Long-term seed burial reveals differences in the seed-banking strategies of naturalized and invasive alien herbs

. 2022 May 25 ; 12 (1) : 8859. [epub] 20220525

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35614334
Odkazy

PubMed 35614334
PubMed Central PMC9132925
DOI 10.1038/s41598-022-12884-0
PII: 10.1038/s41598-022-12884-0
Knihovny.cz E-zdroje

Soil seed viability and germinability dynamics can have a major influence on the establishment and spread of plants introduced beyond their native distribution range. Yet, we lack information on how temporal variability in these traits could affect the invasion process. To address this issue, we conducted an 8-year seed burial experiment examining seed viability and germinability dynamics for 21 invasive and 38 naturalized herbs in the Czech Republic. Seeds of most naturalized and invasive species persisted in the soil for several years. However, naturalized herbs exhibited greater seed longevity, on average, than invasive ones. Phylogenetic logistic models showed that seed viability (but not germinability) dynamics were significantly related to the invasion status of the study species. Seed viability declined earlier and more sharply in invasive species, and the probability of finding viable seeds of invasive species by the end of the experiment was low. Our findings suggest that invasive herbs might take advantage of high seed viability in the years immediately after dispersal, while naturalized species benefit from extended seed viability over time. These differences, however, are not sufficiently strong to explain the invasiveness of the species examined.

Zobrazit více v PubMed

Simberloff D, et al. Impacts of biological invasions: what’s what and the way forward. Trends Ecol. Evol. 2013;28:58–66. doi: 10.1016/j.tree.2012.07.013. PubMed DOI

Pyšek P, et al. Scientists’ warning on invasive alien species. Biol. Rev. 2020;95:1511–1534. doi: 10.1111/brv.12627. PubMed DOI PMC

Daru BH, et al. Widespread homogenization of plant communities in the Anthropocene. Nat. Commun. 2021;12:6983. doi: 10.1038/s41467-021-27186-8. PubMed DOI PMC

Bradley BA, et al. Global change, global trade, and the next wave of plant invasions. Front. Ecol. Environ. 2012;10:20–28. doi: 10.1890/110145. DOI

Pyšek P, Richardson DM. Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W, editor. Biological Invasions. Berlin: Springer; 2007. pp. 97–125.

Pyšek P, et al. Naturalization of central European plants in North America: Species traits, habitats, propagule pressure, residence time. Ecology. 2015;96:762–774. doi: 10.1890/14-1005.1. PubMed DOI

Colautti RI, Grigorovich IA, MacIsaac HJ. Propagule pressure: A null model for biological invasions. Biol. Invasions. 2006;8:1023–1037. doi: 10.1007/s10530-005-3735-y. DOI

Richardson DM, Pyšek P. Naturalization of introduced plants: Ecological drivers of biogeographic patterns. New Phytol. 2012;196:383–396. doi: 10.1111/j.1469-8137.2012.04292.x. PubMed DOI

Moravcová L, Pyšek P, Jarošík V, Pergl J. Getting the right traits: Reproductive and dispersal characteristics predict the invasiveness of herbaceous plant species. PLoS ONE. 2015;10:e0123634. doi: 10.1371/journal.pone.0123634. PubMed DOI PMC

Thompson K, Bakker JP, Bekker RM. Soil Seed Banks of NW Europe: Methodology, Density and Longevity. Cambridge: Cambridge University Press; 1997.

Walck JL, Baskin JM, Baskin CC, Hidayati SN. Defining transient and persistent seed banks in species with pronounced seasonal dormancy and germination patterns. Seed Sci. Res. 2005;15:189–196. doi: 10.1079/SSR2005209. DOI

Gioria M, Le Roux JJ, Hirsch H, Moravcová L, Pyšek P. Characteristics of the soil seed bank of invasive and non-invasive plants in their native and alien distribution range. Biol. Invasions. 2019;21:2313–2332. doi: 10.1007/s10530-019-01978-y. DOI

Gioria M, et al. Persistent soil seed banks promote naturalization and invasiveness in flowering plants. Ecol. Lett. 2021;24:1655–1667. doi: 10.1111/ele.13783. PubMed DOI PMC

Gioria M, Pyšek P, Moravcová L. Soil seed banks in plant invasions: Promoting species invasiveness and long-term impact on plant community dynamics. Preslia. 2012;84:327–350.

Venable DL. Bet hedging in a guild of desert annuals. Ecology. 2007;88:1086–1090. doi: 10.1890/06-1495. PubMed DOI

Venable DL, Brown JS. The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. Am. Nat. 1988;131:360–384. doi: 10.1086/284795. DOI

Adams VM, Marsh DM, Knox JS. Importance of the seed bank for population viability and population monitoring in a threatened wetland herb. Biol. Conserv. 2005;124:425–436. doi: 10.1016/j.biocon.2005.02.001. DOI

Harper J. The Population Biology of Plants. London: Academic Press; 1977.

Warr SJ, Thompson K, Kent M. Seed banks as a neglected area of biogeographic research: A review of literature and sampling techniques. Progr. Phys. Geogr. 1993;17:329–347. doi: 10.1177/030913339301700303. DOI

Thompson K, Bakker JP, Bekker RM, Hodgson J. Ecological correlates of seed persistence in soil in the north-west European flora. J. Ecol. 1998;86:163–169. doi: 10.1046/j.1365-2745.1998.00240.x. DOI

Gioria M, Pyšek P, Baskin C, Carta A. Phylogenetic relatedness mediates persistence and density of soil seed banks. J. Ecol. 2020;108:2121–2131. doi: 10.1111/1365-2745.13437. DOI

Pyšek P, et al. The global invasion success of Central European plants is related to distribution characteristics in their native range and species traits. Divers. Distrib. 2009;15:891–903. doi: 10.1111/j.1472-4642.2009.00602.x. DOI

Gallagher RV, Randall RP, Leishman MR. Trait differences between naturalized and invasive plant species independent of residence time and phylogeny. Conserv. Biol. 2015;29:360–369. doi: 10.1111/cobi.12399. PubMed DOI PMC

Chesson PL, Warner RR. Environmental variability promotes coexistence in lottery competitive systems. Am. Nat. 1981;117:923–943. doi: 10.1086/283778. DOI

Gioria M, Pyšek P. Early bird catches the worm: Germination as a critical step in plant invasion. Biol. Invasions. 2017;19:1055–1080. doi: 10.1007/s10530-016-1349-1. DOI

Gioria M, Pyšek P, Osborne B. Timing is everything: Does early and late germination favor invasions by herbaceous alien plants? J. Plant Ecol. 2018;11:4–16.

Gioria M, Osborne BA. Resource competition in plant invasions: Emerging patterns and research needs. Front. Plant Sci. 2014;5:1–21. doi: 10.3389/fpls.2014.00501. PubMed DOI PMC

D'Antonio CM, Dudley TL, Mack MC. Disturbance and biological invasions: Direct effects and feedbacks. In: Walker L, editor. Ecosystems of Disturbed Ground. Oxford: Elsevier; 1999. pp. 413–452.

Davis MA, Grime JP, Thompson K. Fluctuating resources in plant communities: A general theory of invasibility. J. Ecol. 2000;88:528–534. doi: 10.1046/j.1365-2745.2000.00473.x. DOI

Hierro JL, Villarreal D, Eren Ö, Graham JM, Callaway RM. Disturbance facilitates invasion: The effects are stronger abroad than at home. Am. Nat. 2006;168:144–156. doi: 10.1086/505767. PubMed DOI

Chytrý M, et al. Habitat invasions by alien plants: A quantitative comparison among Mediterranean, subcontinental and oceanic regions of Europe. J. Appl. Ecol. 2008;45:448–458. doi: 10.1111/j.1365-2664.2007.01398.x. DOI

Templeton A, Levin D. Evolutionary consequences of seed pools. Am. Nat. 1979;114:232–249. doi: 10.1086/283471. DOI

Honnay O, Bossuyt B, Jacquemyn H, Shimono A, Uchiyama K. Can a seed bank maintain the genetic variation in the above ground plant population? Oikos. 2008;117:1–5. doi: 10.1111/j.2007.0030-1299.16188.x. DOI

Donohue K, Rubio de Casas R, Burghardt L, Kovach K, Willis CG. Germination, post-germination adaptation, and species ecological ranges. Annu. Rev. Ecol. Evol. Syst. 2010;41:293–319. doi: 10.1146/annurev-ecolsys-102209-144715. DOI

Gioria M, Osborne B, Pyšek P. Soil seed banks under a warming climate. In: Baskin C, Baskin J, editors. Plant Regeneration from Seeds: A global Warming Perspective. London: Academic Press; 2022. pp. 285–298.

Blossey B, Nuzzo V, Davalos A. Climate and rapid local adaptation as drivers of germination and seed bank dynamics of Alliaria petiolata (garlic mustard) in North America. J. Ecol. 2017;105:1485–1495. doi: 10.1111/1365-2745.12854. DOI

Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ, Licari D. Life-history correlates of plant invasiveness at regional and continental scales. Ecol. Lett. 2005;8:1066–1074. doi: 10.1111/j.1461-0248.2005.00809.x. DOI

Richardson DM, Kluge RL. Seed banks of invasive Australian Acacia species in South Africa: Role in invasiveness and options for management. Persp. Plant Ecol. Evol. Syst. 2008;10:161–177. doi: 10.1016/j.ppees.2008.03.001. DOI

Hartzler RG, Buhler DD, Stoltenberg DE. Emergence characteristics of four annual weed species. Weed Sci. 1999;47:578–584. doi: 10.1017/S0043174500092298. DOI

Skálová H, Moravcová L, Čuda J, Pyšek P. Seed-bank dynamics of native and invasive Impatiens species during a five-year field experiment under various environmental conditions. NeoBiota. 2019;50:75–95. doi: 10.3897/neobiota.50.34827. DOI

Moravcová L, Pyšek P, Krinke L, Pergl J, Perglová I, Thompson K. Seed germination, dispersal and seed bank in Heracleum mantegazzianum. In: Pyšek P, Cock MJW, Nentwig W, Ravn H, editors. Ecology and Management of Giant Hogweed (Heracleum mantegazzianum) Wallingford: CAB International; 2007. pp. 74–91.

Gioria M, Osborne B. Assessing the impact of plant invasions on soil seed bank communities: Use of univariate and multivariate statistical approaches. J. Veg. Sci. 2009;20:547–556. doi: 10.1111/j.1654-1103.2009.01054.x. DOI

Long RL, et al. Seed persistence in the field may be predicted by laboratory-controlled aging. Weed Sci. 2008;56:523–528. doi: 10.1614/WS-07-189.1. DOI

Carta A, Bottega S, Spanò C. Aerobic environment ensures viability and antioxidant capacity when seeds are wet with negative effect when moist: Implications for persistence in the soil. Seed Sci. Res. 2018;28:16–23. doi: 10.1017/S0960258517000307. DOI

Pyšek P, et al. Catalogue of alien plants of the Czech Republic (2nd edition): Checklist update, taxonomic diversity and invasion patterns. Preslia. 2012;84:155–255.

Thompson K, Band S, Hodgson J. Seed size and shape predict persistence in soil. Funct. Ecol. 1993;7:236–241. doi: 10.2307/2389893. DOI

Moles AT, Hodson DW, Webb CJ. Seed size and shape and persistence in the soil in the New Zealand flora. Oikos. 2000;89:541–545. doi: 10.1034/j.1600-0706.2000.890313.x. DOI

Leon RG, Owen MDK. Artificial and natural seed banks differ in seedling emergence patterns. Weed Sci. 2004;52:531–537. doi: 10.1614/WS-03-048R2. DOI

Thompson K, Grime PJ. Seasonal variation in seed banks of herbaceous species in ten contrasting habitats. J. Ecol. 1979;67:893–921. doi: 10.2307/2259220. DOI

Lambrinos JG. Spatially variable propagule pressure and herbivory influence invasion of chaparral shrubland by an exotic grass. Oecologia. 2006;147:327–334. doi: 10.1007/s00442-005-0259-1. PubMed DOI

Wainwright CE, Wolkovich EM, Cleland EE. Seasonal priority effects: Implications for invasion and restoration in a semi-arid system. J. Appl. Ecol. 2012;49:234–241. doi: 10.1111/j.1365-2664.2011.02088.x. DOI

Moravcová L, Pyšek P, Jarošík V, Havlíčková V, Zákravský P. Reproductive characteristics of neophytes in the Czech Republic: Traits of invasive and non-invasive species. Preslia. 2010;82:365–390.

Grime JP. Plant Strategies, Vegetation Processes, and Ecosystem Properties. 2. Oxford: John Wiley & Sons; 2001.

Mihulka S, Pyšek P, Pyšek A. Oenothera coronifera, a new alien species for the Czech flora, and Oenothera stricta, recorded again after two centuries. Preslia. 2003;75:263–270.

Fenner M, Thompson K. The Ecology of Seeds. Cambridge: Cambridge University Press; 2005.

Grime JP, Hodgson JG, Hunt R. Comparative Plant Ecology: A Functional Approach to Common British Species. 2. Colvend, Dalbeattie, Kirkcudrightshire, Scotland: Castlepoint Press; 2007.

Gioria M, Osborne B. Similarities in the impact of three large invasive plant species on soil seed bank communities. Biol. Invasions. 2010;12:1671–1683. doi: 10.1007/s10530-009-9580-7. DOI

Gioria M, Pyšek P. The legacy of plant invasions: Changes in the soil seed bank of invaded plant communities. Bioscience. 2016;66:40–53. doi: 10.1093/biosci/biv165. DOI

Carta A, Hanson S, Müller JV. Plant regeneration from seeds responds to phylogenetic relatedness and local adaptation in Mediterranean Romulea (Iridaceae) species. Ecol. Evol. 2016;6:4166–4178. doi: 10.1002/ece3.2150. PubMed DOI PMC

Arène F, Affre L, Doxa A, Saatkamp A. Temperature but not moisture response of germination shows phylogenetic constraints while both interact with seed mass and lifespan. Seed Sci. Res. 2017;27:110–120. doi: 10.1017/S0960258517000083. DOI

Zhang C, Willis CG, Donohue K, Ma Z, Du G. Effects of environment, life-history and phylogeny on germination strategy of 789 angiosperms species on the eastern Tibetan Plateau. Ecol. Indic. 2021;129:107974. doi: 10.1016/j.ecolind.2021.107974. DOI

Zheng J, Guo Z, Wang X. Seed mass of angiosperm woody plants better explained by life history traits than climate across China. Sci. Rep. 2017;7:2741. doi: 10.1038/s41598-017-03076-2. PubMed DOI PMC

Thompson K, Ceriani RM, Bakker JP, Bekker RM. Are seed dormancy and persistence in soil related? Seed Sci. Res. 2003;13:97–100. doi: 10.1079/SSR2003128. DOI

Long RL, et al. The ecophysiology of seed persistence: A mechanistic view of the journey to germination or demise. Biol. Rev. Camb. Philos. Soc. 2015;90:31–59. doi: 10.1111/brv.12095. PubMed DOI

Moodley D, Geerts S, Richardson DM, Wilson JRU. Different traits determine introduction, naturalization and invasion success in woody plants: Proteaceae as a test case. PLoS ONE. 2013;8:e75078. doi: 10.1371/journal.pone.0075078. PubMed DOI PMC

Pyšek P, Sádlo J, Mandák B. Catalogue of alien plants of the Czech Republic. Preslia. 2002;74:97–186.

Pyšek P, Richardson DM, Rejmánek M, Webster G, Williamson M, Kirschner J. Alien plants in checklists and floras: Towards better communication between taxonomists and ecologists. Taxon. 2004;53:131–143. doi: 10.2307/4135498. DOI

WFO World Flora Online. http://www.worldfloraonline.org (2021).

Hadfield JD, Nakagawa S. General quantitative genetic methods for comparative biology: Phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 2010;23:494–508. doi: 10.1111/j.1420-9101.2009.01915.x. PubMed DOI

Ellis RH, Roberts EH. Improved equations for the prediction of seed longevity. Ann. Bot. 1980;45:13–30. doi: 10.1093/oxfordjournals.aob.a085797. DOI

Butler LH, Hay FR, Ellis RH, Smith RD, Murray TB. Priming and re-drying improve the survival of mature seeds of Digitalis purpurea during storage. Ann. Bot. 2009;103:1261–1270. doi: 10.1093/aob/mcp059. PubMed DOI PMC

Jin Y, Qian HV. PhyloMaker: An R package that can generate very large phylogenies for vascular plants. Ecography. 2019;42:1353–1359. doi: 10.1111/ecog.04434. DOI

Qian H, Jin Y. Are phylogenies resolved at the genus level appropriate for studies on phylogenetic structure of species assemblages? Plant Divers. 2021;43:255–263. doi: 10.1016/j.pld.2020.11.005. PubMed DOI PMC

Smith SA, Brown JW. Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 2018;105:302–314. doi: 10.1002/ajb2.1019. PubMed DOI

de Villemereuil P, Nakagawa S. General quantitative genetic methods for comparative biology. In: Garamszegi LZ, editor. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology. Berlin: Springer-Verlag; 2014. pp. 287–303.

Blomberg SP, Garland T, Jr, Ives AR. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution. 2003;57:717–745. doi: 10.1111/j.0014-3820.2003.tb00285.x. PubMed DOI

Revell LJ, Harmon LJ, Collar DC. Phylogenetic signal, evolutionary process, and rate. Syst. Biol. 2008;57:591–601. doi: 10.1080/10635150802302427. PubMed DOI

R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2022). Available online at: https://www.R-project.org

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...