Abstract
The Nile Deep-Sea Fan (NDSF) is located on the passive continental margin off Egypt and is characterized by the occurrence of active fluid seepage such as brine lakes, pockmarks and mud volcanoes. This study characterizes the structure of faunal assemblages of such active seepage systems of the NDSF. Benthic communities associated with reduced, sulphidic microhabitats such as sediments and carbonate crusts were sampled by remotely operated vehicles during two cruises in 2006 (BIONIL) and 2007 (MEDECO). Environmental conditions and biological factors including family-level faunal composition, density and diversity were measured at local and regional scales. Significant differences were detected at different spatial scales: (1) the fauna of reduced habitats differed substantially in activity, diversity and biomass from the non-seep environment at similar water depth, (2) cold seep microhabitats showed differences in community structure and composition related to substratum type as well as to the intensity and location of fluid emissions.
Similar content being viewed by others
References
Aloisi G, Bouloubassi I, Heijs SK, Pancost RD, Pierre C, Sinninghe Damste JS, Gottschal JC, Forney LJ, Rouchy JM (2002) CH4-consuming microorganisms and the formation of carbonate crusts at cold seeps. Earth Planet Sci Lett 203:195–203
Baker MC, Ramirez-Llodra EZ, Tyler P, German CR, Boetius A, Cordes EE, Dubilier N, Fisher CR, Levin LA, Metaxas A, Rowden AA, Santos RS, Shank TM, Van Dover CL, Young CM, Warén A (2010) Biogeography, ecology, and vulnerability of chemosynthetic ecosystems in the deep sea. In: McIntyre A (ed) Life in the World’s Oceans: Diversity, Distribution, and Abundance. Wiley-Blackwell, Hoboken, p 384
Bayon G, Henderson GM, Bohn M (2009a) U-Th stratigraphy of a cold seep carbonate crust. Chem Geol 260:47–56
Bayon G, Loncke L, Dupre S, Ducassou E, Duperron S, Etoubleau J, Foucher JP, Fouquet Y, Gontharet S, Huguen C, Klaucke I, Mascle J, Olu-Le Roy K, Ondreas H, Pierre C, Sibuet M, Stadnitskaia A, Woodside J (2009b) Multi-disciplinary investigations of fluid seepage on an unstable margin: the case of the central Nile deep sea fan. Mar Geol 261:92–104
Bellaiche G, Loncke L, Gaullier V, Mascle J, Courp T, Moreau A, Radan S, Sardou O (2001) The Nile cone and its channel system: new results after the Fanil cruise. Comptes Rendus De L’Academie Des Sciences Série II Fascicule a-Sciences De La Terre Et Des Planètes 333:399–404
Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jorgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626
Campbell KA (2006) Hydrocarbon seep and hydrothermal vent paleoenvironments and paleontology: past developments and future research directions. Palaeogeogr Palaeoclimatol Palaeoecol 232:362–407
Charlou JL, Donval JP, Zitter T, Roy N, Jean-Baptiste P, Foucher JP, Woodside J (2003) Evidence of methane venting and geochemistry of brines on mud volcanoes of the eastern Mediterranean Sea. Deep Sea Res Part I Oceanogr Res Pap 50:941–958
Cita MB, Ryan WBF, Paggi L (1981) Prometheus mud breccia. An example of shale diapirism in the western Mediterranean Ridge. Ann geol Des Pays Hell 13:37–49
Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458
Cordes EE, Becker EL, Hourdez S, Fisher CR (2010) Influence of foundation species, depth, and location on diversity and community composition at Gulf of Mexico lower-slope cold seeps. Deep Sea Res Part II Top Stud Oceanogr 57:1870–1881
de Beer D, Sauter E, Niemann H, Kaul N, Foucher JP, Witte U, Schlüter M, Boetius A (2006) In situ fluxes and zonation of microbial activity in surface sediments of the Hâkon Mosby mud volcano. Limnol Oceanogr 51:1315–1331
Dimitrov LI (2002) Mud volcanoes—the most important pathway for degassing deeply buried sediments. Earth Sci Rev 59:49–76
Duperron S, Halary S, Lorion J, Sibuet M, Gaill F (2008) Unexpected co-occurrence of six bacterial symbionts in the gills of the cold seep mussel Idas sp. (Bivalvia: Mytilidae). Environ Microbiol 10:433–445
Dupré S, Woodside J, Foucher JP, de Lange G, Mascle J, Boetius A, Mastalerz V, Stadnitskaia A, Ondreas H, Huguen C, Harmegnies FO, Gontharet S, Loncke L, Deville E, Niemann H, Omoregie E, Roy KOL, Fiala-Medioni A, Dahlmann A, Caprais JC, Prinzhofer A, Sibuet M, Pierre C, Sinninghe Damste JS (2007) Seafloor geological studies above active gas chimneys off Egypt (Central Nile deep sea fan). Deep Sea Res Part I Oceanogr Res Pap 54:1146–1172
Dupré S, Buffet G, Mascle J, Foucher JP, Gauger S, Boetius A, Marfia C (2008) High-resolution mapping of large gas emitting mud volcanoes on the Egyptian continental margin (Nile deep sea fan) by AUV surveys. Mar Geophys Res 29:275–290
Feseker T, Foucher JP, Harmegnies F (2008) Fluid flow or mud eruptions? Sediment temperature distributions on Håkon Mosby mud volcano, SW Barents Sea slope. Mar Geol 247:194–207
Foucher JP, Westbrook GK, Boetius A, Ceramicola S, Dupre S, Mascle J, Mienert J, Pfannkuche O, Pierre C, Praeg D (2009) Structure and drivers of cold seep ecosystems. Oceanography 22:92–109
Gauthier O, Sarrazin J, Desbruyères D (2010) Measure and mis-measure of species diversity in deep-sea chemosynthetic communities. Mar Ecol Prog Ser 402:285–302
Gini C (1912) Variabilità e Mutabilità. Tipographia di Paolo Cuppini, Bologna
Girnth A-C, Grünke S, Lichtschlag A, Felden J, Knittel K, Wenzhöfer F, de Beer D, Boetius A (2011) A novel, mat-forming Thiomargarita population associated with a sulfidic fluid flow from a deep-sea mud volcano. Environ Microbiol 13:495–505
Gontharet S, Pierre C, Blanc-Valleron MM, Rouchy JM, Fouquet Y, Bayon G, Foucher JP, Woodside J, Mascle J (2007) Nature and origin of diagenetic carbonate crusts and concretions from mud volcanoes and pockmarks of the Nile deep-sea fan (eastern Mediterranean Sea). Deep Sea Res Part II Top Stud Oceanogr 54:1292–1311
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Gray JS (2000) The measurement of marine species diversity, with an application to the benthic fauna of the Norwegian continental shelf. J Exp Mar Biol Ecol 250:23–49
Grünke S, Felden J, Lichtschlag A, Girnth AC, Wenzhöfer F, de Beer D, Boetius A (in press) Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold-seeps of the Nile deep sea fan (Eastern Mediterranean Sea). Geobiology 9
Hessler RR, Jumars PA (1974) Abyssal community analysis from replicate box cores in the central North Pacific. Deep Sea Res 21:185–209
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432
Hovland M, Svensen H (2006) Submarine pingoes: indicators of shallow gas hydrates in a pockmark at Nyegga, Norwegian Sea. Mar Geol 228:15–23
Hovland M, Gardner JV, Judd AG (2002) The significance of pockmarks to understanding fluid flow processes and geohazards. Geofluids 2:127–136
Hovland M, Svensen H, Forsberg CF, Johansen H, Fichler C, Fossa JH, Jonsson R, Rueslatten H (2005) Complex pockmarks with carbonate-ridges off mid-Norway: products of sediment degassing. Mar Geol 218:191–206
Hsu KJ, Montadert L, Bernoulli D, Cita MB, Erickson A, Garrison RE, Kidd RB, Melieres F, Muller C, Wright R (1977) History of Mediterranean salinity crisis. Nature 267:399–403
Huguen C, Mascle J, Woodside J, Zitter T, Foucher JP (2005) Mud volcanoes and mud domes of the Central Mediterranean Ridge: near-bottom and in situ observations. Deep Sea Res Part I Oceanogr Res Pap 52:1911
Huguen C, Foucher JP, Mascle J, Ondreas H, Thouement M, Stadnitskaia A, Pierre C, Bayon G, Loncke L, Boetius A, Bouloubassi I, De Lange G, Caprais JC, Fouquet Y, Woodside J, Dupre S, the NAUTINIL Scientific Party (2009) Menes Caldera, a highly active site of brine seepage in the Eastern Mediterranean Sea: “in situ” observations from the NAUTINIL expedition. Mar Geol 261:138–152
Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586
Jaccard P (1901) Distribution de la flore alpine dans le Bassin des Dranses et dans quelques régions voisines. Bulletin de la société vaudoise des sciences naturelles
Jackson DA (1995) PORTEST: a PROcustean randomization TEST of community environment concordance. Ecosciences 2:297–303
Jerosch K, Schluter M, Foucher JP, Allais AG, Klages M, Edy C (2007) Spatial distribution of mud flows, chemoautotrophic communities, and biogeochemical habitats at Hakon Mosby Mud Volcano. Mar Geol 243:1–17
Jost L (2006) Entropy and diversity. Oikos 113:363–375
Jost G (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439
Judd AG, Hovland M (2007) Seabed fluid flow—the impact on geology, biology and the marine environment
Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi
Kopf AJ (2002) Significance of mud volcanism. Rev Geophys 40:52
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280
Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn
Levin LA (2005) Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes oceanography and marine biology—an annual review, vol 43. Crc Press/Taylor & Francis Group, Boca Raton, pp 1–46
Levin LA, Mendoza GF (2007) Community structure and nutrition of deep methane-seep macrobenthos from the North Pacific (Aleutian) Margin and the Gulf of Mexico (Florida Escarpment). Mar Ecol Evol Perspect 28:131–151
Levin LA, Ziebis W, Mendoza GF, Growney VA, Tryon MD, Mahn C, Gieskes JM, Rathburn AE (2003) Spatial heterogeneity of macrofauna at northern California methane seeps: influence of sulfide concentration and fluid flow. MEPS 265:123–139
Levin LA, Mendoza GF, Gonzalez JP, Thurber AR, Cordes EE (2010) Diversity of bathyal macrofauna on the northeastern Pacific margin: the influence of methane seeps and oxygen minimum zones. Mar Ecol 31:94–110
Liu C, Whittaker RJ, Ma K, Malcolm JR (2007) Unifying and distinguishing diversity ordering methods for comparing communities. Popul Ecol 49:89–100
Loncke L, Mascle J, the Fanil Scientific Party (2004) Mud volcanoes, gas chimneys, pockmarks and mounds in the Nile deep-sea fan (Eastern Mediterranean): geophysical evidences. Mar Pet Geol 21:669
Macdonald IR, Reilly JF, Guinasso NL, Brooks JM, Carney RS, Bryant WA, Bright TJ (1990) Chemosynthetic mussels at a brine-filled pockmark in the Northern Gulf of Mexico. Science 248:1096–1099
Mascle J, Zitter T, Bellaiche G, Droz L, Gaullier V, Loncke L (2001) The Nile deep sea fan: preliminary results from a swath bathymetry survey. Mar Pet Geol 18:471–477
Mascle J, Sardou O, Loncke L, Migeon S, Camera L, Gaullier V (2006) Morphostructure of the Egyptian continental margin: Insights from swath bathymetry surveys. Mar Geophys Res 27:49–59
Menot L, Galéron J, Olu K, Caprais JC, Crassous P, Khripounoff A, Sibuet M (2010) Spatial heterogeneity of macrofaunal communities in and near a giant pockmark area in the deep Gulf of Guinea. Mar Ecol 31:78–93
Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, Knittel K, Gieseke A, Peterknecht K, Pape T, Boetius A, Amann R, Jorgensen BB, Widdel F, Peckmann JR, Pimenov NV, Gulin MB (2002) Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297:1013–1015
Milkov AV (2000) Worldwide distribution of submarine mud volcanoes and associated gas hydrates. Mar Geol 167:29–42
Niemann H, Losekann T, de Beer D, Elvert M, Nadalig T, Knittel K, Amann R, Sauter EJ, Schluter M, Klages M, Foucher JP, Boetius A (2006) Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink. Nature 443:854–858
Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2008) Vegan: community ecology package. R package version 1.15-1. http://cran.r-project.org/, http://vegan.r-forge.r-project.org/
Olu K, Lance S, Sibuet M, Henry P, Fiala-Medioni A, Dinet A (1997) Cold seep communities as indicators of fluid expulsion patterns through mud volcanoes seaward of the Barbados accretionary prism. Deep Sea Res Part I Oceanogr Res Pap 44:811
Olu-Le Roy K, Sibuet M, Fiala-Medioni A, Gofas S, Salas C, Mariotti A, Foucher J-P, Woodside J (2004) Cold seep communities in the deep eastern Mediterranean Sea: composition, symbiosis and spatial distribution on mud volcanoes. Deep Sea Res Part I Oceanogr Res Pap 51:1915
Olu-Le Roy K, Caprais JC, Fifis A, Fabri MC, Galeron J, Budzinsky H, Le Menach K, Khripounoff A, Ondreas H, Sibuet M (2007) Cold-seep assemblages on a giant pockmark off West Africa: spatial patterns and environmental control. Mar Ecol Evol Perspect 28:115–130
Omoregie EO, Mastalerz V, de Lange G, Straub KL, Kappler A, Roy H, Stadnitskaia A, Foucher JP, Boetius A (2008) Biogeochemistry and community composition of iron- and sulfur-precipitating microbial mats at the Chefren mud volcano (Nile deep sea fan, Eastern Mediterranean). Appl Environ Microbiol 74:3198–3215
Patil GP, Taillie C (1982) Diversity as a concept and its measurement. J Am Stat Assoc 77:548–561
Paull CK, Hecker B, Commeau R, Freeman-Lynde RP, Neumann C, Corso WP, Golubic S, Hook JE, Sikes E, Curray J (1984) Biological communities at the Florida Escarpment resemble hydrothermal vent taxa. Science 226:965–967
Paull CK, Ussler W, Holbrook WS, Hill TM, Keaten R, Mienert J, Haflidason H, Johnson JE, Winters WJ, Lorenson TD (2008) Origin of pockmarks and chimney structures on the flanks of the Storegga Slide, offshore Norway. Geo-Mar Lett 28:43–51
Pielou EC (1969) An introduction to mathematical ecology, New York
R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ritt B, Sarrazin J, Caprais J-C, Noël P, Gauthier O, Pierre C, Henry P, Desbruyères D (2010) First insights into the structure and environmental setting of cold-seep communities in the Marmara Sea. Deep Sea Res Part I Oceanogr Res Pap 57:1120–1136
Ritt B, Desbruyeres D, Caprais JC, Khripounoff A, Le Gall C, Gauthier O, Buscail R, Olu K, Sarrazin J (in preparation) Cold seep communities in the deep eastern Mediterranean Sea: composition, spatial patters and environmental control on the Mediterranean Ridge mud volcanoes
Rouse GW, Fauchald K (1997) Cladistics and polychaetes. Zoologica Scripta 26:139–204
Rouse GW, Pleijel F (2001) Polychaetes. Oxford University Press, Oxford
Sahling H, Rickert D, Lee RW, Linke P, Suess E (2002) Macrofaunal community structure and sulfide flux at gas hydrate deposits from the Cascadia convergent margin, NE Pacific. Mar Ecol Prog Ser 231:121–138
Salas C, Woodside J (2002) Lucinoma kazani n. sp. (Mollusca: Bivalvia): evidence of a living benthic community associated with a cold seep in the Eastern Mediterranean Sea. Deep Sea Res Part I Oceanogr Res Pap 49:991–1005
Sanders HL (1968) Marine benthic diversity: a comparative study. Am Nat 102:243–282
Sarradin PM, Caprais JC (1996) Analysis of dissolved gases by headspace sampling gas chromatography with column and detector switching. Preliminary results. Anal Commun 33:371–373
Sarradin PM, Waeles M, Bernagout S, Le Gall C, Sarrazin J, Riso R (2009) Speciation of dissolved copper within an active hydrothermal edifice on the Lucky Strike vent field (MAR, 37° N). Sci Total Environ 407:869–878
Sarrazin J, Juniper SK (1999) Biological characteristics of a hydrothermal edifice mosaic community. Mar Ecol Prog Ser 185:1–19
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423
Sibuet M, Olu K (1998) Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep Sea Res Part II Top Stud Oceanogr 45:517
Simpson EH (1949) Measurement of diversity. Nature 163:688
Smith EB, Scott KM, Nix ER, Korte C, Fisher CR (2000) Growth and condition of seep mussels (Bathymodiolus childressi) at a Gulf of Mexico Brine Pool. Ecology 81:2392–2403
Sommer S, Linke P, Pfannkuche O, Niemann H, Treude T (2009) Benthic respiration in a seep habitat dominated by dense beds of ampharetid polychaetes at the Hikurangi Maring (new Zealand). Mar Geol. doi:10.1016/j.margo.2009.06.003
Southward EC, Andersen AC, Hourdez S (in press) Lamellibrachia anaximandri n. sp., a new vestimentifera tubeworm from the Mediterranean (Annelida). Zoosystema
Thistle D (2003) The deep-sea floor: an overview ecosystems of the deep ocean. Elsevier Science Bv, Amsterdam, pp 5–37
Tothmérész B (1998) On the characterization of scale-dependant diversity. Abstracta Bonatica 22:149–156
Treude T, Smith CR, Wenzhöfer F, Carney E, Bernardino AF, Hannides AK, Krüger M, Boetius A (2009) Biogeochemistry of a deep-sea whale-fall: sulfate reduction, sulfide efflux and methanogenesis. Mar Ecol Prog Ser 382:1–21
Van Gaever S, Moodley L, de Beer D, Vanreusel A (2006) Meiobenthos at the Arctic Håkon Mosby Mud Volcano, with a parental-caring nematode thriving in sulphide-rich sediments. Mar Ecol Prog Ser 321:143–155
Werne JP, Haese RR, Zitter T, Aloisi G, Bouloubassi I, Heijs S, Fiala-Medioni A, Pancost RD, Sinninghe Damste JS, de Lange G (2004) Life at cold seeps: a synthesis of biogeochemical and ecological data from Kazan mud volcano, eastern Mediterranean Sea. Chem Geol 205:367
Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279
Zitter TAC, Woodside JM, Mascle J (2003) The Anaximander Mountains: a clue to the tectonics of southwest Anatolia. Geol J 38:375–394
Zitter TAC, Huguen C, Woodside JM (2005) Geology of mud volcanoes in the eastern Mediterranean from combined sidescan sonar and submersible surveys. Deep Sea Res Part I Oceanogr Res Pap 52:457–475
Acknowledgments
The captains and crews of the R/V Meteor and R/V Pourquoi pas? as well as the pilots of the ROV Quest4000 and Victor6000 are warmly acknowledged for their dedicated assistance and for contributing to the success of the two cruises. The chief scientists of the two cruises were A Boetius (BIONIL 2006) and C. Pierre (MEDECO leg 2). The faunal samples were identified by a network of taxonomists from the Muséum National d’Histoire Naturelle de Paris (France), the German Centre for Marine Biodiversity Research (Germany), the University of Lodz (Poland), the Russian Academy of Sciences of Moscow, the Kamchatka Branch of the Pacific Institute of Geography of Petropavlovsk-Kamchatsky and the Institute of Marine Biology of Vladivostok (Russia). Biogeochemical analyses were supported by Viola Beier, Tomas Wilkop, Janine Felden, Anna Lichtschlag and Dirk de Beer (MPI for Marine Microbiology). The bathymetric maps were made with the data acquired and processed by Jean Mascle (Géosciences Azur) and Stéphanie Dupré (Ifremer). The first version of the manuscript was professionally edited by Carolyn Engel-Gautier. BR’s thesis was entirely funded by the French Institute for the Exploitation of the Sea (Ifremer). This research project benefited from funds from the HERMES and HERMIONE European projects (contract # 511234 and #226354) as well as from the ANR DEEP-OASES (ANR06BDV005) and support from the GDR ECCHIS. Additional funds were available from the DFG (METEOR expedition M70-2) and from the Max Planck Society.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by M. Kühl.
Rights and permissions
About this article
Cite this article
Ritt, B., Pierre, C., Gauthier, O. et al. Diversity and distribution of cold-seep fauna associated with different geological and environmental settings at mud volcanoes and pockmarks of the Nile Deep-Sea Fan. Mar Biol 158, 1187–1210 (2011). https://doi.org/10.1007/s00227-011-1679-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-011-1679-6