Seasonal variability of epipelic microphytobenthos community in two subtidal areas of the Northern Adriatic Sea
Published:
Oct 14, 2024
Keywords:
Benthic diatoms Adriatic Sea diatom life forms subtidal epipelon microphytobenthos
Abstract
We investigated the biodiversity and seasonality of subtidal benthic diatoms at two sites of the Northern Adriatic Sea differently affected by anthropogenic inputs. Sediment samples were collected seasonally, and diatom cells were then separated from the sediment using the density gradient centrifugation method. The total abundance of benthic diatoms ranged between 4,409 ± 1,638 and 77,663 ± 30,415 cells cm-2 and the biomass between 0.41 ± 0.22 and 3.66 ± 2.01 μg C cm-2. At both stations, the benthic diatoms showed a marked seasonal pattern, with maximum abundance, biomass and biodiversity in spring and minimum in summer. Motile life forms, such as Navicula, Nitzschia, Fallacia, and Psammodictyon, dominated in terms of abundance at both stations throughout the study period, while plocon (centric diatoms mainly belonging to Biddulphiaceae) increased under mixing conditions, when they represented the largest contributor to biomass. At both stations and in all seasons, the Si:N:P ratio highlighted the strong P limitation, typical of the Adriatic Sea. The ammonium concentration was the highest component of DIN in spring and summer when we observed the highest and lowest MPB abundance respectively. The preference of diatoms for ammonia, coupled with the increased daylight period, may have enhanced the spring growth, whereas in summer the hypoxic conditions may have caused a decrease. Despite the different environmental conditions, the two stations exhibited similar species compositions and seasonal trends, highlighting relative stability against anthropogenic pressures of a different nature.
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MULE, A., NERI, F., ROMAGNOLI, T., ACCORONI, S., CARIDI, F., CAMPANELLI, A., UBALDI, M., SARNO, D., & TOTTI, C. (2024). Seasonal variability of epipelic microphytobenthos community in two subtidal areas of the Northern Adriatic Sea. Mediterranean Marine Science, 25(3), 650–665. https://doi.org/10.12681/mms.35785
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References
Accoroni, S., Romagnoli, T., Pichierri, S., Totti, C., 2016. Effects of the bloom of harmful benthic dinoflagellate Ostreopsis cf. ovata on the microphytobenthos community in the northern Adriatic Sea. Harmful Algae, 55, 179-190.
Accoroni, S., Totti, C., Razza, E., Congestri, R., Campanelli, A. et al., 2017. Phosphatase activities of a microepiphytic community during a bloom of Ostreopsis cf. ovata in the northern Adriatic Sea. Water Research, 120, 272-279.
Armbrust, E.V., 2009. The life of diatoms in the world’s oceans. Nature, 459, 185-192. Artegiani, A., Bregant, D., Paschini, E., Pinardi, N., Raicich, F. et al., 1997. The Adriatic Sea general circulation. Part I: air-sea interactions and water mass structure. Journal of Physical Oceanography, 27, 1492-1514.
Balsamo, M., Albertelli, G., Ceccherelli, V.U., Coccioni, R., Colangelo, M.A. et al., 2010. Meiofauna of the Adriatic Sea: present knowledge and future perspectives. Chemistry and Ecology, 26, 45-63.
Barranguet, C., Kromkamp, J., Peene, J., 1998. Factors controlling primary production and photosynthetic characteristics of intertidal microphytobenthos. Marine Ecology Progress Series, 173, 117-126.
Bérard-Therriault, L., Cardinal, A., Poulin, M., 1986. Les diatomées (Bacillariophyceae) benthiques de substrats durs des eaux marines et saumâtres du Québec. 6. Naviculales: Cymbellaceae et Gomphonemaceae. Le Naturaliste Canadien, 113, 405-429.
Bernardi Aubry, F., Acri, F., Bastianini, M., Finotto, S., Pugnetti, A., 2022. Differences and similarities in the phytoplankton communities of two coupled transitional and marine ecosystems (the Lagoon of Venice and the Gulf of Venice - Northern Adriatic Sea). Frontiers in Marine Science, 9, 974967.
Blackford, J.C., 2002. The influence of microphytobenthos on the Northern Adriatic ecosystem: A modelling study. Estuarine Coastal and Shelf Science, 55 (1), 109-123.
Blasutto, O., Cibic, T., de Vittor, C., Fonda Umani, S., 2005. Microphytobenthic primary production and sedimentary carbohydrates along salinity gradients in the Lagoons of Grado and Marano (Northern Adriatic Sea). Hydrobiologia, 550 (1), 47-55.
Brzezinski, M.A., 1985. The Si:C:N ratio of marine diatoms: interspecific variability and the effect of some environmental variables. Journal of Phycology, 21, 347-357.
Cahoon, L., 1999. The role of benthic microalgae in neritic ecosystems. Oceanography and Marine Biology, 37, 47-86.
Campanelli, A., Grilli, F., Paschini, E., Marini, M., 2011. The influence of an exceptional Po River flood on the physical and chemical oceanographic properties of the Adriatic Sea. Dynamics of Atmospheres and Oceans, 52 (1-2), 284-297.
Car, A., Hafner, D., Ljubimir, S., Radić, I.D., Bobanović-Ćolić S. et al., 2020. Colonization of bacteria and diatoms on an artificial substrate in a marine lake (eastern Adriatic Sea, NE Mediterranean). Acta Botanica Croatica, 79 (2), 212-227.
Car, A, Hafner, D., Dupčić Radić I., Kaleli, A., Ljubimir, S. et al., 2021. Comparison of benthic diatom community structures on natural and artificial substrates in marine lake (Adriatic Sea). Acta Adriatica, 62 (1), 21-44.
Cardinal, A., Poulin, M., Bérard-Therriault, L. 1984. Les diatomées benthiques de substrats durs des eaux marines et saumâtres du Québec 4. Naviculales, Naviculaceae (à l’exclusion des genres Navicula, Donkinia, Gyrosigma et Pleurosigma). Le Naturaliste Canadien, 111 (4), 369-394.
Cerino, F., Fornasaro, D., Kralj, M., Giani, M., Cabrini, M., 2019. Phytoplankton temporal dynamics in the coastal waters of the north-eastern Adriatic Sea (Mediterranean Sea) from 2010 to 2017. Nature Conservation, 34, 343-372.
Cibic, T., Blasutto, O., Falconi, C., Fonda Umani, S., 2007. Microphytobenthic biomass, species composition and nutrient availability in sublittoral sediments of the Gulf of Trieste (northern Adriatic Sea). Estuarine Coastal and Shelf Science, 75 (1-2), 50-62.
Cibic, T., Comici, C., Bussani, A., Del Negro, P., 2012. Benthic diatom response to changing environmental conditions. Estuarine Coastal and Shelf Science, 115, 158-169.
Cochero, J., Licursi, M., Gómez, N., 2015. Changes in the epipelic diatom assemblage in nutrient rich streams due to the variations of simultaneous stressors. Limnologica, 51, 15-23.
Cozzi, S., Giani, M., 2011. River water and nutrient discharges in the Northern Adriatic Sea: current importance and long-term changes. Continental Shelf Research, 31 (18), 1881-1893.
D’Alelio, D., Cante, M., Russo, G.F., Totti, C., De Stefano, M., 2011. Epizoic diatoms on gastropod shells. When substrate complexity selects for microcommunity complexity. p. 345- 364. In: All flesh is grass: plant-animal interactions. Seckbach, J., Dubinsky, Z. (Eds). Springer.
De Stefano, M., Marino, D., Mazzella, L., 2000. Marine taxa of Cocconeis on leaves of Posidonia oceanica, including a new species and two new varieties. European Journal of Phycology, 35 (3), 225-242.
DeNicola, D.M., McIntire, C.D., 1990. Effects of substrate relief on the distribution of periphyton in laboratory streams, I. Hydrology. Journal of Phycology, 26 (4), 624-633.
D’Ortenzio, F., Ribera d’Alcalà, M., 2008. On the trophic regimes of the Mediterranean Sea: a satellite analysis on the trophic regimes of the Mediterranean Sea. Biogeosciences, 6, 139-148.
Dufrêne, M., Legendre, P., 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 67 (3), 345-366.
Ellwood, N.T.W., Whitton. B.A., 2007. Importance of organic phosphate hydrolyzed in stalks of the lotic diatom Didymosphenia geminata and the possible impact of atmospheric and climatic changes. Hydrobiologia, 592, 121-133.
Facca, C., Sfriso, A., 2007. Epipelic diatom spatial and temporal distribution and relationship with the main environmental parameters in coastal waters. Estuarine Coastal and Shelf Science, 75 (1-2), 35-49.
Facca, C., Sfriso, A., Socal, G., 2002a. Changes in abundance and composition of phytoplankton and microphytobenthos due to increased sediment fluxes in the Venice Lagoon, Italy. Estuarine Coastal and Shelf Science, 54, 773-792.
Facca, C., Sfriso, A., Socal, G., 2002b. Temporal and spatial distribution of diatoms in the surface sediments of the Venice Lagoon. Botanica Marina, 45 (2), 170-183.
Fagherazzi, S., Mariotti. G., Banks, A.T., Morgan E.J., Fulweiler, R.W., 2014. The relationships among hydrodynamics, sediment distribution, and chlorophyll in a mesotidal estuary. Estuarine Coastal and Shelf Science, 144, 54-64.
Franzo, A., Cibic, T., del Negro, P., de Vittor, C., 2015. Spatial distribution of microphytobenthos, meiofauna and macrofauna in the north-western Adriatic Sea: a synoptic study. Limnology and Oceanography, 6 (1-2), 58-75.
Franzo, A., Guilini, K., Cibic, T., Del Negro, P., 2018. Interactions between free-living nematodes and benthic diatoms: insights from the Gulf of Trieste (northern Adriatic Sea). Mediterranean Marine Science, 19 (3), 538-554.
Friedman, G.M., Sanders, J.E., 1978. Principles of sedimentology. Wiley, New York.
Graham, L.E., Graham, J.M., Wilcox, L.W., Cook, M.E., 2016. Algae 3rd edition. LJLM Press, 689 pp.
Griffith, D.M., Veech, J.A., Marsh, C.J., 2016. Cooccur: Probabilistic species co-occurrence analysis in R. Journal of Statistical Software, Code Snippets, 69 (2), 1-17.
Grilli, F., Accoroni, S., Acri, F., Bernardi Aubry, F., Bergami, C. et al., 2020. Seasonal and interannual trends of oceanographic parameters over 40 years in the Northern Adriatic Sea in relation to nutrient loadings using the EMODnet chemistry data portal. Water, 12 (8), 2280.
Hasle, G.R., Syvertsen, E.E., 1997. Marine Diatoms. p. 5-385. In: Identifying Marine Phytoplankton. Tomas, C.R. (Ed). Academic Press, San Diego.
Hillebrand, H., Sommer, U., 1997. Response of epilithic microphytobenthos of the Western Baltic Sea to in situ experiments with nutrient enrichment. Marine Ecology Progress Series, 160, 35-46.
Hillebrand, H., Sommer, U., 1999, The nutrient stoichiometry of benthic microalgal growth: Redfield proportions are optimal. Limnology and Oceanography 44 (2), 440-446.
Hope, J.A., Paterson, D.M., Thrush, S.F., 2019. The role of microphytobenthos in soft-sediment ecological networks and their contribution to the delivery of multiple ecosystem services. Journal of Ecology, 108, 815-830.
Hustedt, F., 1985. The Pennate Diatoms, a translation of Hustedt’s “Die Kieselalgen, 2 Teil”, with suppl. of N.H. Jensen. KOELTZ Scientific Books KOENIGSTEIN: 918 pp.
Lange, K., Liess, A., Piggott, J.J., Townsend, C.R., Matthaei, C.D., 2011. Light, nutrients and grazing interact to determine stream diatom community composition and functional group structure. Freshwater Biology, 56 (2), 264-278.
MacIntyre, H.L., Geider, R.J., Miller, D.C., 1996. Microphyto benthos: the ecological role of the secret garden of unvegetated shallow-water marine habitats. I. Distribution abundance and primary production. Estuaries, 19 (2A), 186-201.
Marić, D., Kraus, R., Godrijan, J., Supić, N., Djakovac, T. et al., 2012. Phytoplankton response to climatic and anthropogenic influences in the northeastern Adriatic during the last four decades. Estuarine Coastal and Shelf Science, 115, 98-112.
Méléder, V., Rincé, Y., Barillé, L., Gaudin, P., Rosa, P., 2007. Spatiotemporal changes in microphytobenthos assemblages in a macrotidal flat (Bourgneuf Bay, France). Journal of Phycology, 43 (6), 1177-1190.
Menden-Deuer, S., Lessard, E.J., 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography, 45 (3), 569-579.
Migné, A., Spilmont, N., Boucher, G., Denis, L., Hubas, C. et al., 2009. Annual budget of benthic production in Mont Saint-Michel Bay considering cloudiness, microphytobenthos migration, and variability of respiration rates with tidal conditions. Continental Shelf Research, 29 (19), 2280-2285.
Miller, D.C., Geider, R.J., Macintyre, H.L., 1996. Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. II. Role in sediment stability and shallow-water food webs. Estuaries 19 (2A), 202-212.
Munda, I.M., 2005. Seasonal fouling by diatoms on artificial substrata at different depths near Piran (Gulf of Trieste, Northern Adriatic). Acta Adriatica, 46 (2), 137-157.
Neri, F., Romagnoli, T., Accoroni, S., Campanelli, A., Marini, M. et al., 2022. Phytoplankton and environmental drivers at a long-term offshore station in the northern Adriatic Sea (1988-2018). Continental Shelf Research, 242, 104746.
Neri, F., Romagnoli, T., Accoroni, S., Ubaldi, M., Garzia, A. et al., 2023. Phytoplankton communities in a coastal and offshore stations of the northern Adriatic Sea approached by network analysis and different statistical descriptors. Estuarine Coastal and Shelf Science, 282, 108224.
Ní Longphuirt, S., Leynaert, A., Guarini, J-M., Chauvaud, L., Claquin, P. et al., 2006. Discovery of microphytobenthos migration in the subtidal zone. Marine Ecology Progress Series, 328, 143-154.
Ní Longphuirt, S., Clavier, J., Grall, J., Chauvaud, L., Le Loc’h, F. et al., 2007. Primary production and spatial distribution of subtidal microphytobenthos in a temperate coastal system, the Bay of Brest, France. Estuarine Coastal and Shelf Science, 74 (3), 367-380.
Oksanen, J., Simpson, G.L., Blanchet, G.F, Kindt, R., Legendre, P. et al., 2022. vegan: Community Ecology Package. R package version 2.6-4. https://CRAN.R-project.org/ package=vegan
Patrick, R., Reimer, C.W. 1966. The diatoms of United States. Vol. 1. Monographs of the Academy of Natural Sciences of Philadelphia, 13, 688 pp.
Patrick, R., Reimer C.W. 1975. The diatoms of United States. Vol. 2, Part 1. Monographs of the Academy of Natural Sciences of Philadelphia, 13, 213. pp.
Parsons, T.R., Maita, Y., Lalli, C.M., 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford.
Peragallo, H., Peragallo, M. 1897-1908. Diatomées marines de France et des districts maritimes voisins. M.J. Tempère (ed.), Grez-sur-Loing., 491 pp.
Pennesi, C., Danovaro, R., 2017. Assessing marine environmental status through microphytobenthos assemblages colonizing the Autonomous Reef Monitoring Structures (ARMS) and their potential in coastal marine restoration. Marine Pollution Bulletin, 125 (1-2), 56-65.
Pinckney, J.L., 2018. A mini-review of the contribution of benthic microalgae to the ecology of the continental shelf in the South Atlantic bight. Estuaries and Coasts, 41 (7), 2070-2078.
Poulin, M., Bérard-Therriault, L., Cardinal, A., 1987. Les Diatomées (Bacillariophyceae) benthiques de substrats durs des eaux marines et saumâtres du Québec. 7. Naviculales (les genres Plagiotropis and Entomoneis). Le Naturaliste Canadien, 114, 67-80.
Poulin, M., Bérard-Therriault, L., Cardinal, A., Hamilton, P.B. 1990. Les Diatomées (Bacillariophyta) benthiques de substrats durs des eaux marines et saumâtres du Québec. 9. Bacillariaceae. Le Naturaliste Canadien, 117, 73-101.
R Core Team, 2021. R: A Language and Environment for Statistical Computing.
Riaux-Gobin, C., Romero, O., 2003. Marine Cocconeis Ehrenberg (Bacillariophyceae) species and related taxa from Kerguelen’s Land (Austral Ocean, Indian Sector). Bibliotheca Diatomologica, 47. J. Cramer in der Gebrüder Borntraeger Verlagsbuchhandlung. Berlin. 189 pp.
Rogelja, M., Cibic, T., Pennesi, C., de Vittor, C., 2016. Microphytobenthic community composition and primary production at gas and thermal vents in the Aeolian Islands (Tyrrhenian Sea, Italy). Marine Environmental Research, 118, 31-44.
Romagnoli, T., Bavestrello, G., Cucchiari, E.M., De Stefano, M., Di Camillo, C.G. et al., 2007. Microalgal communities epibiontic on the marine hydroid Eudendrium racemosum in the Ligurian Sea during an annual cycle. Marine Biology, 151 (2), 537-552.
Romagnoli, T., Totti, C., Accoroni, S., De Stefano, M., Pennesi, C., 2014. SEM analysis of the epibenthic diatoms on Eudendrium racemosum (Hydrozoa) from the Mediterranean Sea. Turkish Journal of Botany, 38 (3), 566-594.
Round, F.E., 1971. Benthic marine diatoms. Oceanography and Marine Biology - An Annual Review, 9, 83-139.
Round, F.E., Crawford, R.M., Mann, D.G., 1990. The diatoms. Biology and morphology of the genera. Cambridge University Press, Cambridge, 747 pp.
Russo, A., Artegiani, A., 1996. Adriatic Sea hydrography. Scientia Marina, 60, 33-43. Sar, E.A., Romero, O., Sunesen, I. 2003. Cocconeis Ehrenberg and Psammococconeis Garcia (Bacillariophyta) from the Gulf of San Matías, Patagonia, Argentina. Diatom Research, 18 (1), 79-106.
Schratzberger, M., Ingels, J., 2018. Meiofauna matters: the roles of meiofauna in benthic ecosystems. Journal of Experimental Marine Biology and Ecology, 502, 12-25.
Sdrigotti, E., Barbariol, V., Welker, C., 1999. Diatom assemblages in coastal shallow waters at the water-sediment interface (Gulf of Trieste, North Adriatic Sea). Annales. Series historia naturalis, 9 (2), 191-202.
Shannon, C.E., 1948. A mathematical theory of communication. The Bell System Technical Journal, 27, 379-423.
Simonsen, R., 1987. Atlas and catalogue of the diatom types of Friederich Hustedt. J. Cramer-Berlin Stuttgart, Vol. 1: 525 pp; Vol. 2: pl. 1-395; Vol. 3: pl. 396-772.
Sospedra, J., Niencheski, L.F.H., Falco, S., Andrade, C.F.F., Attisano, K.K. et al., 2018. Identifying the main sources of silicate in coastal waters of the Southern Gulf of Valencia (Western Mediterranean Sea). Oceanologia, 60 (1), 52-64.
Tolomio, C., Moro, I., Moschin, E., Valandro, A., 1999. Resultats preliminaires sur les diatomées benthiques de substrats meubles dans la lagune de Venise, Italie (Mars 1994-Janvier 1995). Diatom Research, 14 (2), 367-379.
Tolomio, C., Moschin, E., Duzzin, B., 2002. Distribution des diatomées benthiques de substrats meubles dans le bassin sud de la lagune de Venise, Italie. Diatom Research, 17 (2), 401-414.
Totti, C., 2003. Influence of the plume of the River Po on the distribution of subtidal microphytobenthos in the northern Adriatic Sea. Botanica Marina, 46, 161-178.
Totti, C., De Stefano, M., Facca, C., Ghirardelli, L.A., 2004. Microphytobenthos. p. 247-266. In: Mediterranean marine benthos: a manual of methods for its sampling and study. Gambi, M.C., Dappiano, M. (Eds). Biologia Marina Mediterranea, 11 (1), 244-266.
Totti, C., Cucchiari, E., De Stefano, M., Pennesi, C., Romagnoli, T., Bavestrello, G., 2007. Seasonal variations of epilithic diatoms on different hard substrates, in the northern Adriatic Sea. Journal of the Marine Biological Association of the United Kingdom, 87 (3), 649-658.
Totti, C., Poulin, M., Romagnoli, T., Perrone, C., Pennesi, C., De Stefano, M., 2009. Epiphytic diatom communities on intertidal seaweeds from Iceland. Polar Biology, 32 (11), 1681-1691.
Totti, C., Romagnoli, T., De Stefano, M., Di Camillo, C.G., Bavestrello, G., 2011. The diversity of epizoic diatoms. Relationships between diatoms and marine invertebrates. p. 323-343. In: All flesh is grass: plant-animal interactions. Seckbach J., Dubinsky Z. (Eds) Springer.
Totti, C., Romagnoli, T., Accoroni, S., Coluccelli, A., Pellegrini, M. et al., 2019. Phytoplankton communities in the northwestern Adriatic Sea: interdecadal variability over a 30-years period (1988-2016) and relationships with meteoclimatic drivers. Journal of Marine Systems, 193, 137-153.
Underwood, G.J.C., Barnett, M., 2006. What determines species composition in microphytobenthic biofilms? p. 121- 138. In: Functioning of microphytobenthos in estuaries. Kromkamp, J., de Brouwer, J.F.C., Blanchard, G.F., Forster, R.M., Créach, V. (Eds). Royal Netherlands Academy of Arts and Sciences, Amsterdam.
Underwood, G.J.C., Paterson, D.M., 2003. The importance of extracellular carbohydrate production by marine epipelic diatoms. Advances in Botanical Research, 40, 183-240.
Van Der Werff, A., Huls, H., 1957-1974. Diatomeenflora van Nederland. Deen Haag. Afl. 1-9. Van Heurck, H., 1880-1885. Synopsis des Diatomées de Belgique. 132 (Suppl. A, B, C), Anvers, 235 pp.
Vascotto, I., Mozetič, P., Francé, J., 2021. Phytoplankton time-series in a LTER site of the Adriatic Sea: methodological approach to decipher community structure and indicative taxa. Water, 13 (15), 2045.
Veech, J.A., 2013. A probabilistic model for analysing species co-occurrence. Global Ecology and Biogeography, 22 (2), 252-260.
Welker, C., Nichetto, P., 1996. The influence of mucous aggregates on the microphytobenthic community in the Northern Adriatic Sea. P.S.Z.N.: Marine Ecology, 17 (1-3), 473-489.
Welker, C., Sdrigotti, E., Covelli, S., Faganeli, J., 2002. Microphytobenthos in the gulf of Trieste (Northern Adriatic Sea): relationship with labile sedimentary organic matter and nutrients. Estuarine Coastal and Shelf Science, 55 (2), 259-273.
Yamaguchi, H., Arisaka, H., Otsuka, N., Tomaru, A., 2014. Utilization of phosphate diesters by phosphodiesterase-producing marine diatoms. Journal of Plankton Research, 36 (1), 281-285.
