Diversity and composition of pollen loads carried by pollinators are primarily driven by insect traits, not floral community characteristics.

Foraging behavior Heterospecific pollen Pollen transport Pollination Specialization

Journal

Oecologia
ISSN: 1432-1939
Titre abrégé: Oecologia
Pays: Germany
ID NLM: 0150372

Informations de publication

Date de publication:
May 2021
Historique:
received: 29 11 2020
accepted: 29 03 2021
pubmed: 12 4 2021
medline: 26 5 2021
entrez: 11 4 2021
Statut: ppublish

Résumé

Flowering plants require conspecific pollen to reproduce but they often also receive heterospecific pollen, suggesting that pollinators carry mixed pollen loads. However, little is known about drivers of abundance, diversity or composition of pollen carried by pollinators. Are insect-carried pollen loads shaped by pollinator traits, or do they reflect available floral resources? We quantified pollen on 251 individual bees and 95 flies in a florally diverse community. We scored taxonomic order, sex, body size, hairiness and ecological specialization of pollinators, and recorded composition of available flowers. We used phylogenetically controlled model selection to compare relative influences of pollinator traits and floral resources on abundance, diversity and composition of insect-carried pollen. We tested congruence between composition of pollen loads and available flowers. Pollinator size, specialization and type (female bee, male bee, or fly) described pollen abundance, diversity and composition better than floral diversity. Pollen loads varied widely among insects (10-80,000,000 grains, 1-16 species). Pollen loads of male bees were smaller, but vastly more diverse than those of female bees, and equivalent in size but modestly more diverse than those of flies. Pollen load size and diversity were positively correlated with body size but negatively correlated with insect ecological specialization. These traits also drove variation in taxonomic and phylogenetic composition of insect-carried pollen loads, but composition was only weakly congruent with available floral resources. Qualities of pollinators best predict abundance and diversity of carried pollen indicating that functional composition of pollinator communities may be important to structuring heterospecific pollen transfer among plants.

Identifiants

pubmed: 33839922
doi: 10.1007/s00442-021-04911-0
pii: 10.1007/s00442-021-04911-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

131-143

Subventions

Organisme : National Science Foundation
ID : DEB 1452386

Références

Alarcón R (2010) Congruence between visitation and pollen-transport networks in a California plant-pollinator community. Oikos 119:35–44. https://doi.org/10.1111/j.1600-0706.2009.17694.x
doi: 10.1111/j.1600-0706.2009.17694.x
Arceo-Gómez G, Abdala-Roberts L, Jankowiak A et al (2016) Patterns of among- and within-species variation in heterospecific pollen receipt: the importance of ecological generalization. Am J Bot 103:396–407. https://doi.org/10.3732/ajb.1500155
doi: 10.3732/ajb.1500155 pubmed: 26507115
Arceo-Gómez G, Kaczorowski RL, Ashman T-L (2018) A network approach to understanding patterns of co-flowering in diverse communities. Int J Plant Sci 179:569–582. https://doi.org/10.1086/698712
doi: 10.1086/698712
Ashman T-L, Arceo-Gómez G (2013) Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am J Bot 100:1061–1070. https://doi.org/10.3732/ajb.1200496
doi: 10.3732/ajb.1200496 pubmed: 23624924
Ashman T-L, Alonso C, Parra-Tabla V et al (2020a) Pollen on stigmas as proxies of pollinator competition and facilitation: complexities, caveats and future directions. Ann Bot 125:1003–1012. https://doi.org/10.1093/aob/mcaa012
doi: 10.1093/aob/mcaa012 pubmed: 31985008
Ashman T-L, Arceo-Gómez G, Bennett JM et al (2020b) Is heterospecific pollen receipt the missing link in understanding pollen limitation of plant reproduction? Am J Bot 107:845–847. https://doi.org/10.1002/ajb2.1477
doi: 10.1002/ajb2.1477 pubmed: 32445398
Bartoń K (2019). MuMIn: multi-model inference. R package version 1.43.15. https://CRAN.R-project.org/package=MuMIn
Biddick M, Burns KC (2018) Phenotypic trait matching predicts the topology of an insular plant–bird pollination network. Integ Zoo 13:339–347. https://doi.org/10.1111/1749-4877.12319
doi: 10.1111/1749-4877.12319
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:1–12. https://doi.org/10.1186/1472-6785-6-9
doi: 10.1186/1472-6785-6-9
Brosi BJ (2016) Pollinator specialization: from the individual to the community. New Phytol 210:1190–1194. https://doi.org/10.1111/nph.13951
doi: 10.1111/nph.13951 pubmed: 27038018
Cane J, Sipes S (2006) Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Ollerton J, Waser NM (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago
Chesters D (2017) Construction of a species-level tree of life for the insects and utility in taxonomic profiling. Syst Biol 66:426–439
pubmed: 27798407 pmcid: 5837528
Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press
Dormann CF (2011) How to be a specialist? Quantifying specialisation in pollination networks. Net Biol 1:1–20
Dormann CF, Gruber B, Fruend J (2008) Introducing the bipartite P package: analyzing ecological networks. R news 8:8–11
Ebeling A, Klein AM, Tscharntke T (2011) Plant-flower visitor interaction webs: temporal stability and pollinator specialization increases along an experimental plant diversity gradient. Basic Appl Ecol 12:300–309. https://doi.org/10.1016/j.baae.2011.04.005
doi: 10.1016/j.baae.2011.04.005
Eckhardt M, Haider M, Dorn S et al (2014) Pollen mixing in pollen generalist solitary bees: a possible strategy to complement or mitigate unfavourable pollen properties? J Animal Ecol 83:588–597. https://doi.org/10.1111/1365-2656.12168
doi: 10.1111/1365-2656.12168
Ellis AG, Johnson SD (2012) Lack of floral constancy by bee fly pollinators: implications for ethological isolation in an African daisy. Behav Ecol 23:729–734. https://doi.org/10.1093/beheco/ars019
doi: 10.1093/beheco/ars019
Fang Q, Huang SQ (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94:1176–1185. https://doi.org/10.1890/12-1634.1
doi: 10.1890/12-1634.1 pubmed: 23858657
Fowler AE, Stone EC, Irwin RE et al (2020) Sunflower pollen reduces a gut pathogen in worker and queen but not male bumble bees. Ecol Ent 45:1318–1326
doi: 10.1111/een.12915
Fründ J, Linsenmair KE, Blüthgen N (2010) Pollinator diversity and specialization in relation to flower diversity. Oikos 119:1581–1590. https://doi.org/10.1111/j.1600-0706.2010.18450.x
doi: 10.1111/j.1600-0706.2010.18450.x
Garland T, Bennett AF, Rezende EL (2005) Phylogenetic approaches in comparative physiology. J Exp Biol 208:3015–3035. https://doi.org/10.1242/jeb.01745
doi: 10.1242/jeb.01745 pubmed: 16081601
Gomez JM, Bosch J, Perfectti F et al (2008) Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proc R Soc B 275:2241–2249
doi: 10.1098/rspb.2008.0512
Goulnik J, Plantureux S, Van Reeth C et al (2020) Facial area and hairiness of pollinators visiting semi-natural grassland wild plants predict their facial pollen load. Ecol Ent. https://doi.org/10.1111/een.12913
doi: 10.1111/een.12913
Goulson D, Darvill B (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35:55–63. https://doi.org/10.1051/apido
doi: 10.1051/apido
Goulson D, Wright NP (1998) Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae). Behav Ecol 9:213–219. https://doi.org/10.1093/beheco/9.3.213
doi: 10.1093/beheco/9.3.213
Hayes R, Cullen N, Kaczorowski R, et al. (2020). A community-wide description and key of pollen from co-flowering plants of the serpentine seeps of California. Madroño. In review
Hinchliff CE, Smith SA, Allman JF et al (2015) Synthesis of phylogeny and taxonomy into a comprehensive tree of life. PNAS 112:12764–12769
doi: 10.1073/pnas.1423041112
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Meth Ecol Evol 7:1451–1456
doi: 10.1111/2041-210X.12613
Johnson AL, Ashman TL (2018) Consequences of invasion for pollen transfer and pollination revealed in a tropical island ecosystem. New Phytol 221:142–154. https://doi.org/10.1111/nph.15366
doi: 10.1111/nph.15366 pubmed: 30084201
Kaluza BF, Wallace H, Keller A et al (2017) Generalist social bees maximize diversity intake in plant species-rich and resource-abundant environments. Ecosphere 8:e01758. https://doi.org/10.1002/ecs2.1758
doi: 10.1002/ecs2.1758
Kassambara A (2020). Ggpubr:“ggplot2” based publication ready plots. R package version 0.4.0
Kendall LK, Rader R, Gagic V et al (2019) Pollinator size and its consequences: robust estimates of body size in pollinating insects. Ecol Evol 9:1702–1714. https://doi.org/10.1002/ece3.4835
doi: 10.1002/ece3.4835 pubmed: 30847066 pmcid: 6392396
Koski MH, Meindl GA, Arceo-Gómez G et al (2015) Plant–flower visitor networks in a serpentine metacommunity: assessing traits associated with keystone plant species. Arthro Plant Inter 9:9–21. https://doi.org/10.1007/s11829-014-9353-9
doi: 10.1007/s11829-014-9353-9
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
doi: 10.1128/AEM.71.12.8228-8235.2005 pubmed: 16332807 pmcid: 1317376
Lucas A, Bodger O, Brosi BJ et al (2018) Generalisation and specialisation in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding. J Anim Ecol 87:1008–1021. https://doi.org/10.1111/1365-2656.12828
doi: 10.1111/1365-2656.12828 pubmed: 29658115 pmcid: 6032873
Lüdecke D (2020) Sjplot: data visualization for statistics in social science. R package version 2(8):4
McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217
doi: 10.1371/journal.pone.0061217
Michonneau F, Brown JW, Winter DJ (2016) Rotl: an R package to interact with the open tree of life data. Meth Ecol Evol 7:1476–1481
doi: 10.1111/2041-210X.12593
Miller-Struttmann NE, Geib JC, Franklin JD et al (2015) Functional mismatch in a bumble bee pollination mutualism under climate change. Science 349:1541–1544
doi: 10.1126/science.aab0868
Minnaar C, Anderson B, de Jager ML et al (2018) Plant-pollinator interactions along the pathway to paternity. Ann Bot 123:225–245. https://doi.org/10.1093/aob/mcy167
doi: 10.1093/aob/mcy167 pmcid: 6344347
Müller A, Diener S, Schnyder S et al (2006) Quantitative pollen requirements of solitary bees: implications for bee conservation and the evolution of bee-flower relationships. Biol Conser 130:604–615. https://doi.org/10.1016/j.biocon.2006.01.023
doi: 10.1016/j.biocon.2006.01.023
Nandi T, Karmakar P (2018) Apis mellifera pollen loads to understand the pollen foraging pattern used for apicultural practice in a potentially agricultural belt in. Revista de Biol Trop. 66:1597–1605. https://doi.org/10.15517/rbt.v66i4.32697
doi: 10.15517/rbt.v66i4.32697
Ne’emanShavitShaltielShmida GOLA (2006) Foraging by male and female solitary bees with implications for pollination. J Insect Behav 19:383–401. https://doi.org/10.1007/s10905-006-9030-7
doi: 10.1007/s10905-006-9030-7
Oksanen J, Blanchet FG, Friendly M, et al. (2019) Vegan: community ecology package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
doi: 10.1111/j.1600-0706.2010.18644.x
Orford KA, Vaughan IP, Memmott J (2015) The forgotten flies: the importance of non-syrphid diptera as pollinators. Proc R Soc B 282:20142934
doi: 10.1098/rspb.2014.2934
Paradis E, Schliep K (2018) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinform 35:526–528
doi: 10.1093/bioinformatics/bty633
Phillips RD, Peakall R, van der Niet T, Johnson SD (2020) Niche perspectives on plant–pollinator interactions. TPS 25:779–793
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2019). Nlme: linear and nonlinear mixed effects models_. R package version 3.1–140, <URL: https://CRAN.R-project.org/package=nlme >
Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J Plant Ecol 9:233–239
doi: 10.1093/jpe/rtv047
R Core Team (2020). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Rader R, Edwards W, Westcott DA et al (2011) Pollen transport differs among bees and flies in a human-modified landscape. Diver Distrib 17:519–529. https://doi.org/10.1111/j.1472-4642.2011.00757.x
doi: 10.1111/j.1472-4642.2011.00757.x
Raguso RA (2020) Don’t forget the flies: dipteran diversity and its consequences for floral ecology and evolution. Appl Ent Zool 55:1–7
doi: 10.1007/s13355-020-00668-9
Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Meth Ecol Evol 3:217–223
doi: 10.1111/j.2041-210X.2011.00169.x
Ritchie AD, Ruppel R, Jha S (2016) Generalist behavior describes pollen foraging for perceived oligolectic and polylectic bees. Envir Ent 45:909–919. https://doi.org/10.1093/ee/nvw032
doi: 10.1093/ee/nvw032
Roswell M, Dushoff J, Winfree R (2019) Male and female bees show large differences in floral preference. PLoS ONE 14:e0217714. https://doi.org/10.1371/journal.pone.0214909
doi: 10.1371/journal.pone.0214909
Russo L, Danforth B (2017) Pollen preferences among the bee species visiting apple (Malus pumila) in New York. Apidologie 48:806–820. https://doi.org/10.1007/s13592-017-0525-3
doi: 10.1007/s13592-017-0525-3
Schneider CA, Rasband WS, Eliceiri KW (2012). NIH image to ImageJ: 25 years of image analysis. nature methods (Vol. 9)
Slowikowski K, Schep A, Hughes S, et al. (2020). Package ggrepel. Automatically position non-overlapping text labels with ‘ggplot2
Smith C, Weinman L, Gibbs J, Winfree R (2019) Specialist foragers in forest bee communities are small, social or emerge early. J Anim Ecol 88:1158–1167. https://doi.org/10.1111/1365-2656.13003
doi: 10.1111/1365-2656.13003 pubmed: 31063228
Ssymank A, Kearns CA, Pape T et al (2008) Pollinating flies (Diptera): a major contribution to plant diversity and agricultural production. Biodiversity 9:86–89
doi: 10.1080/14888386.2008.9712892
Stang M, Klinkhamer P, Waser NM et al (2009) Size-specific interaction patterns and size matching in a plant-pollinator interaction web. Ann Bot 103:1459–1469. https://doi.org/10.1093/aob/mcp027
doi: 10.1093/aob/mcp027 pubmed: 19228701 pmcid: 2701768
Switzer CM, Russell AL, Papaj DR et al (2019) Sonicating bees demonstrate flexible pollen extraction without instrumental learning. Curr Zool 65:425–436
doi: 10.1093/cz/zoz013
Thomson JD, Fung HF, Ogilvie JE (2019) Effects of spatial patterning of co-flowering plant species on pollination quantity and purity. Ann Bot 123:303–310. https://doi.org/10.1093/aob/mcy120
doi: 10.1093/aob/mcy120 pubmed: 29947735
Vaudo AD, Patch HM, Mortensen DA et al (2016) Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. PNAS 133:E4035–E4042. https://doi.org/10.1073/pnas.1606101113
doi: 10.1073/pnas.1606101113
Wei N, Kaczorowski RL, Arceo-Gómez G et al (2020) Pollinator niche partitioning and asymmetric facilitation contribute to the maintenance of diversity. BioRxiv. https://doi.org/10.1101/2020.03.02.974022
doi: 10.1101/2020.03.02.974022 pubmed: 33173864 pmcid: 7553159
Wickham H (2016) Ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
doi: 10.1007/978-3-319-24277-4
Willmer PG, Stone GN (2004) Behavioral, ecological, and physiological determinants of the activity patterns of bees. Adv Study Behav 34:347–466
doi: 10.1016/S0065-3454(04)34009-X
Winfree R, Gross BJ, Kremen C (2011) Valuing pollination services to agriculture. Ecol Econ. 71:0–88
doi: 10.1016/j.ecolecon.2011.08.001
Woodcock TS, Larson BM, Kevan PG et al (2014) Flies and flowers II: floral attractants and rewards. J Pollin Ecol 12:63–94. https://doi.org/10.26786/1920-7603(2014)5
doi: 10.26786/1920-7603(2014)5

Auteurs

Nevin Cullen (N)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.

Jing Xia (J)

College of Life Sciences, South-Central University for Nationalities, Wuhan, 430074, China.

Na Wei (N)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.
The Holden Arboretum, Kirtland, OH, 44094, USA.

Rainee Kaczorowski (R)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.

Gerardo Arceo-Gómez (G)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.
Department of Biological Sciences, East Tennessee State University, Johnson, TN, 37614, USA.

Elizabeth O'Neill (E)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.

Rebecca Hayes (R)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.

Tia-Lynn Ashman (TL)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA. tia1@pitt.edu.

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