M, Ratnieks FLW (2000) Long-range foraging by the honey-bee, Apis mellifera L. Funct Ecol 14(4):490–496
Bell DT, Muller CH (1973) Dominance of California annual grasslands by Brassica nigra. Am Midl Nat 90(2):277–299. doi:10.2307/2424453
Bell KL, de Vere N, Keller A, Richardson RT, Gous A, Burgess KS, Brosi BJ (2016) Pollen DNA barcoding: current applications and future prospects. Genome 59(9):629–640. doi:10.1139/gen-2015-0200
Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313(5785):351–354. doi:10.1126/science.1127863
Breeze TD, Bailey AP, Balcombe KG, Potts SG (2011) Pollination services in the UK: how important are honey bees? Agric Ecosyst Environ 142(3–4):137–143. doi:10.1016/j.agee.2011.03.020
Burkle LA, Marlin JC, Knight TM (2013) Plant–pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339(6127):1611–1615. doi:10.1126/science.1232728
Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35(4):445–453
Cooper PD, Schaffer WM, Buchmann SL (1985) Temperature regulation of honey bees (Apis mellifera) foraging in the Sonoran desert. J Exp Biol 114:1–15
Couvillon MJ, Schürch R, Ratnieks FLW (2014) Waggle dance distances as integrative indicators of seasonal foraging challenges. PLoS One. doi:10.1371/journal.pone.0093495
Cowling RM, Rundel PW, Lamont BB, Arroyo MK, Arianoutsou M (1996) Plant diversity in Mediterranean-climate regions. Trends Ecol Evol 11(9):362–366
Danner N, Molitor AM, Schiele S, Hartel S, Steffan-Dewenter I (2016) Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecol Appl 26(6):1920–1929. doi:10.1890/15-1840.1
de Vere N, Rich TCG, Ford CR, Trinder SA, Long C, Moore CW, Satterthwaite D, Davies H, Allainguillaume J, Ronca S, Tatarinova T, Garbett H, Walker K, Wilkinson MJ (2012) DNA barcoding the native flowering plants and conifers of Wales. PLoS One 7:6. doi:10.1371/journal.pone.0037945
Dimou M, Thrasyvoulou A (2007) Seasonal variation in vegetation and pollen collected by honeybees in Thessaloniki, Greece. Grana 46(4):292–299. doi:10.1080/00173130701760718
Donaldson-Matasci MC, Dornhaus A (2012) How habitat affects the benefits of communication in collectively foraging honey bees. Behav Ecol Sociobiol 66(4):583–592. doi:10.1007/S00265-011-1306-Z
Donaldson-Matasci M, Dornhaus A (2014) Dance communication affects consistency, but not breadth, of resource use in pollen-foraging honey bees. PLoS One 9(10):e107527. doi:10.1371/journal.pone.0107527
Donnelly K (1978) Simulations to determine the variance and edge-effect of total nearest neighbour distance. Simulation methods in archaeology. Cambridge University Press, Cambridge
Dornhaus A, Chittka L (2004) Why do honey bees dance? Behav Ecol Sociobiol 55(4):395–401. doi:10.1007/S00265-003-0726-9
Doughty J, Hedderson F, Mccubbin A, Dickinson H (1993) Interaction between a coating-borne peptide of the Brassica pollen grain and stigmatic-S (self-incompatibility) locus-specific glycoproteins. Proc Natl Acad Sci USA 90(2):467–471
Dyer FC (2002) The biology of the dance language. Annu Rev Entomol 47:917–949. doi:10.1146/Annurev.Ento.47.091201.145306
Galimberti A, De Mattia F, Bruni I, Scaccabarozzi D, Sandionigi A, Barbuto M, Casiraghi M, Labra M (2014) A DNA barcoding approach to characterize pollen collected by honey bees. PLoS One. doi:10.1371/journal.pone.0109363
Garbuzov M, Couvillon MJ, Schurch R, Ratnieks FLW (2015a) Honey bee dance decoding and pollen-load analysis show limited foraging on spring-flowering oilseed rape, a potential source of neonicotinoid contamination. Agric Ecosyst Environ 203:62–68. doi:10.1016/j.agee.2014.12.009
Garbuzov M, Schurch R, Ratnieks FL (2015b) Eating locally: dance decoding demonstrates that urban honey bees in Brighton, UK, forage mainly in the surrounding urban area. Urban Ecosyst 18(2):411–418. doi:10.1007/s11252-014-0403-y
Gasith A, Resh VH (1999) Streams in Mediterranean climate regions: abiotic influences and biotic responses to predictable seasonal events. Annu Rev Ecol Syst 30:51–81. doi:10.1146/Annurev.Ecolsys.30.1.51
Godoy O, Richardson DM, Valladares F, Castro-Diez P (2009) Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Ann Bot-London 103(3):485–494. doi:10.1093/Aob/Mcn232
Goulson D (2003) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34:1–26. doi:10.1146/annurev.ecolsys.34.011802.132355
Grant V (1950) The flower constancy of bees. Bot Rev 16(7):379–398
Group CPW (2009) A DNA barcode for land plants. Proc Natl Acad Sci USA 106(31):12794–12797. doi:10.1073/Pnas.0905845106
Hung KLJ, Ascher JS, Gibbs J, Irwin RE, Bolger DT (2015) Effects of fragmentation on a distinctive coastal sage scrub bee fauna revealed through incidental captures by pitfall traps. J Insect Conserv 19(1):175–179. doi:10.1007/s10841-015-9763-8
Kaiser-Bunbury CN, Memmott J, Muller CB (2009) Community structure of pollination webs of Mauritian heathland habitats. Perspect Plant Ecol Evol Syst 11(4):241–254. doi:10.1016/J.Ppees.04.001
Kono Y, Kohn JR (2015) Range and frequency of Africanized honey bees in California (USA). PLoS One 10(9):e0137407. doi:10.1371/journal.pone.0137407
Kress WJ, Erickson DL, Jones FA, Swenson NG, Perez R, Sanjur O, Bermingham E (2009) Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proc Natl Acad Sci USA 106(44):18621–18626. doi:10.1073/Pnas.0909820106
Lightner J (2011) San Diego County native plants, 3rd edn. San Diego Flora, San Diego
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10(8):710–717. doi:10.1111/j.1461-0248.2007.01061.x
Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore
Nieh JC (2010) A negative feedback signal that is triggered by peril curbs honey bee recruitment. Curr Biol 20(4):310–315. doi:10.1016/j.cub.2009.12.060
Okada R, Akamatsu T, Iwata K, Ikeno H, Kimura T, Ohashi M, Aonuma H, Ito E (2012) Waggle dance effect: dancing in autumn reduces the mass loss of a honeybee colony. J Exp Biol 215(10):1633–1641. doi:10.1242/Jeb.068650
Okada R, Ikeno H, Kimura T, Ohashi M, Aonuma H, Ito E (2014) Error in the honeybee waggle dance improves foraging flexibility. Sci Rep-Uk 4:4175. doi:10.1038/Srep04175
Oldroyd BP (2007) What’s killing American honey bees? PLoS Biol 5(6):1195–1199. doi:10.1371/journal.pbio.0050168
Ollerton J, Price V, Armbruster WS, Memmott J, Watts S, Waser NM, Totland O, Goulson D, Alarcon R, Stout JC, Tarrant S (2012) Overplaying the role of honey bees as pollinators: a comment on Aebi and Neumann (2011). Trends Ecol Evol 27(3):141–142. doi:10.1016/j.tree.2011.12.001
Paini DR (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: apidae) on native bees: A review. Austral Ecol 29(4):399–407. doi:10.1111/J.1442-9993.2004.01376.X
Petersen G, Johansen B, Seberg O (1996) PCR and sequencing from a single pollen grain. Plant Mol Biol 31(1):189–191
Potts SG, Petanidou T, Roberts S, O’Toole C, Hulbert A, Willmer P (2006) Plant–pollinator biodiversity and pollination services in a complex Mediterranean landscape. Biol Conserv 129(4):519–529. doi:10.1016/j.biocon.2005.11.019
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010a) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353. doi:10.1016/j.tree.2010.01.007
Potts SG, Roberts SPM, Dean R, Marris G, Brown MA, Jones R, Neumann P, Settele J (2010b) Declines of managed honey bees and beekeepers in Europe. J Apic Res 49(1):15–22. doi:10.3896/IBRA.1.49.1.02
Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions - the role of mutualisms. Biol Rev Camb Philos Soc 75(1):65–93. doi:10.1017/S0006323199005435
Rohr RP, Saavedra S, Bascompte J (2014) On the structural stability of mutualistic systems. Science 345(6195):416. doi:10.1126/science.1253497
San Diego Natural History Museum (2008) San Diego County Plant Atlas. http://www.sdplantatlas.org. Accessed 9 Aug 2009
Schneider SS, Hall HG (1997) Diet selection and foraging distances of African and European-African hybrid honey bee colonies in Costa Rica. Insectes Soc 44(2):171–187
Schneider SS, McNally LC (1993) Spatial foraging patterns and colony energy status in the African honey bee, Apis mellifera scutellata. J Insect Behav 6(2):195–210
Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE, Klotz S, Kuhn I, Moora M, Nielsen A, Ohlemuller R, Petanidou T, Potts SG, Pysek P, Stout JC, Sykes MT, Tscheulin T, Vila M, Walther GR, Westphal C, Winter M, Zobel M, Settele J (2010) Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biol Rev 85(4):777–795. doi:10.1111/J.1469-185x.2010.00125.X
Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge
Sherman G, Visscher PK (2002) Honeybee colonies achieve fitness through dancing. Nature 419(6910):920–922. doi:10.1038/Nature01127
Spivak M, Erickson E (1992) Do measurements of worker cell-size reliably distinguish Africanized from European honey-bees (Apis-Mellifera L). Am Bee J 132(4):252–255
Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured landscapes. P Roy Soc Lond B Bio 270(1515):569–575. doi:10.1098/Rspb.2002.2292
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121
Towne WF, Gould JL (1988) The spatial precision of the honey bee’s dance communication. J Insect Behav 1:129–156
Visscher PK, Seeley TD (1982) Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63(6):1790–1801
von Frisch K (1967) The dance language and orientation of bees. Belknap Press of Harvard University Press, Cambridge
Waddington KD, Visscher PK, Herbert TJ, Richter MR (1994) Comparisons of forager distributions from matched honey bee colonies in suburban environments. Behav Ecol Sociobiol 35(6):423–429
Watanabe ME (1994) Pollination worries rise as honey-bees decline. Science 265(5176):1170. doi:10.1126/Science.265.5176.1170
Weidenmuller A, Seeley TD (1999) Imprecision in waggle dances of the honeybee (Apis mellifera) for nearby food sources: error or adaptation? Behav Ecol Sociobiol 46:190–199
Wilson EE, Sidhu CS, LeVan KE, Holway DA (2010) Pollen foraging behaviour of solitary Hawaiian bees revealed through molecular pollen analysis. Mol Ecol 19(21):4823–4829
Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90(8):2068–2076
Woods WA, Heinrich B, Stevenson RD (2005) Honeybee flight metabolic rate: does it depend upon air temperature? J Exp Biol 208(6):1161–1173. doi:10.1242/Jeb.01510
Acknowledgements
We would like to thank David Holway and Joshua Kohn for their comments on this manuscript and for the comments of the anonymous reviewers, who have significantly improved our manuscript. We are indebted to the help of several research assistants: Erin Hourigan, Emerson Lin, Gee Ryu, Rudolf Scherban, and Alexander Tablante. We would also like to thank the San Diego Natural History Museum for their help with database records.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Park, B., Nieh, J.C. Seasonal trends in honey bee pollen foraging revealed through DNA barcoding of bee-collected pollen. Insect. Soc. 64, 425–437 (2017). https://doi.org/10.1007/s00040-017-0565-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-017-0565-8