Abstract
Benthic communities represent a powerful tool for the detection of natural and anthropogenic disturbances, as well as for the assessment of marine ecosystem stability. This paper shows that bivalve assemblages could serve as excellent indicators of disturbance and ecosystem instability. The goal of this study was to compare two sets of data in order to determine the differences between two different periods belonging to bivalve assemblage in the muddy detritic bottom of the northern Adriatic Sea in the post-anoxic period during December 1989, 1990, 1991 and quite a while later, during 2003, 2004 and 2005. Abundances of some indicator species such as Corbula gibba, Modiolarca subpicta and Timoclea ovata were detected during the post-anoxic period. Recruitment in the quality of bivalve assemblages was proved by the ecologic and biotic indexes during 2003, 2004 and 2005, during a period of relatively stable ecological conditions. Fluctuation in bivalve diversity due to the ecological quality of the marine ecosystem in the eastern part of the northern Adriatic Sea is also discussed.
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References
Baden S.P., Loo L.O., Pihl L. & Rosenberg R. 1990. Effects of eutrophication on benthic communities including fish — Swedish west coast. Ambio 19(3): 113–122.
Billett D.S.M., Lampitt A.L., Rice A.L. & Mantoura R.F.C. 1983. Seasonal sedimentation of phytoplankton to deep-sea benthos. Nature 302: 520–522. DOI: 10.1038/302520a0
Bonvicini-Pagliai A.M. & Serpagli F. 1988. Corbula gibba (Olivi) as a time recorder of environmental stress. A first contribution. Rapp. Comm. Int. Mer Médit. 31(Suppl 2): 17.
Borja A., Franco J. & V. Pérez. 2000. A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar. Pollut. Bull. 40(12): 1100–1114. DOI: 10.1016/S0025-326X(00)00061-8
Cabioch L. 1968. Contribution à la connaissance des peuplements benthiques de la Manche occidentale. Cahiers de Biologie Marine, Tome IX, Cahier 5 (Supplément), Paris-Ve: Laboratoire de Zoologie (7, Quai Saint-Bernard), 724 pp. DOI: 10.1002/iroh.19710560107
Clarke K.R. & Warwick R.W. 1994. Change in Marine Communities: An Approach To Statistical Analysis and Interpretation. Natural Environment Research Council, Swindon, UK, 144 pp. ISBN: 1855311402
Costello M.J., Emblow C. & White R.J. (ed.) 2001. European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Collection Patrimoines Naturels, 50, Muséum National d’Histoire Naturelle: Paris, 463 pp. ISBN: 2-85653-538-0
Crema R., Castelli A. & Prevedelli D. 1991. Long term eutrophication effects on macrofaunal communities in the Northern Adriatic Sea. Mar. Pollut. Bull. 22: 503–508. DOI: 10.1016/0025-326X(91)90405-H
Dauer D.M. 1993. Biological criteria, environmental health and estuarine macrobenthic community structure. Mar. Pollut. Bull. 26(5): 249–257.
Degobbis D., Fonda-Umani S., Franco P., Malej A., Precali R. & Smodlaka N. 1995. Changes in the northern Adriatic ecosystem and the hypertrophic appearance of gelatinous aggregates. Sci. Total. Environ. 165(1–3): 43–58. DOI: 10.1016/0048-9697(95)04542-9
Degobbis D., Malej A. & Umani S.F. 1999. The mucilage phenomenon in the northern Adriatic Sea. A critical review of the present scientific hypotheses. Ann. Ist. Super. Sanitá 35(3): 373–381.
Degobbis D., Precali R., Ivančić I., Smodlaka N., Fuks D. & Kveder S. 2000. Long-term changes in the northern Adriatic ecosystem related to anthropogenic eutrophication. Int. J. Environ. Poll. 13(1–6): 495–533. DOI: 10.1504/IJEP.2000.002332
Diaz R.J. & Rosenberg R. 1995. Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Ann. Rev. 33: 245–303.
Diaz R.J. & Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321(5891): 926–929. DOI: 10.1126/science.1156401
Faganeli J., Avčin A., Fanuko N., Malej A., Turk V., Tušnik P., Vriser B. & Vukovic A. 1985. Bottom layer anoxia in the central part of the gulf of Trieste in the late summer 1983. Mar. Pollut. Bull. 16: 75–78. DOI: 10.1016/0025-326X(85)90127-4
Fedra K., Ölscher E.M., Scherübel C., Stachowitsch M. & Wurzian R.S. 1976. On the ecology of a North Adriatic benthic community: Distribution, standing crop and composition of the macrobenthos. Mar. Biol. 38(2): 129–145. DOI: 10.1007/BF00390766
Galloway J.N., Townsend A.R., Erisman J.W., Bekunda M., Cai Z., Freney J.R., Martinelli L.A., Seitzinger S.P. & Sutton. M.A. 2008. Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science 320(5878): 889–892. DOI: 10.1126/science.1136674
Gamulin-Brida H. 1967. The benthic fauna of the Adriatic Sea. Oceanogr. Mar. Biol. Ann. Rev. 5: 535–568.
Giangrande A., Geraci S. & Belmonte G. 1994. Life-cycle and lifehistory diversity in marine invertebrates and the implications in community dynamics. Oceanogr. Mar. Biol. Ann. Rev. 32: 305–333.
Graeffe E. 1903. Review of marine animals in the Gulf of Trieste. VI. Mollusca. Arb. Zool. Inst. Wien, Zool. Sta. Trieste. 14: 89–136.
Gray J.S., Wu R.S. & Or Y.Y. 2002. Effects of hypoxia and organic enrichment on the coastal marine environment. Mar. Ecol-Prog. Ser. 238: 249–279.
Hagerman L. 1998. Physiological flexibility; a necessity for life in anoxic and sulphidic habitats. Hydrobiologia 378–376: 241–254. DOI: 10.1023/A:1017033711985
Holling C.S. 1973. Resilience and stability of ecological systems. Annu. Rev. Ecol. Syst. 4: 1–23. DOI: 10.1146/annurev. es.04.110173.000245
Hrs-Brenko M. 1981. Population studies of Corbula gibba (Olivi), Bivalvia, Corbulidae, in the northern Adriatic Sea. J. Mollus. Stud. 47(1): 17–24.
Hrs-Brenko M. 1998. Considerations on the 1990 and 1991 bivalve repopulations in the northern Adriatic Sea (Croatia). Period. Biol. 100(1): 59–62.
Hrs-Brenko M. 2003. Važnost školjkaša Corbula gibba (Olivi, 1792) (Corbulidae, Molluska Bivalvia) u obnovi pridnenih zajednica u sjevernom Jadranu [The role of bivalve Corbula gibba (Olivi, 1792) (Corbulidae, Mollusca Bivalvia) in the recruitment of benthic communities in the northern Adriatic]. Pomorski Zbornik 41(1): 195–208.
Hrs-Brenko M. 2006. The basket shell, Corbula gibba Olivi, 1792 (Bivalve Mollusks) as a species resistant to environmental disturbances. A review. Acta Adriat. 47(Suppl. 1): 49–64.
Hrs-Brenko M., Medaković D., Labura Ž. & Zahtila E. 1994. Bivalve recovery after a mass mortality in the autumn of 1989 in the northern Adriatic Sea. Period. Biol. 96(Suppl. 4): 455–459.
Jensen J.N. 1988. Recruitment, growth and mortality of juvenile Corbula gibba and Abra alba in the Limfjord, Denmark. Kieler Meeresforsch. Sonderh. 6: 357–365.
Jensen J.N. 1990. Increased abundance and growth of the suspension-feeding bivalve Corbula gibba in a shallow part of the eutrophic Limfjord, Denmark. Neth. J. Sea Res. 27(1): 101–108.
Jørgensen B.B. 1980. Seasonal oxygen depletion in the bottom waters of a Danish fjord and its effects on the benthic community. Oikos 34: 68–76. DOI: 10.1016/0077-7579(90)90038-I
Justić D., Rabalais N.N., Turner R. E & Wiseman Jr. W.J. 1993. Seasonal coupling between riverborne nutrients, net productivity and hypoxia. Mar. Pollut. Bull. 26: 184–189. DOI: 10.1016/0025-326X(93)90620-Y
Koulouri P., Dounas C., Arvanitidis Ch., Koutsoubas D. & A. Eleftheriou. 2006. Molluscan diversity along a Mediterranean soft bottom sublittoral ecotone. Scientia Marina 70(Suppl. 4): 573–583.
Leppäkoski E. 1971. Benthic recolonization of the Bornholm basin (Southern Baltic) in 1969–71, pp. 171–179. In: Zavodnik D. (ed.), Proceedings of the Sixth European Symposium on Marine Biology, Rovinj, Croatia, Yugoslavia September 27–October 2, 1971, Thalassia Jugosl. 7 (1), European Marine Biology Symposia 6.
Levin L.A., Ekau W., Gooday A.J., Jorissen F., Middelburg J.J., Naqvi S.W.A., Neira C., Rabalais N.N. & Zhang J. 2009. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6: 2063–2098. DOI: 10.5194/bg-6-2063-2009
Llansó R.J. 1992. Effects of hypoxia on estuarine benthos: the lower Rappahannock River (Chesapeake Bay), a case study. Estuarine, Coastal and Shelf Science 35(5): 491–515. DOI: 10.1016/S0272-7714(05)80027-7
Margalef R. 1958. Information theory in ecology. Gen. Syst. 3: 36–71.
Miller D.C., Poucher S.L. & Coiro L. 2002. Determination of lethal dissolved oxygen levels for selected marine and estuarine fishes, crustaceans, and a Bivalve. Mar. Biol. 140(2): 287–296. DOI: 10.1007/s002270100702
Muxika I., Borja Á. & Bald J. 2007. Using historical data, expert judgement and multivariate analysis in assessing reference conditions and benthic ecological status, according to the European Water Framework Directive. Mar. Pollut. Bull. 55(1–6): 16–29. DOI: 10.1016/j.marpolbul.2006.05.025
Muus K. 1973. Settling, growth and mortality of young bivalves in the Øresund. Ophelia 12(1–2): 79–116.
Newell R.C., Seiderer L.J., Robinson J.E. & Simpson N.M 2001. London Gateway Port Project benthic biological resource survey of the lower Thames Estuary, July–September 2001. Marine Ecological Surveys Limited, Cornwall.
Nicholson S. & Morton B. 2000. The hypoxia tolerances of subtidal marine bivalves from Hong Kong, pp. 229–239. In: Morton B. (ed.), The marine flora and fauna of Hong Kong and Southern China V, Proceedings of tenth international marine biological workshop: the marine flora and fauna of Hong Kong and Southern China, Hong Kong, 6-26 April 1998, Hong Kong: Hong Kong University Press, 736 pp. ISBN: 9622095259
Nordsieck F. 1969. Die europäischen Meeresmuscheln (Bivalvia) vom Eismeer bis Kapverden, Mittelmeer und Schwarzes Meer. G. Fischer Verlag, Stuttgart, 256 pp.
Occhipinti-Ambrogi A., Favruzzo M. & Savini D. 2002. Multiannual variations of macrobenthos along the Emilia-Romagna coast (Northern Adriatic). PSZN Mar. Ecol. 23(Suppl. s1): 307–319. DOI: 10.1111/j.1439-0485.2002.tb00029.x
Orel G., Marocco A., Vio E., del Piero D. & Seta G. 1987. Sedimenti e biocenosi bentoniche tra la foce del Po ed il golfo di Trieste (Alto Adriatico). Bull. Ecol. 18(2): 229–241.
Orel G. & Mennea B. 1969. I popolamenti bentonici di alcuni tipi di fondo mobile del Golfo di Trieste. Pubbl. Staz. Zool. Napoli 37(Suppl. 2): 261–276.
Ott J. 1992. The Adriatic benthos: Problems and perspectives, pp. 367–378. In: Colombo G., Ferrari I., Ceccherelli V.U. & Rossi, R. (eds), Marine Eutrophication and Population Dynamics, 25th EMBS, Ed. Olsen & Olsen, Fredensborg, Denmark, 395 pp. ISBN: 87-85215-19-8
Parenzan P. 1974. Carta d’identita delle conchiglie del Mediterraneo. Vol. II. Bivalvi. Prima parte Bios Taras Ed. Taranto, 277 pp.
Parenzan P. 1976. Carta d’identita delle conchiglie del Mediterraneo. Vol. II. Bivalvi. Seconda parte Bios Taras Ed. Taranto, 264 pp.
Pearson T.H. & Rosenberg R. 1978. Macrobentic succession in relation to organic enrichment and polluttion of the marine enviroment. Oceanogr. Mar. Biol. Ann. Rev. 16: 229–311.
Pérès J.M. & Picard J. 1964. Nouveau manuel de Bionomie bentique de la mer Méditerranée. Recueil des Travaux de la Station Marine d’Endoume 47(31): 3–137.
Piccinetti C. & Manfrin G. 1969. Osservazioni sulla mortalita di pesci e di altri organismi verificatasi nel 1969 in Adriatico. Note Lab. Biol. Mar. Pesca-Fano 3: 73–92.
Pielou E. 1969. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13: 131–144. DOI: 10.1016/(66)90013-0
Pimm S.L. 1984. The complexity and stability of ecosystems. Nature 307: 321–326. DOI: 10.1038/307321a0
Pruvot C., Empis A. & Dhainaut-Courtois N. 2000. Présence du mollusque Bivalve Corbula gibba (Olivi, 1792) dans les sédiments meubles du port est de Dunkerque (Mer du Nord) = New record of the mollusk Corbula gibba (Olivi, 1792) in the muddy sands of Dunkirk harbour (Nord Sea). B. Soc. Zool. Fr. 125: 75–82.
Rabalais N.N. & Gilbert. D. 2008. Distribution and consequences of hypoxia. Chapter 11, pp. 209–225. In: Urban E.R., Sundby B., Malanotte-Rizzoli P. & Milello J. (eds), Watersheds, Bay, and Bounded Seas: The Science and Management of Semi-Enclosed Marine Systems, Island Press, Washington, D.C. ISBN: 9781597265034
Richards J.G., Farrell A.P. & Brauner C.J. 2009. Hypoxia. In: Farrell A.P. & Brauner C.J. (eds), Fish Physiology 27, San Diego: Academic Press, 528 pp. ISBN: 978-0-12-374632-0
Riedel B., Zuschin M. & Stachowitsch M. 2008. Dead zones: a future worst-case scenario for Northern Adriatic biodiversity, pp. 73–77. In: Briand F. (ed.), Climate warming and related changes in Mediterranean marine biota, CIESM Workshop Monographs 35, 152 pp.
Rosenberg R. 1972. Benthic faunal recovery in a Swedish fjord following the closure of a sulphite pulp mill. Oikos 23(1): 92–108.
Rosenberg R. 1973. Succession in benthic macrofauna in a Swedish fjord subsequent to the closure of a sulphite pulp mill. Oikos 24(2): 244–258.
Rosenberg R. 1976. Benthic faunal dynamics during succession following pollution abatement in a Swedish estuary. Oikos 27 (3): 414–427.
Rosenberg R. 1977. Benthic macrofaunal dynamics, production, and dispersion in an oxygen-deficient estuary of west Sweden. J. Exp. Mar. Biol. Ecol. 26(2): 107–133. DOI: 10.1016/0022-0981(77)90102-2
Sabatini M. & Ballerstedt S. 2005. Nucula nitidosa. A bivalve mollusc. Marine LifeInformation Network: Biology and Sensitivity Key Information Sub-programme [on-line], Plymouth: Marine Biological Association of the United Kingdom.
Seiderer L.J. & Newell R.C. 1999. Analysis of the relationship between sediment composition and benthic community structure in coastal deposits: Implications for marine aggregate dredging. ICES J. Mar. Sci. 56: 757–765. DOI: 10.1006/jmsc.1999.0495
Shannon C.E. & Weaver W. 1949. The Mathematical Theory of Communication. Urbana, Chicago. University of Illinois Press, 255 pp. ISBN: 0252725484
Simboura N & A. Zenetos 2002. Benthic indicators to use in ecological quality classification of Mediterranean soft bottoms marine ecosystems, including a new biotic index. Mediterranean Marine Science 3/2: 77–111.
Solis-Weiss V., Aleffi F., Bettoso N., Rossin P., Orel G. & Fonda-Umani S. 2004. Effects of industrial and urban pollution on the benthic macrofauna in the Bay of Muggia (industrial port of Trieste, Italy). Sci. Total. Environ. 328(1–3): 247–263. DOI: 10.1016/j.scitotenv.2004.01.027
Stachowitsch M. 1984. Mass mortality in the Gulf of Trieste: The course of community destruction. P.S.Z.N.I:Mar. Ecol. 5(3): 243–264. DOI: 10.1111/j.1439-0485.1984.tb00124.x
Stachowitsch M. 1991. Anoxia in the northern Adriatic Sea: rapid death, slow recovery, pp. 119–129. In: Tyson R.V. & Pearson T.H. (eds), Modern and ancient Continental Shelf Anoxia. Geol. Soc. Spec. Publ. 58, 470 pp. ISBN: 0903317672
Stachowitsch M., Fanuko N. & Richter M. 1990. Mucus aggregates in the Adriatic Sea: An overview of stage and occurrences. PSZNI. Mar. Ecol. 11(4): 327–350. DOI: 10.1111/j.1439-0485.1990.tb00387.x
Stachowitsch M., Riedel B., Zuschin M. & Machan R. 2007. Oxygen depletion and benthic mortalities: the first in situ experimental approach to documenting an elusive phenomenon. Limnol. Oceanogr.: Methods 5: 344–352.
Steimle F.W. & Radosh D.J. 1979. Effects on the benthic invertebrate community, pp. 281–293. In: Swanson R.L. & Sindermann C.J. (eds), Oxygen depletion and associated benthic mortalities in the New York Bight, 1976. NOAA Prof. Pap. 11, Rockville, MD. Natl. Oceanic Atmos. Adm., 354 pp. ISBN: 9781153526456
Stierhoff K.L., Targett T.E. & Miller K.L. 2006. Ecophysiological responses of juvenile summer and winter flounder to hypoxia: experimental and modelling analyses of effects on estuarine nursery quality. Mar. Ecol. Prog. Ser. 325: 255–266. DOI: 10.3354/meps325255
Tabatabaie T. & Amiri F. 2010. The impact of industrial pollution on macrobenthic fauna communities. Afr. J. Environ. Sci. Technol. 4(Suppl. 9): 547–557.
Tebble N. 1966. British Bivalve Seashells. A Handbook for Identification. Trustees of the British Museum (Natural History), London, 212 pp. ISBN-10: 0565006460
Theodorou A.J. 1994. The ecological state of the Elefsis Bay prior to the operation of the athens sea outfall. Water Sci. Technol. 30(10): 161–171.
Tomassetti P., Tosti M. & De Santis A. 1997. Distribution of Corbula gibba (Olivi) (Mollusca, Bivalvia) in two areas of the northern Adriatic Sea related to some physical-chemical parameters. Biol. Mar. Mediterr. 4(Suppl. 1): 452–455.
Travizi A. 1998. Recovery of meiofauna after anoxic stress. II. Spatial distribution. Period. Biol. 100(1): 71–79.
Travizi A. 2000. Effect of anoxic stress on density and distribution of sediment meiofauna. Period. Biol. 102(2): 207–215.
UNEP 2004. GEO Year Book 2003. GEO Section/UNEP, Nairobi, 76 pp. ISBN: 9280724150
Vaquer-Sunyer R. & Duarte C. M. 2008. Thresholds of hypoxia for marine biodiversity. Proc. Nat. Acad. Sci. U. S. A. 105: 15452–15457. DOI: 10.1073/pnas.0803833105
Vatova A. 1949. La fauna bentonica dell’alto e medio Adriatico. Nova Thalassia 1(3): 110 pp.
Voltolina D. 1973. A phytoplankton bloom in the lagoon of Venice. Arch. Oceanogr. Limnol. 18(1): 19–37.
Warwick R., Platt H., Clarke K., Agard J. & Gobin J. 1990. Analysis of macrobenthic and meiobenthic community structure in relation to pollution and disturbance in Hamilton harbour, Bermuda. J. Exp. Mar. Biol. Ecol. 138(1–2): 119–142. DOI: 10.1016/0022-0981(90)90180-K
Warwick R.M. & Uncles R. J. 1980. Distribution of benthic macrofauna associations in the Bristol Channel in relation to tidal stress. Mar. Ecol. Prog. Ser. 3: 97–103.
Wilding T.A. 2006. The benthic impacts of the Loch Linnhe artificial reef. Hydrobiologia 555(1): 345–353. DOI: 10.1007/s10750-005-1130-4
Yonge C.M. 1946. On the habits and adaptations of Aloidis (Corbula) gibba. J. Mar. Biol. Ass. U.K. 26(3): 358–376.
Yonge C.M. & Thompson T.E. 1976. Living Marine Molluscs. William Collins Son and Co., Ltd. London, 288 pp. ISBN 0002190990
Zavodnik D., Travizi A. & Jaklin A. 1994. Phytoplankton bloom consequences on benthic organisms. Final reports on research projects dealing with eutrophication problem. MAP Tech. Reports Ser. (Pub.UNEP, Athens) 78: 91–120.
Zenetos A. 1996. Classification and interpretation of the established mediterranean biocoenoses based solely on bivalve molluscs. J. Mar. Biol. Ass. U.K. 76(2): 403–416. DOI: 10.1017/S0025315400030630
Žerjav Meixner V. 2000. Potrošnja kisika i ponašanje školjkaša Corbula gibba (Olivi, 1792) u eksperimentalnim uvjetima [Oxygen consumption and the behaviour of shellfish Corbula gibba (Olivi, 1792) in the experimental conditions]. Thesis, University of Zagreb. 98 pp.
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Nerlović, V., Doğan, A. & Hrs-Brenko, M. Response to oxygen deficiency (depletion): Bivalve assemblages as an indicator of ecosystem instability in the northern Adriatic Sea. Biologia 66, 1114–1126 (2011). https://doi.org/10.2478/s11756-011-0121-3
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DOI: https://doi.org/10.2478/s11756-011-0121-3