Abstract
The present study describes a new species of spionid polychaete, Streblospio eridani n. sp., from the Italian coasts of the Northern Adriatic Sea (Mediterranean Sea). This new spionid species was recorded from shallow lagoon and marine habitats: the soft bottoms of the Sacca di Goro (Po River Delta), on October 2017, and the Lido di Dante (Emilia Romagna), between 2016 and 2017. The re-assessment of spionid specimens from other lagoon systems (the Valli di Comacchio and the Valle di Gorino) led us to recognize the presence of this species in the northern Adriatic Sea since 2009. Streblospio eridani n. sp. had low occurrence and density at the marine site Lido di Dante and at the lagoon sites Valli di Comacchio and Valle di Gorino; whereas it reached the highest density of 21,213.3 ind. m-2 at the Sacca di Goro. Morphologically this new species is characterized by dorsal (occipital) papilla on the first chaetiger, sabre chaetae and hooded hooks first appearing on chaetigers 7, hooks with 4-5 pairs of small secondary teeth, pygidium with ventral lappets, and brooding branchiate structures between chaetigers 13 and 28. In the phylogenetic reconstruction, based on the mitochondrial cytochrome c oxidase subunit I (COI) gene, the Adriatic taxon results clearly indicate that this is distinct from the other species of the genus and formed a well-supported clade with other Streblospio sp. specimens from India. Nucleotide divergences calculated between the Adriatic specimens and the other Streblospio species are higher than the intraspecific range reported for the genus and support the description of a new species. Morphological characters important for differentiation of the new species herein described from congeneric species are discussed and an updated key for Streblospio species is provided.
References
Bevilacqua, S., Mistri, M., Terlizzi, A. & Munari, C. (2018) Assessing the effectiveness of surrogates for species over time: Evidence from decadal monitoring of a Mediterranean transitional water ecosystem. Marine Pollution Bulletin, 131, 507–514.
https://doi.org/10.1016/j.marpolbul.2018.04.047
Bianchi, C.N. & Morri, C. (2000) Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Marine Pollution Bulletin, 40 (5), 367–376.
https://doi.org/10.1016/S0025-326X(00)00027-8
Bianchi, C.N. (2007) Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia, 580, 7–21.
https://doi.org/10.1007/978-1-4020-6156-1_1
Blake, J.A. & Kudenov, J.D. (1978) The Spionidae (Polychaeta) from Southeastern Australia and adjacent areas with a revision of the genera. Memoirs of the National Museum of Victoria, 39, 171–280.
https://doi.org/10.24199/j.mmv.1978.39.11
Boltachova, N.A., Lisitskaya, E.V. & Podzorova, D.V. (2015) The population dynamics and reproduction of Streblospio gynobranchiata (Annelida, Spionidae), an alien polychaete worm, in the Sevastopol Bay (the Black Sea). Ecologica Montenegrina, 4, 22–28.
Buchanan, F. (1890) Hekaterobranchus shrubsolii. A new genus and species of the family Spionidae. Quarterly Journal of Microscopical Science, 31, 175–200.
Carlton, J.T. (1975) Introduced intertidal invertebrates. In: Smith, R.I. & Carlton, J.T. (Eds.), Light’s Manual: Intertidal Invertebrates of the Central California Coast. University of California Press, Berkeley, pp. 17–25.
Çinar, M.E. (2013) Alien polychaete species worldwide: current status and their impacts. Journal of the Marine Biological Association of the United Kingdom, 93 (5), 1257–1278.
https://doi.org/10.1017/S0025315412001646
Çinar, M.E. & Dagli, E. (2013) Polychaetes (Annelida: Polychaeta) from the Aegean and Levantine coasts of Turkey, with descriptions of two new species. Journal of Natural History, 47, 911–947.
https://doi.org/10.1080/00222933.2012.752543
Çinar, M.E., Ergen, Z., Dagli, E. & Petersen, M.E. (2005a) Alien species of spionid polychaetes (Streblospio gynobranchiata and Polydora cornuta) in Izmir Bay, eastern Mediterranean. Journal of the Marine Biological Association of the United Kingdom, 85 (4), 821–827.
https://doi.org/10.1017/S0025315405011768
Çinar, M.E., Bilecenoğlu, M., Öztürk, B., Katağan, T. & Aysel, V. (2005b) Alien species on the coast of Turkey. Mediterranean Marine Science, 6 (2), 119–146.
https://doi.org/10.12681/mms.187
Çinar, M.E., Katağan, T., Öztürk, B., Egemen, Ö., Ergen Z., Kocatas, A., Önen, M., Kirkim, F., Bakir, K., Kurt, G., Dagli, E., Kaymakçi, A., Açik, S., Doğan, A. & Özcan, T. (2006) Temporal changes of soft-bottom zoobenthic communities in and around Alsancak Harbor (Izmir Bay, Aegean Sea), with special attention to the autecology of exotic species. Marine Ecology, 27 (3), 229–246.
https://doi.org/10.1111/j.1439-0485.2006.00102.x
Çinar, M.E., Katağan, T., Koçak, F., Öztürk, B. Ergen, Z. Kocatas, A., Önen, M., Kirkim, F., Bakir, K., Kurt, G., Dağli, E., Açik, S., Doğan, A. & Özcan, T. (2008) Faunal assemblages of the mussel Mytilus galloprovincialis in and around Alsancak Harbour (Izmir Bay, eastern Mediterranean) with special emphasis on alien species. Journal of Marine Systems, 71 (1), 1–17.
https://doi.org/10.1016/j.jmarsys.2007.05.004
Çinar, M.E., Balkis, H., Albayrak, S., Dagli, E. & Karhan, S.Ü. (2009) Distribution of polychaete species (Annelida: Polychaeta) on the polluted soft substrate of the Golden Horn Estuary (Sea of Marmara), with special emphasis on alien species. Cahiers de Biologie Marine, 50 (1), 11–17.
Çinar, M.E., Bilecenoğlu, M., Öztürk, B., Katağan, T., Yokeþ, M.B., Aysel, V., Dagli, E., Açik, S., Özcan, T. & Erdoğan, H. (2011a) An updated review of alien species on the coasts of Turkey. Mediterranean Marine Science, 12 (2), 257–315.
https://doi.org/10.12681/mms.34
Çinar, M.E., Dagli, E. & Açik, S. (2011b) Annelids (Polychaeta and Oligochaeta) from the Sea of Marmara, with descriptions of five new species. Journal of Natural History, 45 (33–34), 2105–2143.
https://doi.org/10.1080/00222933.2011.582966
Çinar, M.E., Katağan, T., Öztürk, B., Bakir, K., Dagli, E., Açik, S., Doğan, A. & Bitlis, B. (2012a) Spatio-temporal distributions of zoobenthos in soft substratum of Izmir Bay (Aegean Sea, eastern Mediterranean), with special emphasis on alien species and ecological quality status. Journal of the Marine Biological Association of the United Kingdom, 92 (7), 1457–1477.
https://doi.org/10.1017/S0025315412000264
Çinar, M.E., Katağan, T., Öztürk, B., Dagli, E., Açik, S., Bitlis, B., Bakir, K. & Doğan, A. (2012b) Spatio-temporal distributions of zoobenthos in Mersin Bay (Levantine Sea, eastern Mediterranean) and the importance of alien species in benthic communities. Marine Biology Research, 8, 954–968.
https://doi.org/10.1080/17451000.2012.706305
Çinar, M.E., Dagli, E. & Kurt Şahin, G. (2014) Checklist of Annelida from the coasts of Turkey. Turkish Journal of Zoology, 38, 734–764.
https://doi.org/10.3906/zoo-1405-72
Çinar, M.E., Dagli, E., Çağlar, S. & Albayrak, S. (2015) Polychaetes from the northern part of the Sea of Marmara with the description of a new species of Polydora (Annelida: Polychaeta: Spionidae). Mediterranean Marine Science, 16/3, 524–532.
https://doi.org/10.12681/mms.1226
Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F., Aguzzi, J., Ballesteros, E., Bianchi, C.N., Corbera, J., Dailianis, T., Danovaro, R., Estrada, M., Froglia, C., Galil, B.S., Gasol, J.M., Gertwagen, R., Gil, J., Guilhaumon, F., Kesner-Reyes, K., Kitsos, M.S., Koukouras, A., Lampadariou, N., Laxamana, E., López-Fé de la Cuadra, C.M., Lotze, H.K., Martin, D., Mouillot, D., Oro, D., Raicevich, S., Rius-Barile, J., Saiz-Salinas, J.I., San Vicente, C., Somot, S., Templado, J., Turon, X., Vafidis, D., Villanueva, R. & Voultsiadou, E. (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS One, 5 (8) e11842.
https://doi.org/10.1371/journal.pone.0011842
Dagli, E. & Çinar, M.E. (2008) Invasion of polluted soft substratum of Izmir Bay (Aegean Sea, eastern Mediterranean) by the spionid polychaete worm, Pseudopolydora paucibranchiata (Polychaeta: Spionidae). Cahiers de Biologie Marine, 49, 87–96.
Dagli, E. & Çinar, M.E. (2011) Species of the subgenus Minuspio (Polychaeta: Spionidae: Prionospio) from the southern coast of Turkey (Levantine Sea, eastern Mediterranean), with the description of two new species. Zootaxa, 3043 (1), 35–53.
https://doi.org/10.11646/zootaxa.3043.1.4
Dagli, E., Çinar, M.E. & Ergen, Z. (2011) Spionidae (Annelida: Polychaeta) from the Aegean Sea (eastern Mediterranean). Italian Journal of Zoology, 78 (Supplement), 49–64.
https://doi.org/10.1080/11250003.2011.567828
Dauer, D.M., Mahon, H.K. & Sardá, R. (2003) Functional morphology and feeding behavior of Streblospio benedicti and S. shrubsolii (Polychaeta: Spionidae). Hydrobiologia, 496, 207–213.
https://doi.org/10.1023/A:1026196831934
Delgado-Blas, V.H., Díaz-Díaz, O. & Víeitez, J.M. (2018) New species of Dispio Hartman, 1951 and Streblospio Webster, 1879 (Polychaeta, Spionidae) from the coast of the Iberian Peninsula. Zootaxa, 4410 (3), 525–538.
https://doi.org/10.11646/Zootaxa.4410.3.6
Ergen, Z., Çinar, M.E., Dağli, E. & Kurt, G. (2006) Seasonal dynamics of soft-bottom polychaetes in Izmir Bay (Aegean Sea, eastern Mediterranean). Scientia Marina, 70 (Supplement 3), 197–207.
https://doi.org/10.3989/scimar.2006.70s3197
Fauvel, P. (1927) Polychetes Sédentaires. Addenda aux Errantes, Archiannélides, Myzostomaires. Faune de France 16. Paul Lechevalier, Paris, 494 pp.
Felsenstein, J. (1985) Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution, 39, 783–791.
https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
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. Molecular Marine Biology and Biotechnology, 3 (5), 294–299.
Fonseca-Genevois, V. & Cazaux, C. (1987) Streblospio benedicti Webster, 1879 (Annélide Polychète) dans I’estuaire de la Loire: biologic et ecologie. Cahiers de Biologic Marine, 28, 231–261.
Foster, N.M. (1971) Spionidae (Polychaeta) of the Gulf of Mexico and the Caribbean Sea. Studies on the Fauna of Curasao and other Caribbean Islands, 36 (129),1–183.
Ghasemi, A.F., Jam, A., Taheri, M. & Foshtomi, M. (2014) Abundance of the alien spionid Streblospio gynobranchiata in relation to sediment composition along the southern coast of the Caspian Sea. Transylvanian Review of Systematical and Ecological Research, 16 (2), 119–126.
https://doi.org/10.1515/trser-2015-0020
Glasby, C.J., Hutchings, P.A., Fauchald, K., Rouse, G.W. & Wilson, R.S. (2000) Class Polychaeta. In: Beesley, P.L., Ross, G.J.B. & Glasby, C.J. (Eds.), Polychaetes & Allies: The Southern Synthesis. Fauna of Australia. Vol. 4°. Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula. Australian Biological Resources Study, Canberra and CSIRO Publishing, Melbourne, pp. 1–465 + 1–12.
Hartman, O. (1936) New species of Spionidae (Annelida Polychaeta) from the coast of California. University of California Publications in Zoology, 41, 45–52.
Hartman, O. (1944) Polychaetous annelids from California including the descriptions of two new genera and nine new species. Allan Hancock Pacific Expeditions, 10 (2), 239–307.
Horst, R. (1909) De anneliden der Zuiderzee. Mededeelingen betreffende de uitkomsten der Zuiderzee Expeditie, no. 5 Tijdschrift der Nederlandsche Dierkundige Vereeniging, Series 2, 11, 138–152.
Imajima, M. (1990) Spionidae (Annelida, Polychaeta) from Japan V. The genera Streblospio and Dispio. Bulletin of the National Science Museum, Series A (Zoology), 16, 155–163.
Kurt Şahin, G. & Çinar, M.E. (2012) A check-list of polychaete species (Annelida: Polychaeta) from the Black Sea. Journal of Black Sea/Mediterranean Environment, 18 (1), 10–48.
Lardicci, C., Ceccherelli, G. & Rossi, F. (1997) Streblospio shrubsolii (Polychaeta: Spionidae): temporal fluctuations in size and reproductive activity. Cahiers de Biologie Marine, 38, 207–214.
Levin, L.A. (1984) Multiple patterns of development in Streblospio benedicti Webster (Spionidae) from three coasts of North America. Biological Bulletin, Woods Hole, 166, 498–508.
https://doi.org/10.2307/1541157
Lezzi, M. (2017) Caulleriella mediterranea, a new species of polychaete (Annelida: Cirratulidae) from the central Mediterranean Sea. The European Zoological Journal, 84, 380–389.
http://doi.org/10.1080/24750263.2017.1343397
Mahon, A.R., Mahon, H.K., Dauer, DM. & Halanyc, K.M. (2009) Discrete genetic boundaries of three Streblospio (Spionidae, Annelida) species and the status of S. shrubsolii. Journal Marine Biology Research, 5 (2), 172–178.
https://doi.org/10.1080/17451000802317683
Martínez, J. & Adarraga, I. (2019) Una nueva especie del género Streblospio Webster, 1879 (Annelida, Spionidae) procedente del sureste del golfo de Vizcaya. Boletín de la Real Sociedad Española de Historia Natural, 113, 9–17.
https://doi.org/10.29077/bol/113/ce02_martinez
McCain, E.R. (2008) Poecilogony as a tool for understanding speciation: Early development of Streblospio benedicti and Streblospio gynobranchiata (Polychaeta: Spionidae). Invertebrate Reproduction & Development, 51 (2), 91–101.
https://doi.org/10.1080/07924259.2008.9652259
Meiβner, K., Bick, A., Guggohz, T. & Gotting, M. (2014) Spionidae (Polychaeta: Canalipalpata: Spionidae) from seamounts in the NE Atlantic. Zootaxa, 3786 (3), 201–245.
https://doi.org/10.11646/zootaxa.3786.3.1
Meiβner, K. & Götting, M. (2015) Spionidae (Annelida: ‘Polychaeta’: Canalipalpata) from Lizard Island, Great Barrier Reef, Australia: the genera Malacoceros, Scolelepis, Spio, Microspio, and Spiophanes. Zootaxa, 4019 (1), 378–413.
https://doi.org/10.11646/zootaxa.4019.1.15
Micheli, F., Halpern, B.S., Walbridge, S., Ciriaco, S., Ferretti, F., Fraschetti, S., Lewison, R., Nykjaer, L. & Rosenberg, A.A. (2013) Cumulative human impacts on Mediterranean and Black Sea marine ecosystems: assessing current pressures and opportunities. PLoS One, 8, e79889.
https://doi.org/10.1371/journal.pone.0079889
Mikac, B. (2015) A sea of worms: polychaete checklist of the Adriatic Sea. Zootaxa, 3943 (1), 1–172.
https://doi.org/10.11646/zootaxa.3943.1.1
Mistri, M., Borja, A., Aleffi, I.F., Lardicci, C., Tagliapietra, D. & Munari, C. (2018) Assessing the ecological status of Italian lagoons using a biomass-based index. Marine Pollution Bulletin, 126, 600–605.
https://doi.org/10.1016/j.marpolbul.2017.09.048
Munari, C. (2013) Benthic community and biological trait composition in respect to artificial coastal defence structures: A study case in the northern Adriatic Sea. Marine Environmental Research, 90, 47–54,
https://doi.org/10.1016/j.marenvres.2013.05.011
Munari, C. (2014) A new species of Cerapopsis (Amphipoda: Corophiidea: Kamakidae) from the Straits of Messina, central Mediterranean Sea. Italian Journal of Zoology, 81, 78–91.
https://doi.org/10.1080/11250003.2013.857730
Radashevsky, V.I. (2012) Spionidae (Annelida) from shallow waters around the British Islands: an identification guide for the NMBAQC Scheme with an overview of spionid morphology and biology. Zootaxa, 3152 (1), 1–35.
https://doi.org/10.11646/zootaxa.3152.1.1
Radashevsky, V.I. & Selifonova, Z.P. (2013) Records of Polydora cornuta and Streblospio gynobranchiata (Annelida, Spionidae) from the Black Sea. Mediterranean Marine Science, 14, 261–269.
https://doi.org/10.12681/mms.415
Rice, S.A. & Levin, L.A. (1998) Streblospio gynobranchiata, a new spionid polychaete species (Annelida: Polychaeta) from Florida and the Gulf of Mexico with an analysis of phylogenetic relationships within the genus Streblospio. Proceedings of the Biological Society of Washington, 111 (3), 694–707.
Rouse, G.W. & Pleijel, F. (2001) Polychaetes. Oxford University Press, Oxford, 354 pp.
Schulze, S.R., Rice, S.A., Simon, J.L. & Karl, S.A. (2000) Evolution of poecilogony and the biogeography of North American populations of the polychaete Streblospio. Evolution, 54 (4), 1247–1259.
https://doi.org/10.1111/j.0014-3820.2000.tb00558.x
Schwarz, G. (1978) Estimation the dimension of a model. Annals of Statistics, 6, 461–464.
https://doi.org/10.1214/aos/1176344136
Selifonova, Z.P. & Bartsits, L.M. (2018) First occurrence of the invasive alien species Streblospio gynobranchiata (Rice & Levin, 1998) and Polydora cornuta Bosc, 1802 (Polychaeta: Spionidae) on the coast of Abkhazia (Sukhum Bay, Black Sea). Ecologica Montenegrina, 18, 129–132.
Taheri, M. & Foshtomi, M.Y. (2011) Community structure and biodiversity of shallow water macrobenthic fauna at Noor coast, South Caspian Sea, Iran. Journal of the Marine Biological Association of the United Kingdom, 91 (3), 607–613.
https://doi.org/10.1017/S0025315410000378
Taheri, M., Seyfabadi, J., Abtahi, B. & Foshtomi, M.Y. (2009) Population changes and reproduction of an alien spionid polychaete, Streblospio gynobranchiata, in shallow waters of the south Caspian Sea. JMBA2—Biodiversity Records, 2, e40, 1–5.
https://doi.org/10.1017/S1755267208000201
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
https://doi.org/10.1093/molbev/msr121
Webster, H.E. (1879) Annelida Chaetopoda of New Jersey. Annual Report of the New York State Museum of Natural History, 32, 101–128.
Zenetos, A., Çinar, M.E., Crocetta, F., Golani, D., Rosso, A., Servello, G., Shenkar, N., Turon, X. & Verlaque, M. (2017) Uncertainties and validation of alien species catalogues: The Mediterranean as an example. Estuarine, Coastal and Shelf Science, 191, 171–187.
https://doi.org/10.1016/j.ecss.2017.03.031