Estimating pollinator performance of visitors to the self-incompatible crop-plant Brassica rapa by single visit deposition and pollen germination: a comparison of methods.

Authors

  • Robert Brian Patchett University of St Andrews
  • Gavin Ballantyne Edinburgh Napier Uiversity
  • Patricia Gillian Willmer University of St Andrews

DOI:

https://doi.org/10.26786/1920-7603(2017)420

Abstract

Estimating the pollen-deposition effectiveness of flower visitors is fundamental to understanding their performance as pollinators. While estimates of visitation rates, pollen loads, and single visit deposition (SVD) are all useful proxies for performance, and so help to reveal the relative effectiveness of different visitors, none take into account the breeding system of the plants, or the quality of pollen deposited. Here we compare the performance of visitors to the self-incompatible plant Brassica rapa (turnip) using SVD and pollen germination. We also report the first use of the staining of Brassica rapa stigma papilla cells (known to reveal a specific reaction to self-pollen) to compare self-pollen deposition between insect visitors. We found that most of the pollen grains deposited by insect visitors (and therefore counted by SVD methods) were non-germinating self-pollen. A smaller proportion of grains were outcrossed and so germinated. There was also a significant positive relationship between environmental conditions (wind speed) and pollen deposition, but not pollen germination.

Both methods identified Bombus spp. as the best-performing visitors on turnip flowers, followed by Eristalis spp., whereas performance estimates for Episyrphus balteatus and ‘other hoverflies’ were no higher than controls for both methods. This study provides further insight into the methodology for estimating pollinator performance, especially in plants when only cross-pollen can germinate.

 

Author Biographies

Robert Brian Patchett, University of St Andrews

 

Gavin Ballantyne, Edinburgh Napier Uiversity

 

Patricia Gillian Willmer, University of St Andrews

 

References

Ästergaard L, Petersen M, Mattsson O, Mundy J (2002) An Arabidopsis callose synthase. Plant Molecular Biology 49:559–566. DOI: https://doi.org/10.1023/A:1015558231400

Ballantyne G, Baldock KCR, Willmer PG (2015) Constructing more informative plant-pollinator networks: visitation and pollen deposition networks in a heathland plant community. Proceedings of the Royal Society B 282:e20151130. DOI: https://doi.org/10.1098/rspb.2015.1130

Ballantyne G, Baldock KCR, Rendell L, Willmer PG (2017) Pollinator importance networks and the crucial value of bees in a highly speciose plant community. Scientific Reports 7:8389. DOI: https://doi.org/10.1038/s41598-017-08798-x

Barrett, SCH (2002) Sexual interference of the floral kind. Heredity 88:154-159. DOI: https://doi.org/10.1038/sj.hdy.6800020

Bartomeus I, Bosch J, Vilà M (2008) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. Annals of Botany 102:417–424. DOI: https://doi.org/10.1093/aob/mcn109

Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48. DOI: https://doi.org/10.18637/jss.v067.i01

Brown BJ, Mitchell RJ, Graham SA (2003) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 80:2328–2336. DOI: https://doi.org/10.1890/0012-9658(2002)083[2328:CFPBAI]2.0.CO;2

Crawley, M (2007) The R book. John Wiley and Sons Ltd, Chichester.

Cross RH, McKay SB, McHughen G, Bonham-Smith PC (2003) Heat-stress effects on reproduction and seed set in Linum usitatissimum L. (flax). Plant, Cell and Environment 26:1013–1020. DOI: https://doi.org/10.1046/j.1365-3040.2003.01006.x

Cruden RW (2000) Pollen grains: why so many? Plant Systematics and Evolution 222: 143-165. DOI: https://doi.org/10.1007/978-3-7091-6306-1_8

Currier H (1957) Callose substance in plant cells. American Journal of Botany 44:478–488. DOI: https://doi.org/10.1002/j.1537-2197.1957.tb10567.x

Falk S (2015) Field guide to the bees of Great Britain and Ireland. Bloomsbury, London.

Fang Q, Huang SQ (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94:1176–1185. DOI: https://doi.org/10.1890/12-1634.1

Friedman J, Barrett SCH (2008) High outcrossing in the annual colonizing species Ambrosia artemisiifolia (Asteraceae). Annals of Botany 101:1303–1309. DOI: https://doi.org/10.1093/aob/mcn039

Frier SD, Somers CM, Sheffield CS (2016) Comparing the performance of native and managed pollinators of Haskap (Lonicera caerulea: Caprifoliaceae), an emerging fruit crop. Agriculture, Ecosystems and Environment 219:42–48. DOI: https://doi.org/10.1016/j.agee.2015.12.011

Galen C, Gregory T, Galloway LF (1989) Costs of self-pollination in a self-incompatible plant, Polemonium viscosum. American Journal of Botany 76:1675–1680. DOI: https://doi.org/10.1002/j.1537-2197.1989.tb15152.x

Galen C, Stanton ML (2003) Sunny-side up: flower heliotropism as a source of parental environmental effects on pollen quality and performance in the snow buttercup, Ranunculus adoneus. American Journal of Botany 90:724–729. DOI: https://doi.org/10.3732/ajb.90.5.724

Gibbs PE (2014) Late-acting self-incompatibility – the pariah breeding system in flowering plants. New Phytologist 203:717–734. DOI: https://doi.org/10.1111/nph.12874

Gross C (2005) Pollination efficiency and pollinator effectiveness. In: Dafni A, Kevan PG, Husband BC (eds.). Practical pollination biology. Enviroquest Ltd, Cambridge, Ontario, pp 83-146.

Hiscock SJ, McInnis SM (2003) Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond. Trends in Plant Science 8:606–613. DOI: https://doi.org/10.1016/j.tplants.2003.10.007

Jones KN (1994) Nonrandom mating in Clarkia gracilis (Onagraceae): a case of cryptic self-incompatibility. American Journal of Botany 81:195–198. DOI: https://doi.org/10.1002/j.1537-2197.1994.tb15429.x

Kearns C, Inouye D (1993) Techniques for pollen biologists. University of Colorado Press, Niwot, Colorado, USA.

Kleijn D, Winfree R, Bartomeus I, Carvalheiro L, Henry M, Isaacs R, Klein A-M, Kremen C, M'Gonigle LK, Rader R, Ricketts TH, Williams NM, Adamson NL, Ascher JS, Báldi A, Batáry P, Benjamin F, Biesmeijer JC, Blitzer EJ, Bommarco R, Brand MR, Bretagnolle V, Button L, Cariveau DP, Chifflet R, Colville JF, Danforth BN, Elle E, Garratt MPD, Herzog F, Holzschuh A, Howlett BG, Jauker F, Jha S, Knop E, Krewenka KM, Le Féon V, Mandelik Y, May E, Park MG, Pisanty G, Reemer M, Riedinger V, Rollin O, Rundlöf M, Sardiñas HS, Scheper J, Sciligo AR, Smith HG, Steffan-Dewenter I, Thorp R, Tscharntke T, Verhulst J, Viana BF, Vaissière BE, Veldtman R, Westphal C, Potts SG (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nature Communications 6:e7414. DOI: https://doi.org/10.1038/ncomms8414

Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B 274:303–313. DOI: https://doi.org/10.1098/rspb.2006.3721

Korner-Nievergelt F, Roth T, Felten S, Guelat J, Almasi B, Korner-Nievergelt P (2015) Bayesian data analysis in ecology: using linear models with R. Elsevier, London, UK. DOI: https://doi.org/10.1016/B978-0-12-801370-0.00004-6

Larson DL, Royer RA, Royer MR (2006) Insect visitation and pollen deposition in an invaded prairie plant community. Biological Conservation 130:148–159. DOI: https://doi.org/10.1016/j.biocon.2005.12.009

Montgomery BR, Rathcke BJ (2012) Effects of floral restrictiveness and stigma size on heterospecific pollen receipt in a prairie community. Oecologia 168:449–458. DOI: https://doi.org/10.1007/s00442-011-2094-x

Moragues E, Traveset A (2005) Effect of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands. Biological Conservation 122:611–619. DOI: https://doi.org/10.1016/j.biocon.2004.09.015

Ne’eman G, Jürgens A, Newstrom-Lloyd L, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biological Reviews 85:435-451. DOI: https://doi.org/10.1111/j.1469-185X.2009.00108.x

Newbigin E, Anderson M, Clarke A (1993) Gametophytic self-incompatibility systems. The Plant Cell. 5:1315–1324. DOI: https://doi.org/10.1105/tpc.5.10.1315

Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x

Orueta D (2002) Thermal relationships between Calendula arvensis inflorescences and Usia aurata bombyliid flies. Ecology 83:3073–3085. DOI: https://doi.org/10.1890/0012-9658(2002)083[3073:TRBCAI]2.0.CO;2

Pontieri V, Sage, TL (1999) Evidence for stigmatic self-incompatibility, pollination induced ovule enlargement and transmitting tissue exudates in the paleoherb, Saururus cernuus L. (Saururaceae). Annals of Botany 84:507–519. DOI: https://doi.org/10.1006/anbo.1999.0947

Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25:345–353. DOI: https://doi.org/10.1016/j.tree.2010.01.007

Sedgley M (1979) Structural changes in the pollinated and unpollinated avocado stigma and style. Journal of Cell Science 38:49–60. DOI: https://doi.org/10.1242/jcs.38.1.49

Shore JS, Barrett SCH (1983) The effect of pollination intensity and incompatible pollen on seed set in Turnera ulmifolia (Turneraceae). Canadian Journal of Botany 62:298–1303. DOI: https://doi.org/10.1139/b84-175

Sulaman W, Arnoldo MA, Yu K, Tulsieram L, Rothstein SJ, Goring DR (1997) Loss of callose in the stigma papillae does not affect the Brassica self-incompatibility phenotype. Planta 203:327–331. DOI: https://doi.org/10.1007/s004250050198

R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Thomas R, Vaughan I, Lello J (2013) Data analysis with R statistical software. Eco-explore, Cardiff, UK.

Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends in Ecology and Evolution 21:208–216. DOI: https://doi.org/10.1016/j.tree.2006.01.006

Willmer PG, Cunnold H, Ballantyne G (2017) Insights from measuring pollen deposition – quantifying the pre-eminence of bees as flower visitors and effective pollinators. Arthropod-Plant Interactions 11:411-425. DOI: https://doi.org/10.1007/s11829-017-9528-2

Wist TJ, Davis AR (2013) Evaluation of inflorescence visitors as pollinators of Echinacea angustifolia (Asteraceae): comparison of techniques. Journal of Economic Entomology 106:2055–2071. DOI: https://doi.org/10.1603/EC13049

Zuur A, Ieno E, Walker N, Saveliev A, Smith G (2009) Mixed effects models and extensions in ecology. Springer, New York. DOI: https://doi.org/10.1007/978-0-387-87458-6

Published

2017-12-05

How to Cite

Patchett, R. B., Ballantyne, G., & Willmer, P. G. (2017). Estimating pollinator performance of visitors to the self-incompatible crop-plant Brassica rapa by single visit deposition and pollen germination: a comparison of methods. Journal of Pollination Ecology, 21. https://doi.org/10.26786/1920-7603(2017)420

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