Abstract
Understanding the patterns and dynamics of biological invasions is a crucial prerequisite to predicting and mitigating their potential ecological and economic impacts. Unfortunately, in many cases such understanding is limited not only by ignorance of invasion history, but also by uncertainty surrounding the ecology, physiology, and even systematics of the invasive taxa themselves. The invasive, colonial euryhaline hydroid Cordylophora has invaded multiple regions outside of its native Ponto-Caspian range. However, extensive morphological and ecological plasticity has prevented consensus on both species-level classification within the genus and the environmental conditions conducive to establishment. The goal of this research was to explore the invasive history and species composition of the genus Cordylophora through molecular analyses. We addressed both issues using DNA sequence data from two mitochondrial loci [the small subunit 16S rRNA and cytochrome c oxidase subunit I (COI)] and one nuclear locus (28S large nuclear rRNA), generated from 27 invasive Cordylophora populations collected throughout the global range of the taxon. Phylogenetic analysis and comparisons of genetic distances between populations suggest the presence of multiple cryptic species within the genus. This conclusion is further supported by the observation of significantly different habitat preferences between invasive lineages. Geographic distribution of lineages is consistent with the introduction of multiple lineages to some non-native regions, indicating that repeated introductions may contribute to the current global distribution of Cordylophora. Applying molecular and morphological analyses to additional populations of Cordylophora is likely to assist in clarifying the taxonomy of this genus and in providing a better understanding of the invasive history of this hydroid.
Similar content being viewed by others
References
Arndt EA (1984) The ecological niche of Cordylophora caspia (Pallas, 1771). Limnologica 15(2):469–477
Arndt EA (1989) Ecological, physiological and historical aspects of brackish water fauna distribution. In: Ryland JS, Tyler PA (eds) Proceedings of 23rd European marine biological symposium: reproduction, genetics and distribution of marine organisms, Olsen and Olsen, Fredensborg, pp 327–338
Berezina NA, Panov VE (2004) Distribution, population structure and salinity tolerance of the invasive amphipod Gmelinoides fasciatus (Stebbing) in the Neva Estuary (Gulf of Finland, Baltic Sea). Hydrobiologia 514:199–206. doi:10.1023/B:hydr.0000018219.28645.3a
Bially A, MacIsaac HJ (2000) Fouling mussels (Dreissena spp.) colonize soft sediments in Lake Erie and facilitate benthic invertebrates. Freshw Biol 43:85–97. doi:10.1046/j.1365-2427.2000.00526.x
Bij de Vaate A, Jazdzewski K, Ketelaars HAM, Gollasch S, van der Velde G (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can J Fish Aquat Sci 59:1159–1174. doi:10.1139/f02-098
Cairns SD, Calder DR, Brinckmann-Voss A, Castro CB, Fautin DG, Pugh PR et al (2002) Common and scientific names of aquatic invertebrates from the United States and Canada: Cnidaria and Ctenophora, 2nd edn. American Fisheries Society Special Publication 28, pp 1–115
Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77(6):1653–1655. doi:10.2307/2265767
Cohen A, Mills C, Berry H, Wonham M, Bingham B, Bookheim B et al (1998) A rapid assessment survey of non-indigenous species in the shallow waters of puget sound. Report of the Puget Sound Expedition. September 8–16, 1998, pp 1–36
Colautti RI, Manca M, Viljanen M, Ketelaars HAM, Bürgi H, MacIsaac HJ et al (2005) Invasion genetics of the Eurasian spiny waterflea: evidence for bottlenecks and gene flow using microsatellites. Mol Ecol 14:1869–1879. doi:10.1111/j.1365-294X.2005.02565.x
Cunningham CW, Buss LW (1993) Molecular evidence for multiple episodes of paedomorphosis in the family Hydractiniidae. Biochem Syst Ecol 21:57–69. doi:10.1016/0305-1978(93)90009-G
Folino NC (2000) The freshwater expansion and classification of the colonial hydroid Cordylophora. In: Marine bioinvasions: proceedings of the first national conference, January 24–27, Massachusetts Institute of Technology Sea Grant College Program, Cambridge, MA, 1999, pp 139–144
Folino-Rorem N, Stoeckel J, Thorn E, Page L (2006) Effects of artificial filamentous substrate on zebra mussel (Dreissena polymorpha) settlement. Biol Invasions 8:89–96. doi:10.1007/s10530-005-0330-1
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299
Gosner KL (1971) Guide to identification of marine and estuarine invertebrates: Cape Hatteras to the Bay of Fundy. Wiley, NY, pp 77–107
Goulletquer P, Bachelet G, Sauriau PG, Noel P (2002) Open Atlantic Coast of Europe—a century of introduced species into French waters. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, The Netherlands, pp 276–290
Govindarajan AF, Boero F, Halanych KM (2006) Phylogenetic analysis with multiple markers indicates repeated loss of the adult medusa stage in Campanulariidae (Hydrozoa, Cnidaria). Mol Phylogenet Evol 38:820–834. doi:10.1016/j.ympev.2005.11.012
Jankowski T, Collins AG, Campbell R (2008) Global diversity of inland water cnidarians. Hydrobiologia 595:35–40. doi:10.1007/s10750-007-9001-9
Janssen J, Berg MB, Lozano SJ (2005) Submerged terra incognita; Lake Michigan’s abundant but unknown rocky shores. In: Edsall T, Munawar M (eds) State of Lake Michigan: ecology, health and management. Ecovision world monograph series. SBP Publishing, Amsterdam, pp 113–139
Jensen KR, Knudsen J (2005) A summary of alien marine benthic invertebrates in Danish waters. Oceanol Hydrobiol Stud 34(1):137–162
Kinne O (1958) Adaptations to salinity variations—some facts and problems. In: Prosser CL (ed) Physiological adaptation. American Physiological Society, Washington, DC, pp 92–106
Kinne O (1964) Non-genetic adaptation to temperature and salinity. Helgol Mar Res 9(1–4):433–458
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16(4):199–204. doi:10.1016/S0169-5347(01)02101-2
Lee CE, Bell MA (1999) Causes and consequences of recent freshwater invasions by saltwater animals. Trends Ecol Evol 14(7):284–288. doi:10.1016/S0169-5347(99)01596-7
Lee CE, Remfert JL, Gelembiuk GW (2003) Evolution of physiological tolerance and performance during freshwater invasions. Integr Comp Biol 43:439–449. doi:10.1093/icb/43.3.439
Lee CE, Remfert JL, Chang YM (2007) Response to selection and evolvability of invasive populations. Genetica 129:179–192. doi:10.1007/s10709-006-9013-9
Leppäkoski E (2005) The first twenty years of invasion biology in the Baltic Sea area. Oceanol Hydrobiol Stud 34(1):5–17
Leppäkoski E, Olenin S (2000) Non-native species and rates of spread: lessons from the brackish Baltic Sea. Biol Invasions 2:151–163. doi:10.1023/A:1010052809567
Miglietta MP, Piraino S, Kubota S, Schuchert P (2007) Species in the genus Turritopsis (Cnidaria, Hydrozoa): a molecular evaluation. J Zool Syst Evol Res 45:11–19. doi:10.1111/j.1439-0469.2006.00379.x
Mills EL, Leach JH, Carlton JT, Secor CL (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. J Great Lakes Res 19:1–54
Nehring S (2002) Biological invasions into German waters: an evaluation of the importance of different human-mediated vectors for nonindigenous macrozoobentic species. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, The Netherlands, pp 373–383
Ojaveer H, Leppäkoski E, Olenin S, Ricciardi A (2002) Ecological impacts of alien species in the Baltic Sea and in the Great Lakes: an inter-ecosystem comparison. In: Leppäkoski E, Olenin S, Gollasch S (eds) Invasive aquatic species of Europe: distributions, impacts, and management. Kluwer, Dordrecht
Paavola M, Olenin S, Leppäkoski E (2005) Are invasive species most successful in habitats of low native species richness across European brackish water seas? Estuar Coast Shelf Sci 64:738–750. doi:10.1016/j.ecss.2005.03.021
Panov VE, Krylov PI, Riccardi N (2004) Role of diapause in dispersal and invasion success by aquatic invertebrates. J Limnol 63(1):56–69
Pienimäki M, Leppäkoski E (2004) Invasion pressure on the Finnish Lake District: invasion corridors and barriers. Biol Invasions 6:331–346. doi:10.1023/B:BINV.0000034607.00490.95
Ricciardi A (2006) Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Divers Distrib 12:425–433. doi:10.1111/j.1366-9516.2006.00262.x
Ricciardi A, Atkinson SK (2004) Distinctiveness magnifies the impact of biological invaders in aquatic ecosystems. Ecol Lett 7:781–784. doi:10.1111/j.1461-0248.2004.00642.x
Roch F (1924) Experimentelle untersuchungen an Cordylophora caspia (Pallas) [=Lacustris Allman] über die Abhängigkeit ihrer geographischen Verbreitung und ihrer Wuchsformen von den physikalischchemischen Bedingungen des Umgebenden. Mediums. Z. Morph. Ökol. Tierre 2:350–426
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180
Roos PJ (1979) Two-stage life cycle of a Cordylophora population in the Netherlands. Hydrobiologia 62(3):231–239
Ruiz GM, Fofonoff P, Hines AH (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44(3, part 2):950–972
Ruiz GM, Fofonoff P, Carlton J, Wonham MJ, Hines AH (2000) Invasion of coastal communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531. doi:10.1146/annurev.ecolsys.31.1.481
Schable NA, Kuenzi AM, Drake CA, Folino-Rorem NC, Darling JA (2008) Microsatellite loci for the invasive colonial hydrozoan Cordylophora caspia. Mol Ecol Resour 8:968–970. doi:10.1111/j.1471-8286.2008.02109.x
Schuchert P (2004) Revision of the European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Families Oceanidae and Pachycordylidae. Rev Suisse Zool 111(2):315–369
Schuchert P (2005) Species boundaries in the hydrozoan genus Coryne. Mol Phylogenet Evol 36:194–199. doi:10.1016/j.ympev.2005.03.021
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629. doi:10.1111/j.1461-0248.2006.00889.x
Smith DG (2001) Pennak’s freshwater invertebrates of the Untied States: Porifera to Crustacea, 4th edn. Wiley, NY, p 638
Smith DG, Werle SF, Klekowski E (2002) The rapid colonization and emerging biology of Cordylophora caspia (Pallas, 1771) (Cnidaria: Clavidae) in the Connecticut River. J Freshwat Ecol 17(3):423–430
Sogin ML, Edman JC (1990) Amplification of ribosomal RNA genes for molecular evolution studies. In: Innes MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 307–314
Stepien CA, Tumeo MA (2006) Invasion genetics of Ponto-Caspian gobies in the Great Lakes: a ‘cryptic’ species of founder effects, and comparative risk analysis. Biol Invasions 8:61–78. doi:10.1007/s10530-005-0237-x
Stepien CA, Brown JE, Neilson ME, Tumeo MA (2005) Genetic diversity of invasive species in the Great Lakes versus their Eurasian source populations: insights for risk analysis. Risk Anal 25:1043–1060. doi:10.1111/j.1539-6924.2005.00655.x
Strayer D (1999) Invasion of fresh waters by saltwater animals. Trends Ecol Evol 14(11):448–449. doi:10.1016/S0169-5347(99)01712-7
Streftaris N, Zenetos A, Papathanassiou E (2005) Globalisation in marine ecosystems: the story of non-indigenous marine species across European seas. Oceanogr Mar Biol Annu Rev 43:419–453
Swofford DL (2000) PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. doi:10.1093/nar/25.24.4876
Thorp JH, Covich AP (2001) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, p 911
Vanderploeg HA, Nalepa TF, Jude DJ, Mills EL, Holeck KT, Liebig JR et al (2002) Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian Great Lakes. Can J Fish Aquat Sci 59:1209–1228. doi:10.1139/f02-087
Verrill AE, Smith SI, Harger O (1873) Catalog of the marine invertebrate animals of the southern coast of New England Report of the United States Fish Commission. 1872(8):537–577
Wasson K, Fenn K, Peasre JS (2005) Habitat differences in marine invasions of central California. Biol Invasions 7:935–948. doi:10.1007/s10530-004-2995-2
Winkler G, Dodson JJ, Lee CE (2008) Heterogeneity within the native range: population genetic analyses of sympatric invasive and noninvasive clades of the freshwater invading copepod Eurytemora affinis. Mol Ecol 17:415–430
Wolff WJ (2000) Recent human-induced invasions of fresh waters by saltwater animals? Aquat Ecol 34:319–321. doi:10.1023/A:1009908010959
Wonham MJ, Carlton JT (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biol Invasions 7:369–392. doi:10.1007/s10530-004-2581-7
Acknowledgments
We are grateful for support from the G.W. Aldeen Memorial Fund and Wheaton Alumni Association from Wheaton College, IL. We also thank Drs. Busch, Page, Kennett and Scott (Wheaton College) for their assistance. Thanks go to Sarah Baxter, Clifford Cunningham, Doug Rorem, Dale Calder, Terry Marsh, Dan Minchin (assistance in Ireland), John Chapman (samples from Oregon), Ilona B. Muskó (samples from Hungry), Beccy Mant (samples from UK), Andy Chang (samples from Antioch and Pitsburg CA), Matt Duggan, Larry Harris, Ward Kriegbaum, Parry Macdonald, Emily Mindrebo, Esther Papp and Hallie Tidwell for their assistance with fieldwork. Samples from Chile and France were collected by Horia Galea and deposited in collections of the Muséum d’histoire naturelle de la Ville de Genève; Drs. Galea and Peter Schuchert kindly supplied genomic DNA from these samples. Though this work was reviewed by US EPA and approved for publication, it may not necessarily reflect official Agency policy.
Author information
Authors and Affiliations
Corresponding author
Additional information
N. C. Folino-Rorem and J. A. Darling contributed equally to this work.
Rights and permissions
About this article
Cite this article
Folino-Rorem, N.C., Darling, J.A. & D’Ausilio, C.A. Genetic analysis reveals multiple cryptic invasive species of the hydrozoan genus Cordylophora . Biol Invasions 11, 1869–1882 (2009). https://doi.org/10.1007/s10530-008-9365-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-008-9365-4