Skip to main content
Log in

After a century in the Mediterranean, the warm-water shipworm Teredo bartschi invades the Lagoon of Venice (Italy), overwintering a few degrees above zero

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

Abstract

During almost a century of permanence in the Mediterranean, the warm water species Teredo bartschi has adapted to progressively colder climates up to overwintering at water temperatures only a few degrees above zero. A fine-grained analysis of discoveries, synonyms, museum collections and grey literature establishes that this species entered the Mediterranean since at least 1935. Coming from tropical waters through the Suez Canal, the species has undergone to a long period of acclimatization in the Levantine Basin of the Mediterranean and then pushed north at the beginning of this century until it has invaded the Lagoon of Venice. The invasion routes are reconstructed and presented. The lagoon of Venice is a microtidal bar-built estuary located in the northernmost part of the Mediterranean and represents the highest latitude reached by the species on a global scale. Here for over ten years, T. bartschi has now become invasive forming stable and abundant populations. This paper presents some biometrics of hard parts such as pallets and shells as well as the description of siphons, useful for the identification and characterization of the species. The shape of the pallets of the Venetian population differs from the Aqaba’s (Giordania) and Mersin’s (Turkey) populations. Phenotypic variation are probably due to environmental effects on morphology.

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

Access this article

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

References

  • Anonymous (1959) The venice system for the classification of marine waters according to salinity. Limnol Oceanogr 3:346–347

  • Agur Z, Safriel UN (1981) Why is the Mediterranean more readily colonized than the Red Sea, by organisms using the Suez Canal as a passageway? Oecologia 49:359–361. https://doi.org/10.1007/BF00347598

    Article  CAS  PubMed  Google Scholar 

  • Al-Hamdani ZK, Appelqvist C, Björdal CG, Gregory D, Manders M (2011) Guidelines for predicting of decay by shipworms in the Baltic Sea. p 47

  • Appelqvist C, Havenhand JN (2016) A phenological shift in the time of recruitment of the shipworm, Teredo navalis L, mirrors marine climate change. Ecol Evol 6:3862–3870. https://doi.org/10.1002/ece3.2126

    Article  PubMed  PubMed Central  Google Scholar 

  • Appelqvist C, Havenhand JN, Toth GB (2015a) Distribution and abundance of teredinid recruits along the Swedish coast—are shipworms invading the Baltic Sea? J Mar Biol Assoc UK 95:783–790. https://doi.org/10.1017/S0025315414001830

    Article  Google Scholar 

  • Appelqvist C, Al-Hamdani ZK, Jonsson PR, Havenhand JN (2015b) Climate envelope modeling and dispersal simulations show little risk of range extension of the shipworm, Teredo navalis (L), in the Baltic Sea. PLoS ONE 10(3):e0119217. https://doi.org/10.1371/journal.pone.0119217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aubert J-J (2015) Trajan’s canal: river navigation from the Nile to the Red Sea. In: De Romanis F, Maiuro M (eds) Across the Ocean: nine essays on Indo-Mediterranean trade. Brill Pubbl, Leiden/Boston, pp 33–42

    Google Scholar 

  • Betcher MA, Fung JM, Han AW, O’Connor R, Seronay R, Concepcion GP et al (2012) Microbial distribution and abundance in the digestive system of five shipworm species (Bivalvia: Teredinidae). PLoS ONE 7(9):e45309. https://doi.org/10.1371/journal.pone.0045309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bienhold C, Pop Ristova P, Wenzhöfer F, Dittmar T, Boetius A (2013) How deep-sea wood falls sustain chemosynthetic life. PLoS ONE 8(1):e53590. https://doi.org/10.1371/journal.pone.0053590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borges LMS, Merckelbach LM, Sampaio I, Cragg SM (2014a) Diversity, environmental requirements, and biogeography of bivalve wood-borers (Teredinidae) in European coastal waters. Front Zool 11:13. https://doi.org/10.1186/1742-9994-11-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Borges LMS, Sivrikaya H, Cragg S (2014b) First records of the warm water shipworm Teredo bartschi (Bivalvia, Teredinidae) in Mersin, southern Turkey and in Olhão. Portugal Bioinvasions Rec 3(1):25–28. https://doi.org/10.3391/bir.2014.3.1.04

    Article  Google Scholar 

  • Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–273. https://doi.org/10.1111/j.1523-1739.1989.tb00086

    Article  Google Scholar 

  • Carlton JT (1995) Shipping Study: The Role of Shipping in the Introduction of Nonindigenous Aquatic Organisms to the Coastal Waters of the United States (other Than the Great Lakes) and an Analysis of Control Options. U.S. Coast Guard, Office of Engineering, Logistics, and Development, p 275

  • Carlton JT, Chapman JWC, Geller JB, Miller JA, Carlton DA, McCuller MI, Treneman N, Steves BP, Ruiz GM (2017) Tsunami-driven rafting: transoceanic species dispersal and implications for marine biogeography. Science 357(6358):1402–1406. https://doi.org/10.1126/science.aao1498

    Article  CAS  PubMed  Google Scholar 

  • Clapp WF (1923) New species of Teredo from Florida. Proc Boston Soc Nat Hist 37:31–38

    Google Scholar 

  • Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, Aguzzi J et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5(8):e11842. https://doi.org/10.1371/journal.pone.0011842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Columbus C (1492–1493) Journal of Christopher Columbus (During his First Voyage, 149293): and Documents Relating the Voyages of John Cabot and Gaspar Corte Real (Cambridge Library Collection - Hakluyt First Series) (Markham C (ed)). Cambridge: Camb U Pr. https://doi.org/10.1017/CBO9780511708411

  • Cooper JP (2009) Egypt’s Nile-Red Sea Canals: Chronology, Location, Seasonality and Function. In Blue LK, Cooper JP, Thomas R, Whitewright J (Eds.), Connected Hinterlands: Proceedings of Red Sea Project IV, Oxford: Archaeopress, pp 195–210

  • Corlett RT (2013) Where are the subtropics? Biotropica 45(3):273–275

  • Cragg SM, Jumel M-C, Al-Horani FA, Hendy IW (2009) The life history characteristics of the wood-boring bivalve Teredo bartschi are suited to the elevated salinity, oligotrophic circulation in the Gulf of Aqaba, Red Sea. J Exp Mar Biol Ecol 375:99–105. https://doi.org/10.1016/j.jembe.2009.05.014

    Article  Google Scholar 

  • Distel DL (2003) The biology of marine wood boring bivalves and their bacterial endosymbionts. In: Goodell B, Nicholas DD, Schultz TP, editors. Wood Deterioration and Preservation. Washington: Am Chem Soc Pr 253–271. https://doi.org/10.1021/bk-2003-0845.ch014

  • Edmonson CH (1962) Teredinidae, ocean travellers. Occasional Papers of the Bernice P Bishop Museum 23(3):45–59

    Google Scholar 

  • EN275 (1992) Test Method for determining the protective effectiveness of a preservative against marine borers. European Committee for Standardization. p 21

  • European Commission (2008) Directive 2008/56/EC – Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for Community action in the field of marine environmental policy (Marine Strategy Framework Directive)

  • Galil BS (2008) Alien species in the Mediterranean Sea—which, when, where, why? In: Davenport J et al. (eds) Chall Mar Ecosyst Hydrobiologia 606:105–116. https://doi.org/10.1007/s10750-008-9342-z

  • Galil B, Marchini A, Occhipinti-Ambrogi A, Ojaveer H (2017) The enlargement of the Suez Canal—Erythraean introductions and management challenges. Management of Biological Invasions 8:141–152

    Article  Google Scholar 

  • Galil BS, Marchini A, Occhipinti-Ambrogi A (2018) Mare Nostrum, Mare Quod Invaditur—The History of Bioinvasions in the Mediterranean Sea. In Histories of Bioinvasions in the Mediterranean, Springer, Cham pp 21–49

  • Geiger R, Pohl W (1953) Revision of Koppen–Geiger Climate Maps of the Earth. Darmstadt, Germany, Justus Perthes

    Google Scholar 

  • Harrington B, the Inkscape developer team (2004–2005) Inkscape. Version 2, June (1991) Copyright (C) 1989, 1991 Free Software Foundation, Inc. 51 Franklin Street, Fifth Floor, Boston, MA 02110 – 1301, USA. http://www.inkscape.org/

  • Hedgpeth JW (1957) Classification of marine environments. In Hedgpeth JW Treatise on Marine Ecology and Paleoecology. Geol Soc Am Mem 67(1):17–27

    Google Scholar 

  • Hill CL, Kofoid CA (eds) (1927) Marine Borers and Their Relation to Marine Construction on on the Pacific coast: Being the Final Report of the San Francisco Bay Marine Piling Committee. San Francisco, CA, p 357

  • Hoagland KE (1986) Effects of temperature, salinity and substratum on larvae of the shipworm Teredo bartschi Clapp and Teredo navalis Linnaeus (Bivalvia: Teredinidae). American Malacological Bulletin 4:89–99

    Google Scholar 

  • Hoagland KE, Crocket L (1978) Analysis of populations of boring and fouling organisms he vicinity of the Oyster Creek Nuclear Generating Station. Quarterly Report September 1978-November 1978. U.S. Nuclear Regulatory Commission, NUREG/CR-0812, 66 pp

  • Hoagland KE, Crocket L (1982a) Ecological Studies of Wood-Boring Bivalves in the Vicinity of the Oyster Creek Nuclear Generating Station Progress Report June-August 1981 - February 1982, U.S. Nuclear Regulatory Commission, NUREG/CR-1939 Vol. 4, p 45

  • Hoagland KE, Crocket L (1982b) Ecological Studies of Wood-Boring Bivalves in the Vicinity of the Oyster Creek Nuclear Generating Station Progress Report December 1981 - February 1982, U.S. Nuclear Regulatory Commission, NUREG/CR-2727 Vol. 2, p 29

  • Hoagland KE, Turner RD (1980) Range extensions of teredinids (shipworms) and polychaetes in the vicinity of a temperate-zone nuclear generating station. Mar Biol 58(1):55–64. https://doi.org/10.1007/BF00386880

    Article  Google Scholar 

  • Isham LB, Tiemey JQ (1953) Some aspects of the larval development and metamorphosis of Teredo (Lyrodus) pedicellata de Quatrefages. Bull Mar Sci Gulf Caribb 2:574–589

    Google Scholar 

  • Katsanevakis S, Wallentinus I, Zenetos A, Leppäkoski E, Çinar ME, Oztürk B, Grabowski M, Golani D, Cardoso AC (2014) Impacts of marine invasive alien species on ecosystem services and biodiversity: a pan-European review. Aquat Invasions 9:391–423. https://doi.org/10.3391/ai.2014.9.4.01

    Article  Google Scholar 

  • Kimball S, Mattis P & the GIMP developer team (1997–2014) GIMP 2.8.22. http://www.gimp.org/

  • Kintisch E (2016) Arctic shipworm discovery alarms archaeologists. Science 351(6276):901. https://doi.org/10.1126/science.351.6276.901

    Article  CAS  PubMed  Google Scholar 

  • Kjerfve B (1994) Coastal lagoon processes. (ed) Elsevier Oceanography Series 60. Elsevier, Amsterdam

  • Lane CE, Tierney JQ, Hennacy RE (1954) The respiration of normal larvae of Teredo bartschi Clapp. Biolological Bulletin 106(3):323–327. https://doi.org/10.2307/1538766

    Article  Google Scholar 

  • Laurent MCZ, Gros O, Brulport JP, Gaill F, Le Bris N (2009) Sunken wood habitat for thiotrophic symbiosis in mangrove swamps. Mar Environ Res 67:83–88. https://doi.org/10.1016/j.marenvres.2008.11.006

    Article  CAS  PubMed  Google Scholar 

  • Leppäkoskii E, Gollasch S, Olenin S (eds) (2002) Invasive Aquatic Species of Europe: Distribution, Impacts and Management. Kluwer Academic Publishers Dordrecht, The Netherlands, p 583. https://doi.org/10.1007/978-94-015-9956-6 ISBN: 1-4020-0837-6

  • Leonel RMV, Lopes S, Aversari M (2002) Distribution of wood-boring bivalves in the Mamanguape River estuary, Paraiba, Brazil. J Mar Biol Assoc UK 82:1039–1040

    Article  Google Scholar 

  • Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–326. https://doi.org/10.1046/j.1523-1739.2003.02038.x

    Article  Google Scholar 

  • Mann R, Gallager SM (1985a) Physiological and biochemical energetics of larvae of Teredo navalis L. and Bankia gouldi (Bartsch) (Bivalvia: Teredinidae). J Exp Mar Biol Ecol 85(3):211–228

    Article  CAS  Google Scholar 

  • Mann R, Gallager SM (1985b) Growth, morphometry and biochemical composition of the wood boring molluscs Teredo navalis L., Bankia gouldi (Bartsch), and Nototeredo knoxi (Bartsch) (Bivalvia: Teredinidae). J Exp Mar Biol Ecol 85(3):229–251

    Article  CAS  Google Scholar 

  • Mann R, Wolf CC (1983) Swimming behaviour of larvae of the ocean quahog Arctica islandica in response to pressure and temperature. Mar Ecol Prog Ser 13:211–218

    Article  Google Scholar 

  • Marcello A (1962) Lacuna floristica del Veneziano e sue condizioni bioclimatiche. Memorie di Biogeografia Adriatica 5:53–118

    Google Scholar 

  • Marchini A, Ferrario J, Sfriso A, Occhipinti-Ambrogi A (2015) Current status and trends of biological invasions in the Lagoon of Venice, a hotspot of marine NIS introductions in the Mediterranean Sea. Biological invasions 17(10):2943–2962

    Article  Google Scholar 

  • MCZBASE (2019) The Database of the Zoological Collections of the Museum of Comparative Zoology - Harvard University, https://mczbase.mcz.harvard.edu/ accessed on September 25th, 2019

  • Meyer HA, Möbius K (1865) Fauna der Kieler Bucht, Bd. I: Die Hinterkiemer Oder Opisthobranchia. Verlag Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Meyerson LA, Mooney HA (2007) Invasive Alien Species in an Era of Globalization. Front Ecol Environ 5(4):199–208. https://doi.org/10.1890/1540-9295(2007)5[199:IASIAE]2.0.CO;2

  • Miller RC (1924a) The boring habits of the shipworm. Sci Monthly 19(4):434–440

    Google Scholar 

  • Miller RC (1924b) The boring mechanism of Teredo. Univ Calif Publ Zool 26(4):41–80

    Google Scholar 

  • Molinaroli E, Guerzoni S, Sarretta A, Masiol M, Pistolato M (2009) Thirty-year changes (1970 to 2000) in bathymetry and sediment texture recorded in the Lagoon of Venice sub-basins, Italy. Mar Geol 258(1–4):115–125

    Article  Google Scholar 

  • Munari L (1974) Contributo alla conoscenza dei teredinidae nel mediterraneo. Conchiglie I Milano 10(34):71–84

    Google Scholar 

  • Munari L (1978) Appunti critici sui pholadacea del Mediterraneo (Mollusca, Bivalvia). Soc Ven Sc Nat - Lavori 3:8–18

    Google Scholar 

  • Navarrete M-F de (1807) Lettera di Cristoforo Colombo Vicerè ed Ammiraglio delle Indie Diretta ai Sovrani di spagna, Nostri Signori Cristianissimi e potentissimi, In: Marmocchi FC (1841) Raccolta di Viaggi dalla scoperta del nuovo continente a Dì Nostri. 2:107–146

  • Paalvast P, van der Velde G (2011a) Distribution, settlement, and growth of first-year individuals of the shipworm Teredo navalis L (Bivalvia: Teredinidae) in the Port of Rotterdam area, the Netherlands. Int Biodeter Biodegr 65(3):379–388. https://doi.org/10.1016/j.marpolbul.2011.05.009

    Article  CAS  Google Scholar 

  • Paalvast P, van der Velde G (2011b) New threats of an old enemy: the distribution of the shipworm Teredo navalis L. (Bivalvia: Teredinidae) related to climate change in the Port of Rotterdam area, the Netherlands. Mar Pollut Bull 62(8):1822–1829. https://doi.org/10.1016/j.marpolbul.2011.05.009

    Article  CAS  PubMed  Google Scholar 

  • Paalvast P, van der Velde G (2013) What is the main food source of the shipworm (Teredo navalis)? A stable isotope approach. J Sea Res 80:58–60. https://doi.org/10.1016/j.seares.2013.03.003

    Article  Google Scholar 

  • Pallary P (1911) Catalogue des Mollusques du littoral méditerranéen de 1’Egypte, vol 7. Memoires de l'Institut Egyptien, p 207

  • Pascual M, Rives B, Schunter C, Macpherson E (2017) Impact of life history traits on gene flow: a multispecies systematic review across oceanographic barriers in the Mediterranean Sea. PLoS ONE 12(5):e017641. https://doi.org/10.1371/journal.pone.0176419

    Article  CAS  Google Scholar 

  • Phillips WD, Phillips CR (1993) The Worlds of Christopher Columbus. Camb U Pr. p 340

  • Pigafetta A (1524) The First voyage round the world, by Magellan by Pigafetta Antonio, ca. 1480/91-ca. 1534. Primo viaggio intorno al globo terraqueo. English; Stanley, Henry Edward John Stanley, Baron, pp 1827–1903

    Google Scholar 

  • Por FD (1978) Lessepsian Migration – the influx of Red Sea Biota into the Mediterranean by way of the Suez Canal Ecol Stud. vol. 23, Springer, p 228

  • Por FD (1990) Lessepsian migration. An appraisal and new data. Bull Inst Oceanogr Monaco no special 7:1–10

    Google Scholar 

  • Quatrefages De JLA (1849) Mémoire sur le genre Taret (Teredo Linn). Ann Sci Nat Zool, Sér 3, 11:19–73, pl. 1–2

  • R Development Core Team (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://nam02.safelinks.protection.outlook.com/?url=http%3A%2F%2Fwww.r-project.org%2F&data=04%7C01%7Ckeppele%40si.edu%7C35c0c329c18c48c2a40308d8c95ab3f0%7C989b5e2a14e44efe93b78cdd5fc5d11c%7C0%7C0%7C637480738706983921%7CUnknown%7CTWFpbGZsb3d8eyJWIjoiMC4wLjAwMDAiLCJQIjoiV2luMzIiLCJBTiI6Ik1haWwiLCJXVCI6Mn0%3D%7C1000&sdata=Lh7k1WdrRsruh8HX6fiNr1eRokBeVk5f%2BKXwZUE4V8c%3D&reserved=0

  • Rancurel P (1954) Teredo elongata Quatrefages: redescription du type des collections du Muséum d’Histoire Naturelle de Paris. Bulletin de l’IFAN. Série A: Sci Naturelles 16(2):455–465. http://www.documentation.ird.fr/hor/fdi:010008978

    Google Scholar 

  • Rayes CA, Beattie J, Duggan IC (2015) Boring through history: an environmental history of the extent, impact and management of marine woodborers in a global and local context, 500 BCE to 1930s CE. Environ Hist 21(4):477–512. https://doi.org/10.3197/096734015X14414683716163

    Article  Google Scholar 

  • Redmount CA (1995) The Wadi Tumilat and the ‘Canal of the Pharaohs’. J Near Eastern Stud 54:127–135. http://www.jstor.com/stable/545471

    Article  Google Scholar 

  • Rilov G, Galil B (2009) Marine Bioinvasions in the Mediterranean Sea – History, Distribution and Ecology. In Rilov G, Crooks JA (Eds) Biological Invasions in Marine Ecosystems– Berlin, Heidelberg: 549–575. https://doi.org/10.1007/978-3-540-79236-9_31

  • Roch F (1957a) Zur Ökologie der Terediniden, holzbohrenden Crustaceen und Balaniden in der Lagune von Venedig. (Vorläufige Mitteilung.) Anz math-nat Kl Öst Akad Wiss. pp 223–227

  • Roch F (1957b) Le Teredinidi della Laguna Veneta e dipendenza dalle condizioni idrografiche locali per quanto riguarda la loro distribuzione geografica. Boll Mus Civ St Nat Venezia 10:87–111

    Google Scholar 

  • Roch F (1940) Die Terediniden des Mittelmeeres. Thalassia 4(3):147, 8 tavv

    Google Scholar 

  • Roch F, Moll F (1935) Über einige neue Teredinidenarten. Sitzber Akad Wiss Wien Math-Naturwiss Kl Biol Mineral Erdk Abt 1 144(5–6):263–279. https://www.zobodat.at/pdf/SBAWW_144_0263-0279.pdf

  • Roch F, Santhakumaran LN (1967) Notes on the Teredinidae from the Lagoon of Venice (Italy). Boll Pesca Piscic Idrobiol Roma 22(1):37–48

    Google Scholar 

  • Romano C, Voight JR, Pérez-Portela R, Martin D (2014) Morphological and genetic diversity of the wood-boring xylophaga (Mollusca, Bivalvia): new species and records from deep-sea Iberian Canyons. PLoS ONE 9(7):e102887. https://doi.org/10.1371/journal.pone.0102887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabelli B, Giannuzzi-Savelli R, Bedulli D (1990) Catalogo annotato dei molluschi marini del Mediterraneo. Bologna. Libreria Naturalistica Bolognese, p 348

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seebens H, Gastner M, Blasius B (2013) The risk of marine bioinvasion caused by global shipping. Ecol Lett 16(6):782–790. https://doi.org/10.1111/ele.12111

    Article  CAS  PubMed  Google Scholar 

  • Sellius G (1733) Historia naturalis teredinis seu xylophagi marini, tubulo-conchoidis speciatim belgici: cum tabulis ad vivum coloratis. Apud Hermannum Besseling: Trajecti ad Rhenum (Utrecht) Netherlands 30(11):1–353, 4 pl

    Google Scholar 

  • Sfriso A, Buosi A, Mistri M, Munari C, Franzoi P, Sfriso AA (2019) Long-term changes of the trophic status in transitional ecosystems of the northern Adriatic Sea, key parameters and future expectations: the lagoon of Venice as a study case. Nat Conserv 34:193–215. https://doi.org/10.3897/natureconservation.34.30473

    Article  Google Scholar 

  • Shefer S, Abelson A, Mokady O, Geffen E (2004) Red to Mediterranean Sea bioinvasion: natural drift through the Suez Canal, or anthropogenic transport? Mol Ecol 13(8):2333–2343. https://doi.org/10.1111/j.1365-294X.2004.02227.x

    Article  CAS  PubMed  Google Scholar 

  • Shipway RJ, Borges LMS, Müller J, Cragg SM (2014) The broadcast spawning Caribbean shipworm, Teredothyra dominicensis (Bivalvia, Teredinidae), has invaded and become established in the eastern Mediterranean Sea. Biol Invasions 16:2037. https://doi.org/10.1007/s10530-014-0646-9

    Article  Google Scholar 

  • Solidoro C, Bandelj V, Bernardi Aubry F, Camatti E, Ciavatta S, Cossarini G, Facca C, Franzoi P, Libralato S, Melaku Canu D, Pastres R, Pranovi F, Raicevich S, Socal G, Sfriso A, Sigovini M, Tagliapietra D, Torricelli P (2010) Response of Venice Lagoon ecosystem to natural and anthropogenic pressures over the last 50 years (ch 19) In: Kennish MJ, Paerl HW (eds.). Coastal Lagoons. Critical Habitats of Environmental Change, CRC Press: 483–511

  • Tagliapietra D, Aloui-Bejaoui N, Bellafiore D, De Wit R, Ferrarin C, Gamito S, Lasserre P, Magni P, Mistri M, Pérez-Ruzafa A, Pranovi F, Reizopoulou S, Rilov G, Solidoro C, Tunberg B, Valiela I, Viaroli P (2011) The Ecological Implications of Climate Change on the Lagoon of Venice, Unesco Report n. 2 Scientific Workshop 26–27 May 2011, UNESCO Venice Office, Venice, Italy, p 45 http://www.unesco.org/new/fileadmin/MULTIMEDIA/FIELD/Venice/pdf/report%202 %20final.pdf

  • Tagliapietra D, Sigovini M, Keppel E, Guarneri I, Palanti S, Veronese N, Abbate A (2019) Bioerosion effects of Sea Level Rise on the Doge’s Palace water doors in Venice (Italy). Facies 65:34. https://doi.org/10.1007/s10347-019-0577-0

    Article  Google Scholar 

  • Tagliapietra D, Volpi Ghirardini A (2006) Notes on coastal lagoon typology in the light of the EU Water Framework Directive: Italy as a case study. Aquat Conserv 16:457–467. https://onlinelibrary.wiley.com/doi/abs/10.1002/aqc.768

  • Tanhua T, Hainbucher D, Schroeder K, Cardin V, Álvarez M, Civitarese G (2013) The Mediterranean Sea system: a review and an introduction to the special issue. Ocean Sci 9:789–803. https://doi.org/10.5194/os-9-789-2013

    Article  Google Scholar 

  • Thiel M, Gutow L (2005) The ecology of rafting in the marine environment. I. The floating substrata. Oceanogr Mar Biol 42:181–264. https://doi.org/10.1201/9780203507810.ch6

    Article  Google Scholar 

  • Tiller L, Bavay A (1905) Les mollusques testacés du Canal de Suez. B Soc Zool Fr 30:170–181

    Google Scholar 

  • Toth GB, Larsson AI, Jonsson PR, Appelqvist C (2015) Natural populations of shipworm larvae are attracted to wood by waterborne chemical cues. PloS ONE 10(5):e0124950. https://doi.org/10.1371/journal.pone.0124950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treneman NC, Carlton JT, Borges LMS, Shipway JR, Raupach MJ, Altermark B (2018) Species diversity and abundance of shipworms (Mollusca: Bivalvia: Teredinidae) in woody marine debris generated by the Great East Japan Earthquake and Tsunami of 2011. Aquat Invasions 13:87–100. https://doi.org/10.3391/ai.2018.13.1.07

    Article  Google Scholar 

  • Tryon GW (1862) Monograph of the family Teredidae. Proc Acad Nat Sci Philadelphia 14:453–482

    Google Scholar 

  • Turbelin AJ, Malamud BD, Francis RA (2017) Mapping the global state of invasive alien species: patterns of invasion and policy responses. Global Ecol Biogeogr 26(1):78–92. https://doi.org/10.1111/geb.12517

    Article  Google Scholar 

  • Turner RD (1966) A survey and illustrated catalogue of the Teredinidae (Mollusca: Bivalvia) The Museum of Comparative Biology Harvard University: Cambridge, MA. p 265

  • Turner RD (1973) First report on marine borers in Oyster Creek, Waretown, New Jersey. Museum of Comparative Zoology, Harvard University. p 30

  • Turner RD, Johnson AC (1971) Biology of marine wood boring molluscs. In: Jones EBG, Eltringham SK (eds) Marine borers, fungi and fouling organisms of wood. Organization for Economic Co-operation and Development, Paris, pp 259–301

    Google Scholar 

  • Urso T, Crivellaro A (2008) Relazione tecnica relativa alle indagini sulla qualità e il degrado del legno di palificazioni per ormeggi nella Laguna di Venezia, Dipartimento Territorio e Sistemi Agro Forestali Università di Padova, Legnaro (PD), Maggio 2008, p 17

  • United States Nuclear Regulatory Commission (1984) Final environmental statement Related to the operation of Millstone Nuclear Power Station Unit 3, Northeast Nuclear Energy Company, Docket No. 50–423, p 67

  • Vallisneri A (1733) Osservazioni utilissime intorno alle Brume delle Navi. Op Fis Med Venezia 2:53–57

    Google Scholar 

  • Velásquez M, López IM (2015) First record of Spathoteredo spatha (Mollusca: Teredinidae) in Venezuela. Rev Mex Biodivers 86(1):262–264. https://doi.org/10.7550/rmb.46308

    Article  Google Scholar 

  • Wolff WJ (2005) Non-indigenous marine and estuarine species in the Netherlands. Zool Med Leiden 79(1):3–116

    Google Scholar 

  • Zambianchi E, Trani M, Falco P (2017) Lagrangian transport of marine litter in the Mediterranean Sea. Front Environ Sci 5:5. https://doi.org/10.3389/fenvs.2017.00005

    Article  Google Scholar 

  • Zenetos Α, Gofas S, Morri C, Rosso A, Violanti D, Raso JE 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. https://doi.org/10.12681/mms.327

    Article  Google Scholar 

Download references

Acknowledgments

Many thanks are due to the editor James T. Carlton (Williams College, MA USA) for his careful, accurate and punctual revision of historical sources, his highly appreciated scientific suggestions and stylistic notes. We are grateful to the reviewers, Nancy C. Treneman, (Oregon Institute of Marine Biology, USA), and a second anonymous colleague, for their careful reading of our manuscript and their valuable comments and suggestions. Thanks to Dr. Luca Perale for performing radiographs at his Vet Lab in Venice and to Mr Loris Dametto (CNR-ISMAR) for its technical help in fieldwork. We thank the Venice Water Authority (Provveditorato Interregionale per le Opere Pubbliche per il Veneto, Trentino Alto Adige e Friuli Venezia Giulia, former Magistrato alle Acque) which kindly provided the SAMANET hydroclimatic data. Thanks are due to Dr. Patrizio Terlicher, Mr. Ferro and to the staff of the Territorial Office for Biodiversity of the State Forestry Corps, Tarvisio (UD, Italy), for the courtesy with which they provided us with the test panels. We thank Dr. Reuben Shipway (University of Portsmouth, UK) who confirmed our taxonomic identifications by DNAbarcoding. Finally, we thank the Italian network Long-Term-Ecological-Research, of which the Venice lagoon is a macrosite (LTEREUIT016) for useful suggestions in the discussion of data.

Funding

This research has been supported by the Italian Flagship Project RITMARE (Ricerca ITaliana per il MARE- The Italian Research for the Sea), coordinated by the Italian National Research Council and funded by the Italian Ministry of Education, University and Research.

Author information

Authors and Affiliations

Authors

Contributions

DT has performed the field and laboratory work, has analysed the data and written the first draft of the manuscript and edited the final version. IG has contributed to field and laboratory work, analysed the data, helped producing the figures, manipulates the images and has edited the manuscript. EK has contributed to field, laboratory work, and has edited the manuscript. MS has contributed to field and laboratory work and helped producing the figures. All authors have been involved in project development and have approved the final manuscript.

Corresponding author

Correspondence to Irene Guarneri.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tagliapietra, D., Guarneri, I., Keppel, E. et al. After a century in the Mediterranean, the warm-water shipworm Teredo bartschi invades the Lagoon of Venice (Italy), overwintering a few degrees above zero. Biol Invasions 23, 1595–1618 (2021). https://doi.org/10.1007/s10530-021-02461-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-021-02461-3

Keywords

Navigation