Abstract
Secondary spread largely determines the distribution and success of invasive species and depends ultimately on the capacity of the invader to disperse and colonise over multiple scales. Spread of the invasive seaweed Codium fragile ssp. fragile (Codium) can occur through the dispersal of vegetative fragments, which can be buoyant or non-buoyant depending on environmental conditions. This study examined the factors influencing the dispersal, settlement, and establishment of these two types of propagules in eelgrass (Zostera marina) meadows of îles de la Madeleine, Canada, where Codium lives epiphytically on eelgrass rhizomes. To measure dispersal, ~1,400 Codium fragments were marked, released, and tracked under different hydrodynamic conditions in areas of high and low eelgrass density. Under all conditions, buoyant fragments dispersed one to two orders of magnitude further than non-buoyant fragments. Dispersal distance was positively correlated with wind speed (a proxy for surface currents in this system) for buoyant fragments and with current speed for non-buoyant fragments. For the latter, dispersal distance was also negatively correlated with eelgrass height and density. Natural deposition of drifting fragments in experimentally-manipulated eelgrass meadows was variable in space and time, but was not affected by eelgrass shoot density. Experimental disturbance of eelgrass meadows enhanced the density, biomass, and percent cover of Codium, suggesting that the exposure of eelgrass rhizomes by natural or anthropogenic disturbance promotes invasion by Codium. Our results highlight the importance of small-scale field experiments in determining the local factors affecting the spread of invasive species.
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References
Bégin C, Scheibling RE (2003) Growth and survival of the invasive green alga Codium fragile ssp. tomentosoides in tide pools on a rocky shore in Nova Scotia. Bot Mar 46:404–412. doi:10.1515/BOT.2003.040
Biber PD (2007) Hydrodynamic transport of drifting macroalgae through a tidal cut. Estuar Coast Shelf Sci 74:565–569. doi:10.1016/j.ecss.2007.04.019
Blakeslee AMH, McKenzie CH, Darling JA, Byers JE, Pringle JM, Roman J (2010) A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long-distance dispersal of an invasive marine crab to Newfoundland. Divers Distrib 16:879–891. doi:10.1111/j.1472-4642.2010.00703.x
Buchan LAJ, Padilla DK (1999) Estimating the probability of long-distance overland dispersal of invading aquatic species. Ecol Appl 9:254–265. doi:10.2307/2641184
Bushing WW (1994) Biogeographic and ecological implications of kelp rafting as a dispersal vector for marine invertebrates. In: Halvorson WL, Maender GJ (eds) The fourth California islands symposium: update on the status of resources. Santa Barbara Museum of Natural History, Santa Barbara, pp 103–110
Cannas SA, Marco DE, Montemurro MA (2006) Long range dispersal and spatial pattern formation in biological invasions. Math Biosci 203:155–170. doi:10.1016/j.mbs.2006.06.005
Carlton JT, Scanlon JA (1985) Progression and dispersal of an introduced alga: Codium fragile ssp. tomentosoides (Chlorophyta) on the Atlantic coast of North America. Bot Mar 28:155–1665. doi:10.1515/botm.1985.28.4.155
D’Amours O, Scheibling RE (2007) Effect of wave exposure on morphology, attachment strength and survival of the invasive green alga Codium fragile ssp. tomentosoides. J Exp Mar Biol Ecol 351:129–142. doi:10.1016/j.jembe.2007.06.018
Dromgoole FI (1982) The buoyant properties of Codium. Bot Mar 25:391–397. doi:10.1515/botm.1982.25.8.391
Drouin A (2013) Établissement et impacts de la macroalgue non indigène Codium fragile ssp. fragile dans les herbiers marins aux îles de la Madeleine. PhD Thesis, Université Laval
Drouin A, McKindsey CW, Johnson LE (2011) Detecting the impacts of notorious invaders: experiments versus observations in the invasion of eelgrass meadows by the green seaweed Codium fragile. Oecologia 168:491–502. doi:10.1007/s00442-011-2086-x
Ellner SP, Schreiber SJ (2012) Temporally variable dispersal and demography can accelerate the spread of invading species. Theor Popul Biol 82:283–298. doi:10.1016/j.tpb.2012.03.005
Forrest BM, Brown SN, Taylor MD, Hurd CL, Hay CH (2000) The role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Paeophyceae). Phycologia 39:547–553. doi:10.2216/i0031-8884-39-6-547.1
Fralick RA, Mathieson AC (1973) Ecological studies of Codium fragile in New England, USA. Mar Biol 19:127–132. doi:10.1007/BF00353583
Gagnon K, McKindsey CW, Johnson LE (2011) Dispersal potential of invasive algae: the determinants of buoyancy in Codium fragile ssp. fragile. Mar Biol 158:2449–2458. doi:10.1007/s00227-011-1746-z
Garbary DJ, Fraser SJ, Hubbard C, Kim KY (2004) Codium fragile: rhizomatous growth in the Zostera thief of eastern Canada. Helgol Mar Res 58:141–146. doi:10.1007/s10152-004-0173-7
Gaylord B, Reed DC, Raimondi PT, Washburn L, McLean SR (2002) A physically based model of macroalgal spore dispersal in the wave and current-dominated nearshore. Ecology 83:1239–1251. doi:10.1890/0012-9658(2002)083[1239:APBMOM]2.0.CO;2
Harwell MC, Orth RJ (2002) Long-distance dispersal potential in a marine macrophyte. Ecology 83:3319–3330. doi:10.2307/3072082
Hastings A, Cuddington K, Davies KF et al (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101. doi:10.1111/j.1461-0248.2004.00687.x
Helmuth B, Veit RR, Holberton R (1994) Long-distance dispersal of a subantarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting. Mar Biol 120:421–426. doi:10.1007/BF00680216
Hengeveld R (1994) Small-step invasion research. Trends Ecol Evol 9:339–342. doi:10.1016/0169-5347(94)90155-4
Higgins SI, Richardson DM (1999) Predicting plant migration rates in a changing world: the role of long-distance dispersal. Am Nat 153:464–475. doi:10.1086/303193
Higgins SI, Nathan R, Cain ML (2003) Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84:1945–1956. doi:10.1890/01-0616
Holmquist JG (1994) Benthic macroalgae as a dispersal mechanism for fauna: influence of a marine tumbleweed. J Exp Mar Biol Ecol 180:235–251. doi:10.1016/0022-0981(94)90069-8
Holway DA (1995) Distribution of the Argentine ant (Linepithema humile) in Northern California. Conserv Biol 9:1634–1637. doi:10.1046/j.1523-1739.1995.09061634.x
Irestedt M, Fabre P-H, Batalha-Filho H et al (2013) The spatio-temporal colonization and diversification across the Indo-Pacific by a “great speciator” (Aves, Erythropitta erythrogaster). Proc R Soc B 280:20130309. doi:10.1098/rspb.2013.0309
Johnson CR, Chapman ARO (2007) Seaweed invasions: introduction and scope. Bot Mar 50:321–325. doi:10.1515/BOT.2007.037
Johnson LE, Padilla DK (1996) Geographic spread of exotic species: ecological lessons and opportunities from the invasion of the zebra mussel Dreissena polymorpha. Biol Conserv 78:23–33. doi:10.1016/0006-3207(96)00015-8
Johnson LE, Ricciardi A, Carlton JT (2001) Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boating. Ecol Appl 11:1789–1799. doi:10.2307/3061096
Johnson LE, Brawley SH, Adey WH (2012) Secondary spread of invasive species: historic patterns and underlying mechanisms of the continuing invasion of the European rockweed Fucus serratus in eastern North America. Biol Invasions 14:79–97. doi:10.1007/s10530-011-9976-z
Johst K, Brandl R, Eber S (2002) Metapopulation persistence in dynamic landscapes: the role of dispersal distance. Oikos 98:263–270. doi:10.1034/j.1600-0706.2002.980208.x
Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020. doi:10.1890/01-0622
Kinlan BP, Gaines SD, Lester SE (2005) Propagule dispersal and the scales of marine community process. Divers Distrib 11:139–148. doi:10.1111/j.1366-9516.2005.00158.x
Kirk H, Paul J, Straka J, Freeland JR (2011) Long-distance dispersal and high genetic diversity are implicated in the invasive spread of the common reed, Phragmites australis (Poaceae), in northeastern North America. Am J Bot. doi:10.3732/ajb.1000278
Koutitonsky VG, Navarro N, Booth D (2002) Descriptive physical oceanography of Great-Entry Lagoon, Gulf of St. Lawrence. Estuar Coast Shelf Sci 54:833–847. doi:10.1006/ecss.2001.0860
Lester SE, Ruttenberg BI, Gaines SD, Kinlan BP (2007) The relationship between dispersal ability and geographic range size. Ecol Lett 10:745–758. doi:10.1111/j.1461-0248.2007.01070.x
Li X-S, Zhang Y-L, Settele J, Franzén M, Schweiger O (2013) Long-distance dispersal and habitat use of the butterfly Byasa impediens in a fragmented subtropical forest. Insect Conserv Divers 6:170–178. doi:10.1111/j.1752-4598.2012.00199.x
Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–136. doi:10.1016/0169-5347(93)90025-K
Lyons DA, Scheibling RE (2009) Range expansion by invasive marine algae: rates and patterns of spread at a regional scale. Divers Distrib 15:762–775. doi:10.1111/j.1472-4642.2009.00580.x
Macreadie PI, Bishop MJ, Booth DJ (2011) Implications of climate change for macrophytic rafts and their hitchhikers. Mar Ecol Prog Ser 443:285–292. doi:10.3354/meps09529
Marco DE, Montemurro MA, Cannas SA (2011) Comparing short and long-distance dispersal: modelling and field case studies. Ecography 34:671–682. doi:10.1111/j.1600-0587.2010.06477.x
Minchinton TE (2006) Rafting on wrack as a mode of dispersal for plants in coastal marshes. Aquat Bot 84:372–376. doi:10.1016/j.aquabot.2006.01.007
Mineur F, Davies AJ, Maggs CA, Verlaque M, Johnson MP (2010) Fronts, jumps and secondary introductions suggested as different invasion patterns in marine species, with an increase in spread rates over time. Proc R Soc B 277:2693–2701. doi:10.1098/rspb.2010.0494
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. doi:10.1890/070064
Muirhead JR, Leung B, Overdijk C, Kelly DW, Nandakumar K, Marchant KR, MacIsaac HJ (2006) Modelling local and long-distance dispersal of invasive emerald ash borer Agrilus planipennis (Coleoptera) in North America. Divers Distrib 12:71–79. doi:10.1111/j.1366-9516.2006.00218.x
Nanba N, Kado R, Ogawa H, Komuro Y (2002) Formation and growth of filamentous thalli from isolated utricles with medullary filaments of Codium fragile spongy thalli. Aquat Bot 73:255–264. doi:10.1016/S0304-3770(02)00036-0
Nogales M, Heleno R, Traveset A, Vargas P (2012) Evidence for overlooked mechanisms of long-distance seed dispersal to and between oceanic islands. New Phytol 194:313–317. doi:10.1111/j.1469-8137.2011.04051.x
Norton TA (1992) Dispersal by macroalgae. Br Phycol J 27:293–301. doi:10.1080/00071619200650271
Occhipinti-Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed marine ecosystems. Mar Pollut Bull 46:542–551. doi:10.1016/S0025-326X(02)00363-6
Parker IM, Simberloff D, Lonsdale WM et al (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19. doi:10.1023/A:1010034312781
Prince JS, Trowbridge CD (2004) Reproduction in the green macroalga Codium (Chlorophyta): characterization of gametes. Bot Mar. doi:10.1515/BOT.2004.062
Reed DC, Laur DR, Ebeling AW (1988) Variation in algal dispersal and recruitment: the importance of episodic events. Ecol Monogr 58:321–335. doi:10.2307/1942543
Reed DC, Raimondi PT, Carr MH, Goldwasser L (2000) The role of dispersal and disturbance in determining spatial heterogeneity in sedentary organisms. Ecology 81:2011–2026. doi:10.2307/177289
Rothäusler E, Gutow L, Thiel M (2012) Floating seaweeds and their communities. In: Wiencke C, Bischof K (eds) Seaweed biology. Springer, Berlin, pp 359–380. doi:10.1007/978-3-642-28451-9_17
Santelices B (1990) Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr Mar Biol 28:177–276
Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae—a growing concern. J Appl Phycol 18:529–541. doi:10.1007/s10811-006-9074-2
Scheibling RE, Melady RA (2008) Effect of water movement and substratum type on vegetative recruitment of the invasive green alga Codium fragile ssp. tomentosoides. Bot Mar 51:341–349. doi:10.1515/BOT.2008.046
Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:159–169. doi:10.1890/1051-0761(2003)013[0159:PDDATS]2.0.CO%3B2
Simard N, Paille N, McKindsey CW (2007) Codium fragile ssp. tomentosoides: revue de littérature et situation aux Îles-de-la-Madeleine. Can Manuscr Rep Fish Aquat Sci 2786, vii + 39 p
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Syst 40:81–102. doi:10.1146/annurev.ecolsys.110308.120304
Stewart HL, Payri CE, Koehl MAR (2007) The role of buoyancy in mitigating reduced light in macroalgal aggregations. J Exp Mar Biol Ecol 343:11–20. doi:10.1016/j.jembe.2006.10.031
Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci 98:1095–1100. doi:10.1073/pnas.98.3.1095
Taylor K, Brummer T, Taper ML, Wing A, Rew LJ (2012) Human-mediated long-distance dispersal: an empirical evaluation of seed dispersal by vehicles. Divers Distrib 18:942–951. doi:10.1111/j.1472-4642.2012.00926.x
Thiel M (2003) Rafting of benthic macrofauna: important factors determining the temporal succession of the assemblage on detached macroalgae. Hydrobiologia 503:49–57. doi:10.1023/B:HYDR.0000008486.37391.60
Trowbridge CD (1998) Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies. Oceanogr Mar Biol 36:1–64
Valentine JP, Magierowski RH, Johnson CR (2007) Mechanisms of invasion: establishment, spread and persistence of introduced seaweed populations. Bot Mar. doi:10.1515/BOT.2007.040
Van den Hoek C (1987) The possible significance of long-range dispersal for the biogeography of seaweeds. Helgol Meeresunters 41:261–272. doi:10.1007/BF02366191
Vander Zanden MJ, Olden JD (2008) A management framework for preventing the secondary spread of aquatic invasive species. Can J Fish Aquat Sci 65:1512–1522. doi:10.1139/F08-099
Vogel P, Cosson J-F, López Jurado LF (2003) Taxonomic status and origin of the shrews (Soricidae) from the Canary islands inferred from a mtDNA comparison with the European Crocidura species. Mol Phylogenet Evol 27:271–282. doi:10.1016/S1055-7903(02)00403-7
Watanabe S, Metaxas A, Scheibling RE (2009) Dispersal potential of the invasive green alga Codium fragile ssp. fragile. J Exp Mar Biol Ecol 381:114–125. doi:10.1016/j.jembe.2009.09.012
Williams SL (2007) Introduced species in seagrass ecosystems: status and concerns. J Exp Mar Biol Ecol 350:89–110. doi:10.1016/j.jembe.2007.05.032
Williams DD, Williams NE (1998) Freshwater invertebrates from the Bermuda Islands and their zoogeographical affinities. Trop Zool 11:353–369. doi:10.1080/03946975.1998.10539371
Wilson JB, Lee WG (1989) Infiltration invasion. Funct Ecol 3:379–380
Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144. doi:10.1016/j.tree.2008.10.007
Acknowledgments
This study was funded by the Canadian Aquatic Invasive Species Network (CAISN) of the Natural Sciences and Engineering Research Council (NSERC) of Canada, Québec-Océan, the Fondation Communautaire Gaspésie-les-Îles, and an NSERC Discovery Grant (LEJ). We greatly appreciate the logistical support of the Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (MAPAQ) in Îles-de-la-Madeleine, especially M. Nadeau, B. Myrand, and F. Gallien. Finally we thank C. Chevrier-Turbide and O.Rhoades for assistance in the field, and V. Jormalainen for advice on statistical methods. We are also grateful for the comments of J. Ruesink and two anonymous reviewers which greatly improved the quality of this manuscript.
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Gagnon, K., McKindsey, C.W. & Johnson, L.E. Roles of dispersal mode, recipient environment and disturbance in the secondary spread of the invasive seaweed Codium fragile . Biol Invasions 17, 1123–1136 (2015). https://doi.org/10.1007/s10530-014-0782-2
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DOI: https://doi.org/10.1007/s10530-014-0782-2