Anales del Jardín Botánico de Madrid, Vol 74, No 1 (2017)

An invasion risk map for non-native aquatic macrophytes of the Iberian Peninsula

Argantonio Rodríguez-Merino
Department of Plant Biology and Ecology, Faculty of Pharmacy, University of Seville, Spain

Rocío Fernández-Zamudio
Doñana Biological Station, CSIC, Spain

Pablo García-Murillo
Department of Plant Biology and Ecology, Faculty of Pharmacy, University of Seville, Spain


Freshwater systems are particularly susceptible to non-native organisms, owing to their high sensitivity to the impacts that are caused by these organisms. Species distribution models, which are based on both environmental and socio-economic variables, facilitate the identification of the most vulnerable areas for the spread of non-native species. We used MaxEnt to predict the potential distribution of 20 non-native aquatic macrophytes in the Iberian Peninsula. Some selected variables, such as the temperature seasonality and the precipitation in the driest quarter, highlight the importance of the climate on their distribution. Notably, the human influence in the territory appears as a key variable in the distribution of studied species. The model discriminated between favorable and unfavorable areas with high accuracy. We used the model to build an invasion risk map of aquatic macrophytes for the Iberian Peninsula that included results from 20 individual models. It showed that the most vulnerable areas are located near to the sea, the major rivers basins, and the high population density areas. These facts suggest the importance of the human impact on the colonization and distribution of non-native aquatic macrophytes in the Iberian Peninsula, and more precisely agricultural development during the Green Revolution at the end of the 70’s. Our work also emphasizes the utility of species distribution models for the prevention and management of biological invasions.


Aquatic plants; bioclimatic factors; biological invasions; ecological niche models; freshwater ecosystems; map risk assessment; MaxEnt; non-native species; socio-economic factors; species distribution model

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Aguiar, F.C.F. & Ferreira, M.T. 2013. Plant invasions in the rivers of the Iberian Peninsula, south-western Europe: A review. Plant Biosystems 147: 1107-1119.

Anthos [2015]. Spanish Plant Information System. Real Jardín Botánico de Madrid CSIC-Fundación Biodiversidad [].

Allan, J.D. 2004. Landscapes and riverscapes: The influence of land use on stream ecosystems. Annual Review of Ecology Evolution and Systematics 35: 257-284.

Aranda, S.C. & Lobo, J.M. 2011. How well does presence-only-based species distribution modelling predict assemblage diversity? A case study of the Tenerife flora. Ecography 34: 31-38.

Barnes, M.A., Jerde, C.L., Wittmann, M.E., Chadderton, W.L., Ding, J., Zhang, J., Purcell, M., Budhathoki, M. & Lodge, D.M. 2014. Geographic selection bias of occurrence data influences transferability of invasive Hydrilla verticillata distribution models. Ecology and Evolution 4: 2584-2593. PMid:25360288 PMCid:PMC4203300

Bou, J. & Font, J. 2016. Situation in Catalonia of Ludwigia peploides (Onagraceae). Butlletí de la Institució Catalana d'Historia Natural 80: 57-58.

Broennimann, O. & Guisan, A. 2008. Predicting current and future biological invasions: both native and invaded ranges matter. Biology Letters 4: 585-589. PMid:18664415 PMCid:PMC2610080

Broennimann, O., Treier, U.A., Muller-Scharer, H., Thuiller, W., Peterson, A.T. & Guisan, A. 2007. Evidence of climatic niche shift during biological invasion. Ecology Letters 10: 701-709. PMid:17594425

Brooks, M.L., D'Antonio, C.M., Richardson, D.M., Grace, J.B., Keeley, J.E., DiTomaso, J.M., Hobbs, R.J., Pellant, M. & Pyke, D. 2004. Effects of invasive alien plants on fire regimes. BioScience 54: 677-688.[0677:EOIAPO]2.0.CO;2

Brundu, G. 2015. Plant invaders in European and Mediterranean inland waters: profiles, distribution, and threats. Hydrobiologia 746: 61-79.

Carter, V. & Rybicki, N.B. 1990. Light attenuation and submersed macrophyte distribution in the tidal Potomac River and estuary. Estuaries 13: 441-452.

Catford, J.A. & Downes, B.J. 2010. Using multi-scale species distribution data to infer drivers of biological invasion in riparian wetlands. Diversity and Distributions 16: 20-32.

Catford, J.A., Vesk, P.A., White, M.D. & Wintle, B.A. 2011. Hotspots of plant invasion predicted by propagule pressure and ecosystem characteristics. Diversity and Distributions 17: 1099-1110.

Chambers, P.A., Lacoul, P., Murphy, K.J. & Thomaz, S.M. 2008. Global diversity of aquatic macrophytes in freshwater. Hydrobiologia 595: 9-26.

Chappuis, E., Gacia, E. & Ballesteros, E. 2011. Changes in aquatic macrophyte flora over the last century in Catalan water bodies (NE Spain). Aquatic Botany 95: 268-277.

Chappuis, E., Ballesteros, E. & Gacia, E. 2012. Distribution and richness of aquatic plants across Europe and Mediterranean countries: patterns, environmental driving factors and comparison with total plant richness. Journal of Vegetation Science 23: 985-997.

Chytr?, M., Py?ek, P., Wild, J., Pino, J., Maskell, L.C. & Vilà, M. 2009. European map of alien plant invasions based on the quantitative assessment across habitats. Diversity and Distributions 15: 98-107.

Cirujano, S., Meco, A., García-Murillo, P. & Chirino Argenta, M. 2014. Flora Acuática Espa-ola. Hidrófitos Vasculares. Real Jardín Botánico de Madrid CSIC, Madrid. PMid:24445412 PMCid:PMC3926629

Collen, B., Whitton, F., Dyer, E.E., Baillie, J.E.M., Cumberlidge, N., Darwall, W.R.T., Pollock, C., Richman, N.I., Soulsby, A.M. & Böhm, M. 2014. Global patterns of freshwater species diversity, threat and endemism. Global Ecology and Biogeography 23: 40-51. PMid:26430385 PMCid:PMC4579866

Crafton, R. E. 2015. Modeling invasion risk for coastal marine species utilizing environmental and transport vector data. Hydrobiologia 746: 349-362.

Dibble, E.D., Thomaz, S.M. & Padial, A.A. 2006. Spatial complexity measured at a multi-scale in three aquatic plant species. Journal of Freshwater Ecology 21: 239-247.

Egertson, C.J., Kopaska, J.A. & Downing, J.A. 2004. A century of change in macrophyte abundance and composition in response to agricultural eutrophication. Hydrobiologia 524: 145-156.

Elith, J. & Leathwick, J.R. 2009. Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics 40: 677-697.

Elith, J., Kearney, M. & Phillips, S. 2010. The art of modelling range-shifting species. Methods in Ecology and Evolution 1: 330-342.

Elith, J., Phillips, S.J., Hastie, T., Dudík, M., Chee, Y.E. & Yates, C.J. 2011. A statistical explanation of MaxEnt for ecologists. Diversity and Distributions 17: 43-57.

Elith, J., Graham, C.H., Anderson, R.P., Dudik, M., Ferrier, S., Guisan, A., Hijmans, R.J., Huettmann, F., Leathwick, J.R., Lehmann, A., Li, J., Lohmann, L.G., Loiselle, B.A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., Overton, J.M., Peterson, A.T., Phillips, S.J., Richardson, K., Scachetti-Pereira, R., Schapire, R.E., Soberon, J., Williams, S., Wisz, M. & Zimmermann, N.E. 2006. Novel methods improve prediction of species' distributions from occurrence data. Ecography 29: 129-151.

ESRI. 2008. ArcGIS Desktop: Release 9.3. Environmental Systems Research Institute, United States of America.

European Environment Agency [2015]. Corine Land Cover dataset [http:// www.eea.europa].

Fajardo, J., Lessmann, J., Bonaccorso, E., Devenish, C. & Mu-oz, J. 2014. Combined use of systematic conservation planning, species distribution modeling, and connectivity analysis reveals severe conservation gaps in a megadiverse country (Peru). Plos One 9: 1-23. PMid:25479411 PMCid:PMC4257666

Fernández-Zamudio, R., Cirujano, S., Sánchez-Carrillo, S., Meco, A. & García-Murillo, P. 2013. Clonal reproduction of Azolla filiculoides Lam.: implications for invasiveness. Limnetica 32: 245-252.

Florencio, M., Fernández-Zamudio, R., Bilton, D.T. & Díaz-Paniagua, C. 2015. The exotic weevil Stenopelmus rufinasus Gyllenhal, 1835 (Coleoptera: Curculionidae) across a "host-free" pond network. Limnetica 34: 79-84.

Galil, B.S., Nehring, S. & Panov, V. 2007. Waterways as invasion highways impact of climate change and globalization. Biological Invasions. W. Nentwig, Springer, Berlin.

Gallardo, B. & Aldridge, D.C. 2013. The dirty dozen: socio-economic factors amplify the invasion potential of 12 high-risk aquatic invasive species in Great Britain and Ireland. Journal of Applied Ecology 50: 757-766.

Gallardo, B., Errea, M.P. & Aldridge, D. 2012. Application of bioclimatic models coupled with network analysis for risk assessment of the killer shrimp, Dikerogammarus villosus, in Great Britain. Biological Invasions 14: 1265-1278.

Gallardo, B., Clavero, M., Sánchez, M.I. & Vilà, M. 2015. Global ecological impacts of invasive species in aquatic ecosystems. Global Change Biology 22: 1-13.

García-Murillo, P., Dana, E.D. & Rodríguez, C. 2005. Pistia stratiotes L. (Araceae) Una planta acuática exótica en las proximidades del Parque Nacional de Do-ana (SW Espa-a). Acta Botanica Malacitana 30: 235-236.

García-Murillo, P., Fernández-Zamudio, R., Cirujano, S., Sousa, A. & Espinar, J.M. 2007. The invasion of Do-ana National Park (SW Spain) by the mosquito fern (Azolla filiculoides Lam.). Limnetica 26: 242-250.

García-Murillo, P. & Fernández-Zamudio, R. 2015. Las plantas de las lagunas temporales de Do-ana. In: Díaz Paniagua, C. (coord.), El sistema de lagunas temporales de Do-ana, una red de hábitats acuáticos singulares. Organismo Autónomo Parques Nacionales, Madrid. PMCid:PMC4410763

GBIF [2015]. Global Biodiversity Information Facility Data Portal [http://].

Harrel, S. & Dibble, E. 2001. Foraging efficiency of juvenile bluegill, Lepomis macrochirus, among different vegetated habitats. Environmental Biology of Fishes 62: 441-453.

Heffner, R.A., Butler, M.J. & Reilly, C.K. 1996. Pseudoreplication revisited. Ecology 77: 2558-2562.

Heiberger, R.M. [2015]. Statistical analysis and data display: Heiberger and Holland. R package version 3.1–23 [].

Hijmans, R.J. & Van Etten, J. 2015. Raster: Geographic analysis and modeling with raster data. R package version 3.1–23 [].

Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.

Hosmer, D.W. & Lemeshow, S. 2000. Applied Logistic Regression. John Wiley & Sons Inc., New York. PMid:10886529

Hulme, P.E. 2006. Beyond control: wider implications for the management of biological invasions. Journal of Applied Ecology 43: 835-847.

Hussner, A. 2012. Alien aquatic plant species in European countries. Weed Research 52: 297-306.

Jiménez-Valverde, A., Peterson, A.T., Soberón, J., Overton, J.M., Aragón, P. & Lobo, J.M. 2011. Use of niche models in invasive species risk assessments. Biological invasions 13: 2785-2797.

Kelly, R., Leach, K., Cameron, A., Maggs, C.A. & Reid, N. 2014. Combining global climate and regional landscape models to improve prediction of invasion risk. Diversity and Distributions 20: 1-11.

Kriticos, D.J. & Brunel, S. 2016. Assessing and managing the current and future pest risk from water hyacinth, (Eichhornia crassipes), an invasive aquatic plant threatening the environment and water security. Plos One 11: 1-18. PMid:27513336 PMCid:PMC4981303

Les, D.H., Crawford, D.J., Kimball, R.T., Moody, M.L. & Landolt, E. 2003. Biogeography of discontinuously distributed hydrophytes: A molecular appraisal of intercontinental disjunctions. International Journal of Plant Sciences 164: 917-932.

Liu, X., Guo, Z., Ke, Z., Wang, S. & Li, Y. 2011. Increasing potential risk of a global aquatic invader in Europe in contrast to other continents under future climate change. Plos One 6: 1-11.

Mack, R.N., Simberloff, D., Mark Lonsdale, W., Evans, H., Clout, M. & Bazzaz, F.A. 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689-710.[0689:BICEGC]2.0.CO;2

Mateo, R.G., Croat, T.B., Felicísimo, A.M. & Mu-oz, J. 2010. Profile or group discriminative techniques? Generating reliable species distribution models using pseudo-absences and target-group absences from natural history collections. Diversity and Distributions 16: 84-94.

Molina, R., Aparicio, A., Lavergne, S., Slingsby, J. & Arroyo, J. 2015. Investigating the evolutionary assembly of a Mediterranean biodiversity hotspot: deep phylogenetic sgnal in the distribution of eudicots across elevational belts. Journal of Biogeography 42: 507-518.

Moss, B. 1990. Engineering and biological approaches to the restoration from eutrophication of shallow lakes in which aquatic plant communities are important components. Hydrobiologia 200-201: 367-377.

Murphy, K.J. 2002. Plant communities and plant diversity in softwater lakes of northern Europe. Aquatic Botany 73: 287-324.

López-López, P., Maiorano, L., Falcucci, A., Barba, E. & Boitani, L. 2011. Hotspots of species richness, threat and endemism for terrestrial vertebrates in SW Europe. Acta Oecologica 37: 399-412.

Pearson, R.G. & Dawson, T.P. 2003. Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecology and Biogeography 12: 361-371.

Pearson, R.G., Raxworthy, C.J., Nakamura, M. & Townsend Peterson, A. 2007. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography 34: 102-117.

Peterson, A.T. 2003. Predicting the geography of species' invasions via ecological niche modeling. The Quarterly Review of Biology 78: 419- 33. PMid:14737826

Phillips, S.J. & Dudík, M. 2008. Modeling of species distributions with MaxEnt: new extensions and a comprehensive evaluation. Ecography 31: 161-175.

Phillips, S.J., Anderson, R.P. & Schapire, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231-259.

Pimentel, D., Zuniga, R. & Morrison, D. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52: 273-288.

Py?ek, P. & Richardson, D.M. 2010. Invasive species, environmental change and management, and health. Annual Review of Environment and Resources 35: 25-55.

Quinn, L.D., Schooler, S.S. & van Klinken, R.D. 2011. Effects of land use and environment on alien and native macrophytes: lessons from a large-scale survey of Australian rivers. Diversity and Distributions 17: 132-143.

R Development Core Team [2014]. R: a language and environment for statistical computing. Version 3.1.2. Foundation for Statistical Computing, Vienna, Austria [].

Rahel, F.J. & Olden, J.D. 2008. Assessing the effects of climate change on aquatic invasive species. Conservation biology 22: 521-533. PMid:18577081

Rennie, M.D. & Jackson, L.J. 2005. The influence of habitat complexity on littoral invertebrate distributions: patterns differ in shallow prairie lakes with and without fish. Canadian Journal of Fisheries and Aquatic Sciences 62: 2088-2099.

Reshetnikov, A. & Ficetola, G. 2011. Potential range of the invasive fish rotan (Perccottus glenii) in the Holarctic. Biological Invasions 13: 2967-2980.

Ricciardi, A. & Kipp, R. 2008. Predicting the number of ecologically harmful exotic species in an aquatic system. Diversity and Distributions 14: 374-380.

Ruiz, T., Martín, E., Lorenzo, G., Albano, E., Morán, R. & Sánchez, J.M. 2008. The Water Hyacinth, Eichhornia crassipes: an invasive plant in the Guadiana River Basin (Spain). Aquatic Invasions 3: 42-53.

Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M. & Wall, D.H. 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770- 1774. PMid:10710299

Sanderson, E.W., Jaiteh, M., Levy, M.A., Redford, K.H., Wannebo, A.V. & Woolmer, G. 2002. The human footprint and the last of the wild. BioScience 52: 891-904.[0891:THFATL]2.0.CO;2

Santamaría, L. 2002. Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecologica 23: 137-154.

Santamaría, L., Montes, C. & Hootsmans, M.J.M. 1996. Influence of environmental parameters on the biomass development of Ruppia drepanensis populations in Do-ana National Park: the importance of conditions affecting the underwater light climate. International Journal of Salt Lake Research 5: 157-180.

SEDAC [2015]. Socioeconomic Data and Applications Center [http://].

Serrano, L. & Díaz Paniagua, C. 2015. Introducción. In: Díaz Paniagua, C. (coord.), El sistema de lagunas temporales de Do-ana, una red de hábitats acuáticos singulares: 9-18. Organismo Autónomo Parques Nacionales. Madrid.

Strayer, D.L. & Dudgeon, D. 2010. Freshwater biodiversity conservation: recent progress and future challenges. Journal of the North American Benthological Society 29: 344-358.

Thuiller, W., Richardson, D.M., Py?ek, P., Midgley, G.F., Hughes, G.O. & Rouget, M. 2005. Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Global Change Biology 11: 2234-2250.

Verloove, F. & Sánchez-Gullón, E. 2008. New records of interesting xenophytes in the Iberian Peninsula. Acta Botanica Malacitana 33: 147-167.

Walther, G.R., Roques, A., Hulme, P.E., Sykes, M.T., Pysek, P., Kuhn, I., Zobel, M., Bacher, S., Botta-Dukat, Z., Bugmann, H., Czucz, B., Dauber, J., Hickler, T., Jarosik, V., Kenis, M., Klotz, S., Minchin, D., Moora, M., Nentwig, W., Ott, J., Panov, V.E., Reineking, B., Robinet, C., Semenchenko, V., Solarz, W., Thuiller, W., Vila, M., Vohland, K. & Settele, J. 2009. Alien species in a warmer world: risks and opportunities. Trends in Ecology and Evolution 24: 686-693. PMid:19712994

Willby, N.J. 2007. Managing invasive aquatic plants: problems and prospects. Aquatic Conservation: Marine and Freshwater Ecosystems 17: 659-665.

Williams, S. & Grosholz, E. 2008. The invasive species challenge in estuarine and coastal environments: marrying management and science. Estuaries and Coasts 31: 3-20.

Wisz, M.S., Hijmans, R.J., Li, J., Peterson, A.T., Graham, C.H., Guisan, A. & NCEAS Predicting Species Distribution Working Group. 2008. Effects of sample size on the performance of species distribution models. Diversity and Distributions 14: 763-773.

Woodward, F.I. & Williams, B.G. 1987. Climate and plant distribution at global and local scales. Vegetatio 69: 189-197.

Worldclim [2015]. Global Climate Data [].

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