A baseline study of macrofauna from the North Adriatic ......Hydroides helmata (Iroso, 1921) Hydroides pseudouncinata pseudouncinata Zibrowius, 1968 Hydroides stoichadon Zibrowius,

A baseline study of macrofauna from the North Adriatic seaports Raša, Rijeka, Bakar and Omišalj

Ana Travizi1, Andrej Jaklin1, Barbara Mikac2, Vedrana Nerlović3, Ivan Balković1

1Ruđer Bošković Institute, Center for Marine Research, Giordano Paliaga 5, Rovinj, Croatia2Vladimira Nazora 26, Pula, Croatia

3University of Split, University Department of Marine Studies, Ruđera Boškovića 37, P.P. 190, Split, Croatia

IntroductionSeaports are recipients of myriad of organic and inorganic pollutants that are directly or indirectly released into marine environment. Recently, maritimetransport and associated port activities are recognized as increasing source of environmental threats, with ballast water as one of main vectors fortransport of non-indigenous species (NIS). Kvarner Bay and the Bay of Rijeka are most heavily exploited shipping routes in Croatia and, therefeore,chosen for this study. The goal was to characterize benthic communities associated with hard- and soft-bottom habitats from the four North Adriaticseaports and to investigate the presence of non-indigenous species.

13th CROATIAN BIOLOGICAL CONGRESS with International ParticipationPoreč, 19-23 of September, 2018

Polyplacophora

Acanthochitona fascicularis (Linnaeus, 1767)Callochiton septemvalvis (Montagu, 1803)Chiton olivaceus Spengler, 1797

Gastropoda

Alvania discors (T. Allan, 1818)Bittium reticulatum (da Costa, 1778)Brachystomia eulimoides (Hanley, 1844)Crisilla depicta (Manzoni, 1868)Cylichna cylindracea (Pennant, 1777)Diodora graeca (Linnaeus, 1758)Hexaplex trunculus (Linnaeus, 1758)Mangelia tenuicosta (Brugnone, 1862)Monophorus perversus (Linnaeus, 1758)Raphitoma linearis (Montagu, 1803)Steromphala adansonii (Payraudeau, 1826)Tritia incrassata (Strøm, 1768)

Bivalvia

Abra alba (W. Wood, 1802)Anomia ephippium Linnaeus, 1758Bryopa aperta (G. B. Sowerby I, 1823)Chamelea gallina (Linnaeus, 1758)Corbula gibba (Olivi, 1792)Hiatella arctica (Linnaeus, 1767)Hiatella rugosa (Linnaeus, 1767)Lima lima (Linnaeus, 1758)Mimachlamys varia (Linnaeus, 1758)Modiolus barbatus (Linnaeus, 1758)Moerella donacina (Linnaeus, 1758)Musculus subpictus (Cantraine, 1835)Myrtea spinifera (Montagu, 1803)Mytilaster minimus (Poli, 1795)Mytilus galloprovincialis Lamarck, 1819Ostrea edulis Linnaeus, 1758Ostrea stentina Payraudeau, 1826 Papillicardium papillosum (Poli, 1791)Parvicardium pinnulatum (Conrad, 1831)Pseudochama gryphina (Lamarck, 1819)Rocellaria dubia (Pennant, 1777)Saxicavella jeffreysi Winckworth, 1930Sphenia binghami W. Turton, 1822Spisula subtruncata (da Costa, 1778)Striarca lactea (Linnaeus, 1758)

Polychaeta

Amphitritides gracilis (Grube, 1860)Arabella iricolor (Montagu, 1804)Aricidea (Aricidea) pseudoarticulata Hobson, 1972Ceratonereis (Composetia) costae (Grube, 1840)Cirriformia filigera (Delle Chiaje, 1828)Cirriformia tentaculata (Montagu, 1808)Cirrophorus furcatus (Hartman, 1957)Dipolydora flava (Claparède, 1870)Dodecaceria concharum Örsted, 1843Dorvillea rubrovittata (Grube, 1855)Eulalia viridis (Linnaeus, 1767)Eunice roussaei Quatrefages, 1866Eunice schizobranchia Claparède, 1870Eunice vittata (Delle Chiaje, 1828)Galathowenia oculata (Zachs, 1923)Haplosyllis spongicola (Grube, 1855)Harmothoe spinifera (Ehlers, 1864)Hilbigneris gracilis (Ehlers, 1868)Hydroides dianthus (Verrill, 1873)Hydroides elegans (Haswell, 1883)Hydroides helmata (Iroso, 1921)Hydroides pseudouncinata pseudouncinata Zibrowius, 1968Hydroides stoichadon Zibrowius, 1971Janua heterostropha (Montagu, 1803)Lagis koreni Malmgren, 1866Laonice cirrata (M. Sars, 1851)Leiochrides australis Augener, 1914Leodice torquata (Quatrefages, 1866)Lepidonotus clava (Montagu, 1808)Levinsenia gracilis (Tauber, 1879)Lumbrineris coccinea (Renier, 1804)Lumbrineris latreilli Audouin & Milne Edwards, 1834Lysidice collaris Grube, 1870Lysidice ninetta Audouin & H Milne Edwards, 1833Lysidice unicornis (Grube, 1840)Magelona minuta Eliason, 1962Marphysa bellii (Audouin & Milne Edwards, 1833)Melinna palmata Grube, 1870Nephtys hystricis McIntosh, 1900Nereis perivisceralis Claparède, 1868Nereis pulsatoria (Savigny, 1822)Nereis rava Ehlers, 1868Owenia fusiformis Delle Chiaje, 1844Palola siciliensis (Grube, 1840)Paradoneis lyra (Southern, 1914)Perinereis cultrifera (Grube, 1840)Phyllodoce mucosa Örsted, 1843Pileolaria berkeleyana (Rioja, 1942)Pileolaria militaris Claparède, 1870Pista cristata (Müller, 1776)Platynereis dumerilii (Audouin & Milne Edwards, 1833)Platynereis nadiae Abbiati & Castelli, 1992Polydora hoplura Claparède, 1868Polyophthalmus pictus (Dujardin, 1839)Protodorvillea kefersteini (McIntosh, 1869)Protolaeospira striata (Quievreux, 1963)Schistomeringos rudolphi (Delle Chiaje, 1828)Serpula concharum Langerhans, 1880Serpula vermicularis Linnaeus, 1767Sigambra tentaculata (Treadwell, 1941)Simplaria pseudomilitaris (Thiriot-Quievreux, 1965)Sphaerosyllis hystrix Claparède, 1863Spiochaetopterus costarum (Claparède, 1869)Spirobranchus polytrema (Philippi, 1844)Spirobranchus triqueter (Linnaeus, 1758)Sternaspis scutata (Ranzani, 1817)Syllis armillaris (O.F. Müller, 1776)Syllis corallicola Verrill, 1900Syllis ferrani Alós & San Martín, 1987Syllis garciai (Campoy, 1982)Syllis gerlachi (Hartmann-Schröder, 1960)Syllis gracilis Grube, 1840Syllis hyalina Grube, 1863Syllis krohnii Ehlers, 1864Syllis rosea (Langerhans, 1879)Syllis variegata Grube, 1860Thelepus cincinnatus (Fabricius, 1780)Timarete filigera (Delle Chiaje, 1828)Trypanosyllis zebra (Grube, 1860)Vermiliopsis infundibulum (Philippi, 1844)Vermiliopsis striaticeps (Grube, 1862)

Table 1. List of recorded species. NIS are given in red.

Material and MethodsSampling was conducted during autumn 2011 at four locations in the Kvarner Bay and Bay of Rijeka. Locations chosen forthe study were: Port of Rijeka (LRI 01, terminal Budimpeštansko), Port of Bakar (LBA 01, terminal Podbok), Omišalj terminal(LOM 01) and Raša port (LRA 01, terminal Bršica). Samples were taken by SCUBA (Figure 1). Material was scraped from hardsubstrata inside a rectangle with surface area of 0.1 m2 at depths of 3, 5 and 7 m and soft-bottom fauna was sampled with ahand corer with a surface area of 0.025 m2 at distances of 0 and 20 m from the wall/pilon. Sampling strategy andmethodology followed modified CRIM Protocol (Hewitt and Martin, 2001). Due to hard substratum, sediment wasn’t sampledat LRI 01.Samples were washed on a 1 mm mesh size sieve in the laboratory. The analysis of macrofauna was carried out using themethod of total census, applied both on higher taxa level (rank of phylum, class and/or order) and species level (only fordominant taxa: Polychaeta, Polyplacophora, Bivalvia, Gastropoda). Species of the respective higher taxa were categorizedin six functional groups regarding tolerance to pollution (Grall i Glémarec, 1977). Analysis of functional compositionfollowed by multimetric analysis (M-AMBI) is provided.

Results and ConclusionsIn total, 121 species of Polyplacophora, Gastropoda, Bivalvia and Polychaeta were recorded on all sampling sites and bothtype of substrata (Table 1). Seventeen higher macrobenthic taxa, and 97 species were identified from the hard substrata,and much less (10 higher taxa, 33 species) from the soft bottom. The results of univariate analyses suggested occurrence ofmodified and impoverished soft-bottom macrofauna and rather diverse hard bottom fauna. Multivariate analysis indicatedsignificant differences of macrofauna communities among surveyed ports. In total, six NIS were detected, all belonging toPolychaeta. Platynereis nadiae was was found in ports of Bakar, Omišalj and Rijeka. Five NIS were reported from the port ofRaša: Hydroides elegans, H. stoichadon, Leiochrides australis, Protolaeospira striata and Pileolaria berkelyana.

a

b c

Figure 1. Taking samples using SCUBA; a: scraping hard substratum using rectangle and netted bag as receptacle; b: scraped pilon surface; c: sampling soft bottom with a hand core.

Pileolaria berkelyana andPlatynereis nadiae were recordedfor the first time in the Adriatic Sea.Polychaeta and Bivalvia dominatedalmost all hard substrata samples,with relative abundance rangingfrom 9.4% (LRI 01, depth 7 m) to 62.9%(LRA 01, depth 3 m) for Polychaetaand 8.4% (LRI 01, depth 3 m) to 51.9%(LRA 01, depth 5 m) for Bivalvia(Figure 2). Polychaeta weregenerally dominant except on stationLOM 01 (Figure 3). Analyses of thezoobenthos functional compositionwere conducted based on speciescomposition and ecological

Figure 2. Relative abundance of higher invertebrate taxa on hard substrata.

Figure 3. Relative abundance of higher invertebrate taxa in soft bottom communities.

characterization of two invertebrate groups, Mollusca and Polychaeta, whichare generally considered good indicators of the ecological quality of a habitat.Hard bottom communities showed to be more diverse than expected for highimpacted environments (d=25-39, H’=3.1-4.2), with unexpectedly highabundance of sensitive (25-75%) and indifferent species (9-59%) (Table 2). Atthe same time, abundance of tolerant and opportunistic species indicatesacceptably lower ecological quality of hard bottom port habitats. Communitystructure based on functional composition of Mollusca and Polychaetasuggests good ecological quality of hard bottom port habitats, but in spite ofthat, it cannot be objectively estimated since methodology for habitatecological quality assessment lacks hard bottom zoobenthos.Compared to hard bottom communities, soft bottom fauna was much poorer atall sites (d=2-11, H’=1-3.9), with somewhat better condition at LBA 01, 20 m fromthe wall. Ecological quality of the sampling sites was estimated based on thevalues of multiparameter biotic index – M-AMBI (Muxika et al., 2007). Resultsshow that ecological quality of the soft bottom port habitats is clearlydiminished (bad or moderate) with only one exception at LBA 01, 20 m from thewall (Table 3). Poorer ecological status was determined at sampling sites 0 mfrom the wall/pilon than at a distance of 20 m at all stations. Results are inconcordance with expectations and literature data concerning port sediments(Pearson & Rosenberg, 1978; Glémarec & Hily,1981).

References• Glémarec M. i C. Hily (1981). Perturbations apportées à la macrofaune benthique de la baie de Concarneau par les

effluents urbains et portuaires. Acta Oecologica, Oecol. Applic., 2, 139-150.• Grall J. & M. Glémarec (1977). Using biotic indices to estimate macrobenthic community perturbation in the bay of

Brest. Estuarine, Coastal and Shelf Science, 44, 43-53.• Hewitt, C.L. & R.B. Martin (2001). Revised protocols for baseline port surveys for introduced marine species: survey

design, sampling protocols and specimen handling, CRIMP Technical Report Number 22, Centre for Research onIntroduced Marine Pests - CSIRO Marine Research, Hobart.

• Muxika I., Á. Borja, J. Bald (2007). Using historical data, expert judgement and multivariate analysis in assessingreference conditions and benthic ecological status, according to European Water Framework Directive. MarinePollutution Bulletin, 55, 16-29.

• Pearson T. H. i R. Rosenberg (1978). Macrobenthic succession in relation to organic enrichment and pollution of themarine environment. Oceanogr. Mar. Biol. Ann. Rev., 16, 229-311.

Table 2. Share of macrofaunal functional groups (Ecological group - EG) in regards to species sensitivity towards pollution in ports Raša (LRA 01), Rijeka (LRI 01), Bakar (LBA 01) and Omišalj (LOM 01). EG I- sensitive species, EG II- indifferent species, EG III-tolerant species, EG IV-first order opportunists, EG V –second order opportunists, NC-non-classified species, d-species richness (Margalef index), H‘-diversity (Shannon-Wiener index).

Sampling site LRA 01 LRI 01 LBA 01 LOM 01

Depth (m) 3 5 7 3 5 7 3 5 7 3 5 7

EG I (%) 35.1 74.7 43.1 25.8 80.2 60.6 40.5 51.1 46.9 47.3 39.7 58.4

EG II (%) 59.1 8.9 53.3 30.6 13.5 27.3 44.3 25.9 30.6 25.1 38.9 18.2

EG III (%) 5.4 8.9 1.2 43.2 6.3 12.1 13.8 22.2 22 27.5 20.5 23.4

EG IV (%) 0.4 7.6 2.4 0.4 0 0 1.4 0.7 0.4 0 0.9 0

EG V (%) 0 0 0 0 0 0 0 0 0 0 0 0

NC (%) 17.5 3.7 19.7 1.1 3 4.8 2.8 0 3.9 5.1 1.3 5.5

d 31 25 39 28 21 22 34 25 34 28 36 29

H' 3.6 3.8 4.5 3.7 3.1 3.7 4.3 3.7 3.8 4 4.2 4.1

Table 3. Share of macrofaunal functional groups (Ecological group - EG) in regards to species sensitivity towards pollution in ports Raša (LRA 01), Bakar (LBA 01) and Omišalj (LOM 01). EG I-sensitive species, EG II- indifferent species, EG III-tolerant species, EG IV-first order opportunists, EG V –second order opportunists, NC-non-classified species, AMBI-AZTI Marine Biotic Index, d-species richness (Margalef index), H‘-diversity (Shannon-Wiener index), M-AMBI-Multimetric AZTI Marine Biotic Index.

Sampling site LRA 01 LBA 01 LOM 01

Distance from the

wall/pilon (m) 0 20 0 20 0 20

EG I (%) 12.8 12.5 18.2 27.3 50 0

EG II (%) 2.1 25 45.5 54.5 0 50

EG III (%) 17 50 27.3 9.1 0 50

EG IV (%) 2.1 12.5 9.1 9.1 50 0

EG V (%) 66 0 0 0 0 0

NC (%) 2.1 11.1 0 15.4 0 0

AMBI 4.6 2.44 1.91 1.5 2.25 2.25

d 9 7 5 11 2 4

H' 1.85 2.64 2.12 3.39 1 1.92

M-AMBI 0.3 0.5 0.48 0.65 0.34 0.43

Ecological

condition bad moderate moderate good bad moderate