Abstract
Rising economic and ecological costs caused by invasive organisms revived research on biological attributes associated with invasiveness, focussing on the question: do invasive taxa have biological attributes favouring (1) propagule pressure; (2) dispersal; and (3) establishment and population growth? Using a literature-derived database on 312 stream macroinvertebrate genera occurring at 527 least human-impacted European sites, we quantitatively examined this question. Compared with native genera, genera with invasive invertebrate species (1) tended to reproduce more frequently and to have higher abundances (i.e. higher propagule pressure); (2) had no particular resistance stages to survive during dispersal; and (3) had significantly more ovoviviparity (enabling colonization by a single individual that typically releases viable offspring), larger size and longer life (providing resistance against mortality), food and feeding habits exploiting food resources in streams more effectively, and tended to be more dominant in their communities (all favouring establishment and population growth). Repeating these analyses excluding “native” flying insects (i.e. genera that presumably invaded from glacial refuges unnoticed by biologists), fewer biological attributes were significantly associated with invasiveness. For both data sets (all genera or insects excluded), their affinity to few biological traits (e.g. ovoviviparity, gill respiration) assigned the same 13 of the 19 invasive genera to the top 19 ranks on a gradient of potential invasiveness, together with native genera that risk to become invasive (e.g. Pisidium, Unio), but also with one endangered native genus (Margaritifera). Overall, our data support the idea that invasiveness can be predicted using biological attributes.
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References
Acosta A, Izzi CF, Stanisci A (2006) Comparison of native and alien plant traits in Mediterranean coastal dunes. Community Ecol 7:35–41
Allan JD (1995) Stream ecology. Chapman & Hall, London
Banarescu P (1990) Zoogeography of fresh waters I. General distribution and dispersal of freshwater animals. Aula-Verlag, Wiesbaden
Bauer G (1988) Threats to the freshwater pearl mussel Margaritifera margaritifera L. in Central Europe. Biol Conserv 45:239–253
Bernez I, Aguiar F, Violle C et al (2006) Invasive river plants from Portuguese floodplains: what can species attributes tell us? Hydrobiologia 570:3–9
Bij de Vaate A, Jazdzewski K, Ketelaars HAM et al (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can J Fish Aquat Sci 59:1159–1174
Bilton D, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181
Burns JH (2006) Relatedness and environment affect traits associated with invasive and noninvasive introduced Commelinaceae. Ecol Appl 16:1367–1376
Cadotte MW, Lovett-Doust J (2001) Ecological and taxonomic differences between native and introduced plants of southwestern Ontario. Ecoscience 8:230–238
Cadotte MW, Murray BR, Lovett-Doust J (2006) Evolutionary and ecological influences of plant invader success in the flora of Ontario. Ecoscience 13:388–395
Chevenet F, Dolédec S, Chessel D (1994) A fuzzy coding approach for the analysis of long-term ecological data. Freshw Biol 31:295–309
Cosgrove PJ, Hastie LC (2001) Conservation of threatened freshwater pearl mussel populations: river management, mussel translocation and conflict resolution. Biol Conserv 99:183–190
Devin S, Beisel J-N (2007) Biological and ecological characteristics of invasive species: a gammarid study. Biol Invasions 9:13–24
Devin S, Piscart C, Beisel J-N et al (2004) Life history traits of the invader Dikerogammarus villosus (Crustacea: Amphipoda) in the Moselle River, France. Int Rev Hydrobiol 89:21–34
Devin S, Beisel J-N, Usseglio-Polatera P et al (2005a) Changes in the functional biodiversity in an invaded freshwater ecosystem: the Moselle River. Hydrobiologia 542:113–120
Devin S, Bollache L, Noel P-Y et al (2005b) Patterns of biological invasions in French freshwater systems by non-indigenous macroinvertebrates. Hydrobiologia 551:137–146
Dolédec S, Olivier J-M, Statzner B (2000) Accurate description of the abundance of taxa and their biological traits in stream invertebrate communities: effects of taxonomic and spatial resolution. Arch Hydrobiol 148:25–43
Dunstan PK, Johnson CR (2004) Invasion rates increase with species richness in a marine epibenthic community by two mechanisms. Oecologia 138:285–292
Elliott JM (1977) Some methods for the statistical analysis of samples of benthic invertebrates, 2nd edn. Freshwater Biological Association Scientific Publication No. 25, Ambleside
Facon B, Machline E, Pointier JP et al (2004) Variation in desiccation tolerance in freshwater snails and its consequences for invasion ability. Biol Invasions 6:283–293
Gayraud S, Statzner B, Bady P et al (2003) Invertebrate traits for the biomonitoring of large European rivers: an initial assessment of alternative metrics. Freshw Biol 48:2045–2064
Glöer P, Meier-Brook C, Ostermann O (1980) Süsswassermollusken, 2nd edn. Deutscher Jugendbund für Naturbeobachtung, Hamburg
Hamilton MA, Murray BR, Cadotte MW et al (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074
Hazlett BA, Acquistapace P, Gherardi F (2002) Differences in memory capabilities in invasive and native crayfish. J Crustacean Biol 22:439–448
Hildrew AG (1992) Food webs and species interactions. In: Calow P, Petts GE (eds) The rivers handbook, vol 1. Blackwell, Oxford, pp 309–330
Illies J (ed) (1978) Limnofauna Europaea, 2nd ed. Fischer Verlag, Stuttgart
Kaestner A (1969) Lehrbuch der speziellen Zoologie I. Wirbellose, vol 1, 3rd edn. Fischer Verlag, Stuttgart
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204
Labrie G, Lucas E, Coderre D (2006) Can developmental and behavioral characteristics of the multicolored Asian lady beetle Harmonia axyridis explain its invasive success? Biol Invasions 8:743–754
Liu J, Dong M, Miao SL et al (2006) Invasive alien plants in China: role of clonality and geographical origin. Biol Invasions 8:1461–1470
Lloret F, Médail F, Brundu G et al (2005) Species attributes and invasion success by alien plants on Mediterranean islands. J Ecol 93:512–520
MacArthur RH, Wilson OE (1967) The theory of island biogeography. Princeton University Press, Princeton
Nyberg CD, Wallentinus I (2005) Can species traits be used to predict marine macroalgal introductions? Biol Invasions 7:265–279
Pöckl M (2007) Strategies of a successful new invader in European fresh waters: fecundity and reproductive potential of the Ponto-Caspian amphipod Dikerogammarus villosus in the Austrian Danube, compared with indigenous Gammarus fossarum and G. roeseli. Freshw Biol 52:50–63
Pratt RB, Black RA (2006) Do invasive trees have a hydraulic advantage over native trees? Biol Invasions 8:1331–1341
Radford IJ, Cousens RD (2000) Invasiveness and comparative life-history traits of exotic and indigenous Senecio species in Australia. Oecologia 125:531–542
R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (see also http://www.R-project.org)
Rehage JS, Sih A (2004) Dispersal behavior, boldness, and the link to invasiveness: a comparison of four Gambusia species. Biol Invasions 6:379–391
Ricciardi A, Serrouya R, Whoriskey FG (1995) Aerial exposure tolerance of zebra and quagga mussels (Bivalvia: Dreissenidae): implications for overland dispersal. Can J Fish Aquat Sci 52:470–477
Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Schmidt E (1978) Odonata. In: Illies J (ed) Limnofauna Europaea, 2nd edn. Fischer Verlag, Stuttgart, pp 274–279
Simberloff DS, Wilson OE (1969) Experimental zoogeography of islands: the colonization of empty islands. Ecology 50:278–296
Smith MD, Knapp AK (2001) Physiological and morphological traits of exotic, invasive exotic, and native plant species in tallgrass prairie. Int J Plant Sci 162:785–792
Statzner B, Lévêque C (2007) Linking productivity, biodiversity and habitat of benthic stream macroinvertebrate communities: potential complications of worldwide and regional patterns. Int Rev Hydrobiol (in press). doi:10.1002/iroh.200610983
Statzner B, Hildrew AG, Resh VH (2001) Species traits and environmental constraints: entomological research and the history of ecological theory. Annu Rev Entomol 46:291–316
Statzner B, Dolédec S, Hugueny B (2004) Biological trait composition of European stream invertebrate communities: assessing the effects of various trait filter types. Ecography 27:470–488
Statzner B, Bonada N, Dolédec S (2007) Conservation of taxonomic and biological trait diversity of European stream macroinvertebrate communities: a case for a collective public database. Biodivers Conserv. doi: 10.1007/s10531-007-9150-1 (in press)
Tachet H, Richoux P, Bournaud M et al (2002) Invertébrés d’eau douce, 2nd corrected impression. CNRS éditions, Paris
Tamburri M, Wasson K, Matsuda M (2002) Ballast water deoxygenation can prevent aquatic introductions while reducing ship corrosion. Biol Conserv 103:331–341
Thienemann A (1950) Verbreitungsgeschichte der Süsswassertierwelt Europas. Schweizerbart, Stuttgart
Tittizer T, Schöll F, Dommermuth M (1994) The development of the macrozoobenthos in the river Rhine in Germany during the 20th century. Water Sci Technol 29:21–28
Tittizer T, Schöll F, Banning M et al (2000) Aquatische Neozoen im Makrozoobenthos der Binnenwasserstraßen Deutschlands. Lauterbornia 39:1–72
Tiunov AV, Hale CM, Holdsworth AR (2006) Invasion patterns of Lumbricidae into previously earthworm-free areas of northeastern Europe and the western Great Lakes region of North America. Biol Invasions 8:1223–1234
Unmack PJ, Fagan WF (2004) Convergence of differentially invaded systems toward invader-dominance: time-lagged invasions as a predictor in desert fish communities. Biol Invasions 6:233–243
Usseglio-Polatera P, Bournaud M, Richoux P et al (2000) Biological and ecological traits of benthic freshwater macroinvertebrates: relationships and definition of groups with similar traits. Freshw Biol 43:175–205
Vila-Gispert A, Moreno-Amich R (2003) Life-history strategies of native and introduced fish species from a Mediterranean lake. Anim Biol 53:47–57
Vila-Gispert A, Alcaraz C, García-Berthou E (2005) Life-history traits of invasive fish in small Mediterranean streams. Biol Invasions 7:107–116
Weber E (2005) Population size and structure of three mussel species (Bivalvia: Unionidae) in a northeastern German river with special regard to influences of environmental factors. Hydrobiologia 537:169–183
Acknowledgements
We thank all researchers and editors who published results in a format such that we could use them for our database and the many colleagues that provided personal information to fill data gaps (all mentioned in previous papers using the data for other purposes). We also acknowledge the comments by an anonymous referee.
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Statzner, B., Bonada, N. & Dolédec, S. Biological attributes discriminating invasive from native European stream macroinvertebrates. Biol Invasions 10, 517–530 (2008). https://doi.org/10.1007/s10530-007-9148-3
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DOI: https://doi.org/10.1007/s10530-007-9148-3