Abstract
Understanding why alien species become dominant in recipient communities requires a biogeographical perspective comparing the ecology of native and introduced populations. The genus Centaurea (Asteraceae) is well-known in invasion ecology because several aggressive invaders, including Centaurea melitensis L., belong to this genus. We compared the competitive ability of C. melitensis individuals from Spain (native range) and Chile (invaded range) when competing against Helenium aromaticum (Hook.) L.H. Bailey, a native relative from Chile. We performed germination bioassays and common garden competition experiments to compare: (1) the germination capacities of C. melitensis (Spain and Chile) and H. aromaticum (2) the potential allelopathic effect of leaf lixiviates of C. melitensis (Spain and Chile) on the seed germination of H. aromaticum, (3) the ability of C. melitensis from both origins to reduce the growth of H. aromaticum. No significant differences in the capacity of seed germination were found among C. melitensis from Chile and Spain and the native H. aromaticum. However, the seed germination of H. aromaticum was inhibited by the presence of C. melitensis leaves from Chile and Spain. Also, the biomass of H. aromaticum was reduced in the presence of C. melitensis, regardless of their origin. Our results demonstrate the competitive superiority of the invasive C. melitensis over H. aromaticum, but we found no evidence of an evolutionary increase in the competitive ability of the invader populations. Therefore, at least part of the invasive potential of C. melitensis seems to be acquired by selective processes in their original range.
Similar content being viewed by others
Availability of data and materials
The datasets generated during the current study will be available in the FIGSHARE repository, https://figshare.com/s/affe156b5afb0ce37bc4.
References
Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686. https://doi.org/10.1890/03-0650
Arroyo MTK, Marticorena C, Matthei O, Cavieres L (2000) Plant invasions in Chile: present patterns and future predictions. In: Mooney HA, Hobbs HA (eds) Invasive Species in a Changing World. Island Press, California, pp 385–421
Atwood JP, Meyerson LA (2011) Beyond EICA: understanding post-establishment evolution requires a broader evaluation of potential selection pressures. NeoBiota 10:7–25. https://doi.org/10.3897/neobiota.10.954
Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive non-indigenous plants: a hypothesis. J Ecol 83:887–889. https://doi.org/10.2307/2261425
Bruno M, Bancheva S, Rosselli S, Maggio A (2013) Sesquiterpenoids in subtribe Centaureinae (Cass.) Dumort (tribe Cardueae, Asteraceae): Distribution, 13C NMR spectral data and biological properties. Phytochemistry 95:19–93. https://doi.org/10.1016/j.phytochem.2013.07.002
Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523. https://doi.org/10.1126/science.290.5491.521
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443. https://doi.org/10.1890/1540-9295(2004)002%5b0436:NWISAT%5d2.0.CO;2
Callaway R, Newingham B, Zabinski CA, Mahall BE (2001) Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbours. Ecol Lett 4:429–433. https://doi.org/10.1046/j.1461-0248.2001.00251.x
Callaway RM, Mahall BE, Wicks C, Pankey J, Zabinski C (2003) Soil fungi and the effects of an invasive forb on grasses: neighbor identity matters. Ecology 84:129–135. https://doi.org/10.1890/0012-9658(2003)084%5b0129:SFATEO%5d2.0.CO;2
Castro SA, Badano E, Guzman D, Cavieres LA (2010) Biological invasion of a refuge habitat: Anthriscus caucalis (Apiaceae) decreases diversity, evenness, and survival of native herbs in the Chilean matorral. Biol Invasions 12:1295–1303. https://doi.org/10.1007/s10530-009-9547-8
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. https://doi.org/10.1046/j.1365-2745.2000.00473.x
Eriksen RL, Desronvil T, Hierro JL, Kesseli R (2012) Morphological differentiation in a common garden experiment among native and non-native specimens of the invasive weed yellow starthistle (Centaurea solstitialis). Biol Invasions 14:1459–1467. https://doi.org/10.1007/s10530-012-0172-6
Fenesi A, Geréd J, Meiners S, Tóthmérész B, Török P, Ruprecht E (2015) Does disturbance enhance the competitive effect of the invasive Solidago canadensis on the performance of two native grasses? Biol Invasions 17:3303–3315. https://doi.org/10.1007/s10530-015-0954-8
Figueroa JA, Castro SA, Marquet PA, Jaksic FM (2004) Exotic plant invasions to the mediterranean region of Chile: causes, history and impacts. Rev Chil Hist Nat 77:465–483. https://doi.org/10.4067/S0716-078X2004000300006
Gerlach JD Jr, Rice KJ (2003) Testing life history correlates of invasiveness using congeneric plant species. Ecol Appl 13:167–179. https://doi.org/10.1890/1051-0761(2003)013%5b0167:TLHCOI%5d2.0.CO;2
Gómez-González S, Cavieres LA, Torres-Morales P, Torres-Díaz C (2009) Competitive effects of the alien invasive Centaurea solstitialis L. on two chilean Baccharis species at different life-cycle stages. Gayana Bot 66:71–83. https://doi.org/10.4067/S0717-66432009000100007
Gómez-González S, Torres-Díaz C, Valencia G, Torres-Morales P, Cavieres LA, Pausas JG (2011a) Anthropogenic fires increase alien and native annual species in the Chilean coastal matorral. Divers Distrib 17:58–67. https://doi.org/10.1111/j.1472-4642.2010.00728.x
Gómez-González S, Torres-Díaz C, Gianoli E (2011b) The effects of fire-related cues on seed germination and viability of Helenium aromaticum (Hook.) H. L. Bailey (Asteraceae). Gayana Bot 68:86–88. https://doi.org/10.4067/S0717-66432011000100007
Gómez-González S, Torres-Díaz C, Bustos-Schindler C, Gianoli E (2011c) Anthropogenic fire drives the evolution of seed traits. PNAS 108:18743–18747. https://doi.org/10.1073/pnas.1108863108
Graebner RC, Callaway RM, Montesinos D (2012) Invasive species grows faster, competes better, and shows greater evolution toward increased seed size and growth than exotic non-invasive congeners. Plant Ecol 213:545–553. https://doi.org/10.1007/s11258-012-0020-x
Grotkopp E, Rejmánek M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94:526–532. https://doi.org/10.3732/ajb.94.4.526
Hajek E, di Castri F (1975) Bioclimatografía de Chile. Ediciones Universidad Católica de Chile, Santiago
He WM, Feng Y, Ridenour WM, Thelen GC, Pollock JL, Diaconu A, Callaway RM (2009) Novel weapons and invasion: biogeographic differences in the competitive effects of Centaurea maculosa and its root exudate (±)-catechin. Oecologia 159:803–815. https://doi.org/10.1007/s00442-008-1234-4
Henery ML, Bowman G, Mráz P, Treier UA, Gex-Fabry E, Schaffner U, Müller-Schärer H (2010) Evidence for a combination of pre-adapted traits and rapid adaptive change in the invasive plant Centaurea stoebe. J Ecol 98:800–813. https://doi.org/10.1111/j.1365-2745.2010.01672.x
Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15. https://doi.org/10.1111/j.0022-0477.2004.00953.x
Hierro JL, Eren Ö, Khetsuriani L, Diaconu A, Török K, Montesinos D, Andonian K, Kikodze D, Janoian L, Villarreal D, Estanga-Mollica ME, Callaway RM (2009) Germination responses of an invasive species in native and non-native ranges. Oikos 118:529–538. https://doi.org/10.1111/j.1600-0706.2009.17283.x
Holmgren M, Avilés R, Sierralta L, Segura AM, Fuentes ER (2000) Why have European herbs so successfully invaded the Chilean matorral? effects of herbivory, soil nutrients, and fire. J Arid Environ 44:197–211. https://doi.org/10.1006/jare.1999.0589
Irimia RE, Lopes SMM, Sotes G, Cavieres L, Eren Ö, Lortie CJ, French K, Hierro JL, Rosche C, Callaway RM, PinhoeMelo TMVD, Montesinos D (2019) Biogeographic differences in the allelopathy of leaf surface extracts of an invasive weed. Biol Invasions 21:3151–3168. https://doi.org/10.1007/s10530-019-02038-1
Jones KW, Sanders DC (1987) The influence of soaking pepper seed in water or potassium salt solutions on germination at three temperatures. J Seed Technol 11:97–102
Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714. https://doi.org/10.1111/j.1461-0248.2005.00769.x
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evolut 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0
Kelsey RG, Locken LJ (1987) Phytotoxic properties of Cnicin, a sesquiterpene lactone from Centaurea maculosa (spotted knapweed). J Chem Ecol 13:19–33. https://doi.org/10.1007/BF01020348
Lamarque LJ, Delzon S, Lortie CJ (2011) Tree invasions: a comparative test of the dominant hypotheses and functional traits. Biol Invasions 13:1969–1989. https://doi.org/10.1007/s10530-011-0015-x
Lejeune KD, Seastedt TR (2001) Centaurea species: the forb that won the west. Conserv Biol 15:1568–1574. https://doi.org/10.1046/j.1523-1739.2001.00242.x
Martín-Forés I, Sánchez-Jardón L, Acosta-Gallo B, del Pozo A, Castro I, de Miguel JM, Ovalle C, Casado MA (2015) From Spain to Chile: environmental filters and success of herbaceous species in Mediterranean-climate regions. Biol Invasions 17:1425–1438. https://doi.org/10.1007/s10530-014-0805-z
Matthei O (1995) Manual de las malezas que crecen en Chile. Alfabeta Impresores, Santiago
Memmott J, Fowler SV, Paynter Q, Sheppard AW, Syrett P (2000) The invertebrate fauna on broom, Cytisus scoparius, in two native and two exotic habitats. Acta Oecol 21:213–222. https://doi.org/10.1016/S1146-609X(00)00124-7
Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. PNAS 98:5446–5451. https://doi.org/10.1073/pnas.091093398
Moroney JR, Rundel PW (2013) Abundance and dispersion of the invasive Mediterranean annual, Centaurea melitensis in its native and non-native ranges. Biol Invasions 15:495–507. https://doi.org/10.1007/s10530-012-0302-1
Moroney JR, Schiffman PM, Brigham CA (2011) Invasive European annual plants impact a rare endemic sunflower. Madroño 58:69–77. https://doi.org/10.3120/0024-9637-58.2.69
Moroney JR, Rundel PW, Sork VL (2013) Phenotypic plasticity and differentiation in fitness-related traits in invasive populations of the mediterranean forb Centaurea melitensis (Asteraceae). Am J Bot 100:2040–2051. https://doi.org/10.3732/ajb.1200543
Muir AD, Majak W (1983) Allelopathic potential of diffuse knapweed (Centaurea diffusa) extracts. Can J Plant Sci 63:989–996. https://doi.org/10.4141/cjps83-124
Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evolut 19:417–422. https://doi.org/10.1016/j.tree.2004.05.010
Niinemets Ü, Valladares F, Ceulemans R (2003) Leaf-level phenotypic variability and plasticity of invasive Rhododendron ponticum and non-invasive Ilex aquifolium co-occurring at two contrasting European sites. Plant, Cell Environ 26:941–956. https://doi.org/10.1046/j.1365-3040.2003.01027.x
Pauchard A, Cavieres LA, Bustamante RO (2004) Comparing alien plant invasions among regions with similar climates: where to from here? Divers Distrib 10:371–375. https://doi.org/10.1111/j.1366-9516.2004.00116.x
Riba M, Rodrigo A, Colas B, Retana J (2002) Fire and species range in Mediterranean landscapes: an experimental comparison of seed and seedling performance among Centaurea taxa. J Biogeogr 29:135–146. https://doi.org/10.1046/j.1365-2699.2002.00652.x
Rodriguez R, Marticorena C, Alarcón D, Baeza C, Cavieres L, Finot VL, Fuentes N, Kiessling A, Mihoc M, Pauchard A, Ruiz E, Sanchez P, Marticorena A (2018) Catalogue of the vascular plants of Chile. Gayana Bot 75:1–430. https://doi.org/10.4067/S0717-66432018000100001
Sotes GJ, Cavieres LA, Montesinos D, Pereira Coutinho AX, Peláez WJ, Lopes SMM, Pinho e Melo TMVD (2015) Inter-regional variation on leaf surface defenses in native and non-native Centaurea solstitialis plants. Biochem Syst Ecol 62:208–218. https://doi.org/10.1016/j.bse.2015.09.003
Vilà M, Weiner J (2004) Are invasive plant species better competitors than native plant species? evidence from pair-wise experiments. Oikos 105:229–238. https://doi.org/10.1111/j.0030-1299.2004.12682.x
Vivanco JM, Bais HP, Stermitz FR, Thelen GC, Callaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–292. https://doi.org/10.1111/j.1461-0248.2004.00576.x
Weir TL, Bais HP, Vivanco JM (2003) Intraspecific and interspecific interactions mediated by a phytotoxin, (–)-catechin, secreted by the roots of Centaurea maculosa (Spotted Knapweed). J Chem Ecol 29:2397–2412. https://doi.org/10.1023/A:1026313031091
Widmer TL, Guermache F, Dolgovskaia MY, Reznik SY (2007) Enhanced growth and seed properties in introduced vs. native populations of yellow starthistle (Centaurea solstitialis). Weed Sci 55:465–473. https://doi.org/10.1614/WS-06-211R.1
Younginger BS, Sirová D, Cruzan MB, Ballhorn DJ (2017) Is biomass a reliable estimate of plant fitness? Appl Plant Sci 5:1600094. https://doi.org/10.3732/apps.1600094
Acknowledgements
This study is part of the research activities of the Institute of Ecology and Biodiversity (IEB), funded by the Agencia Nacional de Investigación y Desarrollo (ANID PIA CCTE AFB-17008). Gastón J. Sotes was funded by a doctoral fellowship (ANID-21100246/2010). Susana Gómez-González was funded by ANID/FONDAP-15110009 and Lohengrin A. Cavieres by ANID/FONDECYT 1171005. The Asociación Universitaria Iberoamericana de Postgrado (AUIP, Spain) also financed some traveling expenses related to this project. Christine Harrower helped with English edition. The authors thank anonymous reviewers for their comments during the revision process.
Funding
This study is part of the research activities of the Institute of Ecology and Biodiversity (IEB), funded by the Agencia Nacional de Investigación y Desarrollo (ANID PIA CCTE AFB-17008). Gastón J. Sotes was funded by a doctoral fellowship (ANID-21100246/2010). Susana Gómez-González was funded by ANID/FONDAP-15110009 and Lohengrin A. Cavieres by ANID/FONDECYT 1171005. The Asociación Universitaria Iberoamericana de Postgrado (AUIP, Spain) also financed some traveling expenses related to this project.
Author information
Authors and Affiliations
Contributions
All of the authors contributed to the conception and design of this study. Preparation of materials, experiments, data collection and analyses were performed by Gastón J. Sotes. Gastón J. Sotes and Susana Gómez-González wrote the draft and Lohengrin A. Cavieres contributed substantially with important comments and editions. All of the authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflicts of interest.
Ethics approval
This study was carried out with permission from the Agricultural and Livestock Services of Chile (SAG).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sotes, G.J., Cavieres, L.A. & Gómez-González, S. High competitive ability of Centaurea melitensis L. (Asteraceae) does not increase in the invaded range. Biol Invasions 23, 693–703 (2021). https://doi.org/10.1007/s10530-020-02396-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-020-02396-1