Comparative floral ecology of bicolor and concolor morphs of Viola pedata (Violaceae) following controlled burns

Authors

  • Peter Bernhardt Saint Louis University
  • Retha Edens-Meier Saint Louis University
  • Dowen Jocson Saint Louis University
  • Justin Zweck Saint Louis University
  • Zong-Xin Ren Kunming Institute of Botany (Chinese Academy of Sciences)
  • Gerardo R. Camilo
  • Michael Arduser Missouri Department of Conservation (retired)

DOI:

https://doi.org/10.26786/1920-7603(2016)3

Abstract

We compared pollination and seed set of bicolor and concolor morphs in self-incompatible, Viola pedata over two seasons in two populations of unequal sizes.  One population grew on a wooded slope (CR) and the second on an exposed glade (SNR).  Both were burned in 2014. The number of flowers produced by concolor plants at SNR was higher in 2014 while the number of flowering bicolors increased at CR in 2015. Petal temperatures, regardless of site, showed that dark purple, posterior petals of bicolors were consistently warmer than their own mauve-lilac, anterior (lip) petals and the all mauve petals of concolors. Major pollen vectors were female bees (Andrenidae, Apidae and Halictidae) but polylectic, Andrena carlinii dominated both sites.  Bees foraged on flowers upside down or right side up but neither mode correlated with either morph. Bees foraged preferentially on concolor at both sites.  Pistils containing pollen tubes were higher in concolor pistils at both sites with a marginally greater number of  tubes penetrating concolor ovules regardless of site or year.  While both populations produced more seeds in 2014 SNR plants always produced more seeds than CR plants.  The increasing numbers of bicolor plants at CR in 2015 suggested that bicolors may equal or outnumber concolors when dark petals offer additional warmth to ectothermic pollinators in a shady (cooler) forest vs. an open, sunny glade. Subtle environmental factors may give a floral trait a selective advantage influencing fitness in an unbalanced polymorphism persisting in localized populations.

Author Biographies

Peter Bernhardt, Saint Louis University

Department of Biology

Professor of Biology

Retha Edens-Meier, Saint Louis University

School of Education

Professor

Dowen Jocson, Saint Louis University

Department of Biology

graduate student (PhD)

Justin Zweck, Saint Louis University

Department of Biology

Graduate Student(PhD)

Zong-Xin Ren, Kunming Institute of Botany (Chinese Academy of Sciences)

Key Laboratory for Plant Diversity and Biogeography of Wast Asia

Associate Professor

Michael Arduser, Missouri Department of Conservation (retired)

Missouri Department of Conservation (retired)

References

Armbruster WS (2002) Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-colour evolution in two genera. Journal of Evolutionary Biology 15: 468-486. https://doi.org/10.1046/j.1420-9101.2002.00399.x DOI: https://doi.org/10.1046/j.1420-9101.2002.00399.x

-----, Perez-Barrales RM, Arroyo J, Edwards ME, Vargas P (2006) Three-dimensional reciprocity of floral morphs in wild flax (Linum suffuticosum): a new twist on heterostyly. New Phytologist 171:581-590. https://doi.org/10.1111/j.1469-8137.2006.01749.x DOI: https://doi.org/10.1111/j.1469-8137.2006.01749.x

Beattie AJ (1969) Pollination ecology of Viola. I. Contents of stigmatic cavities. Wat-sonia 7:142-156.

----- (1971a) Itinerant pollinators in a forest. Madrono 21:120-124.

----- (1971b) Pollination mechanisms in Viola. New Phytologist 70:343-360. https://doi.org/10.1111/j.1469-8137.1971.tb02533.x DOI: https://doi.org/10.1111/j.1469-8137.1971.tb02533.x

----- (1972) The pollination of Viola. 2, Pollen loads of insect-visitors, Watsonia 9:13-25

----- (1974) Floral evolution in Viola. Annals of the Missouri Botanical Garden 61:781-793. https://doi.org/10.2307/2395029 DOI: https://doi.org/10.2307/2395029

----- (1976) Plant dispersion, pollination and gene flow in Viola. Oecologia 25:291-300. https://doi.org/10.1007/BF00345601 DOI: https://doi.org/10.1007/BF00345601

Becker RE, Ewart LC (1990) Pollination, seed set and pollen tube growth investigations in Viola pedata L. Acta Horticulturae 272: 33-36. https://doi.org/10.17660/ActaHortic.1990.272.3 DOI: https://doi.org/10.17660/ActaHortic.1990.272.3

Bernhardt P (1996) Anther adaptations in animal-pollination. In: D'Arcy WG, Keating RC (eds) The Anther: Form, function and phylogeny. Cambridge University Press, Cambridge, pp 192-220.

-----, Edens-Meier R, Westhus EJ, Vance, N (2014) Bee-mediated pollen transfer in two popula-tions of Cypripedium montanum Douglas ex Lindley. Journal of Pollination Ecology 13:188-202. https://doi.org/10.26786/1920-7603(2014)17 DOI: https://doi.org/10.26786/1920-7603(2014)17

-----, Montalvo EA (1979) The pollination of Echeandia macrocarpa (Liliaceae). Brittonia 31:64-71. https://doi.org/10.2307/2806674 DOI: https://doi.org/10.2307/2806674

Breedlove DE (1969) The systematics of Fuchsia section Encliandra (Ona-graceae). University of California Publications in Botany 53:1-69.

Davidse G (1968) A biosystematic investigation of the intermountain yellow violets. MSc Thesis, Utah State University, Logan, Utah.

Carlson JE, Holsinger KE (2013) Direct and indirect selection on floral pigmentation by pollina-tors and seed predators in a colour polymorphic South African shrub. Oecologia 171: 905-919. https://doi.org/10.1007/s00442-012-2453-2 DOI: https://doi.org/10.1007/s00442-012-2453-2

Carroll SB, Goldman P (1994) Analysis of a flower colour polymorphism in Viola pedata (birdfoot violet). Proceedings of the North American Conference on Savannas and Barrens. https://archive.epa.gov/ecopage/web/html/carroll.html.

Clausen J (1926) Genetical and cytological investigations on Viola tricolor L. and V. arvensis Murr. Hereditas 8:1-156. https://doi.org/10.1111/j.1601-5223.1926.tb03159.x DOI: https://doi.org/10.1111/j.1601-5223.1926.tb03159.x

Culley TM (2002) Reproductive Biology and delayed selfing in Viola pubescens (Violaceae), an understory herb with chasmogamous and cleistogamous flowers. Interna-tional Journal of Plant Sciences 163:113-122. https://doi.org/10.1086/324180 DOI: https://doi.org/10.1086/324180

De Jager ML, Ellis AG (2014) Floral polymorphism and the fitness implications of attracting pollinating and florivorous insects. Annals of Botany 113: 213-222. https://doi.org/10.1093/aob/mct189 DOI: https://doi.org/10.1093/aob/mct189

Darwin C (1876) The effects of cross and self fertilization in the vegetable kingdom John Murray, London.

Edens-Meier RM, Vance N, Luo YB, Li P, Bernhardt P (2010) Pollen-pistil interactions in North American and Chinese Cypripedium L. (Orchidaceae). International Journal of Plant Sciences 171:370-381. https://doi.org/10.1086/651225 DOI: https://doi.org/10.1086/651225

Epperson BK, Clegg MT (1987) Frequency-dependent variation for outcrossing rate among flower-colour morphs of Ipomoea purpurea. Evolution 411: 1302-1311. https://doi.org/10.1111/j.1558-5646.1987.tb02468.x DOI: https://doi.org/10.1111/j.1558-5646.1987.tb02468.x

Espindola A, Pellissier L, Alvarez N (2011) Variation in the proportion of flower visitors of Arum maculatum across its distributional range in relation with community-based climatic niche analysis. Oikos 120:728-734. https://doi.org/10.1111/j.1600-0706.2010.18937.x DOI: https://doi.org/10.1111/j.1600-0706.2010.18937.x

Fehr C, Rausher (MD 2004) Effects of variation at the flower-colour A locus on mating system parameters in Ipomoea purpurea. Molecular Evology 13: 1839-1847. https://doi.org/10.1111/j.1365-294X.2004.02182.x DOI: https://doi.org/10.1111/j.1365-294X.2004.02182.x

Freitas L, Sazima M (2003) Floral Biology and pollination mechanisms in two Viola species - from nectar to pollen flowers? Annals of Botany 91:311-317. https://doi.org/10.1093/aob/mcg025 DOI: https://doi.org/10.1093/aob/mcg025

Futuyma DJ (2013) Evolution. Third edition. Sinauer Associates, Inc. Sunderland, Massachusetts.

Gibson WH, Davie EE (1901) Blossom hosts and insect guests: How the heath family, the bluets, the figworts, the orchids and similar wild flowers welcome the bee, the fly, the wasp, the moth and other faithful insects. Newson and Company, New York. https://doi.org/10.5962/bhl.title.37821 DOI: https://doi.org/10.5962/bhl.title.37821

Gomez JM (2000) Phenotypic selection and response to selection in Lobularia maritima: Importance of direct and correlational components of natural selection. Journal of Evolutionary Biology 13:689-699. https://doi.org/10.1046/j.1420-9101.2000.00196.x DOI: https://doi.org/10.1046/j.1420-9101.2000.00196.x

Heinrich B (1993) The hot-blooded insects: Strategies and mechanisms of thermoregulation. Harvard University Press. Cambridge, Massachusetts. https://doi.org/10.4159/harvard.9780674418516 DOI: https://doi.org/10.4159/harvard.9780674418516

Herrera CM (1990) The adaptedness of the floral phenotype in a relict endemic, hawkmoth-pollinated violet. 1. Reproductive correlates of floral variation. Biological Journal of the Linnean Society 40:263-274. https://doi.org/10.1111/j.1095-8312.1990.tb00539.x DOI: https://doi.org/10.1111/j.1095-8312.1990.tb00539.x

----- (1993) Selection on floral morphology and environmental determinants of fecundity in a hawk moth-pollinated violet. Ecological Monographs 63:251-275. https://doi.org/10.2307/2937101 DOI: https://doi.org/10.2307/2937101

Gurevitch J, Scheiner S, Fox, G (2006) The Ecology of Plants. Second edition. Sinauer Associ-ates, Inc. Sunderland, Massachusetts.

Hildebrandt U, Hoef-Emden K, Backhausen S, Bothe H, Bozek M, Siuta A, Kuta E (2006) The rare, endemic zinc violets of Central Europe originate from Viola lutea Huds. Plant Systematics & Evolution 257:205-222. https://doi.org/10.1007/s00606-005-0387-4 DOI: https://doi.org/10.1007/s00606-005-0387-4

Irwin RE, Strauss SY (2005) Flower colour microevolution in wild radish: Evolutionary response to pollinator-mediated selection. The American Naturalist 165:225-237. https://doi.org/10.1086/426714 DOI: https://doi.org/10.1086/426714

Johri BM, Ambegaokar JR, Srivastava PS (1992) Comparative Embryology of Angiosperms. Volume 1. Springer-Verlag, Berlin. https://doi.org/10.1007/978-3-642-76395-3 DOI: https://doi.org/10.1007/978-3-642-76395-3

Kenrick J, Kaul V, Williams EG (1986) Self-incompatibility in Acacia retinodes: Site of pollen-tube arrest is the nucellus. Planta 169:245-50. https://doi.org/10.1007/BF00392321 DOI: https://doi.org/10.1007/BF00392321

Kevan P (1972) Heliotropism in some Arctic flowers. The Canadian Field Naturalist 86:41- 44. https://doi.org/10.5962/p.343519 DOI: https://doi.org/10.5962/p.343519

----- (1975) Sun-tracking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189:723-726. https://doi.org/10.1126/science.189.4204.723 DOI: https://doi.org/10.1126/science.189.4204.723

Lamont BB, Downes KS (2011) Fire-stimulated flowering among resprouters and genophytes in Australia and South Africa. Plant Ecology 212:2111-2125. https://doi.org/10.1007/s11258-011-9987-y DOI: https://doi.org/10.1007/s11258-011-9987-y

Le Maitre DC, Brown PJ (1992) Life cycles and fire-stimulated flowering in geophytes. In: van Wilgen BW, Richardson DM, Kruger FJ, van Hensbergen JH (eds) Fire in South African Mountain Fynbos, Springer0Verlar, New York, pp 145-160. https://doi.org/10.1007/978-3-642-76174-4_8 DOI: https://doi.org/10.1007/978-3-642-76174-4_8

Mabberley DJ (1997) The plant-book. Second edition. Cambridge University Press, Cambridge.

Malberla R, Nattero J (2011) Pollinator response to flower colour polymorphism and floral dis-play in a plant with a single-locus flower colour polymorphism: Consequences for plant re-production. Ecological Research 27: 377-385. https://doi.org/10.1007/s11284-011-0908-2 DOI: https://doi.org/10.1007/s11284-011-0908-2

Marcussen T, Borgen L (2011) Species delimitation in the Ponto-Caucasian Viola sie-heana complex, based on evidence from allozymes, morphology, ploidy levels and crossing experiments. Plant Systematics and Evolution 291:183-196. https://doi.org/10.1007/s00606-010-0377-z DOI: https://doi.org/10.1007/s00606-010-0377-z

Martin P, Houf GF (1993) Glade grasslands in southwest Missouri. Rangelands 15:70-73.

McKinney LE (1992) A taxonomic revision of the acaulescent blue violets (Viola) of North America. Botanical Research Institute of Texas, Inc., Fort Worth, Texas.

Migdalek G, Wozniak M, Slomka A, Godsik B, Jedrzejcyk-Korycinska M, Rostanski A, Bothe H, Kuta E (2013) Morphological differences between violets growing at heavy metal polluted and non-polluted sites. Flora 208:87-96. https://doi.org/10.1016/j.flora.2013.02.001 DOI: https://doi.org/10.1016/j.flora.2013.02.001

Mereda P, Hodalova I, Martonfi P, Kucera J, Lihova J (2008) Intraspecific variation in Viola suavis in Europe: Parallel evolution of white-flowered morphotypes. Annals of Botany 102:443-462. https://doi.org/10.1093/aob/mcn117 DOI: https://doi.org/10.1093/aob/mcn117

Müller H (1883) The fertilization of flowers. London. https://doi.org/10.5962/bhl.title.142366 DOI: https://doi.org/10.5962/bhl.title.142366

Nieuwland JA, Kaczmarek RM (1914) Studies in Viola, I: Proposed segregates of Viola. The American Midland Naturalist 8:207-217. https://doi.org/10.2307/2992979 DOI: https://doi.org/10.2307/2992979

Pellegrino G, Bellusci F, Musacchio A (2008) Double floral mimicry and the magnet species effect in dimorphic co-flowering species, the deceptive orchid Dactylorhiza sam-bucina and rewarding Viola aethnensis. Preslia 80:411-422.

Ramos RR, Venturieri GA, Cuco SM, Castro NM (2005) The site of self-incompatibility action in cupassu (Theobroma grandiflorum). Brazilian Journal of Botany 28:569-578. https://doi.org/10.1590/S0100-84042005000300013 DOI: https://doi.org/10.1590/S0100-84042005000300013

Rausher MD (2008) Evolutionary transitions in floral colour. International Journal of Plant Sci-ences. 169:7-21. https://doi.org/10.1086/523358 DOI: https://doi.org/10.1086/523358

Richards AJ (1986) Plant Breeding Systems. Allen & Unwin, Boston, Massachusetts.

Russell AL, Newman SR, Papaj DR (2016) White flowers finish last: Pollen foraging bumble bees show biased learning in a floral colour polymorphism. Evolutionary Ecology (2016). Doi:10.1007/s10682-016-9848-1. https://doi.org/10.1007/s10682-016-9848-1 DOI: https://doi.org/10.1007/s10682-016-9848-1

Rymer PD, Johnson SD, Savolainen V (2010) Pollinator behavior and plant speciation: can as-sortative mating and disruptive selection maintain distinct morphs in sympatry. New Phytologist 188:426-436. https://doi.org/10.1111/j.1469-8137.2010.03438.x DOI: https://doi.org/10.1111/j.1469-8137.2010.03438.x

Sage T, Sampson B (2003) Evidence for Ovarian Self-incompatibiolity as a cause of self-sterility in the relictual woody angiosperm, Pseudowintera axillaris (Winteraceae). Annals of Botany 91:807-816. https://doi.org/10.1093/aob/mcg085 DOI: https://doi.org/10.1093/aob/mcg085

Sage T, Strumas F, Cole WW, Barrett SCH (1999) Differential ovule development following self- and cross-pollination: the basis of self-sterility in Narcissus triandrus (Amayllidaceae). American Journal of Botany 86: 855-870. https://doi.org/10.2307/2656706 DOI: https://doi.org/10.2307/2656706

Schrader MN, LaBerge WE (1978) The nest biology of the bees: Andrena (Melandrena) regularis Malloch and Andrena (Melandrena) carlini (Hymenoptera: Andrenidae). Biological notes; no. 108. State of Illinois, Dept. of Registration and Education, Natural History Survey Division. https://doi.org/10.5962/bhl.title.15182 DOI: https://doi.org/10.5962/bhl.title.15182

Sobral M, Losada M, Veiga T, Gruitian J, Guitian J, Guitian P (2016) Flower colour preferences of insects and livestock: Effects on Gentiana lutea reproductive success. PeerJ 4:e1685; DOI 10.7717/peerj.1685. https://doi.org/10.7717/peerj.1685 DOI: https://doi.org/10.7717/peerj.1685

Steyermark J (1963) Flora of Missouri. Iowa State Press, Iowa City. https://doi.org/10.31274/isudp.1963.88 DOI: https://doi.org/10.31274/isudp.1963.88

Wang Y (2008) Molecular biology of flower development in Viola pubescens, a species with the chasmogamous-cleistogamous mixed breeding system. PhD Dissertation, Ohio Uni-versity. UMI 3302717.

Weberling F (1989) Morphology of Flowers and Inflorescences. Cambridge University Press. Cambridge.

Willmer P (2011) Pollination and Floral Ecology. Princeton University Press. Princeton, New Jersey. https://doi.org/10.23943/princeton/9780691128610.001.0001 DOI: https://doi.org/10.23943/princeton/9780691128610.001.0001

Winn AA, Moriuchi KS (2009) The maintenance of mixed mating by cleistogamy in the perennial violet Viola septemloba (Violaceae). American Journal of Botany 96:2074-2079. https://doi.org/10.3732/ajb.0900048 DOI: https://doi.org/10.3732/ajb.0900048

Rosettes of concolour morphs of Viola pedata, growing in an exposed, sunny, dolomite glade outnumbered bicolour morphs by 40:1 over two seasons.  In contrast, bicolours equaled or outnumbered concolours in a forested, shady slope over two seasons.  Burnin

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2016-11-17

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Bernhardt, P., Edens-Meier, R., Jocson, D., Zweck, J., Ren, Z.-X., Camilo, G. R., & Arduser, M. (2016). Comparative floral ecology of bicolor and concolor morphs of Viola pedata (Violaceae) following controlled burns. Journal of Pollination Ecology, 19, 57–70. https://doi.org/10.26786/1920-7603(2016)3

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