Further Mediterranean expansion of the non-indigenous bryozoan Celleporaria brunnea: multiple records along the Italian coasts
DOI:
https://doi.org/10.3989/scimar.04174.31AKeywords:
fouling organisms, zoobenthos, harbours, introduced species, shipping, ship hullsAbstract
In the framework of a wider systematic survey aimed at studying non-indigenous species in Italian harbours and marinas, the ascophoran bryozoan Celleporaria brunnea was detected for the first time in the western Mediterranean Sea. The species is presumably native to the Pacific coasts of North America and is distributed from British Columbia to the Galapagos Islands (Ecuador). In the Mediterranean Sea, C. brunnea was first recorded in 2004 in the inner part of Izmir Bay near Alsancak harbour (Turkey) and later reported along the Lebanese coasts. The species was recently detected in Cascais marina in Portugal and in the Arcachon Basin (France), documenting the first records in the eastern Atlantic. The finding in the Italian harbours of La Spezia (Liguria), Olbia (Sardinia) and Lampedusa (off Sicily) marks its western and northernmost occurrence within the Mediterranean basin. Pathways of introduction into the western Mediterranean Sea are discussed, concluding that hull fouling is the most likely vector. The species may be expected to appear soon in other harbours of the Mediterranean basin.
Downloads
References
Agius C., Schembri P.J., Jaccarini V. 1977. A preliminary report on organisms fouling oyster cultures in Malta (Central Mediterranean). Mem. Biol. Mar. Oceanogr. 7: 51-59.
Aliani S., Molcard A. 2003. Hitch-hiking on floating marine debris: macrobenthic species in the Western Mediterranean Sea. Hydrobiologia 503: 59-67. http://dx.doi.org/10.1023/B:HYDR.0000008480.95045.26
André F., Corolla J.-P., Lanza B., Rochefort G. 2014. Bryozoaires d'Europe: Les Carnets du Plongeur. Éditions Neptune Plongée, Gargas, 256 pp.
Barnes D.K.A. 2002. Invasions by marine life on plastic debris. Nature 416: 808-809. http://dx.doi.org/10.1038/416808a PMid:11976671
Boero F. 1994. Fluctuations and variations in coastal marine environments. Mar. Ecol. 15(1): 3-25. http://dx.doi.org/10.1111/j.1439-0485.1994.tb00038.x
Canning-Clode J., Souto J., McCann L. 2013. First record of Celleporaria brunnea (Bryozoa: Lepraliellidae) in Portugal and in the East Atlantic. Mar. Biod. Rec. 6: 1-5. http://dx.doi.org/10.1017/s1755267213000821
Carlton J.T. 1985. Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr. Mar. Biol. Annu. Rev. 23: 313-371.
Carlton J.T. 1987. Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bull. Mar. Sci. 41(2): 452-465.
Carlton J.T. 2009. Deep invasion ecology and the assembly of communities in historical time. In: Rilov G., Crooks J.A. (eds), Biological invasions in marine ecosystems. Springer-Verlag Berlin Heidelberg, Ecological Studies 204, pp. 13-56. http://dx.doi.org/10.1007/978-3-540-79236-9_2
Carlton J.T., Geller J.B. 1993. Ecological roulette: biological invasions and the global transport of non-indigenous marine organisms. Science 261: 78-82. http://dx.doi.org/10.1126/science.261.5117.78 PMid:17750551
Carlton J.T., Hodder J. 1995. Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th century sailing vessel. Mar. Biol. 121: 721-730. http://dx.doi.org/10.1007/BF00349308
Clarke Murray C.C., Pakhomov E.A., Therriault T.W. 2011. Recreational boating: a large unregulated vector transporting marine invasive species. Divers. Distrib. 17: 1161-1172. http://dx.doi.org/10.1111/j.1472-4642.2011.00798.x
Connell S.D. 2000. Floating pontoons create novel habitats for subtidal epibiota. J. Exp. Mar. Biol. Ecol. 247: 183-194. http://dx.doi.org/10.1016/S0022-0981(00)00147-7
Connell S.D. 2001. Urban structures as marine habitats: an experimental comparison of the composition and abundance of subtidal epibiota among pilings, pontoon and rocky reefs. Mar. Environ. Res. 52: 115-125. http://dx.doi.org/10.1016/S0141-1136(00)00266-X
Davidson I.C., Zabin C.J., Chang A.L., et al. 2010. Recreational boats as potential vectors of marine organisms at an invasion hotspot. Aquat. Biol. 11: 179-191. http://dx.doi.org/10.3354/ab00302
d'Hondt J.L. 1988. Bryozoa from the coast of Israel. Italian J. Zool. 55(1-4): 191-203. http://dx.doi.org/10.1080/11250008809386617
Dunstan P.K., Johnson C.R. 2004. Invasion rates increase with species richness in a marine epibenthic community by two mechanisms. Oecologia 138: 285-292. http://dx.doi.org/10.1007/s00442-003-1400-7 PMid:14595554
Floerl O., Inglis G.J. 2003. Potential for the introduction and spread of marine pests by private yachts. Hull fouling as a mechanism for marine invasive species introductions. In: Godwin L.S. (ed) Proceedings of a workshop on current issues and potential management strategies. Honolulu, Hawaii, 12-13 February 2003, 22-28.
Floerl O., Inglis G.J., Dey K., et al. 2009. The importance of transport hubs in stepping-stone invasions. J. Appl. Ecol. 46: 37-45. http://dx.doi.org/10.1111/j.1365-2664.2008.01540.x
Galil B.S. 2009. Taking stock: inventory of alien species in the Mediterranean Sea. Biol. Invasions 11: 359-372. http://dx.doi.org/10.1007/s10530-008-9253-y
Glasby T.M., Connell S.D. 1999. Urban structures as marine habitats. Ambio 28: 595-598.
Godwin S.L. 2003. Hull fouling of maritime vessels as a pathway for marine species invasion to the Hawaiian Islands. Biofouling 19: 123-131. http://dx.doi.org/10.1080/0892701031000061750 PMid:14618713
Gollasch S. 2002. The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling 18(2): 105-121. http://dx.doi.org/10.1080/08927010290011361
Gollasch S., Lenz J., Dammer M., et al. 2000. Survival of tropical ballast water organisms during a cruise from the Indian Ocean to the North Sea. J. Plankton Res. 22(5): 923-937. http://dx.doi.org/10.1093/plankt/22.5.923
Harmelin J.G. 2014. Alien bryozoans in the eastern Mediterranean Sea - new records from the coast of Lebanon. Zootaxa 3893(3): 301-338. http://dx.doi.org/10.11646/zootaxa.3893.3.1 PMid:25544525
Harmelin J.G., Bitar G., Zibrowius H. 2009. Smittinidae (Bryozoa, Cheilostomata) from coastal habitats of Lebanon (Mediterranean Sea), including new and non-indigenous species. Zoosystema 31(1): 163-187. http://dx.doi.org/10.5252/z2009n1a9
Hastings A.B. 1929. Cheilostomatous Polyzoa from the vicinity of the Panama Canal collected by Dr. C. Crossland on the cruise of the S.Y. "St. George". Proc. Zool. Soc. London 99(4): 697-740. http://dx.doi.org/10.1111/j.1096-3642.1929.tb01453.x
Hincks T. 1884. Report on the Polyzoa of the Queen Charlotte Islands. Part 3. Ann. Mag. Natur. Hist. Ser. 5. 13: 49-58.
Johnson L., Ricciardi A., Carlton J.T. 2001. Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boating. Ecol. Appl. 11(6): 1789-1799. http://dx.doi.org/10.1890/1051-0761(2001)011[1789:odoais]2.0.co;2
Koçak F. 2007. A new alien bryozoan Celleporaria brunnea (Hincks, 1884) in the Aegean Sea (eastern Mediterranean). Sci. Mar. 71(1): 191-195.
Lodola A. 2013. Xenodiversity in Marine Protected Areas: three case studies in Italy. PhD Thesis. Pavia Univ. Italy, 243 pp.
Lodola A., Savini D., Occhipinti-Ambrogi A. 2012. First record of Tricellaria inopinata (Bryozoa: Candidae) in the harbours of La Spezia and Olbia, Western Mediterranean Sea (Italy). Mar. Biod. Rec. 5: 1-7. http://dx.doi.org/10.1017/s1755267212000309
Marchini A., Gauzer K., Occhipinti-Ambrogi A. 2004. Spatial and temporal variability of hard-bottom macrofauna in a disturbed coastal lagoon (Sacca di Goro, Po river delta, north-western Adriatic Sea). Mar. Pollut. Bull. 48(11-12): 1084-1095. http://dx.doi.org/10.1016/j.marpolbul.2003.12.015 PMid:15172814
Minchin D. 2007. Rapid coastal survey for targeted alien species associated with floating pontoons in Ireland. Aquat. Invasions 2(1): 63-70. http://dx.doi.org/10.3391/ai.2007.2.1.8
Occhipinti-Ambrogi A. 1991. The spread of Tricellaria inopinata into the Lagoon of Venice: an ecological hypothesis. Bull. Soc. Sci. Nat. Ouest Sér. 1: 299-308.
Occhipinti-Ambrogi A. 2000. Biotic invasions in a Mediterranean Lagoon. Biol. Invasions 2: 165-176. http://dx.doi.org/10.1023/A:1010004926405
Occhipinti-Ambrogi A., Savini D. 2003. Biological invasion as a component of global change in stressed marine ecosystems. Mar. Pollut. Bull. 46: 542-551. http://dx.doi.org/10.1016/S0025-326X(02)00363-6
O'Donoghue C.H., O'Donoghue E. 1926. A second list of the Bryozoa (Polyzoa) from the Vancouver Island region. Contrib. Can. Biol. Fish. 3(1): 47-131. http://dx.doi.org/10.1139/f26-003
Osburn R.C. 1952. Bryozoa of the Pacific coast of America, Part II, Cheilostomata Ascophora. Allan Hancock Pac. Exped. 14(2): 271-611.
Powell N.A. 1969. Indo-Pacific bryozoans new to the Mediterranean coast of Israel. Isr. J. Zool. 18: 157-168.
Roughgarden J., Gaines S., Possingham H. 1988. Recruitment dynamics in complex life cycles. Science 241: 1460-1465. http://dx.doi.org/10.1126/science.11538249 PMid:11538249
Ruiz G.M., Fofonoff P.W., Carlton J.T., et al. 2000. Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu. Rev. Ecol. Syst. 31: 481-531. http://dx.doi.org/10.1146/annurev.ecolsys.31.1.481
Ryland J.S. 1964. The identity of some cyphonautes larvae (Polyzoa). J. Mar. Biol. Ass. UK 44: 645-654. http://dx.doi.org/10.1017/S002531540002782X
Santagata S. 2008a. The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae. J. Morphol. 269: 349-364. http://dx.doi.org/10.1002/jmor.10592 PMid:17960760
Santagata S. 2008b. Evolutionary and structural diversification of the larval nervous system among marine bryozoans. Biol. Bull. 215: 3-23. http://dx.doi.org/10.2307/25470679 PMid:18723633
Santagata S., Zimmer R.L. 2000. Comparing cell patterns of coronate bryozoan larvae with fluorescent probes. In: Herrera Cubilla A., Jackson J.B.C. (eds), Proceedings of the Eleventh International Bryozoology Association Conference, Smithsonian
Tropical Research Institute, Balboa, Republic of Panama, 26-31 January 1998. Smithsonian Tropical Research Institute, pp. 365-375.
Savini D., Marchini A., Forni G., et al. 2006. Touristic harbours and secondary spread of alien species. Biol. Mar. Mediterr. 13: 760-763.
Scheltema R.S. 1986a. Long-distance dispersal by planktonic larvae of shoal-water benthic invertebrates among Central Pacific Islands. Bull. Mar. Sci. 39(2): 241-256.
Scheltema R.S. 1986b. On dispersal and planktonic larvae of benthic invertebrates: an eclectic overview and summary of problems. Bull. Mar. Sci. 39(2): 290-322.
Sciberras M., Schembri P.J. 2007. A critical review of records of alien marine species from the Maltese Islands and surrounding waters (Central Mediterranean). Medit. Mar. Sci. 8(1): 41-66. http://dx.doi.org/10.12681/mms.162
Seo J.E., Min B.S. 2009. A faunistic study on Cheilostomatous Bryozoans from the shoreline of South Korea, with two new species. Korean J. Syst. Zool. 25(1): 19-40. http://dx.doi.org/10.5635/KJSZ.2009.25.1.019
Smith L.D., Wonham M.J., McCann D.L., et al. 1999. Invasion pressure to a ballast-flooded estuary and an assessment of inoculant survival. Biol. Invasions 1: 67-87. http://dx.doi.org/10.1023/A:1010094527218
Soule J.D. 1961. Results of the Puritan-American Museum of Natural History Expedition to western Mexico, 13. Ascophoran Cheilostomata (Bryozoans) of the Gulf of California. Am. Mus. Novit. 2053: 1-65.
Soule D.F., Soule J.D. 1964. The Ectoprocta (Bryozoa) of Scammon's Lagoon, Baja California, Mexico. Am. Mus. Novit. 2199: 1-56.
Soule D.F., Soule J.D., Chaney H.W. 1995. The Bryozoa. In: Blake J.A., Chaney W., Scott P.H., et al. (eds), Taxonomic atlas of the benthic fauna of the Santa Maria Basin and the western Santa Barbara Channel. Irene McCulloch Foundation Monograph Series No. 2. Hancock Institute of Marine Studies, Southern California Univ. Press, 344 pp. PMCid:PMC1382944
Stricker S.A., Reed C.G., Zimmer R.L. 1988. The cyphonautes larva of the marine bryozoan Membranipora membranacea. I. General morphology, body wall, and gut. Can. J. Zool. 66(2): 368-383. http://dx.doi.org/10.1139/z88-054
Watts P.C., Thorpe J.P., Taylor P.D. 1998. Natural and anthropogenic dispersal mechanisms in the marine environment: a study using cheilostome Bryozoa. Philos. Trans. R. Soc. Lond. B. 353: 453-464. http://dx.doi.org/10.1098/rstb.1998.0222 PMCid:PMC1692224
Winston J.E. 1986. An annotated checklist of coral-associated bryozoans. Am. Mus. Novit. 2859: 1-39.
Woollacott R.M., Zimmer R.L. (eds). 1977. Biology of bryozoans. Academic Press. 584 pp.
Yoshioka P.M. 1982. Role of planktonic and benthic factors in the population dynamics of the bryozoan Membranipora membranacea. Ecology 63, 457-468. http://dx.doi.org/10.2307/1938963
Zenetos A., Gofas S., Morri C., et al. 2012. Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union's Marine Strategy Framework Directive (MSFD). Part 2. Introduction, trends and pathways. Medit. Mar. Sci. 13(2): 328-352 http://dx.doi.org/10.12681/mms.327
Published
How to Cite
Issue
Section
License
Copyright (c) 2015 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read here the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.
