Abstract
Despite the dynamic nature of spatial pattern, the temporal variation of spatial structure of marine benthic assemblages is rarely assessed using several temporal scales. We quantified the variability of density and biomass of main benthic species in the intertidal soft-bottom flats at two bights in Chupa Inlet (Kandalaksha Bay, the White Sea). The data cover the 21-year period (1987–2008) of a long-term monitoring survey (1987–present) using a hierarchical sampling design with two temporal (year, season within a year) and three spatial scales (bights—7 km, stations within a bight—10–100 m, and replicate samples—10 s cm apart). We used nested ANOVA to test significance and variance components to compare the relative contribution of different scales of variability of density and biomass of 18 most occurring macrobenthic species. Some species demonstrated high large-scale variability, however, the majority showed high small-scale variability and residual variance. The interactive variability was at least as important as the temporal effects, indicating that the spatial pattern changes through time. The assemblages were more variable at small scales and more stable at larger scales. Potential implications for sampling design are discussed.
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Anderson, M. J., S. D. Connell, B. M. Gillanders, C. E. Diebel, W. M. Blom, J. E. Saunders & T. J. Landers, 2005. Relationships between taxonomic resolution and spatial scales of multivariate variation. Journal of Animal Ecology 74: 1365–2656.
Archambault, P. & E. Bourget, 1996. Scales of coastal heterogeneity and benthic intertidal species richness, diversity and abundance. Marine Ecology Progress Series 136: 111–121.
Azovsky, A. I., E. S. Chertoprood, M. A. Saburova & I. G. Polikarpov, 2004. Spatio-temporal variability of micro- and meiobenthic communities in a White Sea intertidal sandflat. Estuarine, Coastal and Shelf Science 60: 663–671.
Bellehumeur, C. & P. Legendre, 1998. Multiscale sources of variation in ecological variables: modeling spatial dispersion, elaborating sampling designs. Landscape Ecology 13: 15–25.
Bergström, U., G. Englund & E. Bonsdorff, 2002. Small-scale spatial structure of Baltic Sea zoobenthos—inferring processes from patterns. Journal of Experimental Marine Biology and Ecology 281: 123–136.
Beukema, J. J., 1982. Annual variation in reproductive success and biomass of the major macrozoobenthic species living in a tidal flat area of the Wadden Sea. Netherlands Journal of Sea Research 16: 37–45.
Beukema, J. J., 1992. Dynamics of juvenile shrimp Crangon crangon in a tidal-flat nursery of the Wadden Sea after mild and cold winters. Marine Ecology Progress Series 83: 157–165.
Beukema, J. J. & J. de Vlas, 1989. Tidal-current transport of thread-drifting postlarval juveniles of the bivalve Macoma balthica from the Wadden Sea to the North Sea. Marine Ecology Progress Series 52: 193–200.
Beukema, J. J., P. J. C. Honkoop & R. Dekker, 1998. Recruitment in Macoma balthica after mild and cold winters and its possible control by egg production and shrimp predation. Hydrobiologia 375(376): 23–34.
Burkovsky, I. V., A. A. Udalov & A. P. Stoljarov, 1997. The importance of juveniles in structuring a littoral macrobenthic community. Hydrobiologia 355: 1–9.
Butman, C. A., 1987. Larval settlement of soft-sediment invertebrates: the spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processes. Oceanography and Marine Biology Annual Review 25: 113–165.
Caffey, H. M., 1985. Spatial and temporal variation in settlement and recruitment of intertidal barnacles. Ecological Monographs 55: 313–332.
Chapman, M. G., 2002. Patterns of spatial and temporal variation of macrofauna under boulders in a sheltered boulder field. Austral Ecology 27: 211–228.
Chapman, M. G., T. J. Tolhurst, R. J. Murphy & A. J. Underwood, 2010. Complex and inconsistent patterns of variation in benthos, micro-algae and sediment over multiple spatial scales. Marne Ecology Progress Series 398: 33–47.
Commito, J. A., W. E. Dow & B. M. Grupe, 2006. Hierarchical spatial structure in soft-bottom mussel beds. Journal of Experimental Marine Biology and Ecology 330: 27–37.
Crisp, D. J., 1964. The effects of the severe winter of 1962–1963 on marine life in Britain. Journal of Animal Ecology 33: 165–210.
Dethier, M. N. & G. C. Schoch, 2005. The consequences of scale: assessing the distribution of benthic populations in a complex estuarine fjord. Estuarine, Coastal and Shelf Science 62: 253–270.
De Biasi, A. M., L. Benedetti-Cecchi, L. Pacciardi, E. Maggi, S. Vaselli & I. Bertocci, 2003. Spatial heterogeneity in the distribution of plants and benthic invertebrates in the lagoon of Orbetello (Italy). Oceanologica Acta 26: 39–46.
Dulvy, N. K., R. E. Mitchell, D. Watson, C. J. Sweeting & N. V. C. Polunin, 2002. Scale-dependant control of motile epifaunal community structure along a coral reef fishing gradient. Journal of Experimental Marine Biology and Ecology 278: 1–29.
Edgar, G. J. & N. S. Barrett, 2002. Benthic macrofauna in Tasmanian estuaries: scales of distribution and relationship with environmental variables. Journal of Experimental Marine Biology and Ecology 270: 1–24.
Fraschetti, S., A. Terlizzi & L. Benedetti-Cecchi, 2005. Patterns of distribution of marine assemblages from rocky shores: evidence of relevant scales of variation. Marine Ecology Progress Series 296: 13–29.
Giménez, L., A. I. Borthagaray, M. Rodriguez, A. Brazeiro & C. Dmitriadis, 2005. Scale-dependent patterns of macrofaunal distribution in soft-sediment intertidal habitats along a large-scale estuarine gradient. Helgoland Marine Research 59: 224–236.
Giménez, L., C. Dimitriadis, A. Carranza, A. I. Borthagaray & M. Rodríguez, 2006. Unraveling the complex structure of a benthic community: a multiscale-multianalytical approach to an estuarine sandflat. Estuarine, Coastal and Shelf Science 68: 462–472.
Graham, M. H. & M. S. Edwards, 2001. Statistical significance versus fit: estimating the importance of individual factors in ecological analysis of variance. Oikos 93: 505–513.
Hall, S. J., D. Raffaelli & S. F. Thrush, 1994. Patchiness and disturbance in shallow water benthic assemblages. In Giller, P. S., A. G. Hildrew & D. G. Rafaelli (eds), Aquatic Ecology: Scale, Pattern, and Process. Blackwell Scientific Publications, London: 333–375.
Hewitt, J. E., S. F. Thrush, V. J. Cummings & S. J. Turner, 1998. The effect of changing sampling scales on our ability to detect effects of large-scale processes on communities. Journal of Experimental Marine Biology and Ecology 227: 251–264.
Hewitt, J. E., S. F. Thrush, P. K. Dayton & E. Bonsdorff, 2007. The effect of spatial and temporal heterogeneity on the design and analysis of empirical studies on scale-dependent systems. American Naturalist 169: 398–408.
Jarrett, J. N. & J. A. Pechenik, 1997. Temporal variation in cyprid quality and juvenile growth capacity for an intertidal barnacle. Ecology 78: 1262–1265.
Jenkins, S. R., P. Åberg, G. Cervin, R. A. Coleman, J. Delany, P. Della Santina, S. J. Hawkins, E. LaCroix, A. A. Myers, M. Lindegarth, A. -M. Power, M. F. Roberts & R. G. Hartnoll, 2000. Spatial and temporal variation in settlement and recruitment of the intertidal barnacle Semibalanus balanoides (L.) (Crustacea: Cirripedia) over a European scale. Journal of Experimental Marine Biology and Ecology 243: 209–225.
Kendall, M. A. & S. Widdicombe, 1999. Small scale patterns in the structure of macrofaunal assemblages of shallow soft sediments. Journal of Experimental Marine Biology and Ecology 237: 127–140.
Kuznetsov, V. V., 1960. The White Sea and biological features of its flora and fauna. Moscow–Leningrad (In Russian).
Lawrie, S. M. & C. D. McQuaid, 2001. Scales of mussel bed complexity: structure, associated biota and recruitment. Journal of Experimental Marine Biology and Ecology 257: 135–161.
Legendre, P., S. F. Thrush, V. J. Cummings, P. K. Dayton, J. Grant, J. E. Hewitt, A. H. Hines, B. H. McArdle, D. Pridmore, D. C. Schneider, S. J. Turner, R. B. Whitlach & M. R. Wilkinson, 1997. Spatial structure of bivalves in a sandflat: scale and generating processes. Journal of Experimental Marine Biology and Ecology 216: 99–128.
Levin, S. A., 1992. The problem of patterns and scale in ecology. Ecology 73: 1943–1967.
Lisitzin, A. P., et al., 1999. The continental-ocean boundary as a marginal filter in the World Oceans. In Gray, J. S. (ed.), Biogeochemical Cycling and Sediment Ecology. Kluwer Academic Publications, Dordrecht: 69–103.
Lukanin, V. V., A. D. Naumov & V.V. Fedyakov, 1986a. Dynamics of size-frequency structure of blue mussel (Mytilus edulis L.) beds in the White Sea. In Scarlato, O. A. et al. (eds), Ecological Investigations of the Benthic Organisms of the White Sea. Zoological Institute Publishers, Leningrad: 50–63 (In Russian).
Lukanin, V. V., A. D. Naumov & V. V. Fedyakov, 1986b. Cyclic development of Mytilus edulis (L.) population in the White Sea. Doklady Akademii Nauk SSSR 5: 1274–1277 (In Russian).
Lukanin, V. V., A. D. Naumov & V. V. Fedyakov, 1989. Long-term structural and functional changes in an estuary mussel population in the White Sea. Zhurnal obschey biologii 50: 366–371 (In Russian).
Lukanin, V. V., A. D. Naumov & V. V. Fedyakov, 1990. Blue mussel beds: constant inconstancy. Priroda 11: 56–62 (In Russian).
Maximovich, N. V., A. V. Gerasimova & T. A. Kunina, 1991. Dynamics of the structural characteristics of littoral Macoma balthica L. populations (Chupa Bay, White Sea, USSR). Vestnik Sankt Peterburgskogo Universiteta Seriya 3 Biologiya 2: 23–31 (In Russian).
Maximovich, N. V., A. V. Gerasimova & T. A. Kunina, 1992. Productional properties of the Macoma balthica L settlements in Chupa Inlet White Sea. I. Linear growth. Vestnik Sankt Peterburgskogo Universiteta Seriya 3 Biologiya 4: 12–19 (In Russian).
Maximovich, N. V., A. V. Gerasimova & T. A. Kunina, 1993. Productional properties of the Macoma balthica L settlements in Chupa Inlet White Sea. II. Production. Vestnik Sankt Peterburgskogo Universiteta Seriya 3 Biologiya 1: 3–11 (In Russian).
Middelboe, A. L., K. Sand-Jensen & D. Krause-Jensen, 2003. Spatial and interannual variations with depth in eelgrass populations. Journal of Experimental Marine Biology and Ecology 291: 1–15.
Möller, P., 1986. Physical factors and biological interactions regulating infauna in shallow boreal areas. Marine Ecology Progress Series 30: 33–47.
Morrisey, D. J., L. Howitt, A. J. Underwood & J. S. Stark, 1992a. Spatial variation in soft-sediment benthos. Marine Ecology Progress Series 81: 197–204.
Morrisey, D. J., A. J. Underwood, L. Howitt & J. S. Stark, 1992b. Temporal variation in soft-sediment benthos. Journal of Experimental Marine Biology and Ecology 164: 233–245.
Naumov A. D., 2006. Clams of the White Sea. Ecological and faunistic analysis. St. Petersburg (In Russian).
Naumov, A. D., 2007. Long-term investigations of the littoral benthos of the White Sea in the Chupa Inlet (Kandalaksha Bay): seasonal and long-term dynamics of the biomass of the eelgrass Zostera marina. In Complex Investigations of Processes, Characteristics and Resources of Russian seas of North European Basin. Issue 2. Apatity, Print. Kola Centre RAS: 493–502 (In Russian).
Naumov, A. D., 2011. Abnormal casting ashore of starfishes in the Dvina Bay in spring 1990, St. Petersburg (In Russian).
Naumov, A. D., 2012. Long-term fluctuations of soft-bottom intertidal community structure influenced by ice cover at two small sea bights in the Chupa Inlet (Kandalaksha Bay) of the White Sea. doi:10.1007/s10750-012-1339-y.
Naumov, A. D., V. V. Khalaman & M. V. Fokin, 2009. Long-term dynamics of the abundance of several intertidal polychaetes in two inlets of Kandalaksha Bay (White Sea). Russian Journal of Marine Biology 35: 381–387.
Nemirovskaya, I. A., 2004. Hydrocarbons in the Ocean (Snow–Ice–Water–Suspension–Bottom Sediments). Nauchnyi Mir, Moscow (In Russian).
Norén, K. & M. Lindegarth, 2005. Spatial, temporal and interactive variability of infauna in Swedish coastal sediments. Journal of Experimental Marine Biology and Ecology 317: 53–68.
Olabarria, C. & M. G. Chapman, 2001. Comparison of patterns of spatial variation of microgastropods between two contrasting intertidal habitats. Marine Ecology Progress Series 220: 201–211.
O’Neill, R. V., A. R. Johnson & A. W. King, 1989. A hierarchical framework for the analysis of scale. Landscape Ecology 3: 193–205.
Porri, F., C. D. McQuaid & S. Radloff, 2006. Temporal scales of variation in settlement and recruitment of the mussel Perna perna (Linnaeus, 1758). Journal of Experimental Marine Biology and Ecology 332: 178–187.
Quinn, G. P. & M. J. Keough, 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.
Sánchez-Moyano, J. E., I. García-Asencio & J. C. García-Gómez, 2010. Spatial and temporal variation of the benthic macrofauna in a grossly polluted estuary from southwestern Spain. Helgoland Marine Research 64: 155–168.
Savinov, V., T. Savinova & S. Dahle, 2001. Contaminants (Chapter 10). In Berger V., S. Dahle, K. Galaktionov, X. Kosobokova, A. Naumov, T. Rat’kova, V. Savinov & T. Savinova. White Sea. Ecology and Environment. Derzavets Publisher, St. Petersburg–Tromsø: 123–136.
Savinov, V., O. Korneev, A. Rybalko, A. Naumov, A. Kochetkov & N. Grin, 2010. Chlorinated hydrocarbons and polybromated diphenylethers in the White Sea bottom sediments and biota. In Naumov, A. D, A. P. Alekseev & A. A. Sukhotin (eds), Objectives of Exploration, Efficient Exploitation and Conservation of the White Sea Natural Resources. ZIN RAS, St. Petersburg: 157–159 (In Russian).
Searle, S. R., G. Cassella & C. McCulloch, 1992. Variance Components. Wiley, New York.
Solyanko, K., V. Spiridonov & A. Naumov, 2011. Biomass, commonly occurring and dominant species of macrobenthos in Onega Bay (White Sea, Russia): data from three different decades. Marine Ecology 32: 36–48.
Thrush, S. F., 1999. Complex role of predators in structuring soft-sediment macrobenthic communities: implications of changes in spatial scale for experimental studies. Australian Journal of Ecology 24: 344–354.
Thrush, S. F., J. E. Hewitt & R. D. Pridmore, 1989. Patterns in the spatial arrangements of polychaetes and bivalves in intertidal sandflats. Marine biology 102: 529–535.
Thrush, S. F., R. D. Pridmore & J. E. Hewitt, 1994. Impacts on soft-sediment macrofauna: the effects of spatial variation on temporal trends. Ecological Applications 4: 31–41.
Thrush, S. F., D. C. Schneider, P. Legendre, R. B. Whitlatch, P. K. Dayton, J. E. Hewitt, A. H. Hines, V. J. Cummings, S. M. Lawrie, J. Grant, R. D. Pridmore, S. J. Turner & B. H. McArdle, 1997a. Scaling-up from experiments to complex ecological systems: where to next? Journal of Experimental Marine Biology and Ecology 216: 243–254.
Thrush, S. F., V. J. Cummings, P. K. Dayton, R. Ford, J. Grant, J. E. Hewett, A. H. Hines, S. M. Lawrie, R. D. Pridmore, P. Legendre, B. H. McArdle, D. C. Schneider, S. J. Turner, R. B. Whitlatch & M. R. Wilkinson, 1997b. Matching the outcome of small-scale density manipulation experiments with larger scale patterns an example of bivalve adult/juvenile interactions. Journal of Experimental Marine Biology and Ecology 216: 153–169.
Thrush, S. F., S. M. Lawrie, J. E. Hewitt & V. J. Cummings, 1999. The problem of scale: uncertainties and implications for soft-bottom marine communities and their assessment of human impacts. In Gray, J. S., W. Ambrose & A. Szaniawska (eds), Biogeochemical Cycling and Sediment Ecology NATO ARW. Kluwer Scientific, Dordrecht: 195–210.
Turner, M. G., W. H. Romme, R. H. Gardner, R. V. O’Neill & T. K. Kratz, 1993. A revised concept of landscape equilibrium: disturbance and stability on scaled landscapes. Landscape Ecology 8: 213–227.
Turner, S. J., J. Grant, R. D. Pridmore, J. E. Hewitt, M. R. Wilkinson, T. Hume & D. Morrisey, 1997. Bedload and water-column transport and colonisation processes by post-settlement benthic macrofauna: does infaunal density matter? Journal of Experimental Marine Biology and Ecology 216: 51–75.
Underwood, A. J., 1992. Beyond BACI: the detection of environmental impacts on populations in the real, but variable, world. Journal of Experimental Marine Biology and Ecology 161: 145–178.
Underwood, A. J., 1997. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge University Press, Cambridge.
Underwood, A. J. & M. G. Chapman, 1996. Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107: 212–224.
Underwood, A. J. & M. G. Chapman, 2003. Power, precaution, Type II error and sampling design in assessment of environmental impacts. Journal of Experimental Marine Biology and Ecology 296: 49–70.
Underwood, A. J., M. G. Chapman & S. Connell, 2000. Observations in ecology: you can’t make progress on processes without understanding the patterns. Journal of Experimental Marine Biology and Ecology 250: 97–115.
Watt, A. S., 1947. Pattern and process in the plant community. Journal of Ecology 35: 1–22.
Willis, K. J. & R. J. Whittaker, 2002. Species diversity—scale matters. Science 295: 1245–1248.
Wu, J. & O. L. Loucks, 1995. From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology. Quarterly Review of Biology 70: 439–466.
Ysebaert, T. & P. M. J. Herman, 2002. Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, intertidal soft-sediment environment. Marine Ecology Progress Series 244: 105–124.
Zajac, R. N., R. B. Whitlatch & S. F. Thrush, 1998. Recolonization and succession in soft-sediment infaunal communities: the spatial scale of controlling factors. Hydrobiologia 375(376): 227–240.
Acknowledgments
The material was obtained by three persons mainly. Dr. V.V. Fedaykov participated in the work in years 1987–1999, Dr. M.V. Fokin in years 2000–2009 and Dr. A.D. Naumov since 1989 up to present. Our colleagues Dr. K.V. Galaktionov, Dr. K.E. Nikolaev and Dr. I.A. Levakin kindly helped us in winter fieldwork for the last 10 years. We thank numerous students of Saint Petersburg State University for their help in the fieldwork. We would like to thank the anonymous referees for the comments which helped to enhance this paper. This study was funded from different sources: as a scheduled research topic of the Zoological Institute RAS, by the research grant from the Commission of the European Communities INCO-Copernicus-II ICA2-CT-2000-10053, by the program of fundamental research of the Branch of Biological Sciences of Russian Academy of Sciences “Biological resources of Russia: estimation of state and essential principals of monitoring” and by the program of fundamental research of the Presidium of Russian Academy of Sciences “Biological diversity”.
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Guest editor: A. A. Sukhotin / Long-term research on marine ecosystems in the White Sea, Russia
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Varfolomeeva, M., Naumov, A. Long-term temporal and spatial variation of macrobenthos in the intertidal soft-bottom flats of two small bights (Chupa Inlet, Kandalaksha Bay, White Sea). Hydrobiologia 706, 175–189 (2013). https://doi.org/10.1007/s10750-012-1341-4
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DOI: https://doi.org/10.1007/s10750-012-1341-4