Spatial Synchrony in Intertidal Benthic Algal Biomass in Temperate Coastal and Estuarine Ecosystems

Microphytobenthos plays a vital role in estuarine and coastal carbon cycling and food webs. Yet, the role of exogenous factors, and thus the effects of climate change, in regulating microphytobenthic biomass is poorly understood. We aimed to unravel the mechanisms structuring microphytobenthic biomass both within and across ecosystems. The spatiotemporal distribution of the biomass of intertidal benthic algae (dominated by diatoms) was estimated with an unprecedented spatial extent from time-series of Normalized Differential Vegetation Index (NDVI) derived from a 6-year period of daily Aqua MODIS 250-m images of seven temperate, mostly turbid, estuarine and coastal ecosystems. These NDVI time-series were related to meteorological and environmental conditions. Intertidal benthic algal biomass varied seasonally in all ecosystems, in parallel with meteorology and water quality. Seasonal variation was more pronounced in mud than in sand. Interannual variation in biomass was small, but synchronized year-to-year biomass fluctuations occurred in a number of disjointed ecosystems. Air temperature explained interannual fluctuations in biomass in a number of sites, but the synchrony was mainly driven by the wind/wave climate: high wind velocities reduced microphytobenthic biomass, either through increased resuspension or reduced emersion duration. Spatial variation in biomass was largely explained by emersion duration and mud content, both within and across ecosystems. The results imply that effects on microphytobenthic standing stock can be anticipated when the position in the tidal frame is altered, for example due to sea level rise. Increased storminess will also result in a large-scale decrease of biomass.

[1]  F. Round Benthic marine diatoms , 1971 .

[2]  Andrew M. Liebhold,et al.  Spatial Synchrony in Population Dynamics , 2004 .

[3]  P. Gaudin,et al.  Spatiotemporal changes in microphytobenthos assemblages in a macrotidal flat (Bourgneuf Bay,France) 1 , 2007 .

[4]  Hugh L. MacIntyre,et al.  Microphytobenthos: The ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. II. role in sediment stability and shallow-water food webs , 1996 .

[5]  J. Serôdio,et al.  Fortnightly light and temperature variability in estuarine intertidal sediments and implications for microphytobenthos primary productivity , 1999, Aquatic Ecology.

[6]  Richard C. Thompson,et al.  Physical stress and biological control regulate the producer-consumer balance in intertidal biofilms , 2004 .

[7]  David M. Paterson,et al.  Seasonal changes in diatom biomass, sediment stability and biogenic stabilization in the Severn Estuary , 1993, Journal of the Marine Biological Association of the United Kingdom.

[8]  Serge Demers,et al.  Resuspension in the shallow sublittoral zone of a macrotidal estuarine environment: Wind influence1 , 1987 .

[9]  C. Tucker Red and photographic infrared linear combinations for monitoring vegetation , 1979 .

[10]  David A. Siegel,et al.  Climate-driven trends in contemporary ocean productivity , 2006, Nature.

[11]  Rodney M. Forster,et al.  Relationship of intertidal surface sediment chlorophyll concentration to hyperspectral reflectance and chlorophyll fluorescence , 2006 .

[12]  R. Jackson,et al.  Spectral response of a plant canopy with different soil backgrounds , 1985 .

[13]  A. Holland,et al.  Quantitative evidence concerning the stabilization of sediments by marine benthic diatoms , 1974 .

[14]  Paulo Cartaxana,et al.  Effects of chlorophyll fluorescence on the estimation of microphytobenthos biomass using spectral reflectance indices , 2009 .

[15]  C. Heip,et al.  Production and consumption of biological particles in temperate tidal estuaries , 1995 .

[16]  I. Polikarpov,et al.  Spatial structure of an intertidal sandflat microphytobenthic community as related to different spatial scales , 1995 .

[17]  J. Gattuso,et al.  Light availability in the coastal ocean: Impact on the distribution of benthic photosynthetic organisms and their contribution to primary production , 2006 .

[18]  V. N. Jonge,et al.  Dynamics and distribution of microphytobenthic chlorophyll-a in the Western Scheldt estuary (SW Netherlands) , 1995, Hydrobiologia.

[19]  Lucas J. Stal,et al.  The effect of geomorphological structures on potential biostabilisation by microphytobenthos on intertidal mudflats , 2000 .

[20]  Susan L. Williams,et al.  Erratum: The impacts of climate change in coastal marine systems (Ecology Letters (2006) 9 (228-241)) , 2006 .

[21]  P. Richard,et al.  SEASONAL EFFECT ON THE RELATIONSHIP BETWEEN THE PHOTOSYNTHETIC CAPACITY OF INTERTIDAL MICROPHYTOBENTHOS AND TEMPERATURE 1 , 1997 .

[22]  D. Paterson,et al.  Microphytobenthos in contrasting coastal ecosystems: biology and dynamics , 2001 .

[23]  Jon Barry,et al.  Relationships between suspended particulate material, light attenuation and Secchi depth in UK marine waters , 2008 .

[24]  P. Herman,et al.  Organisation of microbenthic communities in intertidal estuarine flats, a case study from the Molenplaat (Westerschelde estuary, The Netherlands). , 1998 .

[25]  Lucas J. Stal,et al.  Interplay between biology and sedimentology in a mudflat (Biezelingse Ham, Westerschelde, The Netherlands) , 2000 .

[26]  C. Moritz,et al.  Modelling the dynamics of the microalgal biomass in semi-enclosed shallow-water ecosystems , 2008 .

[27]  B. L. Welsh,et al.  The effect of tidal resuspension on the distribution of intertidal epipelic algae in an estuary , 1980 .

[28]  P. Richard,et al.  Dynamics of spatial patterns of microphytobenthic biomass: inferences from a geostatistical analysis of two comprehensive surveys in Marennes-Oléron Bay (France) , 1998 .

[29]  G. Underwood,et al.  Primary Production by Phytoplankton and Microphytobenthos in Estuaries , 1999 .

[30]  P. Nienhuis Eutrophication, water management, and the functioning of Dutch estuaries and coastal lagoons , 1992 .

[31]  Hugh L. MacIntyre,et al.  Microphytobenthos: The ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production , 1996 .

[32]  N. Pettorelli,et al.  Using the satellite-derived NDVI to assess ecological responses to environmental change. , 2005, Trends in ecology & evolution.

[33]  F. Colijn,et al.  Species Composition of Benthic Diatoms and Distribution of Chlorophyll a on an Intertidal Flat in the Dutch Wadden Sea , 1981 .

[34]  B. Bates,et al.  Climate change and water. , 2008 .

[35]  W. Admiraal,et al.  Influence of Seasonal Variations of Temperature and Light on the Growth Rate of Cultures and Natural Populations of Intertidal Diatoms , 1980 .

[36]  Richard J. Murphy,et al.  Estimation of surface chlorophyll‐a on an emersed mudflat using field spectrometry: accuracy of ratios and derivative‐based approaches , 2005 .

[37]  Peter M. J. Herman,et al.  Regression-based synergy of optical, shortwave infrared and microwave remote sensing for monitoring the grain-size of intertidal sediments , 2007 .

[38]  B. Jørgensen,et al.  The light field of microbenthic communities: Radiance distribution and microscale optics of sandy coastal sediments , 1994 .

[39]  R. Murphy,et al.  Spatial variation of chlorophyll on estuarine mudflats determined by field-based remote sensing , 2008 .

[40]  J. Beukema,et al.  Variability in annual recruitment success as a determinant of long-term and large-scale variation in annual production of intertidal Wadden Sea mussels (Mytilus edulis) , 2007, Helgoland Marine Research.

[41]  F. E. Round,et al.  PERSISTENT, VERTICAL-MIGRATION RHYTHMS IN BENTHIC MICROFLORA. VI. THE TIDAL AND DIURNAL NATURE OF THE RHYTHM IN THE DIATOM HANTZSCHIA VIRGATA , 1967 .

[42]  V. Brotas,et al.  Adaptations of microphytobenthos assemblages to sediment type and tidal position. , 2009 .

[43]  C. Heip,et al.  The fate of intertidal microphytobenthos carbon: An in situ 13C‐labeling study , 2000 .

[44]  P. Herman,et al.  Distribution and dynamics of intertidal macrobenthos predicted from remote sensing: response to microphytobenthos and environment , 2008 .

[45]  C. Heip,et al.  Ecology of estuarine macrobenthos , 1999 .

[46]  C. H. Lucas,et al.  Observations of resuspended diatoms in the turbid tidal edge [rapid communication] , 2003 .

[47]  C. Heip,et al.  Benthic community structure and sediment processes on an intertidal flat: results from the ECOFLAT project , 2001 .

[48]  L. Cahoon THE ROLE OF BENTHIC MICROALGAE IN NERITIC ECOSYSTEMS , 2002 .

[49]  K. Reise Ecological Comparisons of Sedimentary Shores , 2012, Ecological Studies.

[50]  C. Sotin,et al.  Mapping microphytobenthos biomass by non-linear inversion of visible-infrared hyperspectral images , 2005 .

[51]  A. Huete,et al.  Overview of the radiometric and biophysical performance of the MODIS vegetation indices , 2002 .

[52]  Spatio-temporal distribution of the microphytobenthic biomass in intertidal flats of Tagus Estuary (Portugal) , 1995 .

[53]  J. Beukema,et al.  Common patterns in the fluctuations of macrozoobenthic species living at different places on tidal flats in the Wadden Sea , 1986, Hydrobiologia.

[54]  J. Pinckney,et al.  Biomass and production of benthic microalgal communities in estuarine habitats , 1993 .

[55]  J. Pinckney,et al.  Effects of Tidal Stage and Sun Angles on Intertidal Benthic Microalgal Productivity , 1991 .

[56]  L. P. Souza-Santos,et al.  Spatial distribution and dynamics of microphytobenthos biomass in the Gironde estuary (France) , 1997 .

[57]  V. Brotas,et al.  Spatio-temporal distribution of the microphytobenthic biomass in intertidal flats of Tagus Estuary (Portugal) , 1995, Hydrobiologia.

[58]  E. Sahan,et al.  Community structure and seasonal dynamics of diatom biofilms and associated grazers in intertidal mudflats , 2007 .

[59]  Karen Helen Wiltshire,et al.  Microbiological mediation of spectral reflectance from intertidal cohesive sediments , 1998 .

[60]  J. V. Beusekom,et al.  Wind- and tide-induced resuspension of sediment and microphytobenthos from tidal flats in the Ems estuary , 1995 .

[61]  D. B. Nedwell,et al.  Factors affecting microphytobenthic biomass, species composition and production in the Colne Estuary (UK) , 2002 .

[62]  F. E. Round,et al.  Persistent, vertical-migration rhythms in benthic microflora , 1965 .

[63]  W. Admiraal,et al.  The Seasonal Succession Patterns of Diatom Species on an Intertidal Mudflat: An Experimental Analysis , 1984 .

[64]  M. Trimmer,et al.  Modelling the distribution and growth of ‘problem’ green seaweed in the Medway estuary, UK , 2009, Hydrobiologia.

[65]  G. Underwood SEASONAL AND SPATIAL VARIATION IN EPIPELIC DIATOM ASSEMBLAGES IN THE SEVERN ESTUARY , 1994 .

[66]  A. Huete,et al.  MODIS Vegetation Index Compositing Approach: A Prototype with AVHRR Data , 1999 .