Seed dispersal of anemochoric Abies alba Mill.: lessons learned from seed tracking, seed trap experiments and genetic parentage assignment of seedlings

Authors

  • Jarosław Paluch University of Agriculture, Al. 29 Listopada 46, 31-425 Cracow, Poland
  • Marcin Zarek University of Agriculture, Al. 29 Listopada 46, 31-425 Cracow, Poland

DOI:

https://doi.org/10.15287/afr.2019.1705

Keywords:

Wind dispersal, Seed shadow, Seed-tracking, Gene shadow, Natural regeneration, Inverse modelling

Abstract

Several methods are used to estimate the spatial pattern of seed dispersal. However, each method has specific shortcomings that limit the accuracy and reliability of the resulting dispersal models. In this study we compared seed shadows of the anemochoric species Abies alba Mill. obtained from (1) phenomenological models derived from seed trapping data and inverse modelling, (2) ballistic models based on wind speed at canopy height and an exponential wind profile and (3) empirical models parameterised from seed-tracking data. In addition, we checked whether the empirical model coupled with multiannual wind characteristics provides a dispersal pattern concordant with the gene shadow obtained from parentage assignment between seedlings and overstorey trees. The seed trap and seed-tracking experiments were conducted in 2013 and 2015 with contrasting wind conditions in five study plots located in the Krynica Forest Experimental Station in southern Poland. Genetic data originated from 16 mature stands with dominant A. alba. The study revealed that the distances reached by single seeds strongly vary at the same wind speed at canopy height. The ballistic model overestimated the flight distances of A. alba seeds. Similarly, the empirical model calibrated on data that disregarded seeds trapped in the crowns of neighbouring conifer trees predicted longer flight distances than those derived from the seed trap experiments. The gene shadow obtained from the parentage analysis suggests dispersal patterns concordant with those anticipated by the empirical model based on the seed-tracking experiments, with a possible shift towards an increased proportion of seeds landing close to the source. It was concluded that in dense canopies collisions with canopy elements during seed flight and secondary dispersion of seeds trapped in the canopy zone may considerably shorten the travel distances of A. alba seeds. 

References

Amm A., Pichot C., Dreyfus P., Davi H., Fady B., 2012. Improving the estimation of landscape scale seed dispersal by integrating seedling recruitment. Annals of Forest Science 69: 845-856. DOI: 10.1007/s13595- 012-0208-1 Augspurger C.K. 1986. Morphology and dispersal potential of wind dispersed diaspores of neotropicaltrees. American Journal of Botany 73: 353-363. DOI: 10.1002/j.1537-2197.1986.tb12048.x Bohrer G., Katul G.G., Nathan R., Walko R.L., Avissar R., 2008. Effects of canopy heterogeneity, seed abscission, and inertia on wind-driven dispersal kernels of tree seeds. Journal of Ecology 96: 569-580. DOI: 10.1111/j.1365-2745.2008.01368.x Bullock J.M., 2012. Plant dispersal and the velocity of climate change. In: Clobert J., Baguette M., Benton T.G., Bullock J.M. (eds.), Dispersal Ecology and Evolution, Oxford University Press, Oxford, pp. 366-380. DOI: 10.1093/acprof:oso/9780199608898.003.0029 Bullock J.M., Clarke R.T., 2000. Long distance seed dispersal by wind: measuring and modelling the tail of the curve. Oecologia 124: 506-521. DOI: 10.1007/ PL00008876 Bullock J.M., Moy I.L., 2004. Plants as seed traps: inter-specific interference with dispersal. Acta Oecologica 25: 35-41. DOI: 10.1016/j.actao.2003.10.005 Bullock J.M., Moy I.L., Coulson S.J., Clarke R.T., 2003. Habitat-specific dispersal: environmental effects on the mechanisms and patterns of seed movement in a grassland herb Rhinanthus minor. Ecography 26: 692-704. DOI: 10.1034/j.1600-0587.2003.03525.x Burczyk J., Adams W.T., Birkes D.S., Chybicki I.J., 2006. Using genetic markers to directly estimate gene flow and reproductive success parameters in plants based on naturally regenerated seedlings. Genetics 173: 363-372. DOI: 10.1534/genetics.105.046805 Carlo T.A., Tewksbury J.J., del Río C.M., 2009. A new method to track seed dispersal and recruitment using 15N isotope enrichment. Ecology 90: 3516-3525. DOI: 10.1890/08-1313.1 Chybicki I.J., Burczyk J., 2010. Realized gene flow within mixed stands of Quercus robur L. and Q. petraea (Matt.) L. revealed at the stage of naturally established seedling. Molecular Ecology 19: 2137-2151. DOI: 10.1111/j.1365-294X.2010.04632.x Cionco R.M., 1965. A mathematical model for air flow in a vegetative canopy. Journal of Applied Meteorology 4: 517-522. DOI: 10.1175/1520-0450(1965)004<0517:AMMFAF>2.0. CO;2 Cremer E., Ziegenhagen B., Schulerowitz K., Mengel K., Donges K., Bialozyt R., Hussendörfer E., Liepelt S., 2012. Local seed dispersal in European silver fir (Abies alba Mill.): lessons learned from a seed trap experiment. Trees 26: 987-996. DOI: 10.1007/s00468-012-0676-9 Cremer E., Liepelt S., Sebastiani F., Buonamici A., Michalczyk I.M., Ziegenhagen B., Vendramin G.G., 2006. Identification and characterization of nuclear microsatellite loci in Abies alba Mill. Molecular Ecology Notes 6: 374-376. DOI: 10.1111/j.1471-8286.2005.01238.x De Andrés E.G., Camarero J.J., Martínez I., Coll L., 2014. Uncoupled spatio-temporal patterns of seed dispersal and regeneration in Pyrenean silver fir populations. Forest Ecology and Management 319: 18-28. DOI: 10.1016/j.foreco.2014.01.050 Eisenhut G., 1961. Untersuchungen über die Morphologie und Ökologie der Pollenkörner heimischer und fremdländischer Waldbäume [Studies on the morphology and ecology of native pollen grains of forest trees]. Forstwissenschaftliche Forschungen 15: 1-68. Goudet J., 2002. FSTAT, a program to estimate and test gene diversities and fixation indices (Version 2.9.3.2). Web: http://www.unil.ch/izea/softwares/fstat.html. Accessed: 25 June 2016. Greene D.F., Calogeropoulos C., 2002. Measuring and modelling seed dispersal of terrestrial plants. In: Bullock J.M., Kenward R.E., Hails R.S. (eds.), Dispersal ecology, Blackwell Science, Oxford, pp. 2-21. Greene D.F., Johnson E.A., 1997. Secondary dispersal of tree seeds on snow. Journal of Ecology 85: 329-340. DOI: 10.2307/2960505 Greene D.F., Canham C.D., Coates K.D., Lepage P.T., 2004. An evaluation of alternative dispersal functions for trees. Journal of Ecology 92: 758-766. DOI: 10.1111/j.0022-0477.2004.00921.x Greene D.F., 2005. The role of abscission in long-distance seed dispersal by the wind. Ecology 86: 3105-3110. DOI: 10.1890/04-1430 Grivet D., Smouse P.E., Sork V.L., 2005. A novel approach to an old problem: tracking dispersed seeds. Molecular Ecology 14: 3585-3595. DOI: 10.1111/j.1365- 294X.2005.02680.x Guries R.P., Nordheim E.V., 1984. Flight characteristics and dispersal potential of maple samaras. Forest Science 30: 434-440. Hamrick J.L., Trapnell D.W., 2011. Using population genetic analyses to understand seed dispersal patterns. Acta Oecologica 37: 641-649. DOI: 10.1016/j. actao.2011.05.008 Higgins S.I., Nathan R., Cain M.L., 2003. Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84: 1945-1956. DOI: 10.1890/01-0616 Higgins S.I., Richardson D.M., 1999. Predicting plant migration rates in a changing world: the role of long-distance dispersal. The American Naturalist 153: 464-475. DOI: 10.1086/303193 Horvitz C.C., Schemske D.W., 1994. Effects of dispersers, gaps, and predators on dormancy and seedling emergence in a tropical herb. Ecology 75: 1949-1958. DOI: 10.2307/1941599 Jones A.G., Small C.M., Paczolt K.A., Ratterman N.L., 2010. A practical guide to methods of parentage analysis. Molecular Ecology Resources 10: 6-30. DOI: 10.1111/j.1755-0998.2009.02778.x Kaimal J.C., Finnigan J.J., 1994. Atmospheric boundary layer flows: their structure and measurement. Oxford University Press, New York, 289 p. Kalinowski S.T., Taper M.L., Marshall T.C., 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 6: 1099-1106. DOI: 10.1111/j.1365-294X.2007.03089.x Klein E.K., Bontemps A., Oddou-Muratorio S., 2013. Seed dispersal kernels estimated from genotypes of established seedlings: does density-dependent mortality matter? Methods in Ecology and Evolution 4: 1059- 1069. DOI: 10.1111/2041-210X.12110 Kohlermann L., 1950. Untersuchungen über die Windverbreitung der Früchte und Samen Mitteleuropäischer Waldbäume [Studies on the wind spread of fruits and seeds in Central European forest trees]. Forstwissenschaftliches Centralblatt 69: 606-624. DOI: 10.1007/ BF01815738 Kuparinen A., Katul G., Nathan R., Schurr F.M., 2009. Increases in air temperature can promote wind-driven dispersal and spread of plants. Proceedings of the Royal Society B: Biological Sciences 276: 3081-3087. DOI: 10.1098/rspb.2009.0693 Kuparinen A., 2006. Mechanistic models for wind dispersal. Trends in Plant Science 11: 296-301. DOI:10.1016/j.tplants.2006.04.006 Meagher T.R., Thompson E., 1986. The relationship between single parent and parent pair genetic likelihoods in genealogy reconstruction. Theoretical Population Biology 29: 87-106. DOI: 10.1016/0040-5809(86)90006- 7 Moran E.V., Clark J.S., 2011. Estimating seed and pollen movement in a monoecious plant: a hierarchical Bayesian approach integrating genetic and ecological data. Molecular Ecology 20: 1248-1262. DOI: 10.1111/j.1365-294X.2011.05019.x Nathan R., Katul G.G., Horn H.S., Thomas S.M., Oren R., Avissar R., Pacala S.W., Levin S.A., 2002. Mechanisms of long-distance dispersal of seeds by wind. Nature 418: 409-413. DOI: 10.1038/nature00844 Nathan R, Perry G, Cronin JT, Strand AE, Cain ML 2003. Methods for estimating long-distance dispersal. Oikos 103: 261-273. DOI: 10.1034/j.1600-0706.2003.12146.x Nathan R., Katul G.G., Bohrer G., Kuparinen A., Soons M.B., Thompson S.E., Trakhtenbrot A., Horn S., 2011. Mechanistic models of seed dispersal by wind. Theoretical Ecology 4: 113-132. DOI: 10.1007/s12080-011- 0115-3 Oddou-Muratorio S., Klein E., 2008 Comparing direct vs. indirect estimates of gene flow within a population of a scattered tree species. Molecular Ecology 17: 2743- 2754. DOI: 10.1111/j.1365-294X.2008.03783.x Paluch J., Stępniewska H., 2012. Effect of microsites on the survival, density, and ectomycorrhizal status of shade-tolerant Abies alba regeneration attacked by fungal pathogens. Canadian Journal of Forest Research 42: 720-732. DOI: 10.1139/x2012-015 Paluch J., 2011. Ground seed density patterns under conditions of strongly overlapping seed shadows in Abies alba Mill. stands. European Journal of Forest Research 130: 1009-1022. DOI: 10.1007/s10342-011-0486-4 Paluch J., Kołodziej Z., Skrzyszewski J., Bartkowicz L., Gruba P., 2016. Regeneration patterns of the late-successional Abies alba Mill.: Inhibition in monospecific stands and colonization in mixed stands. Annals of Forest Science 73: 1015-1024. DOI: 10.1007/s13595- 016-0573-2Paluch J., Zarek M., Kempf M., 2019. The effect of population density on gene flow between adult trees and the seedling bank in Abies alba Mill. European Journal of Forest Research 138: 203-217. DOI: 10.1007/s10342- 019-01162-w Paszyński J., Niedzwiedź T., 1999. Klimat [Climate]. In: Starkel L. (ed.), Geografia Polski. Środowisko przyrodnicze, PWN, Warszawa, pp. 288-343. Pielaat A., Lewis M.A., Lele S., de Camino Beck T., 2006. Sequential sampling designs for catching the tail of dispersal kernels. Ecological Modeling 190: 205-222. DOI: 10.1016/j.ecolmodel.2005.02.023 Raybould A.F., Clarke R.T., Bond J.M., Welters R.E., Gliddon C., 2002. Inferring patterns of dispersal from allele frequency data. In: Bullock J.M., Kenward R.E., Hails R. (eds.), Dispersal ecology, Blackwell Science, Oxford, pp. 89-111. Rohmeder E., 1972. Das Saatgut in der Forstwirtschaft [The seeds in forestry]. Parey, Hamburg, 273 p.Sagnard F., Pichot C., Dreyfus P., Jordano P., Fady B., 2007. Modelling seed dispersal to predict seedling recruitment: recolonization dynamics in a plantation forest. Ecological Modeling 203: 464-474. DOI: 10.1016/j. ecolmodel.2006.12.008 Sagnard F., Oddou-Muratorio S., Pichot C., Vendramin G.G., Fady B., 2011. Effects of seed dispersal, adult tree and seedling density on the spatial genetic structure of regeneration at fine temporal and spatial scales. Tree Genetics & Genomes 7: 37-48. DOI: 10.1007/s11295- 010-0313-y Sánchez J.M.C., Greene D.F., Quesada M., 2011. A field test of inverse modeling of seed dispersal. American Journal of Botany 98: 698-703. DOI: 10.3732/ ajb.1000152 Schippers P., Jongejans E., 2005. Release thresholds strongly determine the range of seed dispersal by wind. Ecological Modeling 185: 93-103. DOI: 10.1016/j. ecolmodel.2004.11.018 Schurr F.M., Bond W.J., Midgley G.F., Higgins S.I., 2005. A mechanistic model for secondary seed dispersal by wind and its experimental validation. Journal of Ecology 93: 1017-1028. DOI: 10.1111/j.1365- 2745.2005.01018.x Schütt P., 1991. Tannenarten Europas und Kleinasiens [Fir species in Europe and Asia Minor]. Verlag Birkhäuser, Basel, 136 p. DOI: 10.1007/978-3-0348-7689-6 Skarpaas O., Shea K., Bullock J.M., 2005. Optimizing dispersal study design by Monte Carlo simulation. Journal of Applied Ecology 42: 731-739. DOI: 10.1111/j.1365- 2664.2005.01056.x Skrzypczyńska M., Sudoł-Kornalewicz A., Kornalewicz A., Biczak J., Rodkiewicz S., 2001. Cono-and seminiphagous insects of Abies alba Mill. in the Gorce National Park in Poland during 1996-1998. Journal of Pest Science 74: 138-143. DOI: 10.1046/j.1439- 0280.2001.01027.x Snyder R.E., Chesson P., 2004. How the spatial scales of dispersal, competition, and environmental heterogeneity interact to affect co-existence. The American Naturalist 164: 633-650. DOI: 10.1086/424969 Suszka B., 1983. Rozmnażanie generatywne [Generative propagation]. In Białobok S. (ed.), Jodła pospolita Abies alba Mill., PWN, Warsaw, pp. 175-265. Tackenberg O., 2003. Modeling long distance dispersal of plant diaspores by wind. Ecological Monographs 73: 173-189. DOI: 10.1890/0012-9615(2003)073[0173:MLDOPD]2.0. CO;2 Trepińska J., Kowanetz K., 2000. Dependence of wind direction and speed on the orography in the western part of the Beskidy Mountains. Prace Geograficzne 105: 165-181. Turner M.G., Turner D.M., Romme W.H., Tinker D.B., 2007. Cone production in young post-fire Pinus contorta stands in Greater Yellowstone (USA). Forest Ecology and Management 242: 119-126. DOI: 10.1016/j. foreco.2006.12.032 Vornam B., Decarli N., Gailing O., 2004. Spatial distribution of genetic variation in a natural beechstand (Fagus sylvatica L.) based on microsatellite markers. Conservation Genetics 5: 561-570. DOI:10.1023/B:COGE.0000041025.82917.ac Westcott D.A., Bentrupperbaumer J., Bradford M.G., McKeown A., 2005. Incorporating patterns of disperser behaviour into models of seed dispersal and its effects on estimated dispersal curves. Oecologia 146: 57-67. DOI: 10.1007/s00442-005-0178-1

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2020-03-02

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