Seasonality and Landscape Composition Drive the Diversity of Pollen Collected by Managed Honey Bees

The western honey bee, Apis mellifera, is the most important and widespread managed pollinator species. Honey bee diet is based on nectar and pollen, and pollen diversity and composition, in particular, affect colony health and fitness. As landscape composition is strongly linked to floral resource heterogeneity, it could influence the resource intake of honey bees. This work aimed to explore how the composition of pollen collected by honey bees was modulated by seasonality and landscape composition heterogeneity in a mountainous cultivated area of Northern Italy. We selected 13 locations, and at each location, we placed two honey bee colonies from which we collected pollen samples every month during the whole flowering season for two consecutive years. We then analyzed pollen samples in the laboratory and determined the Shannon diversity index of each pollen sample and the temporal pollen taxon replacement. We extracted the cover of the main habitat types at three spatial scales and tested the effect of landscape diversity and composition using Principal Component Analysis. Honey bees foraged on a high number of floral resources, however, they mostly collected pollen from a small number of taxa, with pollen type composition changing throughout the flowering season. In early spring and late summer, most pollen grains were collected from a few plant species, while from May to August the number of collected pollen types was significantly higher. Landscape composition affected pollen diversity only at the end of the flowering season. While honey bees were able to collect highly diverse pollen throughout spring and summer regardless of landscape composition, in late summer, when pollen collected is fundamental for the overwintering of the colony and its development in the following season, semi-natural areas became crucial for honey bee foraging activities, with pollen diversity increasing with increasing percentages of semi-natural areas. Our research highlighted the importance for honey bees of certain seasonal resources and of semi-natural habitats at the end of the flowering season, which ensure the subsistence of their colonies throughout the year.

[1]  I. Steffan‐Dewenter,et al.  Semi-natural habitats promote winter survival of wild-living honeybees in an agricultural landscape , 2022, Biological Conservation.

[2]  Katherine C. R. Baldock,et al.  Turnover in floral composition explains species diversity and temporal stability in the nectar supply of urban residential gardens , 2022, Journal of Applied Ecology.

[3]  A. Shapcott,et al.  Forest landscapes increase diversity of honeybee diets in the tropics , 2022, Forest Ecology and Management.

[4]  E. Abdel-Rahman,et al.  Pollen diversity and protein content in differentially degraded semi-arid landscapes in Kenya , 2021, Journal of Apicultural Research.

[5]  S. Creer,et al.  Shifts in honeybee foraging reveal historical changes in floral resources , 2021, Communications Biology.

[6]  J C Stout,et al.  Plant protection product residues in plant pollen and nectar: A review of current knowledge. , 2020, Environmental research.

[7]  Peter Martin.  Mohammad El-Labban’s Beekeepers’ Guide for Pollen Identification of Honey , 2020 .

[8]  P. N. Buhl.  The lives of bees: the untold story of the honey bee in the wild , 2020, International Journal of Environmental Studies.

[9]  J. Zalapa,et al.  Surrounding landscape and spatial arrangement of honey bee hives affect pollen foraging and yield in cranberry , 2019 .

[10]  Michael P. Simanonok,et al.  Do the Quality and Quantity of Honey Bee-Collected Pollen Vary Across an Agricultural Land-Use Gradient? , 2019, Environmental Entomology.

[11]  Douglas B. Sponsler,et al.  Characterizing the floral resources of a North American metropolis using a honey bee foraging assay , 2019, bioRxiv.

[12]  Z. Huang,et al.  Seasonal variation of pollen collected by honey bees (Apis mellifera) in developed areas across four regions in the United States , 2019, PloS one.

[13]  L. Garibaldi,et al.  Impacts of honeybee density on crop yield: A meta‐analysis , 2019, Journal of Applied Ecology.

[14]  Philip Donkersley.  Trees for bees , 2019, Agriculture, Ecosystems & Environment.

[15]  M. Schwarz,et al.  Investigating the role of landscape composition on honey bee colony winter mortality: A long-term analysis , 2018, Scientific Reports.

[16]  H. Abou-Shaara.  The foraging behaviour of honey bees, Apis mellifera: a review. , 2018 .

[17]  D. Holway,et al.  The worldwide importance of honey bees as pollinators in natural habitats , 2018, Proceedings of the Royal Society B: Biological Sciences.

[18]  I. Steffan‐Dewenter,et al.  Honey bee foraging ecology: Season but not landscape diversity shapes the amount and diversity of collected pollen , 2017, PloS one.

[19]  M. Woyciechowski,et al.  Ecological stoichiometry of the honeybee: Pollen diversity and adequate species composition are needed to mitigate limitations imposed on the growth and development of bees by pollen quality , 2017, PloS one.

[20]  Mickaël Henry,et al.  A ‘Landscape physiology’ approach for assessing bee health highlights the benefits of floral landscape enrichment and semi-natural habitats , 2017, Scientific Reports.

[21]  J. Odoux,et al.  Variations in the Availability of Pollen Resources Affect Honey Bee Health , 2016, PloS one.

[22]  Mickaël Henry,et al.  Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. , 2015, Ecological applications : a publication of the Ecological Society of America.

[23]  F. Ratnieks,et al.  Eating locally: dance decoding demonstrates that urban honey bees in Brighton, UK, forage mainly in the surrounding urban area , 2015, Urban Ecosystems.

[24]  K. Wilson,et al.  Honeybee nutrition is linked to landscape composition , 2014, Ecology and evolution.

[25]  J. Odoux,et al.  Optimisation d’une méthode de dénombrement de grains de pollen adaptée a l’étude de l’alimentation de l’abeille domestique , 2013 .

[26]  J. Biesmeijer,et al.  Global pollinator declines: trends, impacts and drivers. , 2010, Trends in ecology & evolution.

[27]  K. Crailsheim,et al.  Nutrition and health in honey bees , 2010, Apidologie.

[28]  J. Tautz,et al.  The Buzz about Bees: Biology of a Superorganism , 2008 .

[29]  Ingolf Steffan-Dewenter,et al.  Honeybee foraging in differentially structured landscapes , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  F. Ratnieks,et al.  Long-range foraging by the honey-bee, Apis mellifera L. , 2000 .

[31]  J. Cane,et al.  Pollen nutritional content and digestibility for animals , 2000, Plant Systematics and Evolution.

[32]  R. Morse.  The Dance Language and Orientation of Bees , 1994 .

[33]  N. Koeniger.  The biology of the honey bee , 1988, Insectes Sociaux.

[34]  H. Hepburn,et al.  Honeybees and Wax: An Experimental Natural History , 1986 .

[35]  T. Seeley,et al.  FORAGING STRATEGY OF HONEYBEE COLONIES IN A TEMPERATE DECIDUOUS FOREST , 1982 .

[36]  K. Frisch.  The Dancing Bees: An Account of the Life and Senses of the Honey Bee , 1961 .

[37]  A. Lourenço,et al.  Pollen nutrition in honey bees (Apis mellifera): impact on adult health , 2015, Apidologie.

[38]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[39]  D. Goulson,et al.  Decline and conservation of bumble bees. , 2008, Annual review of entomology.

[40]  Jürgen Tautz,et al.  The Buzz about Bees , 2008 .

[41]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[42]  P. Visscher.  Foraging strategy of honey bee colonies in a temperate deciduous forest. , 1982 .

[43]  Karl von Frisch,et al.  The dancing bees , 1955 .