Seed dispersal in six species of terrestrial orchids in Biebrza National Park (NE Poland)

Emilia Brzosko, Beata Ostrowiecka, Jarosław Kotowicz, Magdalena Bolesta, Aneta Gromotowicz, Małgorzata Gromotowicz, Anna Orzechowska, Justyna Orzołek, Marta Wojdalska

Abstract


Knowledge about seed dispersal is required to explain problems in ecology, phylogeography, and conservation biology. Even though seed dispersal is a fundamental mechanism to understand problems at different levels of biological organization (individual, population, species, landscape), it remains one of the least recognized processes. Similar to other groups of plants, very little is known regarding patterns and distances of seed dispersal in orchids. Orchid seeds are generally assumed to be widely dispersed by wind because of their small size and low weight. Between 2006 and 2008, we conducted a field study of the distances at which orchid seeds are dispersed, and determined factors affecting dispersal. Investigations included 13 populations of six terrestrial orchid species – Cypripedium calceolus, Cephalanthera rubra, Epipactis helleborine, Goodyera repens, Neottia ovata, and Platanthera bifolia. To evaluate seed dispersal in orchid populations, 8.5-cm Petri dishes (traps) with self-adhesive paper were placed along transects, starting from a group of fruiting plants, which were considered to be the dispersal source. Seeds of the investigated orchid species were dispersed over relatively short distances. There were statistically significant negative correlations between seed density and distance from the fruiting plants. Seeds of species with taller fruiting shoots were dispersed farther than those with shorter ones (R = 0.68, p < 0.05). We discuss the causes and consequences of the dispersal patterns of orchid seeds.

Keywords


dispersal vector; long-distance dispersal; short-distance dispersal; terrestrial orchids

Full Text:

PDF

References


Cain ML, Milligan BG, Strand AE. Long-distance seed dispersal in plant populations. Am J Bot. 2000;87(9):1217–1227. https://doi.org/10.2307/2656714

Eriksson O. Seed dispersal and colonization ability of plants – assessment and implications for conservation. Folia Geobot. 2000;35(2):115–123. https://doi.org/10.1007/BF02803091

Nathan R. Long-distance dispersal of plants. Science. 2006;313(5788):786–788. https://doi.org/10.1126/science.1124975

Lorts CM, Briggemant NT, Sang T. Evolution of fruit types and seed dispersal: a phylogenetic and ecological snapshot. J Syst Evol. 2008;46(3):396–404.

Thomson FJ, Moles AT, Auld TD, Kingsford RT. Seed dispersal distance is more strongly correlated with plant height than with seed mass. J Ecol. 2011;99(6):1299–1307. https://doi.org/10.1111/j.1365-2745.2011.01867.x

Heydel F, Cunze S, Bernhardt-Römermann M, Tackenberg O. Long-distance seed dispersal by wind: disentangling the effects of species traits, vegetation types, vertical turbulence and wind speed. Ecol Res. 2014;29(4):641–651. https://doi.org/10.1007/s11284-014-1142-5

Webb CJ. The selection of pollen and seed dispersal in plants. Plant Species Biol. 1998;13(1):57–67. https://doi.org/10.1111/j.1442-1984.1998.tb00248.x

Tremlová K, Münzbergová Z. Importance of species traits for species distribution in fragmented landscapes. Ecology. 2007;88(4):965–977. https://doi.org/10.1890/06-0924

Damschen EI, Baker DV, Bohrer G, Nathan R, Orrock JL, Turner JR, et al. How fragmentation and corridors affect wind dynamics and seed dispersal in open habitats. Proc Natl Acad Sci USA. 2014;111(9):3484–3489. https://doi.org/10.1073/pnas.1308968111

Vanden Broeck A, van Landuyt W, Cox K, de Bruyn L, Gyselings R, Oostermeijer G, et al. High levels of effective long-distance dispersal may blur ecotypic divergence in a rare terrestrial orchid. BMC Ecol. 2014;14:20. https://doi.org/10.1186/1472-6785-14-20

Brzosko E. Dynamics of island populations of Cypripedium calceolus in the Biebrza river valley (NE Poland). Bot J Linn Soc. 2002;139:67–77. https://doi.org/10.1046/j.1095-8339.2002.00049.x

Jacquemyn H, Brys R, Vandepitte K, Honnay O, Roldán-Ruiz I, Wiegand T. A spatially explicit analysis of seedling recruitment in the terrestrial orchid Orchis purpurea. New Phytol. 2007;176(2):448–459. https://doi.org/10.1111/j.1469-8137.2007.02179.x

Jacquemyn H, Wiegand T, Vandepitte K, Brys R, Roldán-Ruiz I, Honnay O. Multigenerational analysis of spatial structure in the terrestrial, food-deceptive orchid Orchis mascula. J Ecol. 2009;97(2):206–216. https://doi.org/10.1111/j.1365-2745.2008.01464.x

Jacquemyn H, Waud M, Merckx VSFT, Lievens B, Brys R. Mycorrhizal diversity, seed germination and long-term changes in population size across nine populations of the terrestrial orchid Neottia ovata. Mol Ecol. 2015;24(13):3269–3280. https://doi.org/10.1111/mec.13236

Okubo A, Levin SA. A theoretical framework for data analysis of wind dispersal of seeds and pollen. Ecology. 1989;70(2):329–338. https://doi.org/10.2307/1937537

Murren CJ, Ellison AM. Seed dispersal characteristics of Brassovola nodosa (Orchidaceae). Am J Bot. 1998;85(5):675–680. https://doi.org/10.2307/2446537

Nathan R, Muller-Landau HC. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol. 2000;15(7):278–285. https://doi.org/10.1016/S0169-5347(00)01874-7

Nathan R, Sapir N, Trakhtenbrot A, Katul GG, Bohrer G, Otte M, et al. Long-distance biological transport processes through the air: can natures complexity be unfolded in silico? Divers Distrib. 2005;11(2):131–137. https://doi.org/10.1111/j.1366-9516.2005.00146.x

Nathan R, Katul GG, Bohrer G, Kuparinen A, Soons MB, Thompson SA, et al. Mechanistic models of seed dispersal by wind. Theor Ecol. 2011;4(2):113–132. https://doi.org/10.1007/s12080-011-0115-3

Thompson SE, Assouline S, Chen L, Trahktenbrot A, Svoray T, Katul GG. Secondary dispersal driven by overland flow in drylands: review and mechanistic model development. Mov Ecol. 2014;2(1):7. https://doi.org/10.1186/2051-3933-2-7

Kollmann J, Grubb PJ. Recruitment of fleshy-fruited species under different shrub species: control by under-canopy environment. Ecol Res. 1999;14(1):9–21. https://doi.org/10.1046/j.1440-1703.1999.141281.x

Rey PJ, Alcántara JM. Recruitment dynamics of a fleshy-fruited plant (Olea europaea): connecting patterns of seed dispersal to seedling establishment. J Ecol. 2000;88(4):622–633. https://doi.org/10.1046/j.1365-2745.2000.00472.x

Gosper CR, Stansbury CD, Vivian-Smith G. Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib. 2005;11(6):549–558. https://doi.org/10.1111/j.1366-9516.2005.00195.x

Schupp EW, Jordano P, Gómez JM. Seed dispersal effectiveness revisited: a conceptual review. New Phytol. 2010;188(2):333–353. https://doi.org/10.1111/j.1469-8137.2010.03402.x

Vander Wall SB, Beck MJ. A comparison of frugivory and scatter-hoarding seed-dispersal syndromes. Bot Rev. 2012;78(1):10–31. https://doi.org/10.1007/s12229-011-9093-9

Forrest AD, Hollinsworth ML, Hollinsworth PM, Sydney C, Bateman RM. Population genetic structure in European populations of Spiranthes romanzoffiana set in the context of other genetic studies on orchids. Heredity. 2004;92(3):218–227. https://doi.org/10.1038/sj.hdy.6800399

Chung MY, Nason JD, Chung MG. Spatial genetic structure in populations of the terrestrial orchid Orchiscyclochila (Orchidaceae). Plant Syst Evol. 2005;254:209–219. https://doi.org/10.1007/s00606-005-0341-5

Phillips RD, Dixon KW, Peakall R. Low population genetic differentiation in the Orchidaceae: implications for the diversification of the family. Mol Ecol. 2012;21(21):5208–5220. https://doi.org/10.1111/mec.12036

Vandepitte K, Gristina AS, de Hert K, Meekers T, Roldan-Ruiz I. Recolonization after habitat restoration leads to decreased genetic variation in populations of a terrestrial orchid. Mol Ecol. 2012;21(17):4206–4215. https://doi.org/10.1111/j.1365-294X.2012.05698.x

Rico Y, Holderegger R, Boehmer HJ, Wagner HH. Directed dispersal by rotational shepherding supports landscape genetic connectivity in a calcareous grassland plant. Mol Ecol. 2014;23(4):832–842. https://doi.org/10.1111/mec.12639

Diez JM. Hierarchical patterns of symbiotic orchid germination linked to adult proximity and environmental gradients. J Ecol. 2007;95(1):159–170. https://doi.org/10.1111/j.1365-2745.2006.01194.x

Loveless MD, Hamrick JL. Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst. 1984;15(1):65–95. https://doi.org/10.1146/annurev.es.15.110184.000433

Hamrick JL, Godt MJW. Conservation genetics of endemic plant species. In: Avise JL, Hamrick JL, editors. Conservation genetics: case histories from nature. New York, NY: Chapman and Hall; 1996. p. 281–304.

Frankham R, Ballou JD, Briscoe DA. Introduction to conservation genetics. Cambridge: Cambridge University Press; 2003.

Matlack GR. Diaspore size, shape, and fall behavior in wind-dispersed plant species. Am J Bot. 1987;74(8):1150–1160. https://doi.org/10.2307/2444151

Dressler R. The orchids – natural history and classification. Cambridge: Harvard University Press; 1981.

Arditti J. Fundamentals of orchid biology. New York, NY: John Wiley; 1992.

Arditti J, Ghani AKA. Numerical and physical properties of orchid seeds and their biological implications. New Phytol. 2000;145:146–569. https://doi.org/10.1046/j.1469-8137.2000.00587.x

Gandawijaja D, Arditti J. The orchids of Krakatau: evidence for a mode of transport. Ann Bot. 1983;52:127–130. https://doi.org/10.1093/oxfordjournals.aob.a086558

Doherty JW. The genus Cypripedium: part 1. North American Native Orchid Journal. 1997;3:5–116.

Alexandersson R, Ågren J. Genetic structure in the nonrewarding, bumblebee-pollinated orchid Calypso bulbosa. Heredity. 2000;85:401–409. https://doi.org/10.1046/j.1365-2540.2000.00777.x

Johansson VA, Müller G, Eriksson O. Dust seed production and dispersal in Swedish Pyroleae species. Nord J Bot. 2014;32:209–214. https://doi.org/10.1111/j.1756-1051.2013.00307.x

Willems JH. Establishment and development of a population of Orchis simia Lamk. in the Netherlands, 1972 to 1981. New Phytol. 1982;91:757–765. https://doi.org/10.1111/j.1469-8137.1982.tb03355.x

Bialozyt R, Ziegenhagen B, Petit RJ. Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol. 2006;19:12–20. https://doi.org/10.1111/j.1420-9101.2005.00995.x

Carey PD. Modelling the spread of Himantoglossum hircinum (L.) Spreng. at a site in the south of England. Bot J Linn Soc. 1998;126:159–172. https://doi.org/10.1111/j.1095-8339.1998.tb02523.x

Sun M, Wong KC. Genetic structure of three orchid species with contrasting mating systems using RAPD and allozyme markers. Am J Bot. 2001;88(12):2180–2188. https://doi.org/10.2307/3558379

Machon N, Bardin P, Mazer SJ, Moret J, Godelle B, Austerlitz F. Relationship between genetic structure and seed and pollen dispersal in the endangered orchid Spiranthes spiralis. New Phytol. 2003;157:677–687. https://doi.org/10.1046/j.1469-8137.2003.00694.x

Jersáková J, Malinová T. Spatial aspects of seed dispersal and seedling recruitment in orchids. New Phytol. 2007;176:237–241. https://doi.org/10.1111/j.1469-8137.2007.02223.x

Tremblay RL, Ackerman JD. Gene flow and effective population size in Lepanthes (Orchidaceae): a case for genetic drift. Biol J Linn Soc. 2001;72:47–62. https://doi.org/10.1111/j.1095-8312.2001.tb01300.x

Dinno A. dunn.test: Dunn’s test of multiple comparisons using rank sums. [Internet]. 2015 [cited 2017 Sep 14]. Available from: https://cran.r-project.org/package=dunn.test

Dinno A. conover.test: Conover–Iman test of multiple comparisons using rank sums. [Internet]. 2015 [cited 2017 Sep 14]. Available from: https://cran.r-project.org/package=conover.test

R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2015.

Harrod RJ, Everett R. Preliminary observations on seed dispersal and seed production of Cypripedium fasciculatum. Northwest Sci. 1993;67:131.

Chung MY, Nason JD, Chung MG. Spatial genetic structure in populations of the terrestrial orchid Cephalanthera longibracteata (Orchidaceae). Am J Bot. 2004;91:52–57. https://doi.org/10.3732/ajb.91.1.52

Suetsugu K, Kawakita A, Kato M. Avian seed dispersal in a mycoheterotrophic orchid Cyrtosia septentrionalis. Nat Plants. 2015;1:15052. https://doi.org/10.1038/nplants.2015.52

Harrod RJ. Characteristics and dispersal of Cypripedium fasciculatum seeds. Northwest Sci. 1994;68:129.

Willson M, Traveset A. The ecology of seed dispersal. In: Fenner M, editor. Seeds: the ecology of regeneration in plant communities. Wallingford: CAB International; 2000. p. 85–110. https://doi.org/10.1079/9780851994321.0085

Shimizu N, Sawa Y, Sawa S. Adaptation and evolution of seed shape on bleeding area in Japanese orchids. Int J Biol. 2012;4:47–53. https://doi.org/10.5539/ijb.v4n2p47

Kiyohara S, Fukunaga H, Sawa S. Characteristics of the falling speed of Japanese orchid seeds. Int J Biol. 2012;4(3):10–12. https://doi.org/10.5539/ijb.v4n3p10

Eriksson O, Kainulainen K. The evolutionary ecology of dust seeds. Perspect Plant Ecol Evol Syst. 2011;13(2):73–87. https://doi.org/10.1016/j.ppees.2011.02.002

Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A. Mechanisms of long-distance seed dispersal. Trends Ecol Evol. 2008;23:638–647. https://doi.org/10.1016/j.tree.2008.08.003

Venable DL, Flores-Martinez A, Muller-Landau H, Barron-Gafford G, Becerra JX. Seed dispersal of desert annuals. Ecology. 2008;89:2218–2227. https://doi.org/10.1890/07-0386.1

Muñoz M, Warner J, Albertazzi FJ. Genetic diversity analysis of the endangered slipper orchid Phragmipedium longifolium in Costa Rica. Plant Syst Evol. 2010;290:217–223. https://doi.org/10.1007/s00606-010-0362-6

Partomihardjo T. Colonisation of orchids on the Krakatau Islands. Telopea. 2003;10(1):299–310. https://doi.org/10.7751/telopea20035620

Castro S, Ferrero V, Loureiro J, Espadaler X, Silveira P, Navarro L. Dispersal mechanisms of the narrow endemic Polygala vayredae: dispersal syndromes and spatio-temporal variation in ant dispersal assemblages. Plant Ecol. 2010;207:359–372. https://doi.org/10.1007/s11258-009-9679-z

Carey PD, Farrell L. Himantoglossum hircinum (L.) Sprengel. Biological flora of the British Isles. J Ecol. 2002;90:206–218.

Schupp EW, Fuentes M. Spatial patterns of seed dispersal and the unification of plant population ecology. Ecoscience. 1995;2(3):267–275. https://doi.org/10.1080/11956860.1995.11682293

Brzosko E, Wróblewska A, Ratkiewicz M. Spatial genetic structure and clonal diversity of island populations of Lady’s slipper (Cypripedium calceolus) from the Biebrza National Park (northeast Poland). Mol Ecol. 2002;11:2499–2509. https://doi.org/10.1046/j.1365-294X.2002.01630.x

Seevers J, Lang F. Management recommendations for mountain lady’s slipper (Cypripedium montanum Douglas ex Lindley) v.2.0 [Internet]. 1998 [cited 2016 Aug 16]. Available from: https://www.blm.gov/or/plans/surveyandmanage/MR/VascularPlants/section10.htm

Batty AL, Dixon KW, Brundrett M, Sivasithamparam K. Constraints to symbiotic germination of terrestrial orchid seed in a Mediterranean bushland. New Phytol. 2001;152:511–520. https://doi.org/10.1046/j.0028-646X.2001.00277.x

Brzosko E, Wróblewska A. Genetic variation and clonal diversity in island Cephalanthera rubra populations from the Biebrza National Park. Bot J Linn Soc. 2003;143:99–108. https://doi.org/10.1046/j.1095-8339.2003.00201.x

Brzosko E, Wróblewska A. Genetic diversity of nectar-rewarding Platanthera chlorantha and nectarless Cephalanthera rubra. Bot J Linn Soc. 2013;171(4):751–763. https://doi.org/10.1111/boj.12025

Brzosko E, Wróblewska A, Jermakowicz E, Hermaniuk A. High level of genetic variation within clonal orchid Goodyera repens. Plant Syst Evol. 2013;299:1537–1548. https://doi.org/10.1007/s00606-013-0817-7

Ellstrand NC. Is gene flow the most important evolutionary force in plants? Am J Bot. 2014;101:737–753. https://doi.org/10.3732/ajb.1400024




DOI: https://doi.org/10.5586/asbp.3557

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society