Patterns of benthic diversity in marine underwater caves of the Marseille Region (France, North-Western Mediterranean Sea)


Veröffentlicht: Οκτ 30, 2024
MARIE DERRIEN
PIERRE CHEVALDONNÉ
THIERRY PÉREZ
Abstract

Underwater caves are remarkable habitats of the Mediterranean Sea. In the present study, we compare the geomorphology of four underwater caves of the Marseille area and the associated sessile assemblages across two contrasted communities (Semi- Dark and Dark-cave communities). Using a non-destructive method of sampling, photoquadrats of the walls of the caves were performed in 2020 to assess the biodiversity and the structure of these communities. In addition, taking advantage of available reference data from 2015, we evaluate the changes in sponge assemblages for the period 2015-2020, focusing on observations of the Semi-Dark cave community. Our results illustrate how the diversity of environmental settings and cave morphologies shape the benthic community composition of the four caves. In all four caves, the Semi-Dark community is the more diverse and harbours the higher number of species when compared to the Dark community. Each cave presents a different species assemblage with in most cases, distinct dominant species which highlight the singularity of each cave. Moreover, our temporal change assessment demonstrates a critical decrease in sponge species richness for all caves, possibly related to the increasing frequency of marine heatwaves that have occurred in the last decade. Although some species (mostly in the Keratosa subclass) seem to be particularly affected, other species such as Chondrosia reniformis appear to have benefitted from the situation. Our findings underline the importance of biodiversity monitoring in a context of a rapidly changing environment, in particular in poorly resilient marine ecosystems such as underwater caves.

Article Details
  • Rubrik
  • Research Article
Downloads
Keine Nutzungsdaten vorhanden.
Literaturhinweise
Balduzzi, A., Cattaneo, R., 1985. Estimation par relèvements photographiques de la distribution de Miniacina miniacea (Sarcomastigophora, Foraminiferida) dans une grotte sous-marine du Golfe de Naples. Rapports de la Commission Internationale pour la Mer Méditerranée, 29 (5), 127-129.
Bell, J.J., 2002. The Sponge Community in a Semi-Submerged Temperate Sea Cave: Density, Diversity and Richness. Marine Ecology, 23 (4), 297-311. Bell, J.J., 2008. The functional roles of marine sponges. Estuarine, Coastal and Shelf Science, 79 (3), 341-353.
Bertolino, M., Betti, F., Bo, M., Cattaneo-Vietti, R., Pansini, M. et al., 2016. Changes and stability of a Mediterranean hard bottom benthic community over 25 years. Journal of the Marine Biological Association of the United Kingdom, 96 (2), 341-350.
Bianchi, C.N., Morri, C., 1994. Studio bionomico comparativo di alcune grotte marine sommerse; definizione di una scala di confinamento. Memorie dell’Istituto italiano di Speleologia, 6, 107-123.
Bianchi, C.N., Morri, C., 2000. Marine Biodiversity of the Mediterranean Sea: Situation, Problems and Prospects for Future Research. Marine Pollution Bulletin, 40 (5), 367-376.
Bibiloni, M.A., Uriz, M.J., Gili, J.M., 1989. Sponge communities in three submarine caves of the Balearic Islands (western Mediterranean): adaptations and faunistic composition. Marine Ecology – Pubblicazioni della Stazione Zoologica di Napoli I, 10, 317-334.
Boury-Esnault, N., Rützler, K., 1997. Thesaurus of sponge morphology. Smithsonian Contributions to Zoology, 596, 1-55.
Bussotti, S., Terlizzi, A., Fraschetti, S., Belmonte, G., Boero, F., 2006. Spatial and temporal variability of sessile benthos in shallow Mediterranean marine caves. Marine Ecology Progress Series, 325, 109-119.
Cárdenas, P., Vacelet, J., Chevaldonné, P., Pérez, T., Xavier, J.R., 2018. From marine caves to the deep sea, a new look at Caminella (Demospongiae, Geodiidae) in the Atlanto-Mediterranean region. Zootaxa, 4466 (1), 174-196.
Castelbon, C., 1972. Etude de la circulation des masses d’eau dans le golfe de Marseille. Téthys, 4, 269-312.
Chevaldonné, P., Lejeusne, C., 2003. Regional warming‐induced species shift in north‐west Mediterranean marine caves. Ecology Letters, 6 (4), 371-379.
Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F. et al., 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS ONE, 5 (8), e11842.
Corriero, G., Scalera Liaci, L., Ruggiero, D., Pansini, M., 2000. The Sponge Community of a Semi‐Submerged Mediterranean Cave. Marine Ecology, 21 (1), 85-96.
Costa, G., Bavestrello, G., Micaroni, V., Pansini, M., Strano, F. et al., 2019. Sponge community variation along the Apulian coasts (Otranto Strait) over a pluri-decennial time span. Does water warming drive a sponge diversity increasing in the Mediterranean Sea? Journal of the Marine Biological Association of the United Kingdom, 99 (7), 1519-1534.
Costa, G., Betti, F., Nepote, E., Cattaneo-Vietti, R., Pansini, M. et al., 2018. Sponge community variations within two semi-submerged caves of the Ligurian Sea (Mediterranean Sea) over a half-century time span. The European Zoological Journal, 85 (1), 381-391.
De Cáceres, M., Sol, D., Lapiedra, O., Legendre, P., 2011. A framework for estimating niche metrics using the resemblance between qualitative resources. Oikos, 120 (9), 1341-1350.
Digenis, M., Arvanitidis, C., Dailianis, T., Gerovasileiou, V., 2022. Comparative Study of Marine Cave Communities in a Protected Area of the South-Eastern Aegean Sea, Greece. Journal of Marine Science and Engineering, 10 (5), 660.
Dimarchopoulou, D., Gerovasileiou, V., Voultsiadou, E., 2018. Spatial variability of sessile benthos in a semi-submerged marine cave of a remote Aegean Island (eastern Mediterranean Sea). Regional Studies in Marine Science, 17, 102-111.
Fichez, R. 1989. Phénomènes d’oligotrophie en milieu aphotique. Étude des grottes sous-marines, comparaison avec les milieux profonds et bilans énérgetiques. Thèse de Doctorat, Université d’Aix-Marseille II, France.
Fichez, R., 1991. Suspended particulate organic matter in a Mediterranean submarine cave. Marine Biology, 108 (1), 167-174.
Garrabou, J., Zabala, M., 2001. Growth Dynamics in Four Mediterranean Demosponges. Estuarine, Coastal and Shelf Science, 52 (3), 293-303.
Garrabou, J., Coma, R., Bensoussan, N., Bally, M., Chevaldonné, P. et al., 2009. Mass mortality in Northwestern Mediterranean rocky benthic communities: Effects of the 2003 heat wave. Global Change Biology, 15 (5), 1090-1103.
Garrabou, J., Gómez-Gras, D., Medrano, A., Cerrano, C., Ponti, M. et al., 2022. Marine heatwaves drive recurrent mass mortalities in the Mediterranean Sea. Global Change Biology, 28 (19), 5708-5725.
Gauff, R.P.M., Davoult, D., Greff, S., Bohner, O., Coudret, J. et al., 2022. Pollution gradient leads to local adaptation and small-scale spatial variability of communities and functions in an urban marine environment. Science of The Total Environment, 838, 155911.
Gerovasileiou, V., Voultsiadou, E., 2012. Marine Caves of the Mediterranean Sea: A Sponge Biodiversity Reservoir within a Biodiversity Hotspot. PLoS one, 7 (7), e39873.
Gerovasileiou, V., Voultsiadou, E., 2016. Sponge diversity gradients in marine caves of the eastern Mediterranean. Journal of the Marine Biological Association of the United Kingdom, 96 (2), 407-416.
Gerovasileiou, V., Bianchi, C.N., 2021. Mediterranean Marine Caves: A Synthesis of Current Knowledge. Oceanography and Marine Biology: An Annual Review, 59, 1-88.
Gerovasileiou, V., Dimitriadis, C., Arvanitidis, C., Voultsiadou, E., 2017. Taxonomic and functional surrogates of sessile benthic diversity in Mediterranean marine caves. PLoS one, 12 (9), e0183707.
Giakoumi, S., Sini, M., Gerovasileiou, V., Mazor, T., Beher, J. et al., 2013. Ecoregion-Based Conservation Planning in the Mediterranean: Dealing with Large-Scale Heterogeneity. PLoS ONE, 8 (10), e76449.
Gómez-Gras, D., Linares, C., de Caralt, S., Cebrian, E., Frleta- Valić, M. et al., 2019. Response diversity in Mediterranean coralligenous assemblages facing climate change: Insights from a multispecific thermotolerance experiment. Ecology and Evolution, 9 (7), 4168-4180.
Goodwin, C., Rodolfo‐Metalpa, R., Picton, B., Hall‐Spencer, J.M., 2014. Effects of ocean acidification on sponge communities. Marine Ecology, 35 (s1), 41-49.
Grenier, M., Ruiz, C., Fourt, M., Santonja, M., Dubois, M. et al., 2018. Sponge inventory of the French Mediterranean waters, with an emphasis on cave-dwelling species. Zootaxa, 4466 (1), 205-228.
Grenier, M., Idan, T., Chevaldonné, P., Pérez, T., 2023. Mediterranean marine keystone species on the brink of extinction. Global Change Biology, 29 (7), 1681-1683.
Harmelin, J.-G., 1969. Bryozoaires des grottes sous-marines obscures de la région marseillaise, faunistique et écologie. Téthys, 1, 793-806.
Harmelin, J.-G. 1985. Bryozoan dominated assemblages in Mediterranean cryptic environments. p. 143. In: Bryozoa: Ordovician to recent, C. Nielsen & G. P. Larwood (Eds). Olsen & Olsen, Fredensborg.
Harmelin, J.-G., Vacelet, J., 1997. Clues to deep-sea biodiversity in a nearshore cave. Vie et Milieu, 47, 351-354.
Harmelin, J. G., Vacelet J., Vasseur, P., 1985. Les grottes sous-marines obscures : Un milieu extrême et un remarquable biotope refuge. Téthys, 11, 214-229.
Harmelin, J.-G., 2000. Ecology of cave and cavity dwelling bryozoans. p. 38–55. In: Proceedings of the 11th International Bryozoology Association Conference, C.A. Herrera & J.B.C. Jackson (Eds). Smithsonian Tropical Research Institute, Panama.
Harmelin, J.-G., Boury-Esnault, N., Fichez, R., Vacelet, J., Zibrowius, H., 2003. Peuplement de la grotte sous-marine de l’ile de Bagaud (Parc National de Port-Cros, France, Méditerranée). Scientific Reports of the Port-Cros National Park, 19, 117-134.
Idan, T., Goren, L., Shefer, S., Brickner, I., Ilan, M., 2020. Does Depth Matter? Reproduction Pattern Plasticity in Two Common Sponge Species Found in Both Mesophotic and Shallow Waters. Frontiers in Marine Science, 7, 610565.
Laborel, J., Vacelet, J., 1958. Étude des peuplements d’une grotte sous-marine du Golfe de Marseille. Bulletin de l’Institut Océanographique de Monaco, 55 (1120), 1-20.
Laborel, J., Vacelet, J., 1959. Les grottes sous-marines obscures en Méditerranée. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences, 248, 2619-2621.
Laborel, J., 1960. Contribution à l’étude des peuplements benthiques sciaphiles sur substrat rocheux en Méditerranée. Recueil des Travaux de la Station Marine d’Endoume, 20 (33), 117-173.
Lejeusne, C., Chevaldonné, P., 2006. Brooding crustaceans in a highly fragmented habitat: The genetic structure of Mediterranean marine cave-dwelling mysid populations. Molecular Ecology, 15 (13), 4123-4140.
Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C.F., Pérez, T., 2010. Climate change effects on a miniature ocean: The highly diverse, highly impacted Mediterranean Sea. Trends in Ecology & Evolution, 25 (4), 250-260.
Longo, C., Giménez, G., Miscioscia, F., Corriero, G., 2023. Sponge Fauna of the Apulian Marine Caves (Southern Italy): Current State of Knowledge. Diversity, 15 (5), 641.
Manconi, R., Ledda, F.D., Serusi, A., Corso, G., Stocchino, G.A., 2009. Sponges of marine caves: Notes on the status of the Mediterranean palaeoendemic Petrobiona massiliana (Porifera: Calcarea: Lithonida) with new records from Sardinia. Italian Journal of Zoology, 76 (3), 306-315.
Manconi, R., Cadeddu, B., Ledda, F., Pronzato, R., 2013. An overview of the Mediterranean cave-dwelling horny sponges (Porifera, Demospongiae). ZooKeys, 281, 1-68.
Martí, R., Uriz, M.J., Ballesteros, E., Turon, X., 2004. Benthic assemblages in two Mediterranean caves: Species diversity and coverage as a function of abiotic parameters and geographic distance. Journal of the Marine Biological Association of the United Kingdom, 84 (3), 557-572.
Michez, N., Aish, A., Amouroux, J-M., Bellan, G., Bellan-Santini, D. et al., 2017. Inventaire national du patrimoine naturel (INPN). https://inpn.mnhn.fr/habitat/cd_hab/978/tab/ especes (Accessed 2 August 2024).
Millet, J., 1977. Levés des grottes immergées sur les côtes de la Provence, de Carry-le-Rouet à Bandol. DRASM / Laboratoire de Géologie et de Paléontologie du Quaternaire, Marseille, France.
Nepote, E., Bianchi, C.N., Morri, C., Ferrari, M., Montefalcone, M., 2017. Impact of a harbour construction on the benthic community of two shallow marine caves. Marine Pollution Bulletin, 114 (1), 35-45.
Oksanen, J., Blanchet, F-G., Kindt, R., Legendre, P., Minchin, P.R. et al., 2018. Vegan: Community ecology package. R package version 2.5-2. https://cran.r-project.org/web/packages/ vegan/index.html (Accessed on July 23, 2024).
Parravicini, V., Guidetti, P., Morri, C., Montefalcone, M., Donato, M. et al., 2010. Consequences of sea water temperature anomalies on a Mediterranean submarine cave ecosystem. Estuarine, Coastal and Shelf Science, 86 (2), 276-282.
Pérès, J.M., Picard, J., 1949. Notes sommaires sur le peuplement des grottes sous-marines de la région de Marseille. Comptes Rendus de la Société de Biogéographie, 227, 42-45.
Pérès, J.M., Picard, J., 1964. Nouveau manuel de bionomie benthique de la Mer Méditerranée. Recueil des Travaux de la Station Marine d’Endoume 47, 3-137. Pérès, J.M., 1967. Mediterranean benthos. Oceanography and Marine Biology: An Annual Review 5, 449-533.
Pérez, T., Garrabou, J., Sartoretto, S., Harmelin, J.-G., Francour, P. et al., 2000. Mortalité massive d’invertébrés marins: Un événement sans précédent en Méditerranée Nord - Occidentale. Comptes Rendus de l’Académie des Sciences - Series III - Sciences de la Vie, 323 (10), 853-865.
Pérez, T., Wafo, E., Fourt, M., Vacelet, J., 2003. Marine Sponges as Biomonitor of Polychlorobiphenyl Contamination: Concentration and Fate of 24 Congeners. Environmental Science & Technology, 37 (10), 2152-2158.
Pérez, T., Ivanisevic, J., Dubois, M., Pedel, L., Thomas, O.P. et al., 2011. Oscarella balibaloi, a new sponge species (Homoscleromorpha: Plakinidae) from the Western Mediterranean Sea: cytological description, reproductive cycle and ecology. Marine Ecology, 32 (2), 174-187.
Pérez, T., Albenga, L., Starmer, J., Chevaldonné, P., 2016. Biodiversité des grottes sous-marines des îles Marquises: Un patrimoine naturel caché et méconnu. pp. 287-310. In: Biodiversité terrestre et marine des îles Marquises, Polynésie française. Galzin R., Duron S.-D. & Meyer J.-Y. (Eds). Société Française d’Ichtyologie, Paris.
Pérez, T., Díaz, M.-C., Ruiz, C., Cóndor-Luján, B., Klautau, M. et al., 2017. How a collaborative integrated taxonomic effort has trained new spongiologists and improved knowledge of Martinique Island (French Antilles, eastern Caribbean Sea) marine biodiversity. PLOS ONE, 12 (3), e0173859.
Pouliquen, L., 1972. Les spongiaires des grottes sous-marines de la région de Marseille : écologie et systématique. Téthys, 3 (4), 717-758.
Radolović, M., Bakran-Petricioli, T., Petricioli, D., Surić, M., Perica, D., 2015. Biological response to geochemical and hydrological processes in a shallow submarine cave. Mediterranean Marine Science, 16 (2), 305-324.
Rastorgueff, P., Harmelin-Vivien, M., Richard, P., Chevaldonné, P., 2011. Feeding strategies and resource partitioning mitigate the effects of oligotrophy for marine cave mysids. Marine Ecology Progress Series, 440, 163-176.
Rastorgueff, P.-A., Chevaldonné, P., Arslan, D., Verna, C., Lejeusne, C., 2014. Cryptic habitats and cryptic diversity: Unexpected patterns of connectivity and phylogeographical breaks in a Mediterranean endemic marine cave mysid. Molecular Ecology, 23 (11), 2825-2843.
Rosso, A., Gerovasileiou, V., Sanfilippo, R., Guido, A., 2019. Bryozoan assemblages from two submarine caves in the Aegean Sea (Eastern Mediterranean). Marine Biodiversity, 49, 707-726.
Sarà, M., 1968. Stratification d’éponges à recouvrement total dans certaines grottes du niveau superficiel. Rapport Commission Internationale sur la Mer Méditerranée 19 (2), 83-85.
Topçu, N.E., Pérez, T., Grégori, G., Harmelin-Vivien, M., 2010. In situ investigation of Spongia officinalis (Demospongiae) particle feeding: Coupling flow cytometry and stable isotope analysis. Journal of Experimental Marine Biology and Ecology, 389 (1-2), 61-69.
Trygonis, V., Sini, M., 2012. photoQuad: A dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. Journal of Experimental Marine Biology and Ecology, 424-425, 99-108.
Vacelet, J., 1959. Répartition générale des éponges et systématique des éponges cornées de la région de Marseille et de quelques stations méditerranéennes. Recueil des Travaux de la Station Marine d’Endoume, 16 (26), 39-101.
Vacelet, J., 1976. Les spongiaires des grottes sous-marines obscures de la Méditerranée et des régions tropicales. Pubblicazioni della Stazione Zoologica di Napoli, 40 (2), 506-515.
Vacelet J., Boury-Esnault N., Harmelin J.G., 1994. Hexactinellid cave, a unique habitat in the scuba zone. Deep Sea Research Part I, 41, 965-973.
Vacelet J., Boury-Esnault N., Harmelin J.G., 1995. Carnivorous sponges. Nature, 373, 333-335.
Vacelet, J., Boury-Esnault, N., 1996. A new species of carnivorous sponge (Demospongiae: Cladorhizidae) from a Mediterranean cave. Bulletin de l’Institut royal des Sciences naturelles de Belgique, Biologie, 66, 109-115.
Vasseur, P., 1984. Les peuplements sessiles sciaphiles des récifs coralliens de la région de Tuléar (S.W. de Madagascar). Oceanis, Paris, 10 (1), 51-83.
Verdura, J., Linares, C., Ballesteros, E., Coma, R., Uriz, M.J. et al., 2019. Biodiversity loss in a Mediterranean ecosystem due to an extreme warming event unveils the role of an engineering gorgonian species. Scientific Reports, 9 (1), 5911.
Zibrowius, H., 1978. Les scléractiniaires des grottes sous-marines en Méditerranée et dans l’Atlantique Nord - Oriental (Portugal, Madère, Canaries, Açores). Pubblicazioni della Stazione Zoologica di Napoli, 40, 516-545.
Zibrowius, H., 1980. Les Scléractiniaires de la Méditerranée et de l’Atlantique Nord - Oriental Mémoires de l’Institut Océanographique de Monaco, 11, 284.