Interaction between Estuarine Microphytobenthos and Physical Forcings: The Role of Atmospheric and Sedimentary Factors

Jerónimo Pan, Constanza N. Bournod, Diana G. Cuadrado, Alejandro Vitale, María Cintia Piccolo

Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina; Instituto Argentino de Oceanografía (IADO), Bahía Blanca, Argentina.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina; Instituto Argentino de Oceanografía (IADO), Bahía Blanca, Argentina; Universidad Nacional del Sur, Bahía Blanca, Argentina.
Estación Costera J. J. Nágera, Departamento de Ciencias Marinas, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina; Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina.

DOI: 10.4236/ijg.2013.42033                

Abstract

The goal of this study was to analyze microbial mats and biofilms from the lower supratidal area of the Bahía Blanca estuary (Argentina), and explore their relationship with sediments and other physical forcings. Thirteen monthly sediment samples (uppermost 10 mm) were taken and their composition and abundance in microorganisms was determined by microscopy. Physical parameters (solar radiation and sediment temperature at -5 cm) were recorded with a frequency of 5 minutes by a coastal environmental monitoring station. Additionally, sediment grain size and moisture content were determined for distinct layers in the uppermost20 mm, and the rate of inundation of the supratidal area was estimated from tidal gauge measurements. There were significant seasonal differences in the biomass of the microphytobenthic groups considered (filamentous cyanobacteria and epipelic diatoms), with the former consistently making up >70% of the total biomass. The relationships between microphytobenthos and sediment temperature and solar radiation fitted to linear regressions, and consistently showed an inverse relationship between microphytobenthic abundance and either one of the physical parameters. The granulometric analysis revealed a unimodal composition of muddy sediments, which were vertically and spatially homogeneous; additionally, there were significant seasonal differences in water content loss with drying conditions prevailing in the summer. Several Microbially-Induced Sedimentary Structures (MISS) were identified in the supratidal zone such as shrinkage cracks, erosional pockets, gas domes, photosynthetic domes, mat chips and sieve-like surfaces. In contrast to studies from analogous environments in the Northern Hemisphere, we found reduced microphytobenthic biomass in summer, which were explained by increased evaporation/desiccation rates as a consequence of increased radiation, despite frequent tidal inundation. In conclusion, the observed density shifts in the benthic microbial communities are attributable to physical forcings dependent upon seasonal variations in interplaying factors such as sediment temperature, solar radiation and tidal inundation.

Keywords

Biofilms; Microbial Mats; Tidal Flat; Solar Radiation; Sediment Grain Size

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	J. L. Pinckney and R. Zingmark, “Biomass and Production of Benthic Microalgal Communities in Estuarine Habitats,” Estuaries, Vol. 16, No. 4, 1993, pp. 887-897. doi:10.2307/1352447
[2]	V. Cariou-Le Gall and G. H. Blanchard, “Monthly HPLC Measurements of Pigment Concentration from an Intertidal Muddy Sediment of Marennes-Oleron Bay, France,” Marine Ecology Progress Series, Vol. 121, 1995, pp. 171-179. doi:10.3354/meps121171
[3]	H. L. MacIntyre, R. J. Geider and D. C. Miller, “Micro-phytobenthos: The Ecological Role of the ‘Secret Garden’ of Unvegetated, Shallow-Water Marine Habitats. Distribution, Abundance and Primary Production,” Estuaries, Vol. 19, No. 2, 1996, pp. 186-201. doi:10.2307/1352224
[4]	L. J. Stal, “Microphytobenthos as a Biogeomorphological Force in Intertidal Sediment Stabilization,” Ecological Engineering, Vol. 36, No. 2, 2010, pp. 236-245. doi:10.1016/j.ecoleng.2008.12.032
[5]	D. M. Paterson, “Short Term Changes in the Erodibility of Intertidal Cohesive Sediments Related to the Migratory Behaviour of Epipelic Diatoms,” Limnology and Oceanography, Vol. 34, No. 1, 1989, pp. 223-234. doi:10.4319/lo.1989.34.1.0223
[6]	D. J. Smith and G. J. C. Underwood, “Exopolymer Production by Intertidal Epipelic Diatoms,” Limnology and Oceanography, Vol. 43, No. 7, 1998, pp. 1578-1591. doi:10.4319/lo.1998.43.7.1578
[7]	S. J. Hay, T. C. Maitland and D. M. Paterson, “The Speed of Diatom Locomotion through Natural and Artificial Substrata,” Diatom Research, Vol. 8, No. 2, 1993, pp. 371-384. doi:10.1080/0269249X.1993.9705268
[8]	D. M. Paterson, R. M. Crawford and C. Little, “Subaerial Exposure and Changes in the Stability of Intertidal Estuarine Sediments,” Estuarine Coastal and Shelf Science, Vol. 30, No. 6, 1990, pp. 541-556. doi:10.1016/0272-7714(90)90091-5
[9]	M. Merz, “Calcification in Cyanobacteria,” In: R. Riding and S. Awramik, Eds., Microbial Sediments, Springer Verlag, Berlin, 2000, pp. 50-56.
[10]	A.W. Decho, “Overview of Biopolymer-Induced Mineralization: What Goes on in Biofilms?” Ecological Engineering, Vol. 36, No. 2, 2010, pp. 137-144. doi:10.1016/j.ecoleng.2009.01.003
[11]	N. Noffke, “Microbial Mats in Sandy Deposits from the Archean Era to Today,” Springer-Verlag, Berlin, 2010.
[12]	N. Noffke, G. Gerdes, T. Klenke and W. E. Krumbein, “Microbially Induced Sedimentary Structures—A New Category within the Classification of Primary Sedimentary Structures,” Journal of Sedimentary Research, Vol. 71, No. 5, 2001, pp. 649-656. doi:10.1306/2DC4095D-0E47-11D7-8643000102C1865D
[13]	J. Schieber, “The Possible Role of Benthic Microbial Mats during the Formation of Carbonaceous Shales in Shallow Proterozoic Basins,” Sedimentology, Vol. 33, No. 4, 1986, pp. 524-536. doi:10.1111/j.1365-3091.1986.tb00758.x
[14]	M. O. Hayes, “Barrier Island Morphology as a Function of Tidal and Wave Regime,” In: S. Leatherman, Ed., Proceedings of the Coastal Symposium of Barrier Islands, New York Academic Press, New York, 1979, pp. 1-28.
[15]	M. C. Piccolo, G. M. E. Perillo and J. M. Arango, “Hidrografía del Estuario del Río Sauce Chico (Bahía Blanca),” Geoacta, Vol. 17, 1990, pp. 13-23.
[16]	D. Beigt, “Balance Energético de las Planicies de Marea del Estuario de Bahía Blanca,” Ph.D. Dissertation, Universidad Nacional del Sur, Bahía Blanca, 2006.
[17]	Nedeco-Arconsult, “Estudio del Dragado del Canal de Acceso al Puerto de Bahía Blanca,” Final Technical Report, Bahía Blanca, 1983.
[18]	M. C. Piccolo and P. G. Diez, “Meteorología del Puerto Coronel Rosales,” In: M. C. Piccolo and M. Hoffmeyer, Eds., Ecosistema del Estuario de Bahía Blanca, UNS, Bahía Blanca, 2004, pp. 87-90.
[19]	E. W. Koch, E. B. Barbier, B. R. Silliman, D. J. Reed, G. M. Perillo, S. D. Hacker, E. F. Granek, J. H. Primavera, N. Muthiga, S. Polasky, B. S. Halpern, C. J. Kennedy, C. V. Kappel and E. Wolanski, “Non-Linearity in Ecosystem Services: Temporal and Spatial Variability in Coastal Protection,” Frontiers in Ecology and the Environment, Vol. 7, No. 1, 2009, pp. 29-37. doi:10.1890/080126
[20]	E. Wolanski, M. M. Brinson, D. R. Cahoon and G. M. E Perillo, “Coastal Wetlands: A Synthesis,” In: G. M. E. Perillo, E. Wolanski, D. R. Cahoon and M. M. Brinson, Eds., Coastal Wetlands: An Integrated Ecosystem Approach, Elsevier, Amsterdam, 2009, pp. 1-62.
[21]	D. G. Cuadrado, N. B. Carmona and C. Bournod, “Biostabilization of Sediments by Microbial Mats in a Temperate Siliciclastic Tidal Flat, Bahía Blanca Estuary (Argentina),” Sedimentary Geology, Vol. 237, No. 1-2, 2011, pp. 95-101. doi:10.1016/j.sedgeo.2011.02.008
[22]	M. LeGresley and G. McDermott, “Counting Chamber Methods for Quantitative Phytoplankton Analysis: Haemocytometer, Palmer-Maloney Cell and Sedgewick-Rafter Cell,” In: B. Karlson, C. Cusack and E. Bresnan, Eds., Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis, IOC Manuals and Guides No. 55, UNESCO, Paris, 2010, pp. 25-30.
[23]	J. Sun and D. Liu, “Geometric Models for Calculating Cell Biovolume and Surface Area for Phytoplankton,” Journal of Plankton Research, Vol. 25, No. 11, 2003, pp. 1331-1346. doi:10.1093/plankt/fbg096
[24]	M. C. Christie, K. R. Dyer, G. Blanchard, A. Cramp, H. J. Mitchener and D. M. Paterson, “Temporal and Spatial Distributions of Moisture and Organic Contents across a Macrotidal Mudflat,” Continental Shelf Research, Vol. 20, No. 10-11, 2000, pp. 1219-1241. doi:10.1016/S0278-4343(00)00020-0
[25]	J. Zar, “Biostatistical Analysis,” 4th Edition, Prentice Hall, Upper Saddle River, 1999.
[26]	S. J. Blott and K. Pye, “GRADISTAT: A Grain Size Distribution and Statistics Package for the Analysis of Unconsolidated Sediments,” Earth Surface Processes and Landforms, Vol. 26, No. 11, 2001, pp. 1237-1248. doi:10.1002/esp.261
[27]	N. Noffke and W. E. Krumbein, “A Quantitative Approach to Sedimentary Surface Structures Contoured by the Interplay of Microbial Colonization and Physical Dynamics,” Sedimentology, Vol. 46, No. 3, 1999, pp. 417-426. doi:10.1046/j.1365-3091.1999.00218.x
[28]	G. Gerdes, “Structures Left by Modern Microbial Mats in Their Host Sediments,” In: J. Schieber, P. K. Bose, P. G. Eriksson, S. Banerjee, S. Sarkar, W. Altermann and O. Catuneanu, Eds., Atlas of Microbial Mat Features Preserved within the Siliciclastic Rock Record, Elsevier, Amsterdam, 2007, pp. 5-38.
[29]	P. G. Eriksson, J. Schieber, E. Bouougri, G. Gerdes, H. Porada, S. Benerjee, P. K. Bose and S. Sarkar, “Classification of Structures Left by Microbial Mats in Their Host Sediments,” In: J. Schieber, P. K. Bose, P. G. Eriksson, S. Banerjee, S. Sarkar, W. Altermann and O. Catuneanu, Eds., Atlas of Microbial Mat Features Preserved within the Siliciclastic Rock Record, Elsevier, Amsterdam, 2007, pp. 39-52.
[30]	S. Bose and H. S. Chafetz, “Topographic Control on Distribution of Modern Microbially Induced Sedimentary Structures (MISS): A Case Study from the Texas Coast,” Sedimentary Geology, Vol. 213, No. 3-4, 2009, pp. 136-149. doi:10.1016/j.sedgeo.2008.11.009
[31]	L. J. Stal, H. van Gemerden and W. E. Krumbein, “Structure and Development of a Benthic Marine Microbial Mat,” FEMS Microbiology Ecology, Vol. 31, No. 2, 1985, pp. 111-125. doi:10.1111/j.1574-6968.1985.tb01138.x
[32]	B. de Winder, N. Staats, L. J. Stal and D. M. Paterson, “Carbohydrate Secretion by Phototrophic Communities in Tidal sediments,” Journal of Sea Research, Vol. 42, No. 2, 1999, pp. 131-146. doi:10.1016/S1385-1101(99)00021-0
[33]	W. Admiraal and H. Peletier, “Influence of Seasonal Variations of Temperature and Light on the Growth Rate of Culture and Natural Populations of Intertidal Diatoms,” Marine Ecology Progress Series, Vol. 2, 1980, pp. 35-43. doi:10.3354/meps002035
[34]	F. Watermann, H. Hillebrand, G. Gerdes, W. E. Krumbein and U. Sommer, “Competition between Benthic Cyanobacteria and Diatoms as Influenced by Different Grain Sizes and Temperatures,” Marine Ecology Progress Series, Vol. 187, 1999, pp. 77-87. doi:10.3354/meps187077
[35]	J. Pan, C. N. Bournod, N. V. Pizani, D. G. Cuadrado and N. B. Carmona, “Characterization of Microbial Mats from a Siliciclastic Tidal Flat (Bahía Blanca Estuary, Argentina),” Geomicrobiology Journal (In press).
[36]	A. Solé, N. Gaju, S. Méndez-álvarez and I. Esteve, “Confocal Laser Scanning Microscopy as a Tool to Determine Cyanobacteria Biomass in Microbial Mats,” Journal of Microscopy, Vol. 204, No. 3, 2001, pp. 258-262. doi:10.1046/j.1365-2818.2001.00951.x
[37]	C. A. Popovich and J. E. Marcovecchio, “Spatial Variability of Phytoplankton and Environmental Factors in a Temperate Estuary of South América (Atlantic Coast, Argentina),” Continental Shelf Research, Vol. 28, No. 2, 2008, pp. 236-244. doi:10.1016/j.csr.2007.08.001
[38]	V. N. de Jonge and J. E. E. van Veusekom, “Contribution of Resuspended Microphytobenthos to Total Phytoplankton in the Ems Estuary and Its Possible Role for Grazers,” Netherlands Journal of Sea Research, Vol. 30, 1992, pp. 91-105. doi:10.1016/0077-7579(92)90049-K
[39]	J. L. Pinckney, H. W. Paerl and B. M. Bebout, “Salinity Control of Benthic Microbial Mat Community Production in a Bahamian Hypersaline Lagoon,” Journal of Experimental Marine Biology and Ecology, Vol. 187, No. 2, 1995, pp. 223-237. doi:10.1016/0022-0981(94)00185-G
[40]	J. Seckbach, P. G. Eriksson, M. M. Walsh, A. Oren and J. Chela-Flores, “Summary and Conclusions,” In: J. Seckbach and A. Oren, Eds., Microbial Mats: Modern and Ancient Microorganisms in Stratified Systems, Springer, Dordrecht, 2010, pp. 585-590. doi:10.1007/978-90-481-3799-2_30
[41]	D. G. Cuadrado, N. B. Carmona and C. N. Bournod, “Mineral Precipitation on Modern Siliciclastic Tidal Flats Colonized by Microbial Mats,” Sedimentary Geology, Vol. 271-272, pp. 58-66. doi:10.1016/j.sedgeo.2012.06.005
[42]	F. E. Anderson and B. A. Howell, “Dewatering of an Unvegetated Muddy Tidal Flat during Exposure-Desiccation or Drainage?” Estuaries, Vol. 6, No. 3, 1984, pp. 225-232. doi:10.2307/1352142
[43]	W. Admiraal, “The Ecology of Estuarine Sediment-Inhabiting Diatoms,” Progress in Phycological Research, Vol. 3, 1984, pp. 269-322.
[44]	J. L. Pinckney, “Development of an Irradiance-Based Ecophysiological Model for Intertidal Benthic Microalgal Production,” In: W. Krumbein, D. Paterson and L. Stal, Eds., Biostabilization of Sediments, Universitat Oldenburg, Oldenburg, 1994, pp. 55-83.
[45]	W. E. Krumbein, “Stromatolites—The Challenge of a Term in Space and Time,” Precambrian Research, Vol. 20, No. 2-4, 1983, pp. 493-531. doi:10.1016/0301-9268(83)90087-6
[46]	H. Beraldi-Campesi and F. García-Pichel, “The Biogenicity of Modern Terrestrial Roll-Up Structures and Its Significance for Ancient Life on Land,” Geobiology, Vol. 9, No. 1, 2011, pp. 10-23. doi:10.1111/j.1472-4669.2010.00258.x