Abstract
An ecological survey of the benthic communities was carried out, at both spatial and temporal scales, in Papapouli Lagoon, the first ecotouristic park in Greece by applying for the first time, ecological network analysis. The application of ecological network analysis provided novel information on the quality of interactions among species, undetected by the most frequently used methods. The sorting of substrate samples enabled the identification and density determination of 40,036 individuals belonging to 31 different taxa, although, strong dominance of only a few species was observed. “Deposit feeders” were the dominant trophic group in all sampling sites and seasons while “suspension feeders” exhibited relatively the lowest abundance. The periodic opening of the sea inlet seems to be of crucial importance. In coastal lagoons, where there is constant communication with the sea, benthic fauna patterns seem to change according to the sea-land gradient. However, in intermittently closed lagoons, such as Papapouli Lagoon, a more homogenous pattern is evident. The obtained networks showed that when communication with the sea is interrupted all the benthic fauna patterns tend to be destabilized and centralized around one species, which in most cases is a “deposit feeder”. When the inlet opens and communication with the sea is restored, the benthic composition seems to be more cohesive, especially in the most distant regions. Knowledge generated by network analysis should provide a valuable tool in order to assess potential environmental changes and assist management decisions.
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Albert, A., H. Jeong and A.L. Barabasi. 1999. Internet: Diameter of the World-Wide Web. Nature 401: 130–131.
Allen, S.E. 1974. Chemical Analysis of Ecological Materials. Blackwell Scientifc Publications, Oxford.
Allesina, S., A. Bodini and M. Pascual. 2009. Functional links and robustness in food webs. Phil. Trans. R Soc. B 364: 1701–1709.
Amanieu, M., J. Ferraris and O. Guelorget. 1979/1980. Structure des communautes et strategies adaptives en milieu lagunaire. Oceanis 5: 833–861.
Anderson, T.K. and M.V.K. Sukhdeo. 2011. Host centrality in food web networks determines parasite diversity. PLoSOne 6:e26798.
Arias, M. and P. Drake. 1994. Structure and production of the benthic macroinvertebrate community in a shallow lagoon in the Bay of Cadiz. Mar. Ecol. Prog. Ser. 115: 151–167.
Arvanitidis, C., P.J. Somerfeld, G. Chatzigeorgiou, S. Reizopoulou, T. Kevrekidis and A. Eleftheriou. 2009. Do multivariate analyses incorporating changes in pattern across taxonomic levels reveal anthropogenic stress in Mediterranean lagoons? J. Exp. Mar. Biol. Ecol. 369: 100–109.
Arvanitidis, C., G. Chatzigeorgiou, D. Koutsoubas, C. Dounas, A. Eleftheriou and P. Koulouri. 2005a. Mediterranean lagoons revisited: weakness and effciency of the rapid biodiversity assessment techniques in a severely fuctuating environment. Biodivers. Conserv. 14: 2347–2359.
Arvanitidis, C., G. Chatzigeorgiou, D. Koutsoubas, T. Kevrekidis, C. Dounas, A. Eleftheriou, P. Koulouri and A. Mogias. 2005b. Estimating lagoonal biodiversity in Greece: comparison of rapid assessment techniques. Helgoland Mar. Res. 59: 177–186.
Barnes, R.S.K. 1994. Macrofauna community structure and life histories in coastal lagoons. In: B. Kjerfve (ed.), Coastal Lagoon Processes, Elsevier, Amsterdam, pp. 311–362.
Bazairi H., A. Bayed, M. Glemarec and C. Hily. 2003. Spatial organization of macrozoobenthic communities in response to environmental factors in a coastal lagoon of the NW African coast (Merja Zerga, Morocco). Oceanol. Acta 26: 457–471.
Bird, E.C.F. 1994. Physical setting and geomorphology of coastal lagoons. In: B. Kjerfve (ed.), Coastal Lagoon Processes, Elsevier, Amsterdam, pp. 9–39.
Blott, S.J. and N. Pye. 2001. Gradistat: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surf. Process Landf. 26: 1237–1248.
Boaventura, D., L. Cancela de Fonseca and C. Teles-Ferreira. 1999. Trophic structure of macrobenthic communities on the Portugese coast. A review of lagoonal, estuarine and rocky littoral habitats. Acta Oecol. 20: 407–415.
Bódis, E., J. Nosek, N. Oertel, B. Tóth, E. Hornung and R. Sousa. 2011. Spatial distribution of bivalves in relation to environmental conditions (middle Danube catchment, Hungary). Community Ecol. 12: 210–219.
Bologna, P.A.X. 2007. Impact of differential predation potential on eelgrass (Zostera marina) faunal community structure. Aquat. Ecol. 41: 221–229.
Borgatti, S.P., G. Everett and L.C. Freeman. 1999. UCINET 5.0 version 1.00, Computer manual. The Library Quarterly: Information, Community, Policy, 71: 285–288.
Borja, A., J. Franco and V. Perez. 2000. A marine biotic index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar. Pollut. Bull. 40: 1100–1114.
Boutsis, G., G.P. Stamou and M.D. Argyropoulou. 2011. Short term effects of soil disinfection with metham sodium and organic alternatives on nematode communities. Community Ecol. 12: 161– 170.
Buchanan, J.B. 1984. Sediment analysis. In: N.A. Holme and A.D. Mc Intyre (eds) Methods for the Study of Marine Benthos, Blackwell Scientifc Publications, Oxford, pp. 41–65.
Byers, J.E., P.E. Gribben, G. Yeager and E.E. Sotka. 2012. Impacts of an abundant introduced ecosystem engineer within mudfats of the southeastern US coast. Biol. Invasions 14: 2587–2600.
Cancela da Fonseca, L., P. Duarte and F. Magalhães. 2001. Trophic group patterns of macrobenthos in brackish coastal systems. Bol Mus. Mun. Funcha. 16: 139–165.
Carvalho, S., A. Moura, M.B. Gaspar, P. Pereira, L. Cancela da Fonseca, M. Falcão, T. Drago, F. Leitão and J. Regala. 2005. Spatial and inter-annual variability of the macrobenthic communities within a coastal lagoon (Óbidos lagoon) and its relationship with environmental parameters. Acta Oecol. 27: 143–159.
Chapin, F.S., J. Lubchenco and H.L. Reynolds. 1995. Biodiversity effects on patterns and processes of communities and ecosystems. In: V.H. Heywood (ed.), Global Biodiversity Assessment, Cambridge University Press, Cambridge, pp. 289–301.
Chintiroglou, C, Ch. Antoniadou and P. Damianidis. 2008. Spatio-temporal variability of zoobenthic communities in a tectonic lagoon (Lake Vouliagmeni, Attika, Greece). J. Mar. Biol. Ass. UK 88: 873–881.
Clarke, K.R. and R.H. Green. 1988. Statistical design and analysis for biological effects study. Mar. Ecol. Prog. Ser. 46: 213–226.
Cognetti, G. and F. Maltagliati. 2000. Biodiversity and adaptive mechanisms in brackish water fauna. Mar. Pollut. Bull. 40: 7–14.
Colombo, G. 1977. Lagoons. In: R.S.K. Barnes (ed.), The Coastline. John Wiley & Sons, Chichester, pp. 63–82.
Constable, A.J. 1999. Ecology of benthic macro-invertebrates in soft-sediment environments: a review of progress towards quantitative models and predictions. Aust. J. Ecol. 24: 452–476.
Dolbeth, M., H. Teixeira, J.C. Marques and M.Ȃ. Pardal. 2009. Feeding guild composition of a macrobenthic subtidal community along a depth gradient. Sci. Mar. 73: 225–237.
Dunne J.A., R.J. Williams, N.D. Martinez, R.A. Wood and D.H. Erwin. 2008. Compilation and network analyses of Cambrian food webs. PLoS Biol. 6:e102.
Dutertre, M., D. Hamon, C. Chevalier and A. Ehrhold. 2013. The use of the relationships between environmental factors and benthic macrofauna distribution in the establishment of a baseline for coastal management. ICES J. Mar. Sci. 70: 294–308.
Eleftheriou, A. and A.D. McIntyre. 1976. The intertidal fauna of sandy beaches. A survey of the Scottish coast. Scott. Fish Res. Rep. 6: 1–61.
Fauchald, K. and P. Jumars. 1979. The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Annu. Rev. 17: 193–284.
Fidalgo e Costa, P., R.F. Oliveira and L. Cancela da Fonseca. 2006. Feeding ecology of Nereis diversicolor (O.F. Müller) (Annelida, Polychaeta) on estuarine and lagoon environments in the southwest coast of Portugal. Panam. J. Aquat. Sci. 1: 114–126.
Freeman, L.C 1979. Centrality in social networks: Conceptual clarifcation. Social Net. 1: 215–239.
Friedkin, N.E. 1991. Theoretical foundations for centrality measures. Am. J. Sociol. 96: 1478–1504.
Fuller, M.M., A. Wanger and B.J. Enquis. 2008. Using network analysis to characterize forest structure. Nat. Resour. Model 21: 225–247.
Gray, J.S. 1981. The Ecology of Marine Sediments. Cambridge University Press, London.
Guelorget, O. and J.P Perthuisot. 1983. Le domaine paralique. Expression géologiques, biologiques du confnement. Travaux du Laboratoire de Géologie de l’Ecole Normale Supérieure, Paris, France
Guelorget, O. and J.P. Perthuisot. 1992. Paralic ecosystems. Biological organization and functioning. Vie Milieu 42: 215–251.
Hanneman, R.A. and M. Riddle. 2005. Introduction to social network methods. Riverside, CA: University of California, Riverside https://doi.org/faculty.ucr.edu/~hanneman. Accessed 15 September 2013
Hill, T. and P. Lewicki. 2007. STATISTICS: Methods and applications. StatSoft, Tulsa, USA
Ings, T.C., J.M. Montoya., J. Bascompte, N. Blüthgen, L. Brown, C.F. Dormann, F. Edwards, D. Figueroa, U. Jacob, J.I. Jones, R.B. Lauridsen, M.E. Ledger, H.M. Lewis, J.M. Olesen, F.J. van Veen, P.H. Warren and G. Woodward. 2009. Ecological networks ‒ beyond food webs. J. Anim. Ecol. 78: 253–269.
Jaramillo, E., S. Muslow, M. Pino and H. Figueroa. 1984. Subtidal benthic macroinfauna in an estuary of south Chile: Distribution pattern in relation to sediment types. Mar. Ecol. 5: 119–133.
Jeong, H., B. Tombor, A. Albert, Z.N. Oltvai and S.L. Barabasi. 2000. The large-scale organization of metabolic networks. Nature 407: 651–654.
Johnson, J.C., J.J. Luczkovich, S.P. Borgatti and T.A.B. Snijders. 2009. Using social network analysis tools in ecology: Markov process transition models applied to the seasonal trophic network dynamics of the Chesapeake Bay. Ecol. Model. 220: 3133–3140.
Jordán, F., T. Okey, B. Bauer and S. Libralato. 2008. Identifying important species: linking structure and function in ecological networks. Ecol. Model. 216: 75–80.
Jordano, P., J. Bascompte and J.M. Olesen. 2006. The ecological consequences of complex topology and nested structure in pollination webs. In: N.M. Waser and J. Ollerton (eds), Plant-pollinator Interactions: From Specialization to Generalization, University of Chicago Press, Chicago, pp. 173–199.
Kapagianni, P.D., G. Boutsis, M.D. Argyropoulou, E.M. Papatheodorou and G.P. Stamou. 2010. The network of interactions among soil quality variables and nematodes: short-term responses to disturbances induced by chemical and organic disinfection. Appl. Soil Ecol. 44: 67–74.
Kelly, D.W., J.T.A. Dick and W.I. Montgomery. 2002. The functional role of Gammarus (Crustacea, Amphipoda): shredders, predators, or both? Hydrobiologia 485: 199–203.
Kevrekidis, T. and A. Koukouras. 1988/89. Life cycle and reproduction of Gammarus aequicauda (Crustacea: Amphipoda) in the Evros Delta (NE Greece). Isr. J. Zool. 35: 137–149.
Kleinberg, J. 2008. The convergence of social and technological networks. Commun. ACM 51: 66–72.
Koukaras, K. 2010. Monitoring report of water physico-chemical parameters (March 2009- May 2010). Technical report, Nearhus GP
Koutsoubas, D., C. Arvanitidis, C. Dounas and L. Drummond. 2000b. Community structure and dynamics of the molluscan fauna in a Mediterranean lagoon (Gialova lagoon, SW Greece). Belg. J. Zool. 130: 135–142.
Koutsoubas, D., C. Dounas, C. Arvanitidis, S. Kornilios, G. Petihakis, G. Triantafyllou and A. Eleftheriou. 2000a. Macrobenthic community structure and disturbance assessment in Gialova Lagoon, Ionian Sea. ICES J. Mar. Sci. 57: 1472–1480.
Krause, A.E., K.A. Frank, D.M. Mason, R.E. Ulanowicz and W.W. Taylor. 2003. Compartments revealed in food-web structure. Nature 426: 282–285.
Lacerda, L.D. 1994. Biochemistry of heavy metals in coastal lagoons. In: B. Kjerfve (ed), Coastal Lagoon Processes, Elsevier, Amsterdam, pp. 221–241.
Lardicci, C., S. Como, S. Corti and F. Rossi. 2001. Recovery of the macrozoobenthic community after severe dystrophic crises in a Mediterranean coastal lagoon (Orbetello, Italy). Mar. Pollut. Bull. 42: 202–214.
Larimore, R.W. 1970. Two shallow-water bottom samplers. Prog. Fish-Cult. 32: 116–119.
Lawton, J.H. and V.K. Brown. 1993. Redundancy in ecosystems. In: E.D. Schulze and H.A. Mooney (eds), Biodiversity and Ecosystem Function, Springer-Verlag, Berlin, pp. 255–270.
Liu, X.D., C.W. Wu and D.W. Ding 2011. Functional modules and bottlenecks in human metabolic network core. J. Biol. Res-Thessaloniki 15: 113–121.
Ludovisi, A., G. Castaldelli and E.A. Fano. 2013. Multi-scale spatio-temporal patchiness of macrozoobenthos in the Sacca di Goro lagoon (Po River Delta, Italy). Transit. Waters Bull. 7: 233–244.
Lusseau, D. and M.E.J. Newman. 2004. Identifying the role that animals play in their social networks. Proc. R. Soc. Lond. B 271: 477–481.
Lusseau, D., B. Wilson, P.S. Hammond, K. Grellier, J.W. Durban, K.K. Parsons, T.R. Barton and P.M. Thompson. 2006. Quantifying the infuence of sociality on population structure in bottlenose dolphins. J. Anim. Ecol. 75: 14–24.
MacArthur, R. and R. Levins. 1967. The limiting similarity, convergence, and divergence of coexisting species. Amer. Nat. 101: 377–385.
Mackneil, C., J.T.A. Dick and R.W. Elwood. 1997. The trophic ecology of freshwater Gammarus sp. (Crustacea:Amphipoda): Problems and perspectives concerning the functional feeding group concept. Biol. Rev. 72: 349–364.
Mancinelli, G. and L. Rossi. 2001. Indirect, size-dependent effects of crustacean mesograzers on the Rhodophyta Gracilaria verru-cosa (Hudson) Papenfuss: evidence from short-term study in the Lesina Lagoon (Italy). Mar. Biol. 138: 1163–1173.
Malea, P., T. Kevrekidis and A. Mogias. 2004. Annual versus perennial growth cycle in Ruppia maritima L.: temporal variation in population characteristics in Mediterranean lagoons (Monolimni and Drana Lagoons, Northern Aegean Sea). Bot. Mar. 47: 357– 366.
May, R.M. 2006. Network structure and the biology of populations. Trends Ecol. Evol. 21: 394–399.
Menéndez, M. and F.A. Comín. 1990. Consumption of macrophytes by invertebrates in Tancada lagoon (NE Spain). Sci. Mar. 54: 139–144.
Mistri, M., E.A. Fano and R. Rossi. 2001a. Redundancy of macro-benthos from lagoonal habitats in the Adriatic Sea. Mar. Ecol. Prog. Ser. 215: 289–296.
Mistri, M., R. Rossi and E.A. Fano. 2001b. Structure and secondary production of a soft bottom macrobenthic community in a brackish lagoon (Sacca di Goro, north-eastern Italy). Est. Coast Shelf Sci. 52: 605–616.
Mogias, A. and T. Kevrekidis. 2005. Macrozoobenthic community structure in a poikilohaline Mediterranean lagoon (Laki Lagoon, northern Aegean). Helgoland Mar. Res. 59: 167–176.
Munari, C., R.M. Warwick and M. Mistri. 2009. Monitoring with benthic fauna in Italian coastal lagoons: new tools for new prospects. Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 575–587.
Munari, C., U. Tessari, R. Rossi and M. Mistri. 2010. The ecological status of Karavasta Lagoon (Albania): closing the stable door before the horse has bolted? Mar. Environ. Res. 69: 10–17.
Muttil, N. and K.W. Chau. 2007. Machine-learning paradigms for selecting ecologically signifcant input variables. Eng. Appl. Artif. Intell. 20: 735–744.
Newman, M.E.J. 2008. Mathematics of networks. In: L.E. Blume and S.N. Durlauf (eds), The New Palgrave Encyclopedia of Economics, 2nd edn, Palgrave Macmillan, Basingstoke, pp. 1–12.
Nicolaidou, A. and M. Karakiri. 1989. The distribution of Amphipoda in a brackish-water lagoon in Greece. Mar. Ecol. 10:131–139.
Nicolaidou, A., M. Karakiri and V. Trichopoulou. 1985. Seasonal changes in the fauna of a brackish-water lagoon. Rapport de la Comité International pour l‘ Exploration Scientifque de la Mer Méditerranée 29: 125–126.
Nicolaidou, A., K. Petrou, K.A. Kormas and S. Reizopoulou. 2006. Inter-annual variability of soft bottom macrofaunal communities in two Ionian Sea lagoons. Hydrobiologia 555: 89–98.
Ortiz, M., D. Levins, L. Campos, F. Berrios, F. Campos, F. Jordán, B. Hermosillo, J. Gonzalez and F. Rodriguez. 2013. Identifying keystone trophic groups in benthic ecosystems: Implications for fsheries management. Ecol. Indic. 25: 133–140.
Pah, A.R., R. Guimera, A.M. Mustoe and L.A.N. Amaral. 2013. Use of a global metabolic network to curate organismal metabolic networks. Sci. Rep. 3: 1–8.
Pearson, T.H. and R. Rosenberg. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Annu. Rev. 16: 229–311.
Pearson, T.H. and R. Rosenberg. 1987. Feast and famine: structuring factors in marine benthic communities. In: J.H.R. Gee and PS. Giller (eds), Organization of Communities, Blackwell Scientific Publications, Oxford, pp. 373–395.
Probert, PK. 1984. Disturbance, sediment stability, and trophic structure of soft-bottom communities. J. Mar. Res. 42: 893–921.
Proulx, R.S., D.E.L. Promislow and PC Phillips. 2005. Network thinking in ecology and evolution. Trends Ecol. Evol. 20: 345– 353.
Reizopoulou, S. and A. Nicolaidou. 2004. Benthic diversity of coastal brackish-water lagoons in western Greece. Aquatic Conserv.: Mar. Freshw. Ecosyst. 14: S93–S102.
Reizopoulou, S., M. Thessalou-Legaki and A. Nicolaidou. 1996. Assessment of disturbance in Mediterranean lagoons: an evaluation of methods. Mar. Biol. 125: 189–197.
Rogdakis, Y, A. Ramfos, K. Koukou, E. Dimitriou and G. Katselis. 2010. Feeding habits and trophic level of sea bass (Dicentrarchus labrax) in the Messolonghi-Etoliko lagoons complex (Western Greece). J. Biol. Res-Thessaloniki 13: 13–26.
Salas, F., C. Marcos, J.M. Neto, J. Patrı, A. Perez-Ruzafa and J.C Marques. 2006. User-friendly guide for using benthic ecological indicators in coastal and marine quality assessment. Ocean Coastal Manage. 49: 308–331.
Sanders, H.L. 1958. Benthic studies in Buzzards Bay. I. Animal-sediment relationships. Limnol. Oceanogr. 3: 245–358.
Santos, J.P, J. Castel and L.P Souza-Santos. 1997. Spatial distribution and dynamics of microphytobenthos biomass in the Gironde estuary (France). Oceanol. Acta 20: 549–556.
Sanz, A. 1986. Évolution des parametres de structure des peuple-ments annélidiens des fonds infralittoraux situés au large du bas-sin d’Arcachon. Cah. Biol. Mar. 27: 133–152.
Sarda, R., I. Valiela, and K. Foreman. 1996. Decadal shifts in a salt marsh macroinfaunal community in response to sustained long- term experimental nutrient enrichment. J. Exp. Mar. Biol. Ecol. 205: 63–81.
Schmera, D., T. Erős and J. Heino. 2013. Habitat filtering determines spatial variation of macroinvertebrate community traits in northern headwater streams. Community Ecol. 14: 77–88.
Scott, J. 2000. Social Network Analysis: A Handbook, 2nd ed. Sage Publications, New York.
Spaulding, M.L. 1994. Modeling of circulation and dispersion in coastal lagoons. In: B. Kjerfve (ed), Coastal Lagoon Processes, Elsevier, Amsterdam, pp. 103–131.
Stamou, G.P., M.D. Argyropoulou, M.A. Tsiafouli, N. Monokrousos, S.P. Sgardelis and E.M. Papatheodorou. 2011. The study of secondary successional patterns in soil using network analysis: The case of conversion from conventional to organic farming. Pedobiologia 54: 253–259.
Van Dolah, R.F. 1978. Factors regulating the distribution and population dynamics of the amphipod Gammarus palustris in an inter-tidal salt marsh community. Ecol. Monogr. 48: 191–217.
Vasas, V. and F. Jordán. 2006. Topological keystone species in ecological interaction networks: Considering link quality and non-trophic effects. Ecol. Model. 196: 365–378.
Wainright S.C., M.P. Weinstein, K.W. Able and C.A. Currin. 2000. Relative importance of benthic microalgae, phytoplankton and the detritus of smooth cordgrass Spartina alterniflora and the common reed Phragmites australis to brackish-marsh food webs. Mar. Ecol. Prog. Ser. 200: 77–91.
Walker, B.H. 1992. Biodiversity and ecological redundancy. Conserv. Biol. 6: 18–23.
Webb, P., R. Perissinotto and T.H. Wooldridge. 1987. Feeding of Mesopodopsis slabberi (Crustacea, Mysidacea) on naturally occurring phytoplankton. Mar. Ecol. Prog. Ser. 38: 115–123.
Wey, T., D.I. Blumstein, W. Shen and F. Jordán. 2008. Social network analysis on animal behaviour: a promising tool for the study of sociality. Anim. Behav. 75: 333–344.
Wright, R.A., L.B. Crowder and T.H. Martin. 1996. Selective predation by blue crabs on the gastropod, Bittium varium: Confrmation from opercula found in the sediments. Estuaries 19: 75–81.
Young, D.K. and D.C. Rhoads. 1971. Animal-sediment relations in Cape Cod Bay, Massachusetts. I. A transect study. Mar. Biol. 11: 242–254.
Ysebaert, T. and P.M.J. Herman. 2002. Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, internal soft-sediment environment. Mar. Ecol. Prog. Ser. 244: 105–124.
Zar, J.H. 1984. Biostatistical Analysis. 2nd edition. Prentice-Hall, New Jersey
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Paraskevopoulou, S., Monokrousos, N., Kappas, I. et al. Spatio-temporal variability of benthic macrofauna in a coastal lagoon assessed by ecological interaction networks. COMMUNITY ECOLOGY 16, 10–22 (2015). https://doi.org/10.1556/168.2015.16.1.2
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DOI: https://doi.org/10.1556/168.2015.16.1.2