Skip to main content

Advertisement

Log in

Cryptic invaders: nonindigenous and cryptogenic freshwater Bryozoa and Entoprocta in the St. Lawrence River

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The distributions of most cosmopolitan invertebrate species are assumed to result from natural processes. Cryptic invertebrates with obscure biogeographic origins are often considered native by default, resulting in potentially severe underestimation of the extent of human-assisted invasions. This problem is exemplified by freshwater Bryozoa (Ectoprocta) and Entoprocta—small and widely distributed invertebrates commonly found in lakes and rivers. A benthic survey of a thermally modified section of the St. Lawrence River revealed the presence of two nonindigenous bryozoans: Carter’s moss animal Lophopodella carteri (Hyatt) and the crystal moss animal Lophopus crystallinus Pallas. Also discovered was a cryptogenic entoproct, the goblet worm Urnatella gracilis Leidy. These species were collected as statoblasts and (in the case of U. gracilis) colonial fragments downstream of the Gentilly-2 nuclear power plant at Bécancoeur, Quebec. Local densities of both U. gracilis and L. carteri increased by an order of magnitude at sites closer to the power plant. The occurrence of Lophopus crystallinus statoblasts in St. Lawrence River sediments is the first documented physical evidence of the species in North America. Contrary to the presumed natural Holarctic distribution of L. crystallinus, our literature review found that published historical records of L. crystallinus in the United States are erroneous or unsubstantiated. We propose that L. crystallinus is a western Palearctic species recently introduced to the St. Lawrence River, most likely as statoblasts discharged with ballast water from transoceanic ships.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bailey SA, Duggan IC, Jenkins PT, MacIsaac HJ (2005) Invertebrate resting stages in residual ballast sediment of transoceanic ships. Can J Fish Aquat Sci 62:1090–1103

    Article  Google Scholar 

  • Balounová Z, Pechoušková E, Rajchard J, Joza V, Šinko J (2013) World-wide distribution of the bryozoan Pectinatella magnifica (Leidy 1851). Eur J Environ Sci 3:96–100

    Google Scholar 

  • Bushnell JH (1973) The freshwater Ectoprocta: a zoogeographical discussion. In: Larwood GP (ed) Living and fossil Bryozoa: recent advances in research. Academic Press, London, pp 503–521

    Google Scholar 

  • Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks J (eds) Marine bioinvasions: ecology, conservation and management perspectives. Springer-Verlag, New York, pp 13–56

    Google Scholar 

  • Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crustacean Biol 11:386–400

    Article  Google Scholar 

  • Cooper CM, Burris JW (1984) Bryozoans—possible indicators of environmental quality in Bear Creek, Mississippi. J Environ Qual 13:127–130

    Article  Google Scholar 

  • Davenport CB (1899) Synopses of North American invertebrates. I. Fresh-water Bryozoa. Am Nat 33(391):593–596

    Article  Google Scholar 

  • D’Hondt J-L, Morgillo A, Gontier B (2002) Urnatella gracilis Leidy, 1851, un Entoprocte d’eau douce nouveau pour la faune française. Bulletin mensuel de la Société linnéenne de Lyon 71(7):269–274

    Google Scholar 

  • Figuerola J, Green AJ, Black K, Okamura B (2004) Influence of gut morphology on passive transport of freshwater bryozoans by waterfowl in Doñana (southwestern Spain). Can J Zool 82:835–840

    Article  Google Scholar 

  • Francis DR (2001) Bryozoan statoblasts. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments. Zoological indicators, vol 4. Kluwer, Dordrecht, pp 105–123

    Chapter  Google Scholar 

  • Freeland JR, Romualdi C, Okamura B (2000) Gene flow and genetic diversity: a comparison of freshwater bryozoan populations in Europe and North America. Heredity 85:498–508

    Article  PubMed  Google Scholar 

  • Hartikainen H, Johnes P, Moncrieff C, Okamura B (2009) Bryozoan populations reflect nutrient enrichment and productivity gradients in rivers. Freshw Biol 54:2320–2334

    Article  CAS  Google Scholar 

  • Hill S, Okamura B (2005) A review of the ecology of Lophopus crystallinus (Plumatellida, Lophopodidae), a rare species within the U.K. Denisia 28:193–201

    Google Scholar 

  • Hill S, Sayer CD, Hammond PM, Rimmer VK, Davidson TA, Hoare DJ, Burgess A, Okamura B (2007) Are rare species rare or just overlooked? Assessing the distribution of the freshwater bryozoan, Lophopus crystallinus. Biol Conserv 135:223–234

    Article  Google Scholar 

  • Hyatt A (1868) Observations on Polyzoa, Suborder Phylactolaemata. Proceedings of the Essex Institute (1866–1868), Salem, pp 1–103

    Google Scholar 

  • Jones LA, Ricciardi A (2005) Influence of physicochemical factors on the distribution and biomass of invasive mussels (Dreissena polymorpha and Dreissena bugensis) in the St. Lawrence River. Can J Fish Aquat Sci 62:1953–1962

    Article  CAS  Google Scholar 

  • Karatayev AY, Burlakova LE, Padilla DK, Mastitsky SE, Olenin S (2009) Invaders are not a random selection of species. Biol Invasions 11:2009–2019

    Article  Google Scholar 

  • Kipp R, Bailey SA, MacIsaac H, Ricciardi A (2010) Transoceanic ships as vectors for nonindigenous freshwater bryozoans. Divers Distrib 16:77–83

    Article  Google Scholar 

  • Kofoid CA (1908) The plankton of the Illinois River, 1894–1899, with introductory notes upon the hydrography of the Illinois River and its Basin. Part II. Constituent organisms and their season distribution. Bull Illinois State Lab Nat Hist 8:1–361

    Google Scholar 

  • Kraepelin K (1887) Die Deutschen Süsswasser-Bryozoen: Eine Monographie. I. Anatomisch-systematischer Teil. Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg 10:1–168

    Google Scholar 

  • Lacourt AW (1968) A monograph of the freshwater Bryozoa—Phylactolaemata. Zoologische Verhandelingen 93:1–159

    Google Scholar 

  • Langlois DL, Vaillancourt G (1990) Étude de la structure et de la composition des communautés d’invertébrés benthiques du fleuve Saint-Laurent au voisinage de la centrale nucléaire de Gentilly (Québec). In: Messier D, Legendre P, Delisle CE (eds) Symposium sur le Saint-Laurent: un fleuve à reconquérir. Association des biologistes du Québec et Centre Saint-Laurent, Montreal. pp 661–687

  • Leidy J (1858) Remarks on Polyzoa. Proc Acad Nat Sci Phila 10(1858):188–190

    Google Scholar 

  • Massard JA, Geimer G (2008) Global diversity of bryozoans (Bryozoa or Ectoprocta) in freshwater: an update. Bulletin de la Societé des Naturalistes Luxembourgeois 109:139–148

    Google Scholar 

  • Masters CO (1940) Notes on subtropical plants and animals in Ohio. Ohio J Sci 40:147–148

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Muttkowski RA (1918) The fauna of Lake Mendota: a qualitative and quantitative survey with special reference to the insects. Trans Wis Acad Sci Arts Lett 19:374–482

    Google Scholar 

  • Protasov AA (1995) On the thermal factor importance in Urnatella gracilis distribution. Vestnik Zoologii 0(2–3):94–96

    Google Scholar 

  • Ray GL (2005) Invasive estuarine and marine animals of California. ANSRP Technical Notes Collection (ERDC/TN ANSRP-05-2), U.S. Army Engineer Research and Development Center, Vicksburg

    Google Scholar 

  • Ricciardi A (2006) Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Divers Distrib 12:425–433

    Article  Google Scholar 

  • Ricciardi A (2015) Ecology of invasive alien invertebrates. In: Thorp JH, Rogers DC, Tockner K (eds) Thorp and Covich’s freshwater invertebrates. Elsevier, Amsterdam, pp 83–91

    Google Scholar 

  • Ricciardi A, Reiswig HM (1994) Taxonomy, distribution and ecology of the freshwater bryozoans (Ectoprocta) of eastern Canada. Can J Zool 72:339–359

    Article  Google Scholar 

  • Rogick MD (1935) Studies on fresh-water Bryozoa. II. The Bryozoa of Lake Erie. Trans Am Microsc Soc 54:245–263

    Article  Google Scholar 

  • Rogick MD (1936) Studies on fresh-water Bryozoa. IV. On the variation of statoblasts of Lophopodella carteri. Trans Am Microsc Soc 55:327–333

    Article  Google Scholar 

  • Rup MP, Bailey SA, Wiley CJ, Minton MS, Miller AW, Ruiz GM, MacIsaac HJ (2010) Domestic ballast operations on the Great Lakes: potential importance of Lakers as a vector for introduction and spread of nonindigenous species. Can J Fish Aquat Sci 67:256–268

    Article  Google Scholar 

  • Sanzhak YO, Lyashenko AV, Gontar VI (2012) First finding of freshwater bryozoans Lophopodella carteri Hyatt, 1866 in the Kylian Delta of the Danube River. Russ J Biol Invasions 3(1):29–33

    Article  Google Scholar 

  • Simard MA, Paquet A, Jutras C, Robitaille Y, Blier PU, Courtois R, Martel AL (2012) North American range extension of the invasive Asian clam in a St. Lawrence River power station thermal plume. Aquat Invasions 7:81–89

    Article  Google Scholar 

  • Taticchi MI, Pieroni G, Elia AC (2008) First finding of Plumatella vaihiriae (Hastings, 1929) (Bryozoa, Phylactolaemata) in Europe. Ital J Zool 75:411–416

    Article  Google Scholar 

  • Vranovsky M (1994) On the record of Urnatella gracilis Leidy, 1851 (Kamptozoa) in East Slovakia, with remarks on its ecology and geographical distribution. Biologia 49:659–666

    Google Scholar 

  • Walker CE, Herrmann SJ, Nimmo DR, Beaver JR (2013) Range extensions for three new invasive species in Pueblo Reservoir, Colorado, USA: water flea Daphnia lumholtzi (G. O. Sars, 1885), calanoid copepod Eurytemora affinis (Poppe, 1880), and freshwater bryozoan Lophopodella carteri (Hyatt, 1865). BioInvasions Rec 2:207–214

    Article  Google Scholar 

  • Watermolen D (2004) Freshwater bryozoan records from Wisconsin. Bureau of Integrated Science Services, Wisconsin Department of Natural Resources, Madison

    Google Scholar 

  • Wood TS (1989) Ectoproct bryozoans of Ohio. Ohio Biol Surv Bull New Series 8(2):1–70

    Google Scholar 

  • Wood TS (2002) Freshwater bryozoans: a zoogeographical reassessment. In: Wyse Jackson PN, Buttler JC, Spencer Jones ME (eds) Bryozoan studies 2001. Swets and Zeitlinger, Lisse, pp 39–345

    Google Scholar 

  • Wood TS (2010) Bryozoans. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates, 3rd edn. Academic Press, San Diego, pp 437–454

    Chapter  Google Scholar 

  • Wood TS, Marsh TG (1996) The sinking floatoblasts of Lophopodella carteri (Bryozoa: Phylactolaemata). In: Gordon DP, Smith AM, Grant-Mackie JA (eds) Bryozoans in space and time. National Institute of Water and Atmospheric Research, Wellington, pp 383–389

    Google Scholar 

  • Wood TS, Okamura B (1998) Asajirella gelatinosa in Panama: a bryozoan range extension in the Western Hemisphere (Ectoprocta : Phylactolaemata). Hydrobiologia 390:19–23

    Article  Google Scholar 

Download references

Acknowledgments

We thank three anonymous reviewers for their comments, and Prof. Timothy S. Wood (Wright State University) for providing information on reports of L. crystallinus. We also acknowledge the following people for their assistance in the lab and in the field: Kara Lynn Beckman, Marie-Claire Chiasson, Emilija Cvetanovska, Natasha Dudek, Charlotte Lapeyre, Andrea Morden, Ian Perrera, Dustin Raab, Katherine Shaw, Isabel Tom, Karen Wang, and Yinci Yan. Funding by an NSERC Julie Payette Scholarship to K.H. and an NSERC Discovery Grant to A.R. is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anthony Ricciardi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 35 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hamelin, K.M., Castañeda, R.A. & Ricciardi, A. Cryptic invaders: nonindigenous and cryptogenic freshwater Bryozoa and Entoprocta in the St. Lawrence River. Biol Invasions 18, 1737–1744 (2016). https://doi.org/10.1007/s10530-016-1116-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1116-3

Keywords