Abstract
The spread of non-native invasive plants is closely linked to land use changes imposed by human activities such as the expansion of urbanizations and agricultural activities that result in the loss and fragmentation of native forests. While the conditions generated in fragmented forests may provide suitable new habitat for the arrival and establishment of invasive plant propagules, we know little about the reproductive performance of established invasive populations growing in fragmented conditions. We assess sexual reproduction of Ligustrum lucidum in continuous and fragmented forests across 2 years. We also measure soil quality parameters in 1 year to determine their relative influence in shaping its reproduction in both landscape conditions. We observed a strong decrease in reproductive success at the population level in fragmented habitats. However, reproduction at the individual level showed no differences in seed production per tree between landscape conditions, implying no changes in pollination service. Simultaneously, soils of continuous forests had higher water content, total nitrogen, organic matter and carbon. These soil quality parameters were positively correlated with seed production and seedling number per plot within the same year. Thus, reproductive failure in fragmented forests would not be the result of Allee effects but the consequence of less favorable abiotic soil conditions. In current dynamic and changing climatic scenarios imposed by human activities, water and nutrient demanding invasive plants like L. lucidum might be as likely as or even more susceptible to these changes than native ones. Climatic shifts acting in concert with land use changes may either ameliorate invasion spread in abiotically eroded fragmented habitats or boost invasion into novel environments, resulting in new distribution spread patterns.
Similar content being viewed by others
References
Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980
Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188
Aikio S, Duncan RP, Hulme PE (2012) The vulnerability of habitats to plant invasion: disentangling the roles of propagule pressure, time and sampling effort. Global Ecol Biogeogr 21:778–786
Angeloni F, Ouborg NJ, Leimu R (2011) Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biol Conserv 144:35–43
Aragón R, Groom M (2003) Invasion by Ligustrum lucidum (Oleaceae) in NW Argentina: early stage characteristics in different habitat types. Rev Biol Trop 51:59–70
Aragón R, Morales JM (2003) Species composition and invasión in NW Argentinian secondary forest: effects of land use history, environment and landscape. J Veg Sci 14:195–204
Aslan CE, Rejmánek M, Klinger R (2012) Combining efficient methods to detect spread of woody invaders in urban–rural matrix landscapes: an exploration using two species of Oleaceae. J App Ecol 49:331–338
Baker HG (1955) Self-compatibility and establishment after ‘long distance’ dispersal. Evolution 9:347–348
Barrett SCH, Colautti RI, Eckert CG (2008) Plant reproductive systems and evolution during biological invasion. Mol Ecol 17:373–383
Bates D and Maechler M (2009) lme4: linear mixed-effects models using S4 classes. R Q7 package version 0.999375-32. Available at http://CRAN.R-project.org/package=lme4
Blank RR, Qualls RG, Young JA (2002) Lepidium latifolium: plant nutrient competition-soil interactions. Biol Fertil Soils 35:458–464
Breen AN, Richards JH (2008) Irrigation and fertilization effects on seed number, size, germination and seedling growth: implications for desert shrub establishment. Oecologia 157:13–19
Cappuccino N (2004) Allee effect in an invasive alien plant, pale swallow-wort Vincetoxicum rossicum (Asclepiadaceae). Oikos 106:3–8
Crawley MJ (2007) The R book. Wiley, West Sussex
de Vere N, Jongejans E, Plowman A, Eirene W (2009) Population size and habitat quality affect genetic diversity and fitness in the clonal herb Cirsium dissectum. Oecologia 159:59–68
Decker KL, Allen CR, Acosta L et al (2012) Land use, landscapes and biological invasions. Invas Plant Sci Manag 5:108–116
Drake JM, Lodge DM (2006) Allee effects, propagule pressure and the probability of establishment: risk analysis for biological invasions. Biol Invasions 8:365–375
Duguay S, Eigenbrod F, Fahrig L (2007) Effects of surrounding urbanization on non-native flora in small forest patches. Landsc Ecol 22:589–599
Eckert CG, Kalisz S, Geber MA et al (2009) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43
Elam DR, Ridley CE, Goodell K, Ellstrand NC (2007) Population size and relatedness affect fitness of a self-incompatible invasive plant. P Natl Acad Sci USA 104:549–552
Eschtruth AK, Battles JJ (2009) Assessing the relative importance of disturbance, herbivory, diversity, and propagule pressure in exotic plant invasion. Ecol Monogr 79:265–280
Ferreras AE, Torres C, Galetto L (2008) Fruit removal of an invasive exotic species (Ligustrum lucidum) in a fragmented landscape. J Arid Environ 72:1573–1580
Firestone JL, Jasieniuk M (2012) Seed production is reduced by small population size in natural populations of the invasive grass Lolium multiflorum. Biol Invasions 14:2519–2529
Galen C (2005) It never rains but then it pours: the diverse effects of water on flower integrity and function. In: Reekie EG, Bazzaz FA (eds) Reproductive allocation in plants. Elsevier Academic Press, Vermont, pp 77–95
Gavier GI, Bucher EH (2004) Deforestation of the Sierras Chicas from Córdoba (Argentina) within the period 1970–1997. Rev Acad Nac Cs 110:1–27
Gavier-Pizarro GI, Kuemmerle T, Hoyos LE, Stewart SI, Huebner CD, Keuler NS, Radeloff VC (2012) Monitoring the invasion of an exotic tree (Ligustrum lucidum) from 1983 to 2006 with Landsat TM/ETM + satellite data and support vector machines in Córdoba, Argentina. Remote Sens Environ 122:134–145
González-Moreno P, Pino J, Gassó N, Vila M (2013) Landscape context modulates alien plant invasion in Mediterranean forest edges. Biol Invasions 15:547–557
Grau HR, Aragón R (2000) Ecología de los árboles invasores de la Sierra de San Javier. In: Grau HR, Aragón R (eds) Arboles exóticos de las Yungas Argentinas. LIEY-UNT, Tucumán, pp 5–20
Hao JH, Qiang S, Chrobock T, van Kleunen M, Liu QQ (2011) A test of baker’s law: breeding systems of invasive species of Asteraceae in China. Biol Invasions 13:571–580
Harmon-Threatt AN, Burns JH, Shemyakina LA, Knight TM (2009) Breeding system and pollination ecology of introduced plants compared to their native relatives. Am J Bot 96:1544–1550
Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337
Howard PJA, Howard DM (1990) Use of organic carbon and loss on ignition to estimate soil organic matter in different soil types and horizons. Biol Fert Soils 9:306–310
Hoyos LE, Gavier-Pizarro GI, Kuemmerle T, Bucher EH, Radeloff VC, Tecco PA (2010) Invasion of glossy privet (Ligustrum lucidum) and native forest loss in the Sierras Chicas of Córdoba, Argentina. Biol Invasions 12:3261–3275
Hudson BD (1994) Soil organic matter and available water capacity. J Soil Water Conserv 49:189–194
Jauni M, Hyvönen T (2012) Interactions between alien plant species traits and habitat characteristics in agricultural landscapes in Finland. Biol Invasions 14:47–63
Jesse LC, Nason JD, Obrycki JJ, Moloney KA (2010) Quantifying the levels of sexual reproduction and clonal spread in the invasive plant, Rosa multiflora. Biol Invasions 12:1847–1854
Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York
Karlen DL, Andrews SS, Wienhold BJ, Zobeck TM (2008) Soil quality assessment: past, present and future. J Integr Biosci 6:3–14
Kelly AE, Goulden ML (2008) Rapid shifts in plant distribution with recent climate change. Proc Natl Acad Sci USA 105:11823–11826
Kolb A (2005) Reduced reproductive success and offspring survival in fragmented populations of the forest herb Phyteuma spicatum. J Ecol 93:1226–1237
Lambretch SC, Santiago LS, DeVan CM, Cervera JC, Stripe CM, Buckingham LA, Pasquini SC (2011) Plant water status and hydraulic conductance during flowering in the southern California coastal sage shrub Salvia mellifera (Lamiaceae). Am J Bot 98:1286–1292
Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–9452
Leishman ML, Thomson VP (2005) Experimental evidence for the effects of additional water, nutrients and physical disturbance on invasive plants in low fertility Hawkesbury sandstone soils, Sydney, Australia. J Ecol 93:38–49
Li JY, Wang JQ, Chen K, Liu JJ (2006) Effects of water stress on water status and embolism in greening tree species in Beijing. J Beijing For Univ 28:12–16
Lindenmayer DB, Fischer J (2006) Habitat fragmentation and landscape change. An ecological and conservation synthesis. Island Press, Washington, DC
Luti R, Bertran de Solis MA et al (1979) Vegetación. In: Vázquez JB, Miatello RA, Roqué ME (eds) Geografía física de la provincia de Córdoba. Editorial Boldt, Buenos Aires, pp 297–368
Maguire JD (1962) Speed of germination—aid in selection and evaluation for seedling emergence and vigor. Crop Sci 2:176–177
Matezans S, Escudero A, Valladares F (2009) Impact of three global change drivers on a Mediterranean shrub. Ecology 90:2609–2621
Milbau A, Stout JC, Graae BJ, Nijs I (2009) A hierarchical framework for integrating invasibility experiments incorporating different factors and spatial scales. Biol Invasions 11:941–950
Montaldo NH (1993) Dispersión por aves y éxito reproductivo de dos especies de Ligustrum (Oleaceae) en un relicto de selva subtropical en la Argentina. Rev Chil Hist Nat 66:75–85
Morris WF, Doak DF (2002) Quantitative conservation biology: theory and practice of population viability analyses. Sinauer, Sunderland
Mosher ES, Silander J, Andrew ML (2009) The role of land-use history in major invasion by woody plant species in the northeastern North American landscape. Biol Invasions 11:2317–2328
Panetta FD (2000) Fates of fruits and seeds of Ligustrum lucidum W.T.Ait. and L. sinense Lour. maintained under natural rainfall or irrigation. Aust J Bot 48:701–705
Petanidou T, Godfree RC, Song DS, Kantsa A, Dupont YL, Waser NM (2012) Self-compatibility and plant invasiveness: comparing species in native and invasive ranges. Perspect Plant Ecol Evol Syst 14:3–12
Pinheiro J, Bates D, Debroy S, Sarkar D, The R Core team (2009) nlme: Linear and nonlinear mixed effects models. R package version 3.1-96
Quiroz CL, Cavieres LA, Pauchard A (2011) Assessing the importance of disturbance, site conditions, and the biotic barrier for dandelion invasion in an Alpine habitat. Biol Invasions 13:2889–2899
Rambuda TD, Johnson SD (2004) Breeding systems of invasive alien plants in South Africa: does Baker’s rule apply? Divers Distrib 10:409–416
Raveh A (1973) The adaptation of the nitrate specific electrode for soil and plant analysis. Soil Sci 116:388–389
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org
Rio ME, Achaval L (1904) Geografìa de la Provincia de Córdoba. Publicación official, Vol uno, p 569
Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Syst 40:81–102
Six J, Carpentier A, van Kessel C, Merckx R, Harris D, Horwath WR, Lüscher A (2001) Impact of elevated CO2 on soil organic matter dynamics as related to changes in aggregate turnover and residue quality. Plant Soil 234:27–36
Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, et al (1993) Methods of soil analysis. Part 3—chemical methods. American Society of Agronomy, Soil Science Society of America, Madison, p 1390
Tecco PA, Gurvich DE, Díaz S, Pérez-Harguindeguy N, Cabido M (2006) Positive interaction between invasive plants: the influence of Pyracantha angustifolia on the recruitment of native and exotic woody species. Austral Ecol 31:293–300
Tsaliki M, Diekmann M (2010) Effects of habitat fragmentation and soil quality on reproduction in two heathland Genista species. Plant Biol 12:622–629
van Kleunen M, Johnson SD (2005) Testing for ecological and genetic Allee effects in the invasive shrub Senna didymobotrya (Fabaceae). Am J Bot 92:1124–1130
Vergeer P, Rengelink R, Copal A, Ouborg NJ (2003) The interacting effects of genetic variation, habitat quality and population size on performance of Succisa pratensis. J Ecol 91:18–26
Vila M, Ibáñez I (2011) Plant invasions in the landscape. Landscape Ecol 26:461–472
von Euler T, Agren J, Ehrlén J (2012) Floral display and habitat quality affect cost of reproduction in Primula farinosa. Oikos 121:1400–1407
Wagner J, Lüscher A, Hillebrand C, Kobald B, Spitaler N, Larcher W (2001) Sexual reproduction of Lolium perenne L. and Trifolium repens L. under free air CO2 enrichment (FACE) at two levels of nitrogen application. Plant Cell Environ 24:957–965
Walters MB, Reich PB (2000) Seed size, nitrogen supply, and growth rate affect tree seedling survival in deep shade. Ecology 81:1887–1901
Weil R, Magdoff F (2004) Significance of soil organic matter to soil quality and health. In: Magdoff F, Weil R (eds) Soil organic matter in sustainable agriculture. CRC Press, Boca Raton, pp 1–43
Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7:270
Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen M (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076
Winter C, Lehmann S, Diekmann M (2008) Determinants of reproductive success: a comparative study of five endangered river corridor plants in fragmented habitats. Biol Conserv 141:1095–1104
With KA (2002) The landscape ecology of invasive spread. Conserv Biol 16:1192–1203
Acknowledgments
We appreciate the help of Veronica Ergo, Felipe Rincón and Leonardo Ontivero for fieldwork assistance. We are grateful to Luciano Cagnolo for statistical analysis suggestions, and to Diego Gurvich, and three anonymous referees for substantially improving early drafts of this work. Our work was supported by CONICET (PIP 0790 and 0019) and FONCyT (PICT 2011-1606). N.A.A. is a fellowship holder of CONICET, E.K. and R.A. are researchers of the same institution.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Aguirre-Acosta, N., Kowaljow, E. & Aguilar, R. Reproductive performance of the invasive tree Ligustrum lucidum in a subtropical dry forest: does habitat fragmentation boost or limit invasion?. Biol Invasions 16, 1397–1410 (2014). https://doi.org/10.1007/s10530-013-0577-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-013-0577-x