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Environmental quality assessment of El Bibane lagoon (Tunisia) using taxonomic and functional diversity of meiofauna and nematodes

  • Soufiane Jouili (a1), Naceur Essid (a1), Federica Semprucci (a2), Fehmi Boufahja (a1), Ahmed Nasri (a1), Hamouda Beyrem (a1) and Ezzeddine Mahmoudi (a1)...
Abstract

The lagoon of El Bibane (Tunisia) is a Mediterranean coastal area that is affected by an increasing human impact. Thus, an estimation of its biodiversity and an ecological quality assessment are very urgent. This study investigates the meiofaunal and nematode communities of the El Bibane lagoon both from a taxonomic and a functional point of view. Nematodes were the dominant group as is common in brackish water systems. The nematode community was made up of 62 genera in 22 families. Xyalidae, Chromadoridae and Cyatholaimidae were the richest and most abundant families. The taxonomic composition and biodiversity of nematodes were comparable to those found in other European and Mediterranean transitional areas. Both meiofauna and nematodes showed a clear subdivision between marginal and central areas. The central stations, represented by fine sediments and higher amounts of organic carbon, seemed to be characterized by low meiofaunal densities, nematode diversity and a strong dominance of 1B and 2B trophic guilds. These trends could be related not only to the grain size and organic load, but also to a possible influence of tidal currents that can transport pollutants in the central area of the lagoon coming from the adjacent coastal areas. Shannon diversity and life strategies are not always in agreement in defining the ecological quality, but an overall worse ecological quality was detected especially at S6. The results of this study are an important starting point for the future monitoring of the potential and actual human impact on the El Bibane area over time.

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Corresponding author
Correspondence should be addressed to: F. Semprucci, Dipartimento di Scienze Biomolecolari (DiSB), University of Urbino, 61029 Urbino, Italy email: federica.semprucci@uniurb.it
References
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Abigail, A., Atwood, J., August, P., Byron, C., Cobb, S., Foster, C., Fry, C., Gold, A., Hagos, K., Heffner, L., Kellogg, D.Q., Lellis-Dibble, K.J., Opaluch, J.J., Oviatt, C., Pfeiffer-Herbert, A., Rohr, N., Smith, L., Smythe, T., Swift, J. and Vinhateiro, N. (2009) Coastal lagoons and climate change: ecological and social ramifications in the U.S. Atlantic and Gulf coast ecosystems. Ecology and Society 14, 8.
Adão, H., Alves, A.S., Patrício, J., Neto, J.M., Costa, M.J. and Marques, J. C. (2009) Spatial distribution of subtidal Nematoda communities along the salinity gradient in southern European estuaries. Acta Oecologica 35, 287300.
Affouri, A., Dezileau, L. and Kallel, N. (2016) Extreme flood events reconstruction during the last century in the El Bibane lagoon (Southeast of Tunisia): a multi-proxy approach. Climate of the Past Discussion. doi: 10.5194/cp-2016-40.
Armenteros, M., Ruiz-Abierno, A., Fernández-Garce, R., Pérez-García, J.A., Díaz-Asencio, L., Vincx, M. and Decraemer, W. (2009) Biodiversity patterns of free-living marine nematodes in a tropical bay: Cienfuegos, Caribbean Sea. Estuarine Coastal Shelf Science 85, 179189.
Austen, M.C., McEvoy, A.J. and Warwick, R.M. (1994) The specificity of meiobenthic community responses to different pollutants: results from microcosm experiments. Marine Pollution Bulletin 28, 557563.
Balsamo, M., Albertelli, G., Ceccherelli, V.U., Coccioni, R., Colangelo, M.A., Curini-Galletti, M., Danovaro, R., D'Addabbo, R., Leonardis, C., Fabiano, M., Frontalini, F., Gallo, M., Gambi, C., Guidi, L., Moreno, M., Pusceddu, A., Sandulli, R., Semprucci, F., Todaro, M.A. and Tongiorgi, P. (2010) Meiofauna of the Adriatic Sea: current state of knowledge and future perspectives. Chemistry and Ecology 26, 1, 4563.
Balsamo, M., Semprucci, F., Frontalini, F. and Coccioni, R. (2012) Meiofauna as a tool for marine ecosystem biomonitoring. In Cruzado, A. (ed.) Marine ecosystems. Rijeka: InTech Publisher. Volume 4, pp. 77104.
Barhoumi, B., Jouili, S., Elbarhoumi, A., Derouiche, A., El Megdiche, Y., Bouabdallah, S., Touil, S. and Driss, M.R. (2016) Organochlorines in the surface sediments of the Bahiret el Bibane lagoon (Tunisia, Southwestern Mediterranean Sea). Chemistry and Ecology. doi: 10.1080/02757540.2016.1195817.
Barnes, N., Bamber, R., Moncrieff, C., Sheader, M. and Ferrero, T. (2008) Meiofauna in closed coastal saline lagoons in the United Kingdom: structure and biodiversity of nematode assemblage. Estuarine and Coastal Shelf Science 79, 328340.
Barnes, R.S.K. (1980) Coastal lagoons. The natural history of a neglected habitat. Cambridge: Cambridge University Press.
Bernardello, M., Secco, T., Pellizzato, F., Chinellato, M., Sfriso, A. and Pavoni, B. (2006) The changing state of contamination in the lagoon of Venice. Part 2: heavy metals. Chemosphere 64, 13341345.
Beyrem, H. and Aïssa, P. (2000) Les nématodes libres, organismes-sentinelles de l’évolution des concentrations d'hydrocarbures dans la baie de Bizerte (Tunisie). Cahiers de Biologie Marine 41, 329342.
Beyrem, H., Boufahja, F., Hedfi, A., Essid, N., Aïssa, P. and Mahmoudi, E. (2011) Laboratory study on individual and combined effects of cobalt- and zinc-spiked sediment on meiobenthic nematodes. Biological Trace Elements Research 144, 790803.
Bongers, T. (1990) The maturity index: an ecological measure of an environmental disturbance based on nematode species composition. Oecologia 83, 1419.
Bongers, T., Alkemade, R. and Yeates, G.W. (1991) Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the Maturity Index. Marine Ecology Progress Series 76, 135142.
Boufahja, F., Vitiello, J. and Aissa, P. (2014) More than 35 years of studies on marine nematodes from Tunisia: a checklist of species and their distribution. Zootaxa 3786, 269300.
BRL Ingenierie Idea Consult (2008) Preparation d'un plan de gestion de la lagune des Bibans, diagnostics et mesures d'urgence. Groupe STUDI, Tunis, Tunisia.
Buchanan, J.B. (1984) Sediment analysis. In Holme, N.A. and McIntyre, A.D. (eds) Methods for the study of marine benthos. Boston, MA: Blackwell Scientific Publications, pp. 4165.
Cibic, T., Blasutto, O. and Bettoso, N. (2009) Microalgal–meiofaunal interactions in a sublittoral site of the Gulf of Trieste (northern Adriatic Sea, Italy): a three-year study. Journal of Experimental Marine Biology and Ecology 370, 144154.
Cibic, T., Franzo, A., Celussi, M., Fabbro, C. and Del Negro, P. (2012) Benthic ecosystem functioning in hydrocarbon and heavy-metal contaminated sediments of an Adriatic lagoon. Marine Ecology Progress Series 458, 6987.
Clarke, K.R. and Gorley, R.N. (2006) PRIMER v6: user manual/tutorial. Plymouth: Primer-E.
Danovaro, R., Fabiano, M. and Vincx, M. (1995) Meiofauna response to the Agip Abruzzo oil spill in subtidal sediments of the Ligurian Sea. Marine Pollution Bulletin 30, 133145.
Danovaro, R., Gambi, C., Mirto, S., Sandulli, R. and Cecchierelli, V.U. (2004) Meiofauna. In Gambi, M.C. and Dappiano, M. (eds) Mediterranean marine benthos: a manual of methods for its samplings and study. Biologia Marina Mediterranea 11, 5597.
Elliot, M. and Quintino, V. (2007) The Estuarine Quality Paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin 54, 640645.
Essid, N. (2008) Caractérisation de la pollution organique et minèrale des sèdiments de la lagune de bizerte et impact écologique sur les peuplements des nèmatodes libres: étude grande èchelle et au niveau díun parc mytilicole. Thèse de doctorat en sciences biologiques, facultè des sciences de bizerte. 303 pp.
Essid, N. and Aïssa, P. (2002) Etude quantitative des nématodes libres des secteurs nord et est de la lagune de Bizerte (Tunisie). Bulletin de Institut National des Sciences et Technologies de la Mer 29, 5363.
Fabbrocini, A., Guarino, A., Scirocco, T., Franchi, M. and D'Adamo, R. (2005) Integrated biomonitoring assessment of the Lesina Lagoon (Southern Adriatic Coast, Italy): preliminary results. Chemistry and Ecology 21, 479489.
Ferrero, T.J., Debenham, N.J. and Lambshead, P.J.D. (2008) The nematodes of the Thames estuary: assemblage structure and biodiversity, with a test of Attrill's linear model. Estuarine and Coastal Shelf Science 79, 409418.
Fonseca, G., Maria, T.F., Kandratavicius, N., Venekey, V., Gheller, P.F. and Gallucci, F. (2014) Testing for nematode–granulometry relationships. Marine Biodiversity 44, 435443.
Frontalini, F., Semprucci, F., Armynot du Châtelet, E., Francescangeli, F., Margaritelli, G., Rettori, R., Spagnoli, F., Balsamo, M. and Coccioni, R. (2014) Biodiversity trends of the meiofauna and foraminifera assemblages of Lake Varano (southern Italy). Proceedings of the Biological Society of Washington 127, 722.
Gerlach, S.A. (1954) Das Sublittoral der sandigen Meeresküstenals Lebensraum einer Mikrofauna. Kieler Meeresforschungen 10, 121129.
Gheskiere, T., Vincx, M., Urban-Malinga, B., Rossano, C. and Scapini, F. (2005) Nematodes from wave-dominated sandy beaches: diversity, zonation patterns and testing of the isocommunities concept. Estuarine, Coastal and Shelf Science 62, 365375.
Guelorget, O., Frisoni, G.F. and Perthuisot, J.P. (1982) Contribution à l’étude biologique de la Bahiret el Biban, lagune du Sud-Est tunisien. Mémoires de la Société Géologique de France 144, 173186.
Guerrini, A., Colangelo, M.A. and Ceccherelli, V.U. (1998) Recolonization patterns of meiobenthic communities in brackish vegetated and unvegetated habitats after induced hypoxia/anoxia. Hydrobiologia 375/376, 7387.
Guilini, K., Bezerra, T.N., Deprez, T., Fonseca, G., Holovachov, O., Leduc, D., Miljutin, D., Moens, T., Sharma, J., Smol, N., Tchesunov, A., Mokievsky, V., Vanaverbeke, J., Vanreusel, A. and Vincx, M. (2016) NeMys: World database of free-living marine nematodes. Accessed at http://nemys.ugent.be on 20.7.2016.
Gyedu-Ababio, T.K. (2011) Pollution status of two river estuaries in the Eastern Cape, South Africa, based on benthic meiofauna analyses. Journal of Water Resource and Protection 3, 473486.
Gyedu-Ababio, T.K. and Baird, D. (2006) Response of meiofauna and nematode communities to increased levels of contaminants in a laboratory microcosm experiment. Ecotoxicology and Environmental Safety 63, 443450.
Gyedu-Ababio, T.K., Furstenberg, J.P., Baird, D. and Vanreusel, A. (1999) Nematodes as indicators of pollution: a case study from the Swartkops river system, South Africa. Hydrobiologia 397, 155169.
Heip, C., Vincx, M. and Vranken, G. (1985) The ecology of marine nematodes. Oceanography and Marine Biology Annual Review 23, 399489.
Hendelberg, M. and Jensen, P. (1993) Vertical distribution of the nematode fauna in coastal sediment influenced by seasonal hypoxia in the bottom water. Ophelia 37, 8394.
Ingels, J., Kiriakoulakis, K., Wolff, G.A. and Vanreusel, A. (2009) Nematode diversity and its relation to the quantity and quality of sedimentary organic matter in the deep Nazaré Canyon, Western Iberian Margin. Deep Sea Research Part I 56, 15211539.
Jelassi, R., Khemaissia, H., Zimmer, M., Garbe-Schönberg, D. and Nasri-Ammar, K. (2015) Biodiversity of Talitridae family (Crustacea, Amphipoda) in some Tunisian coastal lagoons. Zoological Studies 54, 17.
Kotta, J. and Boucher, G. (2001) Interregional variation of free-living nematode assemblages in tropical coral sands. Cahiers de Biologie Marine 42, 315326.
Leduc, D. and Probert, P.K. (2009) The effect of bacterivorous nematodes on detritus incorporation by macrofaunal detritivores: a study using stable isotope and fatty acid analyses. Journal of Experimental Marine Biology and Ecology 371, 130139.
Lemoalle, J. (1986) Etude de la lagune El Bibane. 1. Les conditions de milieu. Rapports et Documents – INSTOP, 378.
Lemoelle, J., Vidy, G. and Franc, J. (1984) Rapport d’étude sur la lagune El Bibane (partie scientifique). Inst. Français de Rech. Sci. Pour le Dvl. En Coop. ORSTOM. CGP: 1117.
Mahmoudi, E. (2003) La méiofaune de deux lagunes perturbées: Ghar el melh et Bou Ghrara. Thèse de Doctorat, Faculté des Sciences de Bizerte. 348 pp.
Mahmoudi, E., Beyrem, H. and Aïssa, P. (2002a) Réponse des nématodes libres à la qualité des eaux et des sédiments de la lagune de Ghar El Melh (Tunisie) en été 1999. Cahiers de Biologie Marine 43, 8393.
Mahmoudi, E., Beyrem, H., Baccar, L. and Aïssa, P. (2002b) Response of free-living nematodes to the quality of water and sediment at Bou Ghrara lagoon (Tunisia) during winter 2000. Mediterranean Marine Science 3, 133146.
Medail, F. and Quezel, P. (1999) Biodiversity hotspots in the Mediterranean basin: setting global conservation priorities. Conservation Biology 13, 15101513.
Medhioub, K. (1979) La Bahiret El Biban. Etude géochimique et sédimenlogique d'une lagune du Sud – Est tunisien. Travail du Laboratoire de Géologie. Presse de 1′école Normale Supérieure 13, 150 pp.
Medhioub, K. and Perthuisot, A. (1977) Le comportement géochimique des eaux de la Bhiret El-Biban: Conséquences sur la pêche. Bulletin de l'Office National de Pêche, Tunisie 1, 2335.
Medhioub, K. and Perthuisot, J.P. (1981) The influence of peripheral sabkhas on the geochemistry and sedimentology of a Tunisian lagoon: Bahiret el Biban. Sedimentology 28, 679688.
Michiels, I. and Traunspurger, W. (2004) A three year study of seasonal dynamics of a zoobenthos community in a eutrophic lake. Nematology 6, 655669.
Millward, R.N. and Grant, A. (1995) Assessing the impact of copper on nematode communities from a chronically metal enriched estuary using pollution-induced community tolerance. Marine Pollution Bulletin 30, 701706.
Mirto, S. and Danovaro, R. (2004) Meiofaunal colonisation on artificial substrates: a tool for biomonitoring the environmental quality on coastal marine systems. Marine Pollution Bulletin 48, 919926.
Moens, T. and Vincx, M. (1997) Observations on the feeding ecology of estuarine nematodes. Journal of the Marine Biological Association of the United Kingdom 77, 211227.
Moreno, M., Semprucci, F., Vezzulli, L., Balsamo, M., Fabiano, M. and Albertelli, G. (2011) The use of nematodes in assessing ecological quality status in the Mediterranean coastal ecosystems. Ecological Indicators 11, 328336.
Neira, C., Sellanes, J., Soto, A., Gutiérrez, D. and Gallardo, V.A. (2001) Meiofauna and sedimentary organic matter off Central Chile: response to changes caused by the 1997–1998 El Niño. Oceanologica Acta 24, 313328.
Netto, S.A. and Valgas, I. (2010) The response of nematode assemblages to intensive mussel farming in coastal sediments (Southern Brazil). Environmental Monitoring and Assessment 162, 8193.
Netto, S.A., Warwick, R.M. and Attrill, M.J. (1999) Meiobenthic and macrobenthic community structure in carbonate sediments of Rocas Atoll (North-east, Brazil). Estuarine Coastal and Shelf Science 48, 3950.
Nixon, S. (1995) Clean coastal waters: understanding and reducing the effects of nutrient pollution. Washington, DC: National Research Council, Committee on the Causes and Management of Eutrophication, Ocean Studies Board, Water Science and Technology Board. 428 pp.
Pérez-Ruzafa, A., Marcos, C. and Pérez-Ruzafa, I.M. (2011) Mediterranean coastal lagoons in an ecosystem and aquatic resources management context. Physics and Chemistry of the Earth 36, 160166.
Pergent, G. and Zaouali, J. (1992) Analyse phénologique et lépidochronologique de Posidonia oceanica dans une lagune hyperhaline du Sud tunisien. Rapports et PV des réunions de la Commission Internationale pour l'Exploration Scientifique de la Méditerranée 33, 4849. Monaco: CIESM.
Pilarczyk, K.W. and Zeidler, R.B. (1996) Offshore breakwaters and shore evolution control. Rotterdam: A.A. Balkema.
Platt, H.M. and Warwick, R.M. (1983) Free-living marine nematodes. Part I. British Enoploids. Synopses of the British Fauna. Cambridge: Cambridge University Press.
Platt, H.M. and Warwick, R.M. (1988) Free-living marine nematodes. Part II. British Chromadorids. Synopses of the British Fauna. Cambridge: Cambridge University Press.
Pusceddu, A., Bianchelli, S., Gambi, C. and Danovaro, R. (2011) Assessment of benthic trophic status of marine coastal ecosystems: significance of meiofaunal rare taxa. Estuarine, Coastal and Shelf Science 93, 420430.
Pusceddu, A., Gambi, C., Manini, E. and Danovaro, R. et al. (2007) Trophic state, ecosystem efficiency and biodiversity of transitional aquatic ecosystems: analysis of environmental quality based on different benthic indicators. Chemistry and Ecology 23, 505515.
Rabaoui, L., Balti, R., El Zrelli, R. and Tlig-Zouari, S. (2013) Assessment of heavy metal pollution in the Gulf of Gabes (Tunisia) using four mollusc species. Mediterranean Marine Sci ence 15, 4558.
Remane, A. (1933) Verteilung und Organisation der benthonischen Mikrofauna der Kieler Bucht. Wissenschaftliche Meeresuntersuchungen Kiel 21, 161221.
Romdhane, M.S. (2002) État des réserves de la Biosphère de la Tunisie, la réserve de la Biosphère de l'Ichkeul. Commission Nationale du MAB Tunisie.
Sandulli, R., Semprucci, F. and Balsamo, M. (2014) Taxonomic and functional biodiversity variations of meiobenthic and nematode assemblages across an extreme environment: a study case in a Blue Hole cave. Italian Journal of Zoology 81, 508516.
Schratzberger, M., Lampadariou, N., Somerfield, P.J., Vandepitte, L. and Vanden Berghe, E. (2009) The impact of seabed disturbance on nematode communities: linking field and laboratory observations. Marine Biology 156, 709724.
Schratzberger, M. and Warwick, R.M. (1998) Effects of intensity and frequency of organic enrichment on two estuarine nematodes communities. Marine Ecology Progress Series 164, 8394.
Semprucci, F., Balsamo, M. and Frontalini, F. (2014a) The nematode assemblage of a coastal lagoon (Lake Varano, Southern Italy): ecology and biodiversity patterns. Scientia Marina 78, 579588.
Semprucci, F., Balsamo, M. and Sandulli, R. (2016) Assessment of the ecological quality (EcoQ) of the Venice lagoon using the structure and biodiversity of the meiofaunal assemblages. Ecological Indicators 67C, 451457.
Semprucci, F., Colantoni, P., Baldelli, G., Rocchi, M. and Balsamo, M. (2010) The distribution of meiofauna on back-reef sandy platforms in the Maldives (Indian Ocean). Marine Ecology: An Evolutionary Perspective 31, 592607.
Semprucci, F., Colantoni, P., Sbrocca, C., Baldelli, G. and Balsamo, M. (2014b) Spatial patterns of distribution of meiofaunal and nematode assemblages in the Huvadhoo lagoon (Maldives, Indian Ocean). Journal of the Marine Biological Association of the United Kingdom 94, 13771385.
Semprucci, F., Frontalini, F., Covazzi-Harriague, A., Coccioni, R. and Balsamo, M. (2013) Meio- and macrofauna in the marine area of the Monte St. Bartolo Natural Park (Central Adriatic Sea, Italy). Scientia Marina 77, 189199.
Semprucci, F., Losi, V. and Moreno, M. (2015) A review of Italian research on free-living marine nematodes and the future perspectives on their use as ecological indicators (EcoInds). Mediterranean Marine Science 16, 352365.
Steyaert, M., Vanaverbeke, J., Vanreusel, A., Barranguet, C., Lucas, C. and Vincx, M. (2003) The importance of fine-scale, vertical profiles in characterizing nematode community structure. Estuarine and Coastal Shelf Science 58, 353366.
Sutherland, T.F., Levings, C.D., Petersen, S.A., Poon, P. and Piercey, B. (2007) The use of meiofauna as an indicator of benthic organic enrichment associated with salmonid aquaculture. Marine Pollution Bulletin 54, 12491261.
Ürkmez, D., Sezgin, M. and Bat, L. (2014) Use of nematode maturity index for the determination of ecological quality status: a case study from the Black Sea. Journal of the Black Sea/Mediterranean Environment 20, 96107.
Vanaverbeke, J., Gheskiere, T., Steyaert, M. and Vincx, M. (2002) Nematode assemblages from subtidal sandbanks in the southern bight of the North Sea: effect of small sedimentological differences. Journal of Sea Research 48, 197207.
Vanaverbeke, J., Merckx, B., Degraer, S. and Vincx, M. (2011) Sediment-related distribution patterns of nematodes and macrofauna: two sides of the benthic coin? Marine Environmental Research 71, 3140.
Viaroli, P., Bartoli, M., Giordani, G., Magni, P. and Welsh, D.T. (2004) Biogeochemical indicators as tools for assessing sediment quality/vulnerability in transitional aquatic ecosystems. Aquatic Conservation, Marine and Freshwater Ecosystem 14, S19S29.
Vitiello, P. and Aïssa, P. (1985) Structure des peuplements de nématodes en milieu lagunaire pollué. 110ème Congrès National des Sociétés Savantes, Montpellier. Sciences II, 115126.
Warwick, R.M. (1993) The effects of organic enrichment on the benthic meio- and microfauna with particular reference to the fish-farming in Scottish sea-lochs. Scottish Natural Heritage review, No. 18. Edinburgh: Scottish Natural Heritage.
Warwick, R.M., Platt, H.M. and Somerfield, P.J. (1998) Free-living marine nematodes. Part III. British Monohysterids. Synopsis of British fauna (new series) No. 53. Shrewsbury: Field Studies Council, 296 pp.
Wieser, W. (1953) Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden. Eine ökologisch-morphologische Studie. Arkive fur Zoologi 4, 439484.
Zeppilli, D., Sarrazin, J., Leduc, D., Martinez Arbizu, P., Fontaneto, D., Fontanier, C., Gooday, A.J., Kristensen, R.M., Ivanenko, V.N., Sørensen, M.V., Vanreusel, A., Thébault, J., Mea, M., Allio, N., Andro, T., Arvigo, A., Castrec, J., Danielo, M., Foulon, V., Fumeron, R., Hermabessiere, L., Hulot, V., James, T., Langonne-Augen, R., Le Bot, T., Long, M., Mahabror, D., Morel, Q., Pantalos, M., Pouplard, E., Raimondeau, L., Rio-Cabello, A., Seite, S., Traisnel, G., Urvoy, K., Van Der Stegen, T., Weyand, M. and Fernandes, D. (2015) Is the meiofauna a good indicator for climate change and anthropogenic impacts? Marine Biodiversity 45, 505535.
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