Seasonality of floral resources in relation to bee activity in agroecosystems

Abstract The contribution of wild insects to crop pollination is becoming increasingly important as global demand for crops dependent on animal pollination increases. If wild insect populations are to persist in agricultural landscapes, there must be sufficient resources over time and space. The temporal, within‐season component of floral resource availability has rarely been investigated, despite growing recognition of its likely importance for pollinator populations. Here, we examined the visitation rates of common bee genera and the spatiotemporal availability of floral resources in agroecosystems over one season to determine whether local wild bee activity was limited by landscape floral resource abundance, and if so, whether it was limited by the present or past abundance of landscape floral resources. Visitation rates and landscape floral resources were measured in 27 agricultural sites in Ontario and Québec, Canada, across four time periods and three spatial scales. Floral resources were determined based on species‐specific floral volume measurements, which we found to be highly correlated with published measurements of nectar sugar mass and pollen volume. Total floral volume at varying spatial scales predicted visits for commonly observed bee genera. We found Lasioglossum and Halictus visits were highest in landscapes that provided either a stable or increasing amount of floral resources over the season. Andrena visits were highest in landscapes with high floral resources at the start of the season, and Bombus visits appeared to be positively related to greater cumulative seasonal abundance of floral resources. These findings together suggest the importance of early‐season floral resources to bees. Megachile visits were negatively associated with the present abundance of floral resources, perhaps reflecting pollinator movement or dilution. Our research provides insight into how seasonal fluctuations in floral resources affect bee activity and how life history traits of bee genera influence their responses to food availability within agroecosystems.

[1]  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.

[2]  J. Memmott,et al.  Phenology of farmland floral resources reveals seasonal gaps in nectar availability for bumblebees , 2019, Journal of Applied Ecology.

[3]  O. Olsson,et al.  Flowering resources distract pollinators from crops: Model predictions from landscape simulations , 2019, Journal of Applied Ecology.

[4]  N. Loeuille.  Faculty Opinions recommendation of Historical nectar assessment reveals the fall and rise of floral resources in Britain. , 2019, Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature.

[5]  Kyle T. Martins,et al.  Complementary crops and landscape features sustain wild bee communities. , 2018, Ecological applications : a publication of the Ecological Society of America.

[6]  Casper W. Berg,et al.  glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling , 2017, R J..

[7]  Jane E. Ogilvie,et al.  Interactions between bee foraging and floral resource phenology shape bee populations and communities. , 2017, Current opinion in insect science.

[8]  M. Vilà,et al.  Mass‐flowering crops dilute pollinator abundance in agricultural landscapes across Europe , 2016, Ecology letters.

[9]  Lauren C. Ponisio,et al.  Hedgerow presence does not enhance indicators of nest‐site habitat quality or nesting rates of ground‐nesting bees , 2016 .

[10]  Mark A. Goddard,et al.  Food for Pollinators: Quantifying the Nectar and Pollen Resources of Urban Flower Meadows , 2016, PloS one.

[11]  J. Field,et al.  Social polymorphism in the sweat bee Lasioglossum (Evylaeus) calceatum , 2016, Insectes Sociaux.

[12]  N. Williams,et al.  Bumble bee colony dynamics: quantifying the importance of land use and floral resources for colony growth and queen production. , 2016, Ecology letters.

[13]  A. Crespí,et al.  Evaluation of native plant flower characteristics for conservation biological control of Prays oleae , 2016, Bulletin of Entomological Research.

[14]  C. Gratton,et al.  Diverse landscapes have a higher abundance and species richness of spring wild bees by providing complementary floral resources over bees’ foraging periods , 2016, Landscape Ecology.

[15]  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.

[16]  I. Steffan‐Dewenter,et al.  Maize pollen foraging by honey bees in relation to crop area and landscape context , 2014 .

[17]  R. Bommarco,et al.  Late-season mass-flowering red clover increases bumble bee queen and male densities , 2014 .

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

[19]  T. Tscharntke,et al.  Contrasting effects of mass-flowering crops on bee pollination of hedge plants at different spatial and temporal scales. , 2013, Ecological applications : a publication of the Ecological Society of America.

[20]  Alana L. Burley,et al.  A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. , 2013, Ecology letters.

[21]  J. Baudry,et al.  Solitary bee abundance and species richness in dynamic agricultural landscapes , 2013 .

[22]  C. Kremen,et al.  Complementary habitat use by wild bees in agro-natural landscapes. , 2012, Ecological applications : a publication of the Ecological Society of America.

[23]  J. Regetz,et al.  Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. , 2012, Ecology.

[24]  J. Sivinski,et al.  Conserving natural enemies with flowering plants: Estimating floral attractiveness to parasitic Hymenoptera and attraction’s relationship to flower and plant morphology , 2011 .

[25]  D. Bebber,et al.  The Circe Principle Explains How Resource-Rich Land Can Waylay Pollinators in Fragmented Landscapes , 2011, Current Biology.

[26]  Jane Memmott,et al.  Sampling method influences the structure of plant–pollinator networks , 2011 .

[27]  S. Potts,et al.  Conservation ecology of bees: populations, species and communities , 2009, Apidologie.

[28]  L. Packer,et al.  Leafcutter and mason bees of the genus Megachile Latreille (Hymenoptera: Megachilidae) in Canada and Alaska , 2011 .

[29]  K. Goodell,et al.  The role of resources and risks in regulating wild bee populations. , 2011, Annual review of entomology.

[30]  J. Neff,et al.  The evolution of a pollen diet: Host choice and diet breadth of Andrena bees (Hymenoptera: Andrenidae) , 2011, Apidologie.

[31]  S. Dorn,et al.  Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances , 2010 .

[32]  J. Baudoin,et al.  Reproductive biology of the andromonoecious Cucumis melo subsp. agrestis (Cucurbitaceae). , 2009, Annals of botany.

[33]  V. Larraz,et al.  Nectar exploitation by herbivores and their parasitoids is a function of flower species and relative humidity. , 2009 .

[34]  T. Tscharntke,et al.  Mass flowering oilseed rape improves early colony growth but not sexual reproduction of bumblebees , 2009 .

[35]  Y. Bayoumi,et al.  The value of honey bees (Apis mellifera, L.) as pollinators of summer seed watermelon (Citrullus lanatus colothynthoides L.) in Egypt. , 2009 .

[36]  J. Ledent,et al.  Floral Biology of Common Buckwheat (Fagopyrum esculentum Moench) , 2009 .

[37]  Jeff Ollerton,et al.  Year‐to‐year variation in the topology of a plant–pollinator interaction network , 2008 .

[38]  G. Daily,et al.  Optimal design of agricultural landscapes for pollination services , 2008 .

[39]  E. Smets,et al.  Comparative pollen morphology and ultrastructure of Mentheae subtribe Nepetinae (Lamiaceae) , 2008 .

[40]  J. Ascher,et al.  Bee Richness and Abundance in New York City Urban Gardens , 2008 .

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

[42]  L. Packer.  The Bee Genera of Eastern Canada , 2007 .

[43]  Sarah S. Greenleaf,et al.  Bee foraging ranges and their relationship to body size , 2007, Oecologia.

[44]  J. Ledent,et al.  Morph Differences and Honeybee Morph Preference in the Distylous Species Fagopyrum esculentum Moench , 2006, International Journal of Plant Sciences.

[45]  S. Diener,et al.  Quantitative pollen requirements of solitary bees: Implications for bee conservation and the evolution of bee–flower relationships , 2006 .

[46]  R. Morse,et al.  Nectar and pollen production in pumpkin (Cucurbita pepo L.) , 2006 .

[47]  J. Cane.  Bees, pollination, and the challenges of sprawl , 2005 .

[48]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[49]  L. Harder,et al.  Sexual reproduction and variation in floral morphology in an ephemeral vernal lily, Eyythronium americanum , 1985, Oecologia.

[50]  Neal M. Williams,et al.  Crop pollination from native bees at risk from agricultural intensification , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Teja Tscharntke,et al.  SCALE‐DEPENDENT EFFECTS OF LANDSCAPE CONTEXT ON THREE POLLINATOR GUILDS , 2002 .

[52]  J. C. Semple,et al.  The biology of Canadian weeds. 113. Symphyotrichum lanceolatum (Willd.) Nesom [Aster lanceolatus Willd.] and S. lateriflorum (L.) Löve & Löve [Aster lateriflorus (L.) Britt.] , 2001 .

[53]  T. Ashman,et al.  Dissecting the causes of variation in intra-inflorescence allocation in a sexually polymorphic species, Fragaria virginiana (Rosaceae). , 2000, American journal of botany.

[54]  J Memmott,et al.  The structure of a plant-pollinator food web. , 1999, Ecology letters.

[55]  Katrina M. Dlugosch,et al.  Nectar and hostplant scarcity limit populations of an endangered Oregon butterfly , 1999, Oecologia.

[56]  Michael J. Hutchings,et al.  Glechoma hederacea L. (Nepeta glechoma Benth., N. hederacea (L.) Trev.) , 1999 .

[57]  V. Kosenko.  Contributions to the pollen morphology and taxonomy of the Liliaceae , 1999 .

[58]  W. Wcislo.  The Evolution of Social Behavior in Insects and Arachnids: Behavioral environments of sweat bees (Halictinae) in relation to variability in social organization , 1997 .

[59]  E. Grafius,et al.  Wildflowers as Nectar Sources for Diadegma insulare (Hymenoptera: Ichneumonidae), a Parasitoid of Diamondback Moth (Lepidoptera: Yponomeutidae) , 1995 .

[60]  K. Holl.  Nectar Resources and Their Influence on Butterfly Communities on Reclaimed Coal Surface Mines , 1995 .

[61]  L. Packer,et al.  Annual variation in survival and reproduction of the primitively eusocial sweat bee Halictus ligatus (Hymenoptera: Halictidae) , 1995 .

[62]  P. Kevan,et al.  FORAGING DYNAMICS OF PEPONAPIS PRUINOSA (HYMENOPTERA: ANTHOPHORIDAE) ON PUMPKIN (CUCURBITA PEPO) IN SOUTHERN ONTARIO , 1995, The Canadian Entomologist.

[63]  C. E. Caviness,et al.  Natural Cross‐Pollination of Twelve Soybean Cultivars in Arkansas , 1994 .

[64]  M. Nepi,et al.  Pollination, Pollen Viability and Pistil Receptivity in Cucurbita pepo , 1993 .

[65]  R. Primack,et al.  Seasonal changes in sexual allocation within flowers of Chelidonium majus (Papaveraceae) , 1991 .

[66]  C. Messersmith,et al.  The biology of Canadian weeds. 94. Sonchus arvensis L. , 1990 .

[67]  L. Harder,et al.  THE BUMBLE BEES OF EASTERN CANADA , 1988, The Canadian Entomologist.

[68]  R. Hebda,et al.  Pollen morphology of the Rosaceae of western Canada. II: Dryas, Fragaria, Holodiscus , 1988 .

[69]  I. V. Hall,et al.  THE BIOLOGY OF CANADIAN WEEDS.: 84. Oenothera biennis L. , 1988 .

[70]  O. Pellmyr.  The Pollination Biology of Actaea pachypoda and A. rubra (Including A. erythrocarpa) in Northern Michigan and Finland , 1985 .

[71]  Lawrence D. Harder,et al.  Morphology as a Predictor of Flower Choice by Bumble Bees , 1985 .

[72]  J. V. van Damme.  Gynodioecy in Plantago lanceolata L. III. Sexual reproduction and the maintenance of male steriles , 1984 .

[73]  R. D. Sweet,et al.  THE BIOLOGY OF CANADIAN WEEDS.: 58. Galinsoga parviflora and G. quadriradiata (= G. ciliata). , 1983 .

[74]  Janet R. Sullivan.  COMPARATIVE REPRODUCTIVE BIOLOGY OF ACER PENSYLVANICUM AND A. SPICATUM (ACERACEAE) , 1983 .

[75]  W. Laberge.  The Zoogeography of Andrena Fabricus (Hymenoptera: Andrenidae) of the Western Hemisphere , 1983 .

[76]  R. M. Arnold.  Pollination, Predation, and seed set in Linaria vulgaris (Scrophulariaceae) , 1982 .

[77]  P. B. Cavers,et al.  The biology of Canadian weeds. 47. Plantago lanceolata L. , 1980 .

[78]  E. Erickson,et al.  Wild Bees on Soybeans, Glycine max , 1980 .

[79]  R. Cruden,et al.  VISCIN THREADS, POLLINATION EFFICIENCY AND LOW POLLEN‐OVULE RATIOS , 1979 .

[80]  J. Shannon,et al.  Honey Bee Pollination Increases Soybean Yields in the Mississippi Delta Region of Arkansas and Missouri , 1978 .

[81]  R. Cruden.  POLLEN‐OVULE RATIOS: A CONSERVATIVE INDICATOR OF BREEDING SYSTEMS IN FLOWERING PLANTS , 1977, Evolution; international journal of organic evolution.

[82]  B. Heinrich.  Resource Partitioning Among Some Eusocial Insects: Bumblebees , 1976 .

[83]  D. Biesboer.  Pollen Morphology of the Aceraceae , 1975 .

[84]  U. Olsson.  A Biometric Study of the Pollen Morphology of Linaria Vulgaris (L.) Miller and L. Repens (L.) Miller (Schrophulariaceae) and their Hybrid Progeny in F1 and F2 Generations , 1974 .

[85]  P. D. Hurd,et al.  Ecology of the squash and gourd bee, Peponapis pruinosa, on cultivated cucurbits in California (Hymenoptera: Apoidea) , 1974 .

[86]  T. B. Mitchell.  Bees of the Eastern United States , 1960 .