original scientific paper UDK 594.1:591.5(497.5 Li m ski k.) MACROiNVERTEBRATE FAUNA ASSOCIATED WITH NATURAL POPULATIONS OF MEDITERRANEAN MUSSEL (MYTILUS GALL OPR O VI NCI A L IS LAMARCK, 1819) IN LIM CHANNEL, ISTRA Vari j a EMRIČ B.Sc. in biology, HR-21312 Podstrana, Krizine 16 dipl. biol., HR-21312 Podstrana, Križine 16 ABSTRACT The macroinvertebrate fauna associated with Mytilus galloprovincialis Lmk. in the intertidal rocky shore in the Lim Channel, Istra is reported. Ninety two species from eleven phyla were recorded in samples taken during April ­October 1994, In terms of species richness the community was dominated by the molluscs (42 species), polychetes (21 spp.) and arthropods (12 s pp.), representing 81.4% of the total associated fauna. In terms of abundance the dominant species among the mussel shells (epibiont) was barnacle Balanus perforates Bruguiere, while small brooding bivalve Lasaea rubra Montagu dominated amongst the byssal threads. Key words: mediterranean mussel, Mytilus galloprovincialis, macrofauna, epibionts, infauna, community structure Kijučne besede; užitna klapavica, Mytilus galloprovincialis, makrofavna, epibionti, infavna, sestava združbe INTRODUCTIO N Mediterranean mussel (Mytilus galloprovincialis) often occupies lower intertidal and infralitoral fringe of rocky shore, especially on moderately wave-exposed sites and areas with slightly lower salinity and abun­dance of suspended organic matter, that is: eutrophized water and even heavilly polluted harbours (Bellan-San­tini, 1969). Mussels attach firmly to the substrate by means of byssal threads and form high density assem­blages {Okamura, 1986; Lintas & Seed, 1994). Within interstices of mussel clump (matrix), the accumulated sediment, mussel faeces and pseudofaeces, living and dead mussel shells create "infralitoral micro-niches" that offer certain degree of protection from wave-action and higher humidity to infralitoral organisms with restricted tolerances (Bellan-Santini, 1969; Suchanek, 1985). So, mussel clumps develop into structurally complex enti­ties which provide refuge and habitat for wide variety of associated organisms (Ong-Che & Morton, 1994). But, for a number of sedentary and hemi-sesile organisms (e.g. barnacles, limpets) from intertidal and infralitoral fringe, the mussel shells represent only "secondary space'1 (Dayton, 1971) for settlement due to intensive competition for available space. Previous research in the Lim Channel documented midlitoral and upper infralitoral rocky shore commu­nities (Poropat, 1979), natural populations of bivalves, including mussels (Zahtila, 1987) and study on bio­fouling on the shells of living mussels (Igič, 1975). STUDIED AREA Lim Channel is a long bay (11 km), morphologically similar to a fjord. It is situated on the west coast of the I stri an Peninsula, between Rovinj and Poreč, extending from east to west. Minimal sea water temperature (March) is about 10°C and maximum (August) some 24°C. During autumn and winter heavy rains wash the ground from the coast into the sea. Suspended mud particles cause decrease in water transparency, but this also represents abundant input of organic matter. At the head of the Channel several permanent fresh-water springs cause periodica! decrease in surface salinity (correlated with tidal rhythm) which influence midlitoral communities (Marinkovič-Roje, 1958). Van) a EMRlt : MACR O INVERTEBRAT E FAUN A ASSOCIATE D WIT H NATURA L POPULATION S O F MEDITERRANEA N MUSSEL ... 67-72 MATERIALS AN D METHODS In the Lim Channel mussels form almost intermittent bell in the intertida! zone (average height 0.4 m) and infralitoral fringe. Samples were collected during April ­October 1994 at 14 stations (Fig, 1). The sampling unit was a 25x25 cm square with the most homogenous mussel cover of the substrate. The entire square was covered with nylon bag to prevent mobile forms escaping and infaunal organisms washed off through wave-action and then carefully scraped from substrate by a blunt knife (Bellan-Santini, 1969). Samples were preserved in 4% neutral formalin. Some organisms were Fig. 1: Study area (top) and sampling stations in the Lim Channel (below). Slika /: Zemljevid obravnavanega območja (zgoraj) in vzorčevalne postaje v Limskem kanalu (spodaj). identified only to higher taxonomic categories (e.g. class, phyla) and treated as single entitles. RESULTS AN D DISCUSSIO N In samples taken in April and October 1994, a total of 91 species from 11 phyla were recorded (Table 1). The most abundant phyla in terms of species richness were the molluscs (41 species), Annelida (21 spp.) and arthropods (12 spp.) Phyla April October Total Pori fera 2 2 2 Cnidarla 2 1 2 Platyhelminîhes 1 1 1 Sipuncula 1 2 2 Nemertina 1 1 Mollusca 38 33 41 Annelida 18 20 21 Aithropoda 10 9 12 Bryozoa 1 1 1 Echinodermata 4 4 4 Tunicata 1 3 4 Total 79 77 91 Table 1 ; Faunal composition of the associated fauna. Tabela 1: FavnistiCna sestava zdrutbe. The biota associated with mussels (Fig. 2) can be generally divided into three functional groups (according to Suchanek, 1985): epibionts - organisms which grow on mussel shells themselves, e.g. barnacles (Balanus spp., Chthamalus stellatus}, ascidians, bryozoans, oysters (Ostrea edulis) mobile fauna - move freely throughout the matrix and are represented by small crustaceans and free-roving gastropods (juvenile Gibhula spp., Monodonta spp., Alvania cimex, Odostomia scalaris) infaunai taxa - typically restricted to, and often dependent upon the organic rich sediment and comprise organisms that are more typical of soft sediment environment e.g. polychetes (Cirriformia tenlaculata), small ophitirids (Ampbipbolis squamata), sipunculans (Aspidosiphon kovalevskii). Ong-Che & Morton (1992) add the fourth category ­small bivaives in the mass of mussel byssal threads (Lasaea rubra, Musculus costulatus, Cardita calyculata, Hi at el la arctica). Vanja SMRiČ: M AC ROI N V E RTE8 R ATE FAUNA ASSOCIATED WITH NATURAL POPULATIONS OF MEDITERRANEAN MUSSEL .... 67-7 PORiFERA Cliona celata Grant, 1826 Cliona viridis Schmidt, 1898 CNiDARIA Actinia equina (Linnaeus, 1 766} Balanophyllia europaea (Risso, 1826} PLATYHELMiNTHES Turbellaria indet. SIPUNCUIA Aspidosiphon kovaievskii (Murina, 1964} Phaxolosoma granulaium (l.euckart, 1828) NEMERTINA Nemertina indet, MOLLUSC A Acanthochitona communis (Risso, 1826) Acanthochitona fascicularis (Linnaeus, 1767) Lepidochitona corrugata (Reeve, 1848) Alvania cimex Linnaeus, 1758 Alvania discors (Alfan, 1818) Bittium reticulatum (Da Costa, 1778) Diodora italica (De f ranee, 1820} Eatonina cossurae (CaScara, 1841) Cibbula divaricate {Linnaeus, 1753} Cibbula racketli{Payraucleau, 1826) Cibbula rarilineata (Michaud, 1829) Cibbula varia (Linnaeus, 1758) Hexaphx truriculus (Linnaeus, 1758) LHtorina neriloides (Linnaeus, 1758} Monotonia articulat.3 Lamarck, 1822 Monodonta mutabilis {Philippi, 1846) Monodonta turbinata (Bom, 1778) Nassarius incrassaius (Strom, 1768) Odostomia scalaris MacCillivray, 1843 Ovatella myosotis (Draparnaud, 1801} Patella caerulea s. iat. Runcina sp, 1 cf. adriatica (Thompson, 1981) Runcina sp. 2 Verrnems triqueier Bivona, 1832 Anomla ephippium (Linnaeus, 1758) Area noae Linnaeus, 1758 Cardita calyculata (Linnaeus, 1758) Chaina gryphopides Linnaeus, 1758 Gaitrocbaena dubia (Pennant, 1777} Hiatella arclica (Linnaeus, 1767) Hiaiella rugosa {Pennant, 5 767) Ims !run (Linnaeus, 1758} tasaea rubra (Montagu, 1808} Modiolus barbatus (Linnaeus, 1758) Musculus coslulaius (Risso, 1826) Mytilaster minimus (Poli, 1 795) Oslrea edulis Linnaeus, 1758 Ostreola parenzani Seltepasi, 1978 Pelricola subslrialula (Montagu, 1808) Petri co I a sp. Ruditapes decussatus (Linnaeus, 1758} ANNELIDA Amphitrides gracilis (Grube, 1860) Ceralonereis coslae(Grube, 1860} Cirriiormia tenlaculata (Montagu, 1 865) Fabricia sabella adriatica Banse, 1956 Lepklonotus clava (Montagu, 1808) Luirtbririeris furichalensis (Kinberg, ] 865} Lumbrineris impatiens (Claparede, 1868) Lysidice ninetla Audouin & Milne-Ed wards, 1833 Nereis zonata Mahngren, I 867 Nereis sp. Notophyllum foliosiim (Sars, 1835) Mystides limbata Saint-joseph, 1888 Perinereh cultrifera (Grube, 1840} Phyflodoce maculata (Linnaeus, 1767) Serpula sp. Spirorbis sp. Syllis gracilis Grube, f 840 Terebetla lapidaria Linnaeus, 1767 Typosyllii krobnil(Ehters, 1864) Vermiliopsis infundibulum (Phiiippi, 1844) ARTHROPODA Balanus arnphilrile Darwin, 1854 Balanus eburneus Gould, 1841 Balanus perforatum Bruguiere, 1 789 Balanus trigonus Darwin, 1854 Chthamalus stellatus (Poli, 1791) Fachygrapsus inarmoratus {Fabricius, 1787) Pinnotheres pinnotheres (Linnaeus, 1 758) Pinnotheres pisum (Linnaeus, 1 767} Porceliana plalhycheies (Pennant, 1777) Ligia itaiica Fabricius, 1837 Ainphipoda indet. Isopoda indet. BRVOZOA Bryozoa indet. ECHINODERMATA Coscinasterias tenuispina (Lamarck, 1816} AmphiphoUs squamata (Delie Chiaje, 1828} Opbiotbrix fragilis {Abifdgaard, 1789) Paracentrotus lividus (Lamarck, 1816) TUNICATA Botryllus schlosseri Palias, 1 774 Styela plicata (leseueur, 1823} Tunicata indet. 1 Tunicata indet. 2 Table 2: List of species recorded from the /VI. gal­loprovincialis community in the Lim Channel in April and October 1994. Tabela 2: Seznam vrst, ugotovljenih v združbi z M. gal­loprovincialis v Limskem kanalu aprila in oktobra 1994. Before any further analysis it should be underlined that a number of species reported in Table 2 normally occupy the supraiitoral, midlitoral and/or infralitoral fringe, e.g. crustaceans Ligia itaiica and Pachygrapsus marmoratus and gastropods Patella spp. and that they are not dependent upon mussel community, However, juvenile specimens of topshells (Monodonta spp,, Gibbula spp.}, limpets (Patella spp.) and also sea-anemones (Actinia equina) may find protection from desiccation and overheating within mussel clumps (Poropat, 1979; pers. observ,), Vanja EMRi ô MACR O SNVffiT Et! RATE FAUN A ASSOCIATE D WiT H NATURA L POPULATION S O F MEDITERRANEA N MUSSEL ..., b7-?2 Figure 2; Structure of the mussel community. Slika 2: Sestava združbe z užitno klapavico. Some species which occurred only once or were represented only by a few specimens can be regarded as accidental or transient members of the mussel community. According to Zavodnik (1970), the so-called "strange elements" can enter the community passively carried by currents and waves during larva! stage and actively searching for food or adequate reproduction ground. In our research a few specimens of Ruditapes decussatus were found buried in mud and shell debris trapped by byssal threads, it is obvious that the larva somehow managed to survive in this habitat, rocky intertidal transformed through development of the mussel bed. On the other hand, reported whelk Hexaplex trunculus and sea-star Coscinasterias tenuispina prey on mussels and during high tide thus deliberately move along the mussel bed. Rare pea-crabs Pinnotheres pinnotheres and P. pisum are comensal species, and normally live inside alive mussels (Seed, 1971) and their occurrence, although rare, is thus not unexpected. Epibionts - Barnacles (Balanus spp., Ch. stellatus), oysters (O. edulis) and polychetes with calcareous tube (Spirorbis sp.) settle on the mussel shells and thus colonize available "secondary space" {Dayton, 1971). Some species demonstrate gregariousness by settling closely to or directly on adults of same and/or related species. This is characteristic of barnacles and oysters (IgiC, 1975). Epibiotic complex on mussels was dominated (in terms of numbers) by B. perforatus, especially in October, due to intensive reproduction and settling at higher temperatures. This cirriped formed colonies numbered as many as 40-60 individuals. B. eburneus was only sporadically observed in October, because it reproduces only in summer ([gič, 1975). Despite their dense settlement, most juvenile barnacles (base diameter to 2 mm) were dead, IgiC (1975) also reported high mortality, up to 85% during the first month, it should be mentioned that the reported barnacle species (with the exception of Ch. stellatus) are usually not intertidal, though Barnes & Crisp (1956) reported intertidal B. pertoratus (England), attached directly to primary substrate, rarely on mussels. Fast-growing epibionts, e.g. ascidian Botryllus schlosseri, can within month completely overgrow the host-shell and impede the opening of valves, thus causing death of mussel or oyster (Igtd, 1975), As far as our research of the mussel bed is concerned, the accidental ascidians succumbed to desiccation due to the periodic emersion of the infralitoral fringe, Mobile fauna - Small gastropods find protection from external perturbations and infralitoral micro-habitat within mussel matrix. According to jaklin (1988), the forementioned species (Table 2) e.g. Bittium reticulatum, Alvania cimex, carnivorous Nassarius (-Hinia) incras­sata, are typical representatives of the soft-bottom infralitoral belt, Small crustaceans (amphipods, isopocls) were numerous in mussel community at the mouth of the channel, exposed to waves. Infaunai iaxa - In the bottom layer of the accumulated sediment several species of polychetes were quite frequent if not numerous, e.g. Perinereies cultrifera, Syllis gracilis. Nereis zonata, Cirriforrnia tenlaculata. Befian-Santini (1969) also reported fore-mentioned species in intertidal populations of M. gallo­provincialis in the harbour of Marseille. Giangrande (1988) reported S. gracilis, N. zonata and Ceratonereis costae just below the sea surface under the cover of photophilic alga. Tsuchiya & Nishihira (1986) pointed that the occurrence and the numbers of C. tentaculata, a detriiofagous, infralitoral species, increase with the accumulation of sediment and organic debris, Bivalves within mussel byssal threads - large M. galfoprovincialis (30-60 mm) completely covered the substrate and dominated the community in terms of biomass. It should be mentioned, however, that smaller mytilid species Mytifaster minimus (10-15 mm) outnum­bered mussel several times and in most mussel beds Mytiiaster formed dense and thick bottom layer. Vanja EMRlC; MACROINVERTEBRAT E FAUN A ASSOCIATE D WITI-NATURA L POPULATION S O f MEDITERRANEA N MUSSEL ..., G7-72 Figure 3: Intertidal community at the head of the Urn Channel. SUka 3: Združba v bibavičnem pasu ob vhodu v Umski kanal, 1- Ostreola parenzani, 2- Mytilus galioprovincialis, 3­Ulva rigida, 4-Valonia u tri cul a ris, 5- Enteromorpha intestinal is, 6- Catenelia opuntia, 7- Littorina neritoides, 8- Ligia italica, 9- Monodonta turbinata, 10- Patella caerulea, 11- Bal anus perforatus, 12- 8. trigonus, 13­Cbtbamalus stellatus, 14- Mytilaster minimus desiccation, that is - survival in the intertidal fringe (Okamura, 1986). Apart from M. minimus, the most abundant member of the associated fauna was the small (up to 3-4 mm) bivalve Lasaea rubra Montagu, accounting from 18 to 80% of total number of specimens. Although brooding L. rubra is well adapted to intertidal life, it needs certain protection from desiccation. Its presence within mussel clumps has been previously reported (Bouchet, 1961; Bellan-Santini, 1969; Lintas & Seed, 1994). Poropat (1979) reported L. rubra as a regular intertidal inhabitant in the Lim Channel, often among mussels. During our research somewhat uneven and patchy distribution of L. rubra was reported, from a few specimens to a few hundreds of specimens per sample unit, This is explained by brooding, viviparous reproduction: adult releases several already formed though smaller young directly into established population and they attach themselves within the "family" group (Morton et al., 1957). At the head of the Lim Channel fresh-water springs cause periodical decrease of surface salinity and fine mud particles settle on the rocks. Figure 3 shows detail of intertidal community with a few mussels and oysters. Tender thalii of Ulvales (Ulva rigida, Valonia utricularis, Enteromorpha intestinalis) also indicate lower salinity (Munda, 1977), ACKNOWLEDGEMENTS Mytilaster (=Brachidontes) minimus usually occupies rocky intertidal belt, preferably on wave-exposed shores, and forms autonomous beds (Boucbet, 1961). Bellan-Santini (1969) reported, however, that in calm bays and harbours (slightly polluted ones) Mytilaster finds protection from desiccation within clumps of larger M. galioprovincialis. In the Lim Channel Mytilaster is also incorporated into mussel bed on wave-sheltered rocks (Zahtila, 1987). Although the reduced free-water supply for incorporated bivalves may cause reduction in growth the group living offers, at the same time, protection from This article forms a part of the thesis submitted for a M.Sc. degree at the University of Zagreb, This study was conducted at the Laboratory for Ecology and Systematics, Center for Marine Research, Rovinj under supervision of Prof. D. Zavodnik. I wish to express my thank for assistance in species determination: Dr. D. Zavodnik (Sipuncula, Echinodermata), Dr. M. Hrs-Brenko (Bivalvia), A. Jaklin, M.Sc. (Gastropoda), Dr. E. Zahtila (Polychaeta), Dr. Z. Stevdd (Brachyura), Dr. Lj. igic (Cirripedia), POVZETEK Avtorica obravnava nevretenčarsko makrofavno v povezavi z užitno klapavico Mytilus galioprovincialis Lmk. v bibavičnem pasu skalnega obrežja v Umskem kanalu. V obdobju od aprila do oktobra 1994 je bilo med vzorčenjem ugotovljenih 92 vrst iz 11 debel. Po bogatosti vrst so prevladovali mehkužci (42 vrst), mnogoščetinci (21 vrst) in clenonožci (12 vrst) ali 81,4% celotne združene favne. Po Številčnosti so na školjčnih lupinah prevladovali vitičnjaki Balanus perforatus Bruguiere, med bisusnimi nitkami pa školjkice Lasaea rubra. Vanja EMRlC: MACROINVERTEBRAT E FAUN A ASSOCIATE D WIT H NATURA L POPULATION S OF MEDITERRANEA N MUSSt'l .... b7-7i LITERATURE Barnes, H., Crisp, D.). 1956, Evidence of self-fertilization in certain species of barnacles, j. Exp. Mar. Biol. Ecol., 35,:631 -639, Bellan-Saniini, D. 1969. 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