Pollen carryover between sequential foraging trips by a solitary bee: Implications for distant outcrossing

Authors

  • James H Cane USDA-ARS Bee Biology Lab
  • Byron Love

DOI:

https://doi.org/10.26786/1920-7603(2018)15

Abstract

Animal pollination depends on foragers moving pollen between conspecific flowers and plants. Pollinating bees often exhibit patch fidelity and frequent grooming during a foraging trip, which results in intensely localized pollen carryover. If their host’s seed dispersal is likewise limited, then spatial mosaics of small genetic neighbourhoods should result. However, spatial distributions of genetic markers of seeds often reveal infrequent long-distance gene flow mediated by pollinating bees, seemingly at odds with expectations of bees’ local patch fidelity and suggesting an additional mechanism at work.

A greenhouse experiment that used nesting Osmia californica bees foraging at sunflowers tested the pollination fate of any bodily pollen that lingers on females even after they discharge a pollen load at their nest. Once a provisioning female had returned to her nest, we moved the nest with her inside from a cage with male-fertile sunflowers to a cage with male-sterile sunflowers. There females quickly resumed foraging. They nearly always pollinated and set seed at the first male-sterile flowerhead that they visited, the result of fertile bodily pollen carried over from the previous foraging trip. Every visit to a second male-sterile flowerhead set additional seed.

If, as seems likely, outbound nesting females sometimes switch between host patches, then this mechanism of pollen carryover could explain occasional distant pollen-mediated gene flow events, as summarizes in a graphic model. Carryover should mitigate inbreeding depression in threatened plant populations, or conversely, sometimes contaminate seed crops, with relevance for spatially isolating foundation seed fields and coexistence of GMO and conventional crops.

References

Allison PD (2012) Logistic regression using SAS: Theory and application. SAS Institute, Cary, North Carolina USA.

Bassani M, Pacini E, Franchi GG (1994) Humidity stress responses in pollen of anemophilous and entomophilous species. Grana 33:146-150.

Beekman M, Ratnieks F (2000) Long-range foraging by the honey-bee, Apis mellifera L. Functional Ecology 14:490-496.

Bosch J (1994) The nesting behaviour of the mason bee Osmia cornuta (Latr.) with special reference to its pollinating potential (Hymenoptera, Megachilidae). Apidologie 25:84-93.

Bosch J, Blas M (1994) Foraging behaviour and pollination efficiency of Osmia cornuta and Apis mellifera on almond (Hymenoptera, Megachilidae and Apidae). Applied Entomology and Zoology 29:1-9.

Bradner NR, Frakes RV, Stephen WP (1965) Effects of bee species and isolation distance on possible varietal contamination in alfalfa. Agronomy Journal 57:247-248.

Cane JH (2011) Specialist Osmia bees forage indiscriminately among hybridizing Balsamorhiza floral hosts. Oecologia 167:107-116.

Cane JH (2017) Specialist bees collect Asteraceae pollen by distinctive abdominal drumming (Osmia) or tapping (Melissodes, Svastra). Arthropod-Plant Interactions 11:257-261.

Castellanos MC, Wilson P, Thomson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57:2742-2752.

Cavalcante MC, Oliveira FF, Maues MM, Freitas BM (2012) Pollination requirements and the foraging behaviour of potential pollinators of cultivated Brazil Nut (Bertholletia excelsa Bonpl.) trees in central Amazon rainforest. Psyche 2012:1-9.

Clark JS, Lewis M, Horvath L (2001) Invasion by extremes: population spread with variation in dispersal and reproduction. The American Naturalist 157:537-554.

Cresswell JE, Bassom AP, Bell SA, Collins SJ, Kelly TB (1995) Predicted pollen dispersal by honey-bees and three species of bumble-bees foraging on oil-seed rape: a comparison of three models. Functional Ecology 9:829-841.

Cresswell JE, Osborne JL, Bell SA (2002) A model of pollinator-mediated gene flow between plant populations with numerical solutions for bumblebees pollinating oilseed rape. Oikos 98:375-384.

Cripps C, Rust RW (1989) Pollen preferences of seven Osmia species (Hymenoptera: Megachilidae). Environmental Entomology 18:133-138.

DeGrandi-Hoffman G, Hoopingarner R, Klomparens K (1986) Influence of honey bee (Hymenoptera: Apidae) in-hive pollen transfer on cross-pollination and fruit set in apple. Environmental Entomology 15:723-725.

Dick CW, Etchelecu G, Austerlitz F (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Molecular Ecology 12:753-764.

Fenster CB, Vekemans X, Hardy OJ (2003) Quantifying gene flow from spatial genetic structure data in a metapopulation of Chamaecrista fasciculata (Leguminosae). Evolution 57:995-1007.

Franchi GG, Piotto B, Nepi M, Baskin CC, Baskin JM, Pacini E (2011) Pollen and seed desiccation tolerance in relation to degree of developmental arrest, dispersal, and survival. Journal of Experimental Botany 62:5267-5281.

Free JB, Durrant AJ (1966) The transport of pollen by honeybees from one foraging trip to the next. Journal of Horticultural Science 41:87-89.

Frohlich DR, Tepedino VJ (1986) Sex ratio, parental investment, and interparent variability in nesting success in a solitary bee. Evolution 40:142-151.

Goodell K (2003) Food availability affects Osmia pumila (Hymenoptera: Megachilidae) foraging, reproduction, and brood parasitism. Oecologia 134:518-527.

Greene SL, Kesoju SR, Martin RC, Kramer M (2015) Occurrence of transgenic feral alfalfa (Medicago sativa subsp. sativa L.) in alfalfa seed production areas in the United States. Plos One 10:e0143296.

Handel SN (1983) Contrasting gene flow patterns and genetic subdivision in adjacent populations of Cucumis sativus (Cucurbitaceae). Evolution 37:760-771.

Hatjina F, Free JB, Paxton RJ (1999) Hive-entrance pollen transfer devices to increase the cross-pollination potential of honey bees. II. Examination of three materials and pollen viability. Journal of Apicultural Research 38:3-9.

Holmquist K, Mitchell RJ, Karron JD (2012) Influence of pollinator grooming on pollen-mediated gene dispersal in Mimulus ringens (Phrymaceae). Plant Species Biology 27:77-85.

Jha S, Dick CW (2010) Native bees mediate long-distance pollen dispersal in a shade coffee landscape mosaic. Proceedings of the National Academy of Sciences 107:13760-13764.

Kohn JR, Casper BB (1992) Pollen-mediated gene flow in Cucurbita foetidissima (Cucurbitaceae). American Journal of Botany 79:57-62.

Loper GM, DeGrandi-Hoffman G (1994) Does in-hive pollen transfer by honey bees contribute to cross-pollination and seed set in hybrid cotton? Apidologie 25:94-102.

Maeta Y (1978) Comparative studies on the biology of the bees of the genus Osmia of Japan, with special reference to their managements for pollinations of crops (Hymenoptera: Megachilidae). Bulletin of the Tohoku National Agricultural Experiment Station 57:195-209.

Matsumoto S, Abe A, Maejima T (2009) Foraging behaviour of Osmia cornifrons in an apple orchard. Scientia Horticulturae 121:73-79.

Neff JL (2008) Components of nest provisioning behaviour in solitary bees (Hymenoptera : Apoidea). Apidologie 39:30-45.

O'Malley DM, Buckley DP, Prance GT, Bawa KS (1988) Genetics of Brazil nut (Bertholletia excelsa Humb. & Bonpl.: Lecythidaceae). 2. Mating system. Theoretical and Applied Genetics 76:929-932.

Osborne JL, Clark SJ, Morris RJ, Williams IH, Riley JR, Smith AD, Reynolds DR, Edwards AS (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. Journal of Applied Ecology 36:519-533.

Otero-Arnaiz A, Casas A, Hamrick JL (2005) Direct and indirect estimates of gene flow among wild and managed populations of Polaskia chichipe, an endemic columnar cactus in Central Mexico. Molecular Ecology 14:4313-4322.

Parker AJ, Tran JL, Ison JL, Bai JD, Weis AE, Thomson JD (2015) Pollen packing affects the function of pollen on corbiculate bees but not non-corbiculate bees. Arthropod-Plant Interactions 9:197-203.

Parker FD, Frohlich DR (1983) Hybrid sunflower pollination by a manageable composite specialist: the sunflower leafcutter bee (Hymenoptera: Megachilidae). Environmental Entomology 12:576-581.

Paschke M, Abs C, Schmid B (2002) Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae). American Journal of Botany 89:1250-1259.

Pasquet RS, Peltier A, Hufford MB, Oudin E, Saulnier J, Paul L, Knudsen JT, Herren HR, Gepts P (2008) Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proceedings of the National Academy of Sciences 105:13456-13461.

Phillips JK, Klostermeyer EC (1978) Nesting behaviour of Osmia lignaria propinqua Cresson (Hymenoptera: Megachilidae). Journal of the Kansas Entomological Society 51:91-108.

Rasmussen IR, Brodsgaard B (1992) Gene flow inferred from seed dispersal and pollinator behaviour compared to DNA analysis of restriction site variation in a patchy population of Lotus corniculatus L. Oecologia 89:277-283.

Rieger MA, Lamond M, Preston C, Powles SB, Roush RT (2002) Pollen-mediated movement of herbicide resistance between commercial canola fields. Science 296:2386-2388.

Schulke B, Waser NM (2001) Long-distance pollinator flights and pollen dispersal between populations of Delphinium nuttallianum. Oecologia 127:239-245.

Seeley TD (1995) The wisdom of the hive. Harvard Univ. Press, Cambridge, MA.

St.Armand PC, Skinner DZ, Peaden RN (2000) Risk of alfalfa transgene dissemination and scale-dependent effects. Theoretical and Applied Genetics 101:107-114.

Tepedino VJ, Sipes SD, Griswold TL (1999) The reproductive biology and effective pollinators of the endangered beardtongue Penstemon penlandii (Scrophulariaceae). Plant Systematics and Evolution 219:39-54.

Thomson JD (1986) Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. Journal of Ecology 74:329-341.

Thomson JD, Price MV, Waser NM, Stratton DA (1986) Comparative studies of pollen and fluorescent dye transport by bumble bees visiting Erythronium grandiflorum. Oecologia 69:561-566.

Thomson JD, Thomson BA (1989) Dispersal of Erythronium grandiflorum pollen by bumblebees: implications for gene flow and reproductive success. Evolution 43:657-661.

Torchio PF (1989) In-nest biologies and development of immature stages of three Osmia species (Hymenoptera: Megachilidae). Annals of the Entomological Society of America 82:599-615.

Van Deynze AE, Fitzpatrick SM, Hammon B, McCaslin MH, Putnam DH, Teuber LR, Undersander DJ (2008) Gene flow in alfalfa: biology, mitigation, and potential impact on production. Council for Agricultural Science and Technology Special Publ. no. 28, Ames, Iowa .

Van Deynze AE, Sundstrom FJ, Bradford KJ (2005) Pollen-mediated gene flow in California cotton depends on pollinator activity. Crop Science 45:1565-1570.

von Frisch K (1967) The Dance Language and Orientation of Bees. Harvard Univ. Press, Cambridge.

Waddington KD (1979) Flight patterns of three species of sweat bees (Halictidae) foraging at Convolvulus arvensis. Journal of the Kansas Entomological Society 52:751-758.

Ward M, Dick CW, Gribel R, Lowe AJ (2005) To self, or not to self... A review of outcrossing and pollen-mediated gene flow in neotropical trees. Heredity 95:246-254.

Waser NM (1982) A comparison of distances flown by different visitors to flowers of the same species. Oecologia 55:251-257.

Waser NM (1988) Comparative pollen and dye transfer by pollinators of Delphinium nelsonii. Functional Ecology 2:41-48.

Woodgate JL, Makinson JC, Lim KS, Reynolds AM, Chittka L (2016) Life-long radar tracking of bumblebees. Plos One 11:e0160333.

Zurbuchen A, Cheesman S, Klaiber J, Müller A, Hein S, Dorn S (2010a) Long foraging distances impose high costs on offspring production in solitary bees. Journal of Animal Ecology 79:674-681.

Zurbuchen A, Landert L, Klaiber J, Müller A, Hein S, Dorn S (2010b) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biological Conservation 143:669-676.

Downloads

Published

2019-01-23

How to Cite

Cane, J. H., & Love, B. (2019). Pollen carryover between sequential foraging trips by a solitary bee: Implications for distant outcrossing. Journal of Pollination Ecology, 24, 136–143. https://doi.org/10.26786/1920-7603(2018)15

Issue

Section

Articles