Abstract
The seasonal variation in biogenic fluxes of NH4 +, PO4 3− and SiO2 calculated from the nutrient excretion rates of dominant bivalves (Ruditapes philippinarum and Arcuatula [=Musculista] senhousia), and pore-water nutrient (NH4 +, PO4 3−, SiO2 and NO3 − + NO2 −), sedimentary acid-volatile sulfide (AVS) and benthic chlorophyll-a (Chl-a) concentrations was assessed on an intertidal sandflat in the Seto Inland Sea (Japan) from summer 1994 to autumn 1995. In spite of the large variability between sampling dates and stations, significant correlations between biogenic nutrient fluxes and pore-water nutrient concentrations were found, suggesting a seasonal linkage between bivalve-mediated biological processes and chemical features of sediments. This linkage was stronger in surface (0–0.5 cm) than subsurface (0.5–2 cm) sediments, consistent with the autoecological characteristics of R. philippinarum and A. senhousia inhabiting the uppermost sediment layer. Significant temporal variation in pore-water NO3 − + NO2 −, sedimentary AVS and benthic Chl-a concentrations was also found, which was related to both occasional extreme events (e.g., dystrophy) and alternating periods of production and decomposition. This study may serve twofold in (1) contributing to unravel the ecological structure and functioning of natural tidal flats, and the scale of seasonal variability in biotic and sedimentary parameters and (2) providing useful information for assessing the effectiveness of the physico-chemical and biological structure of artificial tidal flats which are growing in number and extension worldwide.
Similar content being viewed by others
References
Aldous A, McCormick P, Ferguson C, Graham S, Craft C (2005) Hydrologic regime controls soil phosphorus fluxes in restoration and undisturbed wetlands. Restor Ecol 13:341–347
Aoki S, Yanagiuchi T, Mizuno Y, Okamoto K, Hino A (2011) Differences in bivalve assemblages of artificial and natural tidal flats in inner Tokyo Bay. Nippon Suisan Gakk 77:606–615 (in Japanese)
Asmus H, Asmus RM, Reise K (1990) Exchange processes in an intertidal mussel bed: a Sylt-flume study in the Wadden Sea. Ber Biol Anst Helgol 6:1–79
Asmus RM, Sprung M, Asmus H (2000) Nutrient fluxes in intertidal communities of a South European lagoon (Ria Formosa) – similarities and differences with a northern Wadden Sea bay (Sylt-Romo Bay). Hydrobiologia 436:217–235
Bartoli M, Nizzoli D, Viaroli P, Turolla E, Castaldelli G, Fano EA, Rossi R (2001) Impact of Tapes philippinarum on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia 455:203–212
Bartoli M, Longhi D, Nizzoli N, Como C, Magni P, Viaroli P (2009) Short term effects of hypoxia and bioturbation on solute fluxes, denitrification and buffering capacity in a shallow dystrophic pond. J Exp Mar Biol Ecol 381:39–47
Bayne BL, Scullard C (1977) Rates of nitrogen excretion by species of Mytilus (Bivalvia: mollusca). J Mar Biol Ass UK 57:355–369
Castel J, Labourg PJ, Escaravage V, Auby I, Garcia ME (1989) Influence of seagrass beds and oyster parks on the abundance and biomass patterns of meio- and macrobenthos in tidal flats. Estuar Coast Shelf Sci 28:71–85
Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152
Crooks JA, Khim HS (1999) Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. J Exp Mar Biol Ecol 240:53–75
Dame RF, Zingmark RG, Haskin E (1984) Oyster reefs as processors of estuarine materials. J Exp Mar Biol Ecol 83:239–247
Dame R, Dankers N, Prins T, Jongsma H, Smaal A (1991) The influence of mussel beds on nutrients in the western Wadden Sea and Eastern Scheldt estuaries. Estuaries 14:130–138
Davoult D, Migné A, Créach A, Gévaert F, Hubas C, Spilmont N, Boucher G (2009) Spatio-temporal variability of intertidal benthic primary production and respiration in the western part of the Mont Saint-Michel Bay (Western English Channel, France). Hydrobiologia 620:163–172
Doering PH, Kelly JR, Oviatt CA, Sowers T (1987) Effect of the hard clam Mercenaria mercenaria on benthic fluxes of inorganic nutrients and gases. Mar Biol 94:377–383
Donadi S, van der Heide T, van der Zee EM, Eklöf JS, van de Koppel J, Weerman EJ, Piersma T, Olff H, Klemens Eriksson B (2013) Cross-habitat interactions among bivalve species control community structure on intertidal flats. Ecology 94:489–498
Eguchi M, Fujii C, Miyamoto H, Shigematsu T, Yamochi S (2002) Dissolved oxygen consumption by bottom sediments of an artificial tidal flat in Japan. Fish Sci 68(S1):596–599
French K, Robertson S, O’Donnell MA (2004) Differences in invertebrate infaunal assemblages of constructed and natural tidal flats in New South Wales, Australia. Estuar Coast Shelf Sci 61:173–183
Giménez L, Dimitriadis C, Carranza A, Borthagaray AI, Rodríguez M (2006) Unravelling the complex structure of a benthic community: a multiscale-multianalytical approach to an estuarine sandflat. Estuar Coast Shelf Sci 68:462–472
Goulletquer P, Heral M, Deslous-Paoli JM, Prou J, Garnier J, Razet D, Boromthanarat W (1989) Ecophysiologie et bilan énergétique de la palourde japonaise d’élevage Ruditapes philippinarum. J Exp Mar Biol Ecol 132:85–108 (in French)
Guarini JM, Blanchard GF, Bacher C, Gros P, Boucher G et al (1998) Dynamics of spatial patterns of microphytobenthic biomass: interferences from a geostatistical analysis of two comprehensive surveys in Marennes-Oléron Bay (France). Mar Ecol Prog Ser 166:131–141
Hatano T, Murakami K, Ishii H, Kadowaki A, Kuwae T, Nakase K (2013) Characteristics of nitrogen and phosphorus budgets at a tidal flat in Tokyo port wild bird park. J JSCE 1(1):145–161
Huettel M (1990) Influence of the lugworm Arenicola marina on porewater nutrient profiles of sand flat sediments. Mar Ecol Prog Ser 62:241–248
Hutchison L, Montagna P, Yoskowitz D, Scholz D, Tunnell J (2013) Stakeholder perceptions of coastal habitat ecosystem services. Estuar Coasts. doi:10.1007/s12237-013-9647-7
Ichimi K, Kawamura T, Yamamoto A, Tada K, Harrison PJ (2012) Extremely high growth rate of the small diatom Chaetoceros salsugineum isolated from an estuary in the eastern Seto Inland Sea, Japan. J Phycol 48:1284–1288
Imanaka S, Okamoto K, Aoki S, Hino A (2002) Relationship between the distribution of short-neck clam Ruditapes philippinarum and sediment environment on the artificial tidal flat and natural shores in Hamana Bay. Fish Sci 68(S1):449–450
Ishii R, Nakano Y, Nakai S, Nishijima W, Okada M (2008) Benthic ecosystem development in an artificial tidal flat constructed from dredged spoil. Mar Poll Bull 56:2059–2066
Kanaya G, Nakamura Y, Koizumi T, Yamada K, Koshikawa H, Kohzu A, Maki H (2013) Temporal changes in carbon and nitrogen stable isotope ratios of macrozoobenthos on an artificial tidal flat facing a hypertrophic canal, inner Tokyo Bay. Mar Poll Bull 71:179–189
Kasai A, Horie H, Sakamoto W (2004) Selection of food sources by Ruditapes philippinarum and Mactra veneriformis (Bivalva: mollusca) determined from stable isotope analysis. Fish Sci 70:11–20
Klump JV, Martens CS (1989) Seasonality of nutrient regeneration in an organic-rich coastal sediment: kinetic modeling of changing pore-water nutrient and sulfate distributions. Limnol Oceanogr 34:559–577
Komorita T, Kajihara R, Tsutsumi H, Shibanuma S, Yamada T, Higaki N, Montani S (2010) Reevaluation of the nutrient mineralization process by infaunal bivalves (Ruditapes philippinarum) in a shallow lagoon in Hokkaido, Japan. J Exp Mar Biol Ecol 383:8–16
Komorita T, Kajihara R, Tsutsumi H, Shibanuma S, Yamada T, Montani S (2014) Food sources for Ruditapes philippinarum in a coastal lagoon determined by mass balance and stable isotope approaches. PLoS ONE 9(1):e86732
Kuwae T, Hosokawa Y, Eguchi N (1998) Dissolved inorganic nitrogen cycling in Banzu intertidal sand-flat, Japan. Mangr Salt Marsh 2:167–175
Kuwae T, Kibe E, Nakamura Y (2003) Effect of emersion and immersion on the porewater dynamics of an intertidal sandflat in Tokyo Bay. Estuar Coast Shelf Sci 57:929–940
Kuwae T, Miyoshi E, Hosokawa S, Ichimi K, Hosoya J, Amano T, Moriya T, Kondoh M, Ydenberg RC, Elner RW (2012) Variable and complex food web structures revealed by exploring missing trophic links between birds and biofilm. Ecol Lett 15:347–356
Lee JG, Nishijima W, Mukai T, Takimoto K, Seiki T, Hiraoka K, Okada M (1998) Factors to determine the functions and structures in natural and constructed tidal flats. Wat Res 32:2601–2606
Lerat Y, Lasserre P, le Corre P (1990) Seasonal changes in pore water concentrations of nutrients and their diffusive fluxes at the sediment-water interface. J Exp Mar Biol Ecol 135:135–160
Lorenzen CJ (1967) Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol Oceanogr 12:343–346
Magni P, Montani S (1997) Development of benthic microalgal assemblages on an intertidal flat in the Seto Inland Sea, Japan: effects of environmental variability. La Mer 35:137–148
Magni P, Montani S (2000) Water chemistry variability in the lower intertidal zone of an estuary in the Seto Inland Sea, Japan: seasonal patterns of nutrients and particulate compounds. Hydrobiologia 432:9–23
Magni P, Montani S (2005) Laboratory experiments on bivalve excretion rates of nutrients. In: Lehr JH, Keeley J (Eds), Water Encyclopedia, vol. Wiley, Hoboken, pp 6–11
Magni P, Montani S (2006) Seasonal patterns of pore-water nutrients, benthic chlorophyll a and sedimentary AVS in a macrobenthos-rich tidal flat. Hydrobiologia 571:297–311
Magni P, Montani S, Takada C, Tsutsumi H (2000) Temporal scaling and relevance of bivalve nutrient excretion on a tidal flat of the Seto Inland Sea, Japan. Mar Ecol Prog Ser 198:139–155
Magni P, Montani S, Tada K (2002) Semidiurnal dynamics of salinity, nutrients and suspended particulate matter in an estuary in the Seto Inland Sea, Japan, during a spring tide cycle. J Oceanogr 58:389–402
Magni P, Como S, Montani S, Tsutsumi H (2006) Interlinked temporal changes in environmental conditions, chemical characteristics of sediments and macrofaunal assemblages in an estuarine intertidal sandflat (Seto Island Sea, Japan). Mar Biol 149(5):1185–1197
Mann R, Glomb SJ (1978) The effect of temperature on growth and ammonia excretion of the Manila clam Tapes japonica. Estuar Coast Shelf Sci 6:335–339
Marinelli RL, Jahnke RA, Craven DB, Nelson JR, Eckman JE (1998) Sediment nutrient dynamics on the South Atlantic Bight continental shelf. Limnol Oceanogr 43:1305–1320
Montani S, Magni P, Shimamoto M, Abe N, Okutani K (1998) The effect of a tidal cycle on the dynamics of nutrients in a tidal estuary in the Seto Inland Sea, Japan. J Oceanogr 54:65–76
Montani S, Magni P, Abe N (2003) Seasonal and interannual patterns of intertidal microphytobenthos in combination with laboratory and areal production estimates. Mar Ecol Prog Ser 249:79–91
Morrisey DJ, Underwood AJ, Howitt L, Stark JS (1992) Temporal variation in soft-sediment benthos. J Exp Mar Biol Ecol 164:233–245
Mortimer RJG, Davey JT, Krom MD, Watson PG, Frickers PE, Clifton RJ (1999) The effect of macrofauna on porewater profiles and nutrient fluxes in the intertidal zone of the Humber estuary. Estuar Coast Shelf Sci 48:683–699
Nam J, Ryu J, Fluharty D, Koh CH, Dyson K, Chang WK, Choi HJ, Kang D, Khim JS, Lee CH (2010) Designation processes for marine protected areas in the coastal wetlands of South Korea. Ocean Coast Manag 53:703–710
Nishijima W, Nakano Y, Nakai S, Okuda T, Imai T, Okada M (2014) Macrobenthic succession and characteristics of a man-made intertidal sandflat constructed in the diversion channel of the Ohta River Estuary. Mar Poll Bull 82:101–108
Nizzoli D, Welsh DT, Viaroli P (2011) Seasonal nitrogen and phosphorus dynamics during benthic clam and suspended mussel cultivation. Mar Poll Bull 62:1276–1287
Ohmura T, Arai Y, Kondo T Hosokawa Y (2010) Utilization of adaptive management technique for restoration of large-scale tidal flat in Tokyo bay. Proceedings of ASME 29th international conference on ocean, offshore and arctic engineering vol 3, pp 1–9
Parsons TR, Maita M, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford
Prather CM, Pelini SL, Laws A, Rivest E, Woltz M, Bloch CP, Del Toro I, Ho CK, Kominoski J, Newbold TAS, Parsons S, Joern A (2013) Invertebrates, ecosystem services and climate change. Biol Rev 88:327–348
Prins TC, Smaal AC (1994) The role of the blue mussel Mytilus edulis in the cycling of nutrients in Oosterschelde estuary (the Netherlands). Hydrobiologia 282(283):413–429
Ricciardi A, Bourget E (1998) Weight to weight conversion factors for marine benthic invertebrates. Mar Ecol Prog Ser 163:245–251
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rysgaard S, Christensen PB, Nielsen LP (1995) Seasonal variation in nitrification and denitrification in estuarine sediment colonized by benthic microalgae and bioturbating infauna. Mar Ecol Prog Ser 126:111–121
Sandwell DR, Pilditch CA, Lohrer AM (2009) Density dependent effects of an infaunal suspension-feeding bivalve (Austrovenus stutchburyi) on sandflat nutrient fluxes and microphytobenthic productivity. J Exp Mar Biol Ecol 373:16–25
Schlüter L, Josefsen SB (1994) Annual variation in condition, respiration and remineralisation of Mytilus edulis L. in the Sound, Denmark. Helgol Meer 48:419–430
Smith AS, Jacinthe P-A (2014) A mesocosm study of the effects of wet–dry cycles on nutrient release from constructed wetlands in agricultural landscapes. Environ Sci-Proc Imp 16:106–115
Spilmont N, Seuront L, Meziane T, Welsh DT (2011) There’s more to the picture than meets the eye: sampling microphytobenthos in a heterogeneous environment. Estuar Coast Shelf Sci 95:470–476
Stief P (2013) Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10:7829–7846
Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Fish Res Board Can Bull 167:310
Trimmer M, Nedwell DB, Sivyer DB, Malcolm SJ (1998) Nitrogen fluxes through the lower estuary of the river Great Ouse, England: the role of the bottom sediments. Mar Ecol Prog Ser 163:109–124
Underwood AJ (1997) Experiments in ecology. Their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge 504 pp
Wang WW, Li DJ, Zhou JL, Gao L (2011) Nutrient dynamics in pore water of tidal marshes near the Yangtze Estuary and Hangzhou Bay, China. Environ Earth Sci 63:1067–1077
Welsh DT (2003) It’s a dirty job but someone has to do it: the role of marine benthic macrofauna in organic matter turnover and nutrient recycling to the water column. Chem Ecol 193:321–342
Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design, 3rd edn. McGraw Hill, New York
Yamochi S (2008) Succession of macrobenthic fauna and nitrogen budget at two artificial tidal flats in Osaka Bay, Japan. Mar Poll Bull 57:137–141
Yamochi S (2013) Effects of desiccation and salinity on the outbreak of a green tide of Ulva pertusa in a created salt marsh along the coast of Osaka Bay, Japan. Estuar Coast Shelf Sci 116:21–28
Yamochi S, Yanagawa R, Oda K (2003) Nitrogen budget at two artificial tidal flats along the coastal area of Osaka Bay, Japan. Water Pollution VII: Modelling, Measuring and Prediction Book Series: International Series on Progress. In: Water Resources 9:93–102
Yang HY, Chen B, Barter M, Piersma T, Zhou CF, Li FS, Zhang ZW (2011) Impacts of tidal land reclamation in Bohai Bay, China: ongoing losses of critical Yellow Sea waterbird staging and wintering sites. Bird Conserv Int 21:241–259
Zainal K, Al-Madan I, Al-Sayed H, Khamis A, Al Shuhaby S, Al Hisaby A, Elhoussiny W, Khalaf E (2012) The cumulative impacts of reclamation and dredging on the marine ecology and land-use in the Kingdom of Bahrain. Mar Poll Bull 64:1452–1458
Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, Upper Saddle River
Zhang L, Wang L, Yin K, Lü Y, Zhang D, Yang Y, Huang X (2013) Pore water nutrient characteristics and the fluxes across the sediment in the Pearl River estuary and adjacent waters, China. Estuar Coast Shelf Sci 133:182–192
Acknowledgments
This study was partly supported by a research fund (No. 22380102) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant-in-Aid of Scientific Research) and by the Flagship Project RITMARE—The Italian Research for the Sea—coordinated by the Italian National Research Council and funded by the Italian Ministry of Education, University and Research. We gratefully acknowledge the constructive criticisms of two anonymous reviewers which helped us improve manuscript’s clarity.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Huettel.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Magni, P., Como, S., Montani, S. et al. Interlinked seasonal variation in biogenic nutrient fluxes and pore-water nutrient concentrations in intertidal sediments. Mar Biol 161, 2767–2779 (2014). https://doi.org/10.1007/s00227-014-2541-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-014-2541-4