Abstract
Understanding shifts in traits across the course of an invasion can significantly increase our understanding of mechanisms underpinning range expansion. For example, shifts to traits associated with faster growth may be advantageous in range edge populations of invasive species to decrease generation time and thus promote rapid range expansion. We tested whether populations at the expanding range edges of two coastal plant species invasive in eastern Australia (Gladiolus gueinzii Kunze and Hydrocotyle bonariensis Lam.) possessed different carbon capture strategies compared with range core populations where they were first introduced. Pairwise leaf trait relationships between specific leaf area (SLA), photosynthetic rate (Amass), foliar nitrogen (Nmass) and foliar phosphorus (Pmass) were investigated for range edge and range core populations using standardised major axis (SMA) regression. Across species, SMA regression slopes for range core and range edge populations for all pairwise comparisons did not differ significantly from each other, suggesting that each species has a similar carbon capture strategy across its range. However, at a species level, H. bonariensis displayed significant shifts in trait values along a common regression slope for many pairwise comparisons. Range edge populations were found to have higher values for Nmass, Amass and SLA compared to range core populations and displayed greater nutrient use efficiency, suggesting that range edge populations are positioned further along the leaf economics spectrum towards faster growth strategies. In contrast, for G. gueinzii, leaf traits were positioned along a common regression slope with no difference in the trait values of range core and range edge populations. Our results suggest that there is selection for faster carbon capture strategies at range edges for some introduced species undergoing range expansion and this may be a contributing factor in explaining rapid range advance.
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Alexander HM, Price S, Houser R et al (2007) Is there reduction in disease and pre-dispersal seed predation at the border of a host plant’s range? Field and herbarium studies of Carex blanda. J Ecol 95:446–457. https://doi.org/10.1111/j.1365-2745.2007.01228.x
Amundsen PA, Salonen E, Niva T et al (2012) Invader population speeds up life history during colonization. Biol Invasions 14:1501–1513. https://doi.org/10.1007/s10530-012-0175-3
Berthouly-Salazar C, van Rensburg BJ, Le Roux JJ, van Vuuren BJ, Hui C (2012) Spatial sorting drives morphological variation in the invasive bird, Acridotheris tristis. PLoS ONE 7:1–9. https://doi.org/10.1371/journal.pone.0038145
Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889. https://doi.org/10.2307/2261425
Boeye J, Travis JMJ, Stoks R, Bonte D (2013) More rapid climate change promotes evolutionary rescue through selection for increased dispersal distance. Evol Appl 6:353–364. https://doi.org/10.1111/eva.12004
Bøhn T, Sandlund OT, Amundsen P, Primicerio R (2004) Rapidly changing life history during invasion. Oikos 106:138–150. https://doi.org/10.1111/j.0030-1299.2004.13022.x
Brown GP, Shilton C, Phillips BL, Shine R (2007) Invasion, stress, and spinal arthritis in cane toads. Proc Natl Acad Sci USA 104:17698–17700. https://doi.org/10.1073/pnas.0705057104
Brown GP, Kelehear C, Shine R (2013) The early toad gets the worm: cane toads at an invasion front benefit from higher prey availability. J Anim Ecol 82:854–862. https://doi.org/10.1111/1365-2656.12048
Carol J, Benejam L, Benito J, García-Berthou E (2009) Growth and diet of European catfish (Silurus glanis) in early and late invasion stages. Fundam Appl Limnol Arch Hydrobiol 174:317–328. https://doi.org/10.1127/1863-9135/2009/0174-0317
Chuang A, Peterson CR (2016) Expanding population edges: theories, traits, and trade-offs. Glob Chang Biol 22:494–512. https://doi.org/10.1111/gcb.13107
Clavera M, García-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110. https://doi.org/10.1016/j.tree.2005.01.003
Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10:248–252. https://doi.org/10.1016/S0169-5347(00)89081-3
Cwynar LC, MacDonald GM (1987) Geographical variation in lodgepole pine in relation to population history. Am Nat 130:526–543. https://doi.org/10.2307/2678832
Dangremond EM, Feller IC (2016) Precocious reproduction increases at the leading edge of a mangrove range expansion. Ecol Evol 6:5087–5092. https://doi.org/10.10002/ece3.2270
Evans GA, Kilkenny FF, Galloway LF (2013) Evolution of competitive ability within Lonicera japonica’s invaded range. Int J Plant Sci 174:740–748. https://doi.org/10.1086/669928
Feiner ZS, Aday DD, Rice JA (2012) Phenotypic shifts in white perch life history strategy across stages of invasion. Biol Invasions 14:2315–2329. https://doi.org/10.1007/s10530-012-0231-z
González APR, Chrtek J, Dobrev PI, Dumalasová V, Fehrer J et al (2016) Stress-induced memory alters growth of clonal offspring of white clover (Trifolium repens). Am J Bot 103:1567–1574. https://doi.org/10.3732/ajb.1500526
González-Rodríguez V, Villar R, Navarro-Cerrillo RM (2011) Maternal influences on seed mass effect and initial seedling growth in four Quercus species. Acta Oecol 37:1–9. https://doi.org/10.1016/j.actao.2010.10.006
Hanski I, Saastamoinen M, Ovaskainen O (2006) Dispersal-related life-history trade-offs in a butterfly metapopulation. J Anim Ecol 75:91–100. https://doi.org/10.1111/j.1365-2656.2005.01024.x
Hedja M, Pyšek P, Jarošík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol 97:393–403. https://doi.org/10.1111/j.1365-2745.2009.01480.x
Herban T, Šerá B, Klimešová J (2015) Clonal growth and sexual reproduction: tradeoffs and environmental constraints. Oikos 124:469–476. https://doi.org/10.1111/oik.01692
Heyligers PC (1998) Some New South Wales coastal plant distributions: a comparison of herbarium records with transect survey data. Cunninghamia 5:645–664
Heyligers PC (1999) Dispersal of the exotic coastal dune plants Gladiolus gueinzii and Trachyandra divaricata in Australia. Cunninghamia 6:315–330
Heyligers PC (2008) Flora of the Stockton and Port Hunter sandy foreshores with comments on fifteen notable introduced species. Cunninghamia 10:493–511
Houston BE, Rooke AC, Borwnscombe JW, Fox MG (2013) Overwinter survival, energy storage and reproductive allocation in the invasive round goby (Neogobius melanostomus) from a river system. Ecol Freshw Fish 23:224–233. https://doi.org/10.1111/eff.12071
Huang F, Peng S (2016) Intraspecific competitive ability declines towards the edge of the expanding range of the invasive vine Mikania micrantha. Oecologia 181:115–123. https://doi.org/10.1007/s00442-015-3526-9
Huang F, Peng S, Chen B, Liao H, Huang Q et al (2015) Rapid evolution of dispersal-related traits during range expansion of an invasive vine Mikania micrantha. Oikos 124:1023–1030. https://doi.org/10.1111/oik.01820
Hughes CL, Hill JK, Dytham C (2003) Evolutionary trade-offs between reproduction and dispersal in populations at expanding range boundaries. Proc Biol Sci 270:S147–S150. https://doi.org/10.1098/rsbl.2003.0049
Kambo D, Kotanen PM (2014) Latitudinal trends in herbivory and performance of an invasive species, common burdock (Arctium minus). Biol Invasions 16:101–112. https://doi.org/10.1007/s10530-013-0506-z
Kilkenny FF, Galloway LF (2013) Adaptive divergence at the margin of an invaded range. Evolution 67:722–731. https://doi.org/10.1111/j.1558-5646.2012.01829.x
Kilkenny FF, Galloway LF (2016) Evolution of marginal populations of an invasive vine increases the likelihood of future spread. New Phytol 209:1773–1780. https://doi.org/10.1111/nph.13702
Kubisch A, Fronhofer EA, Poethke HJ, Hovestadt T (2013) Kin competition as a major driving force for invasions. Am Nat 181:700–706. https://doi.org/10.1086/670008
Leishman MR, Haslehurst T, Ares A, Baruch Z (2007) Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytol 176:635–643. https://doi.org/10.1111/j.1469-8137.2007.02189.x
Leishman MR, Thomson VP, Cooke J (2010) Native and exotic invasive plants have fundamentally similar carbon capture strategies. J Ecol 98:28–42. https://doi.org/10.1111/j.1365-2745.2009.01608.x
Ling SD, Johnson CR, Frusher S, King CK (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Glob Chang Biol 14:907–915. https://doi.org/10.1111/j.1365-2486.2008.01543.x
Lopez DP, Jungman AA, Rehage JS (2012) Nonnative African jewelfish are more fit but not bolder at the invasion front: a trait comparison across an Everglades range expansion. Biol Invasions 14:2159–2174. https://doi.org/10.1007/s10530-012-0221-1
Macel M, Dostálek T, Esch S, Bucharová A, van Dam NM et al (2017) Evolutionary responses to climate change in a range expanding plant. Oecologia 184:543–554. https://doi.org/10.1007/s00442-017-3864-x
Masson L, Brownscombe JW, Fox MG (2016) Fine scale spatio-temporal life history shifts in an invasive species at its expansion front. Biol Invasions 18:775–792. https://doi.org/10.1007/s10530-015-1047-4
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492. https://doi.org/10.1890/070064
Moran EV, Alexander JM (2014) Evolutionary responses to global change: lessons from invasive species. Ecol Lett 17:637–649. https://doi.org/10.1111/ele.12262
Murray B, Phillips M (2012) Temporal introduction patterns of invasive alien plant species to Australia. NeoBiota 13:1. https://doi.org/10.3897/neobiota.13.2422
Pérez-Harguindeguy N, Díaz S, Vendramini F, Cornelissen JHC, Gurvich DE et al (2003) Leaf traits and herbivore selection in the field and in cafeteria experiments. Austral Ecol 28:642–650. https://doi.org/10.1046/j.1442-9993.2003.01321.x
Phillips BL (2009) The evolution of growth rates on an expanding range edge. Biol Lett 5:802–804. https://doi.org/10.1098/rsbl.2009.0367
Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803. https://doi.org/10.1038/439803a
Phillips BL, Brown GP, Shine R (2010) Life-history evolution in range-shifting populations. Ecology 91:1617–1627. https://doi.org/10.1890/09-0910.1
Platenkamp GAJ, Shaw RG (1993) Environmental and genetic maternal effects on seed characters in Nemophila menziesii. Evolution 47:540–555. https://doi.org/10.1111/j.1558-5646.1993.tb02112.x
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci 94:13730–13734. https://doi.org/10.1073/pnas.94.25.13730
Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C et al (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969. https://doi.org/10.1890/0012-9658(1999)080%5b1955:goltra%5d2.0.co;2
Sagarin RD, Gaines SD (2002) Geographical abundance distributions of coastal invertebrates: using one-dimensional ranges to test biogeographic hypotheses. J Biogeogr 29:985–997. https://doi.org/10.1046/j.1365-2699.2002.00705.x
Samis KE, Eckert CG (2007) Testing the abundant center model using range-wide demographic surveys of two coastal dune plants. Ecology 88:1747–1758. https://doi.org/10.1890/06-1153.1
Sanford E, Holzman SB, Haney RA, Rand DM, Bertness MD (2006) Larval tolerance, gene flow, and the northern geographic range limits of fiddler crabs. Ecology 87:2882–2894. https://doi.org/10.1890/0012-9658(2006)87
Siemann E, Rogers WE (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4:514–518. https://doi.org/10.1046/j.1461-0248.2001.00274.x
Siemann E, Rogers WE, Dewalt SJ (2006) Rapid adaptation of insect herbivores to an invasive plant. Proc R Soc B 273:2763–2769. https://doi.org/10.1098/rspb.2006.3644
Simmons AD, Thomas CD (2004) Changes in dispersal during species’ range expansions. Am Nat 164:378–395. https://doi.org/10.1086/423430
Tabassum S, Leishman MR (2018a) Does enemy damage vary across the range of exotic plant species? Evidence from two coastal dune plant species in eastern Australia. Oecologia 186:303–309. https://doi.org/10.1007/s00442-017-4008-z
Tabassum S, Leishman MR (2018b) Have your cake and eat it too: greater dispersal ability and faster germination towards range edges of an invasive plant species in eastern Australia. Biol Invasions 20:1199–1210. https://doi.org/10.1007/s10530-017-1620-0
Tabassum S, Leishman MR (2019) It doesn’t take two to tango: increased capacity for self-fertilization towards range edges of two coastal invasive plant species in eastern Australia. Biol Invasions 21:2489–2501. https://doi.org/10.1007/s10530-019-01989-9
Therry L, Lefevre E, Bonte D, Stoks R (2014a) Increased activity and growth rate in the non-dispersive aquatic larval stage of a damselfly at an expanding range edge. Freshw Biol 59:1266–1277. https://doi.org/10.1111/fwb.12346
Therry L, Nilsson-Örtman V, Bonte D, Stoks R (2014b) Rapid evolution of larval life history, adult immune function and flight muscles in a poleward-moving damselfly. J Evol Biol 27:141–152. https://doi.org/10.1111/jeb.12281
Therry L, Zawal A, Bonte D, Stoks R (2014c) What factors shape female phenotypes of a poleward-moving damselfly at the edge of its range? Biol J Linn Soc 112:556–568. https://doi.org/10.1111/bij.12295
Travis JMJ, Dytham C (2002) Dispersal evolution during invasions. Evol Ecol Res 4:1119–1129
van Kleunen M, Fischer M (2003) Effects of four generations of density-dependent selection on life history traits and their plasticity in a clonally propagated plant. J Evol Biol 16:474–484. https://doi.org/10.1046/j.1420-9101.2003.00532.x
van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. https://doi.org/10.1111/j.1461-0248.2009.01418.x
Van Petegem KHP, Boeye J, Stoks R, Bonte D (2016) Spatial selection and local adaptation jointly shape life-history evolution during range expansion. Am Nat 188:485–498. https://doi.org/10.1086/688666
Vergeer P, Kunin WE (2011) Life history variation in Arabidopsis lyrata across its range: effects of climate, population size and herbivory. Oikos 120:979–990. https://doi.org/10.1111/j.1600-0706.2010.18944.x
Warton DI, Duursma RA, Falster DS, Taskinen S (2012) SMATR 3—an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259. https://doi.org/10.1111/j.2041-210X.2011.00153.x
Weiner J, Martinez S, Muller-Scharer H, Stol P, Schmid B (1997) How important are environmental maternal effects in plants? A study with Centaurea maculosa. J Ecol 85:133–142. https://doi.org/10.2307/2960645
Wright IJ, Westoby M, Reich PB, Oleksyn J, Ackerly DD et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Acknowledgements
We thank Joshua Griffiths, Veronica Shaw, Claire Laws, Guyo Gufu, James Lawson and Rachael Gallagher for kind assistance in the field. We thank Muhammad Masood for assistance with glasshouse operations and conducting the leaf nitrogen analysis and David Appleton from the University of Queensland for conducting leaf phosphorus analysis. Joshua Griffiths and Anthony Manea provided helpful comments on earlier versions of this manuscript. This research was supported by the Tony Price Award from the Department of Biological Sciences at Macquarie University and a Research Training Program scholarship from the Australian Government, awarded to S.T.
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Tabassum, S., Leishman, M.R. Mixed evidence for shifts to faster carbon capture strategies towards range edges of two coastal invasive plants in eastern Australia. Biol Invasions 22, 563–575 (2020). https://doi.org/10.1007/s10530-019-02111-9
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DOI: https://doi.org/10.1007/s10530-019-02111-9