Effect of climate, anther morphology and pollination syndrome on pollen availability in Penstemon

Factors that affect pollen availability in Penstemon

Authors

  • Rosa A Rodríguez-Peña The Ohio State University
  • Andrea D. Wolfe Department of Evolution, Ecology and Organismal Biology, The Ohio State University

DOI:

https://doi.org/10.26786/1920-7603(2023)703

Keywords:

solanoid morphology, climate, open-top-chamber, Penstemon, pollination syndrome, pollen presentation

Abstract

Traditionally, pollen presentation is thought to be a function of pollinator type and visitation frequency. However, despite the repeated observation that pollen presentation is influenced by flower morphology and abiotic factors, these aspects have been little studied in the wild. Here, we evaluated the effect of climate, anther morphology, and pollination syndrome on anther dehiscence time (the length of time an anther takes to fully dehisce after a flower opens). We recorded anther dehiscence time in twelve species of Penstemon including the four major anther types and the two most common pollination syndromes. We also conducted an experiment to measure the effect of humidity and temperature on anther dehiscence. We found that anther morphology was correlated with anther dehiscence time. Anthers with wide openings take the longest time to dehiscence. These results provide some support for the hypothesis that anther dehiscence time has evolved to decrease pollen wastage. Contrary to the assumption that bird-pollinated species have simultaneous pollen presentation, hummingbird-pollinated species had longer anther dehiscence time than most bee-pollinated species. The experiment revealed that high humidity and low temperature increase anther dehiscence time. Our results suggest that pollen presentation is influenced by anther morphology, pollination syndrome, and the physical environment. Optimal pollen presentation presumably maximizes conspecific pollen transfer and reduces pollen thieving.

Author Biographies

Rosa A Rodríguez-Peña, The Ohio State University

1Department of Evolution, Ecology and Organismal Biology, The Ohio State University, 318 W. 12th Avenue, Columbus, OH, USA

2Institutt for Biovitenskap, Universitetet i Bergen, Thormøhlens gate 53 A/B, Bergen, Norway

Andrea D. Wolfe, Department of Evolution, Ecology and Organismal Biology, The Ohio State University

Department of Evolution, Ecology and Organismal Biology, The Ohio State University, 318 W. 12th Avenue, Columbus, OH, USA

References

Bonner LJ, Dickinson HG (1990) Anther dehiscence in Lycopersicon esculentum Mill. I. Structural aspects. The New Phytologist 115:367-375. DOI: https://doi.org/10.1111/j.1469-8137.1990.tb00463.x

Brito VLG, Fendrich TG, Smidt EC, Varassin IG, Goldenberg R (2016) Shifts from specialised to generalised pollination systems in Miconieae (Melastomataceae) and their relation with anther morphology and seed number. Plant Biology 18:585-593. DOI: https://doi.org/10.1111/plb.12432

Brown JH, Kodric-Brown A (1979) Convergence, competition, and mimicry in a temperate community of hummingbird-pollinated flowers. Ecology 60:1022-1035. DOI: https://doi.org/10.2307/1936870

Buchmann SL (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of Experimental Pollination Biology.pp 73-113.

Burck W (1906) On the influence of the nectaries and other sugarcontaining tissues in the flower on the opening of the anthers. Proc. Sect. Sci. , K. Akad. Wet. Amst 9:390-396.

Cane JH, Dunne R (2014) Generalist bees pollinate red-flowered Penstemon eatonii: Duality in the hummingbird pollination syndrome. The American Midland Naturalist 171:365-370. DOI: https://doi.org/10.1674/0003-0031-171.2.365

Cane JH, Schiffhauer D (2003) Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). American Journal of Botany 90:1425-1432. DOI: https://doi.org/10.3732/ajb.90.10.1425

Cardinal S, Buchmann SL, Russell AL (2018) The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila). Evolution 72:590-600. DOI: https://doi.org/10.1111/evo.13446

Castellanos MC, Wilson P, Keller SJ, Wolfe AD, Thomson JD (2006) Anther evolution: Pollen presentation strategies when pollinators differ. The American Naturalist 167:288-296. DOI: https://doi.org/10.1086/498854

Coulter JM, Barnes CR, Cowles HC (1911) A textbook of botany for colleges and universities: Ecology. American Book Company. DOI: https://doi.org/10.5962/bhl.title.56446

Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35:375-403. DOI: https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Fernando DD, Cass DD (1997) Developmental assessment of sexual reproduction in Butomus umbellatus (Butomaceae): Male reproductive component. Annals of Botany 80:449-456. DOI: https://doi.org/10.1006/anbo.1997.0466

Free JB (1962) The behaviour of honeybees visiting field beans (Vicia faba). The Journal of Animal Ecology 31:497-502. DOI: https://doi.org/10.2307/2049

Freeman, C. C., 2019. Penstemon. In: Flora of North America Editorial Committee, eds. 1993+. Flora of North America North of Mexico. 21+ vols. Vol. 17, pp. 82-255. New York and Oxford.

Gentry AH (1974) Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6:64-68. DOI: https://doi.org/10.2307/2989698

Goodwin RM (1986) Kiwifruit flowers: Anther dehiscence and daily collection of pollen by honey bees. New Zealand Journal of Experimental Agriculture 14:449-452. DOI: https://doi.org/10.1080/03015521.1986.10423064

Grant V (1994) Modes and origins of mechanical and ethological isolation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America 91:3-10. DOI: https://doi.org/10.1073/pnas.91.1.3

Grant V, Grant KA (1965) Flower pollination in the phlox family. Columbia University Press.

Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. The American Naturalist 133:323-344. DOI: https://doi.org/10.1086/284922

Heinrich B (1977) The physiology of exercise in the bumblebee: Bumblebees are limited in their superb athletic performance by extremes of air temperature, but by regulating their body temperature they achieve considerable control. American Scientist 65:455-465.

Heinrich B, Esch H (1994) Thermoregulation in bees. American Scientist 82:164-170.

Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science 176:597-602. DOI: https://doi.org/10.1126/science.176.4035.597

Hendry AP, Day T (2005) Population structure attributable to reproductive time: Isolation by time and adaptation by time. Molecular Ecology 14:901-916. DOI: https://doi.org/10.1111/j.1365-294X.2005.02480.x

Holsinger KE, Thomson JD (1994) Pollen discounting in Erythronium grandiflorum: Mass-action estimates from pollen transfer dynamics. The American Naturalist 144:799-812. DOI: https://doi.org/10.1086/285707

Hughes CE (1997) Variation in anther and pollen morphology in Leucaena Benth. (Leguminosae-Mimosoideae). Botanical Journal of the Linnean Society 123:177-196. DOI: https://doi.org/10.1111/j.1095-8339.1997.tb01412.x

Inouye DW (1980) The terminology of floral larceny. Ecology 61:1251-1253. DOI: https://doi.org/10.2307/1936841

Katzer AM, Wessinger CA, Hileman LC (2019) Nectary size is a pollination syndrome trait in Penstemon. The New Phytologist 223:377-384. DOI: https://doi.org/10.1111/nph.15769

Kiel CA, Daniel TF, Darbyshire I, McDade LA (2017) Unraveling relationships in the morphologically diverse and taxonomically challenging “justicioid” lineage (Acanthaceae: Justicieae). Taxon 66:645-674. DOI: https://doi.org/10.12705/663.8

Krupnick GA, Weis AE, Campbell DR (1999) The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80:125-134. DOI: https://doi.org/10.1890/0012-9658(1999)080[0125:TCOFHF]2.0.CO;2

Martén-Rodríguez S, Almarales-Castro A, Fenster CB (2009) Evaluation of pollination syndromes in Antillean Gesneriaceae: Evidence for bat, hummingbird and generalized flowers. The Journal of Ecology 97:348-359. DOI: https://doi.org/10.1111/j.1365-2745.2008.01465.x

Murray BG (1981) The origins of adaptive interspecific territorialism. Biological Reviews of the Cambridge Philosophical Society 56:1-22. DOI: https://doi.org/10.1111/j.1469-185X.1981.tb00341.x

Parker AJ, Williams NM, Thomson JD (2018) Geographic patterns and pollination ecotypes in Claytonia virginica. Evolution 72:202-210. DOI: https://doi.org/10.1111/evo.13381

Pearson S, Parker A, Hadley P, Kitchener HM (1995) The effect of photoperiod and temperature on reproductive development of cape daisy (Osteospermum jucundum cv.“Pink Whirls”). Scientia Horticulturae 62:225-235. DOI: https://doi.org/10.1016/0304-4238(95)00792-R

Percival MS (1955) The presentation of pollen in certain angiosperms and its collection by Apis mellifera. The New Phytologist 54:353-368. DOI: https://doi.org/10.1111/j.1469-8137.1955.tb06192.x

Reynolds RJ, Westbrook MJ, Rohde AS, Cridland JM, Fenster CB, Dudash MR (2009) Pollinator specialization and pollination syndromes of three related North American Silene. Ecology 90:2077-2087. DOI: https://doi.org/10.1890/08-1141.1

Ricketts TH (2004) Tropical forest fragments enhance pollinator activity in nearby coffee crops. Conservation Biology 18:1262-1271. DOI: https://doi.org/10.1111/j.1523-1739.2004.00227.x

Rodríguez-Peña RA, Wolfe AD (2022) Flower morphology variation in five species of Penstemon (Plantaginaceae) displaying Hymenoptera pollination syndrome. Accepted for publication in Botanical Sciences. DOI: https://doi.org/10.17129/botsci.3084

Sarala BS, Lokesha R, Vasudeva R (1999) Anther dimorphism, differential anther dehiscence, pollen viability and pollination success in Caesalpinia pulcherrimma L. (Fabaceae). Current Science 76:1490-1494.

Schemske DW, Bradshaw HD Jr (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proceedings of the National Academy of Sciences of the United States of America 96:11910-11915. DOI: https://doi.org/10.1073/pnas.96.21.11910

Schmid R (1976) Fly pollination of Penstemon davidsonii and P. procerus (Scrophulariaceae). Madroño 23:400-402.

Schmid R, Alpert PH (1977) A test of Burck’s hypothesis relating anther dehiscence to nectar secretion. The New Phytologist 78:487-498. DOI: https://doi.org/10.1111/j.1469-8137.1977.tb04855.x

Soliva M, Widmer A (1999) Genetic and floral divergence among sympatric populations of Gymnadenia conopsea s.l. (Orchideaceae) with different flowering phenology. International Journal of Plant Sciences 160:897-905. DOI: https://doi.org/10.1086/314192

Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annual Review of Ecology and Systematics 1:307-326. DOI: https://doi.org/10.1146/annurev.es.01.110170.001515

Straw RM (1956) Floral isolation in Penstemon. The American Naturalist 90:47-53. DOI: https://doi.org/10.1086/281906

Straw RM (1963) Bee-fly pollination of Penstemon ambiguus. Ecology 44:818-819. DOI: https://doi.org/10.2307/1933041

Synge AD (1947) Pollen collection by honeybees (Apis mellifera). The Journal of Animal Ecology 16:122-138. DOI: https://doi.org/10.2307/1492

Therneau T (2021) A package for survival analysis in R; R Package version 3.2-7. 2020.

Therneau TM, Grambsch PM (2000) The Cox model. In: Therneau TM, Grambsch PM (eds) Modeling survival data: Extending the Cox model. Springer New York, New York, NY, pp 39-77. DOI: https://doi.org/10.1007/978-1-4757-3294-8_3

Thomson JD, Goodell K (2001) Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. The Journal of Applied Ecology 38:1032-1044. DOI: https://doi.org/10.1046/j.1365-2664.2001.00657.x

Thomson JD, Thomson BA (1992) Pollen presentation and viability schedules and their consequences for reproductive success through animal pollination. In: Wyatt R (ed) Ecology and evolution of plant reproduction: New approaches. Chapman and Hall, New York, NY, pp 1-24.

Thomson JD, Wilson P, Valenzuela M, Malzone M (2000) Pollen presentation and pollination syndromes, with special reference to Penstemon. Plant Species Biology 15:11-29. DOI: https://doi.org/10.1046/j.1442-1984.2000.00026.x

Thorp RW (2000) The collection of pollen by bees. In: Pollen and pollination. Springer, Viena, pp 211-223. DOI: https://doi.org/10.1007/978-3-7091-6306-1_11

Vapaavuori E, Timo Oksanen, Jarmo K. Holopainen, Toini Holopainen, Juha Heiskanen, Riitta Julkunen-Tiitto, Anne Kasurinen, Jukka Laitinen1, Elina Oksanen, Petri Peltonen, Marja Poteri, Tapani Repo, Johanna Riikonen and Leena Syrjälä. 2002. Open-top chamber fumigation of cloned silver birch (Betula pendula Roth) trees to elevated CO2 and ozone: description of the fumigation system and the experimental site. Finnish Forest Research Institute, Research Papers 838, Suonenjoki

Welshofer KB, Zarnetske PL, Lany NK, Thompson LAE (2018) Open-top chambers for temperature manipulation in taller-stature plant communities. Methods in Ecology and Evolution 9:254-259. DOI: https://doi.org/10.1111/2041-210X.12863

Wilson P (1995) Variation in the intensity of pollination in Drosera tracyi: Selection is strongest when resources are intermediate. Evolutionary Ecology 9:382-396. DOI: https://doi.org/10.1007/BF01237761

Wilson P, Castellanos MC, Hogue JN, Thomson JD, Scott Armbruster W (2004) A multivariate search for pollination syndromes among penstemons. Oikos 104:345-361. DOI: https://doi.org/10.1111/j.0030-1299.2004.12819.x

Wolfe AD, Randle CP, Datwyler SL, Morawetz JJ, Arguedas N, Diaz J (2006) Phylogeny, taxonomic affinities, and biogeography of Penstemon (Plantaginaceae) based on ITS and cpDNA sequence data. American Journal of Botany 93:1699-1713. DOI: https://doi.org/10.3732/ajb.93.11.1699

Zhang L, Barrett SC, Gao JY, Chen J, Cole WW, Liu Y, Bai ZL, Li QJ (2005) Predicting mating patterns from pollination syndromes: The case of “sapromyiophily” in Tacca chantrieri (Taccaceae). American Journal of Botany 92:517-524. DOI: https://doi.org/10.3732/ajb.92.3.517

Published

2023-12-15

How to Cite

Rodríguez-Peña, R. A., & Wolfe, A. D. (2023). Effect of climate, anther morphology and pollination syndrome on pollen availability in Penstemon: Factors that affect pollen availability in Penstemon. Journal of Pollination Ecology, 35, 296–311. https://doi.org/10.26786/1920-7603(2023)703

Issue

Section

Articles

Similar Articles

<< < 12 13 14 15 16 17 18 19 20 21 > >> 

You may also start an advanced similarity search for this article.