Pollination ecology and floral function of Brown’s peony (Paeonia brownii) in the Blue Mountains of northeastern Oregon
DOI:
https://doi.org/10.26786/1920-7603(2013)2Abstract
Brown’s peony, Paeonia brownii (Paeoniaceae), is one of only two peony species native to the Western Hemisphere, yet its pollination ecology and breeding system have never been documented. Using flowering individuals of an endemic colony in the Blue Mountains of Oregon, U.S., we investigated the peony’s pollination system and floral function. We also examined pollen/carpel interactions through experimental pollinations aided by fluorescence microscopy. Paeonia brownii appears to be self compatible and mostly protogynous with floral traits of a generalist pollination system. The flowers appear to attract insects by producing abundant floral nectar secreted from lobes of a perigynous disc throughout their 9-15-days of anthesis. The most common pollen vectors were wasp queens (Vespidae), the large flower fly Criorhina caudata (Syrphidae), and females of Lasioglossum spp. (Halictidae), all of which foraged exclusively for nectar. Whether collected from foraging wasps and flies, anthers, or stigmas, about half the pollen grains appeared fertile. The number of ovules per carpel was about 19. Seed set (seeds/ovule) of naturally pollinated flowers was about 20% with about 4 viable seeds per follicle. The number of fertile pollen grains transferred to the stigma under natural conditions was highly variable but generally low, which may have contributed in part to the low rate of seed set. This study raises further questions about the role of pollen sterility, floral nectar and vespid wasps in shaping a pollinator system that is unusual in Paeonia.
References
Akre RD, Myhre EA (1992) Nesting biology and behavior of the baldfaced hornet, Dolichovespula maculata (L.) Hymenoptera: Vespidae in the Pacific Northwest. Melanderia 47:1-30.
Andrieu E, Debussche M, Galloni M, Thompson JD (2007) The interplay of pollination, costs of reproduction and plant size in maternal fertility limitation in perennial Paeonia officinalis. Oecologia 152:515-524. DOI: https://doi.org/10.1007/s00442-007-0662-x
Baker HG, Baker I (1983) A brief historical review of the chemistry of floral nectar. In: Bentley B, Elias T (eds) The Biology of Nectaries. Columbia University Press, New York, 126-152.
Baker HG, Baker I (1986) The occurrence and significance of amino acids in floral nectars. Plant Systematics and Evolution 151:175-186. DOI: https://doi.org/10.1007/BF02430273
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, 192−220.
Bernhardt P, Dafni A (2000) Breeding system and pollination biology of Mandragora officinarum L. (Solanaceae) in northern Israel. Det Norske Videnskaps-Akadami. I. Mat.-Naturv, Klasse Skrifter 39:215-234.
Buck M, Marshall SA, Cheung DKB (2008) Identification Atlas of the Vespidae (Hymenoptera, Aculeata) of the northeastern Nearctic region. Canadian Journal of Arthropod Identification No 5 (PDF version).
Camp WH, Hubbard MM (1963) Vascular supply and structure of the ovule and aril in peony and the aril in nutmeg. American Journal of Botany 50:174-178. DOI: https://doi.org/10.1002/j.1537-2197.1963.tb07192.x
Cohen SA, Michaud DP (1993) Synthesis of a fluorescent derivatizing reagent 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for analysis of hydrolysate amino acids via high performance liquid chromatography. Analytical Biochemistry 211:279-287. DOI: https://doi.org/10.1006/abio.1993.1270
Crumb SE (1956) The larvae of the Phalaenidae. United States Department of Agriculture Technical Bulletin No1135, Washington DC.
Domínguez CA, Dirzo R, Bullock SH (1989) On the function of floral nectar in Croton suberosus (Euphorbiaceae). Oikos 56:109–114. DOI: https://doi.org/10.2307/3566093
Edwards, R (1980) Social wasps their biology and control. Rentokil Library, East Grinstead UK.
Galindo- González J, Ornelas JF (2002) Interference between wasps and hummingbirds at a feeder. Foresta Veracruzana 4:39-44.
Goldblatt P, Bernhardt P (1990) Pollination biology of Nivenia (Iridaceae) and the presence of heterostylous self-compatibility. Israel Journal of Botany 39:93-111.
Goldblatt P, Bernhardt P, Vogan P, Manning JC (2004) Pollination by fungus gnats (Diptera: Mycetophilidae) and self-recognition sites in Tolmiea menziesii (Saxifragaceae). Plant Systematics and Evolution 244:55-¬67. DOI: https://doi.org/10.1007/s00606-003-0067-1
Goulson D, Wright NP (1997) Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae). Behavioral Ecology 9:213-219. DOI: https://doi.org/10.1093/beheco/9.3.213
Grant, V (1975) Genetics of flowering plants. Columbia University Press, New York.
Greene A, Akre RD, Landolt PJ (1978) Behavior of the yellowjacket social parasite, Dolichovespula arctica (Rohwer) (Hymenoptera: Vespidae). Melanderia 29:1-28.
Guo Q, Brown JH, Valone TJ, Kachman SD (2000) Constraints of seed size on plant distribution and abundance. Ecology 81:2149-2155. DOI: https://doi.org/10.1890/0012-9658(2000)081[2149:COSSOP]2.0.CO;2
Halket JM, Zaikin VG (2003) Derivatization in mass spectrometry -1. Silylation. European Journal of Mass Spectrometry 9:1-21. DOI: https://doi.org/10.1255/ejms.527
Hardwick DF (1996) A monograph of the North American Heliothentinae (Lepidoptera; Noctuidae). Hardwick DF, Ottowa.
Hiepko P (1964) Das zentrifugale androecium der Paeoniaceae. Deutsche Botanische Gesellschaft 77:427-435. DOI: https://doi.org/10.1111/j.1438-8677.1964.tb03559.x
Hitchcock CL, Cronquist A, Ownbey M, Thompson JW (1964) Vascular plants of the Pacific Northwest Part 2. Salicaceae to Saxifragaceae. University of Washington Press, Seattle.
Hong D, Pan K, Hong Y (1998) Taxonomy of the Paeonia delavayi complex (Paeoniaceae). Annals of Missouri Botanical Garden 85:554-564. DOI: https://doi.org/10.2307/2992016
Inouye DW, Gill DE, Dudash MR, Fenster, CB (1994) A model and lexicon for pollen fate. American Journal of Botany 81:1517-1530. DOI: https://doi.org/10.1002/j.1537-2197.1994.tb11462.x
Jing XM, Zheng GH (1999) Four species of wild peony seed dormancy and germination characteristics, and its relationship to the brink. Acta Phytophysiologica Sinica 25. (Translated from Chinese, no pagination.).
Kearns CA (1992) Anthophilous fly distribution across an elevation gradient. American Midland Naturalist 127:172-182. DOI: https://doi.org/10.2307/2426332
Kearns CA (2001) North American dipteran pollinators: assessing their value and conservation status. Conservation Ecology 5: [online] URL: http://www.consecol.org/vol5/iss1/art5/. DOI: https://doi.org/10.5751/ES-00262-050105
Kearns CA, Inouye DW (1994) Fly pollination of Linum lewisii (Linaceae). American Journal of Botany 8:1091-1095.
Kurczewski FE (1968) Vespula maculifrons (Hymenoptera: Vespidae) preying on the European earwig Forficula auicularia. Journal of the New York Entomological Society 76:84-86.
Liebert AE, Gamboa GJ, Stamp NE, Curtis TR, Monnet KM, Turillazzi S, Starks PT (2006) Genetics, behavior, and ecology of a wasp invasion: Polistes dominulus in North America. Annales Zoologici Fennici 43:595-624.
Luo YB, Pei YL, Pan KY, Hong DY (1998) A study on pollination biology of Paeonia suffruticosa subsp. spontanea (Paeoniaceae). Acta Phytotaxonomica Sinica 36:134-144.
MacKensie JK, Landolt PJ, Zack RS (2006) Attraction to ornamental peony (Paeonia lactiflora, Paeoniaceae) by Polistes dominulus Christ (Hymenoptera: Vespidae) demonstrated using olfactometers. Journal of the Kansas Entomological Society 79:231-238. DOI: https://doi.org/10.2317/601.23.1
Madeiros PM, Simoneit RT (2007) Analysis of sugars in environmental samples by gas chromatography-mass spectrometry. Journal of Chromatography 1141:271-278. DOI: https://doi.org/10.1016/j.chroma.2006.12.017
Manugistics (2000) STATGRAPHICS 5 Plus. Manugistics, Inc, Rockville, MD.
Matsuura M, Yamane S (1990) Biology of the vespine wasps. Springer-Verlag, Berlin. DOI: https://doi.org/10.1007/978-3-642-75230-8
Nicolson, SW, Thornburg, RW (2007) Nectar chemistry In: Nicolson SW et al. (eds) Nectaries and Nectar. Springer, New York, 215-263. DOI: https://doi.org/10.1007/978-1-4020-5937-7_5
Ogden, EC, Raynor GS, JHayers JV, Lewis DM (1974) Manual of Sampling Airborne Pollen. Hafner Press, London.
Page M (2005) The Gardener’s Peony: Herbaceous and Tree Peonies. Timber Press, Portland, OR.
Proctor M, Yeo P, Lack A (19960 The Natural History of Pollination. Timber Press, Portland, OR.
Rhoades DF, Bergdahl JC (1981) Adaptive significance of toxic nectar. The American Naturalist. 117:798-803. DOI: https://doi.org/10.1086/283765
Richter MR (2000) Social wasp (Hymenoptera: Vespidae) foraging behavior. Annual Review of Entomology 45:121-150. DOI: https://doi.org/10.1146/annurev.ento.45.1.121
Sahli HF, Conner, JK (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brassicaceae). American Journal of Botany 94:203-209. DOI: https://doi.org/10.3732/ajb.94.2.203
Sánchez-Lafuente AM (2002) Floral variation in the generalist perennial herb Paeonia broteroi (Paeoniaceae): Differences between regions with different pollinators and herbivores. American Journal of Botany 89:1260-1269. DOI: https://doi.org/10.3732/ajb.89.8.1260
Sánchez-Lafuente AM, Rey PJ, Alcántara JM, Valera F (1999) Breeding system and the role of floral visitors in seed production of a “few-flowered” perennial herb., Paeonia broteroi Boiss and Reut. (Paeoniaceae). Ecoscience 6:163-172. DOI: https://doi.org/10.1080/11956860.1999.11682517
Saunders, AP, Stebbins, LP (1938) Cytogenetic studies in Paeonia I. the compatibility of the species and the appearance of the hybrids. Genetics 23:65-82. DOI: https://doi.org/10.1093/genetics/23.1.65
Schlising RA (1976) Reproductive proficiency in Paeonia californica (Paeoniaceae). American Journal of Botany 63:1095-1103. DOI: https://doi.org/10.1002/j.1537-2197.1976.tb13194.x
Shuttleworth A, Johnson SD (2006) Specialised pollination by large spider-hunting wasps and self-incompatibility in the African milkweed Pachycarpus asperifolius. International Journal of Plant Science 167:177-1186. DOI: https://doi.org/10.1086/507685
Spradbery JP (1973) Wasps. University of Washington Press, Seattle.
Stamp NE, Bowers MD (1988) Direct and indirect effects of predatory wasps (Polistes sp.: Vespidae) on gregarious caterpillars (Hemileuca lucina: Saturniidae). Oecologia 75:619-624. DOI: https://doi.org/10.1007/BF00776428
Stebbins GL (1938) The Western American species of Paeonia. Madrono 4:252-260.
Stebbins GL, Ellerton S (1939) Structural hybridity in Paeonia californica and P. brownii . Journal of Genetics 38:1-36. DOI: https://doi.org/10.1007/BF02982164
Stebbins GL, Major J (1965) Endemism and speciation in the California flora. Ecological Monographs 35:1-35. DOI: https://doi.org/10.2307/1942216
Stern WT (1946) A study of the genus Paeonia. The Royal Horticultural Society, London.
Sutherland JP, Sullivan MS, Poppy GM (1999) The influence of floral character on the foraging behaviour of the hoverfly, Episyrphus balteatus. Entomologia Experimentalis et Applicata 93:157-164. DOI: https://doi.org/10.1046/j.1570-7458.1999.00574.x
Terrab A, García-Castaño JL, Romero JM, Berjano R, DeVega C, Talavera S (2007) Analysis of amino acids in nectar from Silene colorata Poiret (Caryophyllaceae). Botanical Journal of the Linnean Society 155:49-56. DOI: https://doi.org/10.1111/j.1095-8339.2007.00673.x
USDA Forest Service (1988) Range plant handbook. (Reprint of original 1937 publication). Dover Press, New York.
Vance NC (2012) Finding Brown’s peony a sweet attraction. Kalmiopsis 19:1-6.
Vance NC, Bernhardt P, Edens R (2004) Pollination and seed production in Xerophyllum tenax (Melanthiaceae) in the Cascade Range of central Oregon. American Journal of Botany 91:2060-2068. DOI: https://doi.org/10.3732/ajb.91.12.2060
Walters JL (1956) Spontaneous meiotic chromosome breakage in natural populations of Paeonia californica. American journal of Botany 43:342-354. DOI: https://doi.org/10.1002/j.1537-2197.1956.tb10500.x
Walters JL (1962) Megasporogenesis and gametophyte selection in Paeonia californica. American Journal of Botany 49:789-794. DOI: https://doi.org/10.1002/j.1537-2197.1962.tb15010.x
Zhang D, Sang T (1998) Chromosomal rearrangement of P. brownii and P. californica revealed by fluorescence in situ hybridization. Genome 41: 848-853. DOI: https://doi.org/10.1139/g98-079
Zhou S, Hong D, Pan K (1999) Pollination biology of Paeonia jishanensis T. Hong and W. Z. Zhao (Paeoniaceae) with special emphasis on pollen and stigma biology. Botanical Journal of the Linnean Society 130:43-52 DOI: https://doi.org/10.1006/bojl.1998.0239
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2013 Peter Bernhardt, Retha Meier, Nan Vance

This work is licensed under a Creative Commons Attribution 4.0 International License.



