Influence of benthic macrofauna community shifts on ecosystem functioning in shallow estuaries

Frontiers in Marine Science

Volumn 1, Issue SEP, 2014, Pages

  Kristensen, Erik ^a   Delefosse, Matthieu ^a   Quintana, Cintia O ^a   Flindt, Mogens R ^a   Valdemarsen, Thomas ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Benthic metabolism; Benthic pelagic coupling; Bioturbation; Functional trait; Infaunal polychaetes; Nutrient cycling; Sediment biogeochemistry

Indexed keywords

EID: 85008884137     PISSN: None     EISSN: 22967745     Source Type: Journal    
DOI: 10.3389/fmars.2014.00041     Document Type: Review

References (96)

1. Aller, R. C. (1994). Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation. Chem. Geol. 114, 331-345. doi: 10.1016/0009-2541(94)90062-0
2. Ballantyne, F., Menge, D. N. L., Ostling, A., and Hosseini, P. (2008). Nutrient recycling affects autotroph and ecosystem stoichiometry. Am. Nat. 171, 511-523. doi: 10.1086/528967
3. Banta, G. T., Holmer, M., Jensen, M. H., and Kristensen, E. (1999). Effects of two polychaete worms, Nereis diversicolor and Arenicola marina, on aerobic and anaerobic decomposition in sandy marine sediment. Aquat. Microb. Ecol. 19, 189-204. doi: 10.3354/ame019189
4. Beaugrand, G. (2004). The North Sea regime shift: evidence, causes, mechanisms and consequences. Prog. Oceanogr. 60, 245-262. doi: 10.1016/j.pocean.2004.02.018
5. Bertics, V., and Ziebis, W. (2010). Bioturbation and the role of microniches for sulfate reduction in coastal marine sediments. Environ. Microbiol. 12, 3022-3034. doi: 10.1111/j.1462-2920.2010.02279.x
6. Beukema, J. J., and De Vlas, J. (1979). Population parameters of the lugworm Arenicola marina, lving on tidal flats in the Dutch Wadden Sea. Neth. J. Sea Res. 13, 331-353. doi: 10.1016/0077-7579(79)90010-3
7. Blank, M., Laine, A. O., Jürss, K., and Bastrop, R. (2008). Molecular identification key based on PCR/RFLP for three polychaete sibling species of the genus Marenzelleria, and the species' current distribution in the Baltic Sea. Helgol. Mar. Res. 62, 129-141. doi: 10.1007/s10152-007-0081-8
8. Boero, F. (1999). "Community ecology: a life cycle perspective, " in Perspectives in Ecology, ed A. Farina (Leiden: Backyus Publishers), 335-342.
9. Boero, F., and Bonsdorff, E. (2007). A conceptual framework for marine biodiversity and ecosystem functioning. Mar. Ecol. 28, 134-145. doi: 10.1111/j.1439-0485.2007.00171.x
10. Bonaglia, S., Bartoli, M., Gunnarsson, J. S., Rahm, L., Raymond, C., Svensson, O., et al. (2013). Effect of reoxygenation and Marenzelleria spp. bioturbation on Baltic Sea sediment metabolism. Mar. Ecol. Prog. Ser. 482, 43-55. doi: 10.3354/meps10232
11. Bonsdorff, E., Norkko, A., and Boström, C. (1995). "Recruitment and population maintenance of the bivalve Macoma balthica (L.)-factors affecting settling success and early survival on shallow sandy bottoms, " in Biology and Ecology of Shallow Coastal Waters. Proceedings of the 28th EMBS, 1993, eds A. Eleftheriou, A. D. Ansell, and C. J. Smith (Fredensborg: Olsen & Olsen), 253-260.
12. Brady, D. C., Testa, J. M., Di Toro, D. M., Boynton, W. R., and Kemp, W. M. (2013). Sediment flux modeling: calibration and application for coastal systems. Estuar. Coast. Shelf Sci. 117, 107-124. doi: 10.1016/j.ecss.2012.11.003
13. Braeckman, U., Provoost, P., Gribsholt, B., Van Gansbeke, D., Middelburg, J. J., Soetaert, K., et al. (2010). Role of macrofauna functional traits and density in biogeochemical fluxes and bioturbation. Mar. Ecol. Prog. Ser. 399, 173-186. doi: 10.3354/meps08336
14. Brigolin, D., Lovato, T., Rubino, A., and Pastres, R. (2011). Coupling early-diagenesis and pelagic biogeochemical models for estimating the seasonal variability of N and P fluxes at the sediment-water interface: application to the northwestern Adriatic coastal zone. J. Mar. Syst. 87, 239-255. doi: 10.1016/j.jmarsys.2011.04.006
15. Bulling, M. T., White, P. C. L., Raffaelli, D., and Pierce, G. J. (2006). Using model systems to address the biodiversity-ecosystem functioning process. Mar. Ecol. Prog. Ser. 311, 295-309. doi: 10.3354/meps311295
16. Christensen, B., Vedel, A., and Kristensen, E. (2000). Carbon and nitrogen fluxes in sediment inhabited by suspension-feeding (Nereis diversicolor) and non-suspension-feeding (Nereis virens) polychaetes. Mar. Ecol. Prog. Ser. 192, 203-217. doi: 10.3354/meps192203
17. Crowe, T. P., Cusson, M., Bulleri, F., Davoult, D., Arenas, F., Aspden, R., et al. (2013). Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning. PLoS ONE 8:e66238. doi: 10.1371/journal.pone.0066238
18. Delefosse, M., Banta, G. T., Canal-Vergés, P., Penha-Lopes, G., Quintana, C. O., Valdemarsen, T., et al. (2012). Macrobenthic community response to the Marenzelleria viridis (Polychaeta) invasion of a Danish estuary. Mar. Ecol. Prog. Ser. 461, 83-94. doi: 10.3354/meps09821
19. Delefosse, M., and Kristensen, E. (2012). Burial of Zostera marina seeds in sediment inhabited by three polychaetes: laboratory and field studies. J. Sea Res. 71, 41-49. doi: 10.1016/j.seares.2012.04.006
20. Doering, P. H. (1989). On the contribution of the benthos to pelagic production. J. Mar. Res. 47, 371-383. doi: 10.1357/002224089785076253
21. Dornhoffer, T., Waldbusser, G. G., and Meile, C. (2012). Burrow patchiness and oxygen fluxes in bioirrigated sediments. J. Exp. Mar. Biol. Ecol. 412, 81-86. doi: 10.1016/j.jembe.2011.11.004
22. Eriksson, B. K., van der Heide, T., van de Koppel, J., Piersma, T., van der Veer, H. W., and Olff, H. (2010). Major changes in the ecology of the Wadden Sea: human impacts, ecosystem engineering and sediment dynamics. Ecosystems 13, 752-764. doi: 10.1007/s10021-010-9352-3
23. Essink, K. (1999). Dispersal and development of Marenzelleria spp. (Polychaeta, Spionidae) populations in NW Europe and The Netherlands. Helgol. Meeresunters. 52, 367-372. doi: 10.1007/BF02908910
24. Evrard, V., Glud, R. N., and Cook, P. L. M. (2013). The kinetics of denitrification in permeable sediments. Biogeochemistry 113, 563-572. doi: 10.1007/s10533-012-9789-x
25. Flach, E. C. (1992). The influence of four macrozoobenthic species on the abundance of the amphipod Corophium volutator on tidal flats of the Wadden Sea. Neth. J. Sea Res. 29, 379-394. doi: 10.1016/0077-7579(92)90077-R
26. Fyns Amt. (1997). Vandmiljøovervågning-Kystvande 1996. Odense: Fyns Amt.
27. Fyns Amt. (2004). Vandmiljøovervågning-Kystvande 2003. Odense: Fyns Amt.
28. Grall, J., and Chauvaud, L. (2002). Marine eutrophication and benthos: the need for new approaches and concepts. Glob. Change Biol. 8, 813-830. doi: 10.1046/j.1365-2486.2002.00519.x
29. Grenz, C., Cloern, J. E., Hager, S. W., and Cole, B. E. (2000). Dynamics of nutrient cycling and related benthic nutrient and oxygen fluxes during a spring phytoplankton bloom in South San Francisco Bay (USA). Mar. Ecol. Prog. Ser. 197, 67-80. doi: 10.3354/meps197067
30. Greve, T. M., Krause-Jensen, D., Rasmussen, M. B., and Christensen, P. B. (2005). Means of rapid eelgrass (Zostera marina L.) recolonization in former dieback areas. Aquat. Bot. 82, 143-156. doi: 10.1016/j.aquabot.2005.03.004
31. Hansen, K., and Kristensen, E. (1997). Impact of macrofaunal recolonization on benthic metabolism and nutrient fluxes in a shallow marine sediment previously overgrown with macroalgal mats. Estuar. Coast. Shelf Sci. 45, 613-628. doi: 10.1006/ecss.1996.0229
32. Hansen, K., and Kristensen, E. (1998). The impact of the polychaete Nereis diversicolor and enrichment with macroalgal (Chaetomorpha linum) detritus on benthic metabolism and nutrient dynamics in organic-poor and organic-rich sediment. J. Exp. Mar. Biol. Ecol. 231, 201-223. doi: 10.1016/S0022-0981(98)00070-7
33. Hare, S. R., and Mantua, N. J. (2000). Emperical evidence for North Pacific regime shifts in 1977 and 1989. Prog. Oceanogr. 47, 103-145. doi: 10.1016/S0079-6611(00)00033-1
34. Hauxwell, J., Cebrián, J., Furlong, C., and Valiela, I. (2001). Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82, 1007-1022. doi: 10.1890/0012-9658(2001)082[1007:MCCTEZ]2.0.CO;2
35. Hedges, J. I., and Keil, R. G. (1995). Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar. Chem. 49, 81-115. doi: 10.1016/0304-4203(95)00008-F
36. Hochard, S., Pinazoa, C., Rochelle-Newall, E., and Pringault, O. (2012). Benthic pelagic coupling in a shallow oligotrophic ecosystem: importance of microphytobenthos and physical forcing. Ecol. Model. 247, 307-318. doi: 10.1016/j.ecolmodel.2012.07.038
37. Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., et al. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3-35. doi: 10.1890/04-0922
38. Hulthe, G., Hulth, S., and Hall, P. O. J. (1998). Effect of oxygen on degradation rate of refractory and labile organic matter in continental margin sediments. Geochim. Cosmochim. Acta 62, 1319-1328. doi: 10.1016/S0016-7037(98)00044-1
39. Ieno, E. N., Solan, M., Batty, P., and Pierce, G. J. (2006). How biodiversity affects ecosystem functioning: roles of infaunal species richness, identity and density in the marine benthos. Mar. Ecol. Prog. Ser. 311, 263-271. doi: 10.3354/meps311263
40. Jovanovic, Z., Larsen, M., Quintana, C. O., Kristensen, E., and Glud, R. N. (2014). Oxygen dynamics and porewater transport in sediments inhabited by the invasive polychaete Marenzelleria viridis. Mar. Ecol. Prog. Ser. 504, 181-192. doi: 10.3354/meps10737
41. Karlson, K., Hulth, S., Ringdahl, K., and Rosenberg, R. (2005). Experimental recolonisation of Baltic Sea reduced sediments: survival of benthic macrofauna and effects on nutrient cycling. Mar. Ecol. Prog. Ser. 294, 35-49. doi: 10.3354/meps294035
42. Kessler, A. J., Glud, R. N., Cardenas, M. B., Larsen, M., Bourke, M. F., and Cook, P. L. M. (2012). Quantifying denitrification in rippled permeable sands through combined flume experiments and modeling. Limnol. Oceanogr. 57, 1217-1232. doi: 10.4319/lo.2012.57.4.1217
43. Koed, A., Rasmussen, G., and Rasmussen, E. B. (1997). Havørredbestandene i Odense Å og Stavids Å Systemerne i Relation til Fynsværket. DFU-Report 29-97, Frederiksberg: DSR Print.
44. Kotta, J., Kotta, I., Simm, M., Lankov, A., Lauringson, V., Põllumäe, A., et al. (2006). Ecological consequences of biological invasions: three invertebrate case studies in the north-eastern Baltic Sea. Helgol. Mar. Res. 60, 106-112. doi: 10.1007/s10152-006-0027-6
45. Kristensen, E. (2000). Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426, 1-24. doi: 10.1023/A:1003980226194
46. Kristensen, E. (2001). Impact of polychaetes (Nereis spp. and Arenicola marina) on carbon biogeochemistry in coastal marine sediment. Geochem. Trans. 2, 92-104. doi: 10.1186/1467-4866-2-92
47. Kristensen, E., Delefosse, M., Quintana, C. O., Banta, G. T., Petersen, H. C., and Jørgensen, B. (2013). Distribution pattern of benthic invertebrates in Danish estuaries: the use of Taylor's power law as a species-specific indicator of dispersion and behavior. J. Sea Res. 77, 70-78. doi: 10.1016/j.seares.2012.10.003
48. Kristensen, E., and Hansen, K. (1999). Transport of carbon dioxide and ammonium in bioturbated (Nereis diversicolor) coastal, marine sediments. Biogeochemistry 45, 147-168. doi: 10.1007/BF01106779
49. Kristensen, E., Hansen, T., Delefosse, M., Banta, G. T., and Quintana, C. O. (2011). Contrasting effects of the polychaetes Marenzelleria viridis and Nereis diversicolor on benthic metabolism and solute transport in sandy coastal sediment. Mar. Ecol. Prog. Ser. 425, 125-139. doi: 10.3354/meps09007
50. 2, NO-3 and SO2-4), with emphasis on substrate origin, degradation kinetics and the role of bioturbation. Geochim. Cosmochim. Acta 65, 419-434. doi: 10.1016/S0016-7037(00)00532-9
51. Kristensen, E., Penha-Lopes, G., Delefosse, M., Valdemarsen, T., Quintana, C. O., and Banta, G. T. (2012). What is bioturbation? Need for a precise definition for fauna in aquatic sciences. Mar. Ecol. Prog. Ser. 446, 285-302. doi: 10.3354/meps09506
52. Kronvang, B., Andersen, H. E., Børgesen, C., Dalgaard, T., Larsen, S. E., Bøgestrand, J., et al. (2008). Effects of policy measures implemented in Denmark on nitrogen pollution of the aquatic environment. Environ. Sci. Policy 11, 144-152. doi: 10.1016/j.envsci.2007.10.007
53. Lindqvist, S., Gilbert, F., Eriksson, S. P., and Hulth, S. (2013). Activities by Hediste diversicolor under different light regimes: experimental quantification of particle reworking using time-resolved imaging. J. Exp. Mar. Biol. Ecol. 448, 240-249. doi: 10.1016/j.jembe.2013.06.014
54. Lohrer, A. M., Halliday, N. J., Thrush, S. F., Hewitt, J. E., and Rodil, I. F. (2010). Ecosystem functioning in a disturbance-recovery context: contribution of macrofauna to primary production and nutrient release on intertidal sandflats. J. Exp. Mar. Biol. Ecol. 390, 6-13. doi: 10.1016/j.jembe.2010.04.035
55. Lohrer, A. M., Thrush, S. F., and Gibbs, M. M. (2004). Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431, 1092-1095. doi: 10.1038/nature03042
56. Mauna, A. C., Acha, E. M., Lasta, M. L., and Iribarne, O. O. (2011). The influence of a large SW Atlantic shelf-break frontal system on epibenthic community composition, trophic guilds, and diversity. J. Sea Res. 66, 39-46. doi: 10.1016/j.seares.2011.04.014
57. Na, T., Gribsholt, B., Galaktionov, O. S., Lee, T., and Meysman, F. J. R. (2008). Influence of advective bio-irrigation on carbon and nitrogen cycling in sandy sediments. J. Mar. Res. 66: 691-722. doi: 10.1357/002224008787536826
58. Nielsen, O. I., Gribsholt, B., Kristensen, E., and Revsbech, N. P. (2004). Microscale distribution of oxygen and nitrate in sediment inhabited by Nereis diversicolor; spatial patterns and estimated reaction rates. Aquat. Microb. Ecol. 34, 23-32. doi: 10.3354/ame034023
59. Nizzoli, D., Bartoli, M., Cooper, M., Welsh, D. T., Underwood, G. J. C., and Viaroli, P. (2007). Implications for oxygen, nutrient fluxes and denitrification rates during the early stage of sediment colonisation by the polychaete Nereis spp. in four estuaries. Estuar. Coast. Shelf Sci. 75, 125-134. doi: 10.1016/j.ecss.2007.03.035
60. Norkko, A., Villnäs, A., Norkko, J., Valanko, S., and Pilditch, C. (2013). Size matters: implications of the loss of large individuals for ecosystem function. Sci. Rep. 3, 2646. doi: 10.1038/srep02646
61. Papaspyrou, S., Kristensen, E., and Christensen, B. (2007). Arenicola marina (Polychaeta) and organic matter mineralisation in sandy marine sediments; in situ and microcosm comparison. Estuar. Coast. Shelf Sci. 72, 213-222. doi: 10.1016/j.ecss.2006.10.020
62. Papaspyrou, S., Thessalou-Legaki, M., and Kristensen, E. (2010). The influence of infaunal (Nereis diversicolor) abundance on degradation of organic matter in sandy sediments. J. Exp. Mar. Biol. Ecol. 393, 148-157. doi: 10.1016/j.jembe.2010.07.015
63. Pérez-Ruzafa, A., Marcos, C., Pérez-Ruzafa, I. M., and Pérez-Marcos, M. (2011). Coastal lagoons: "transitional ecosystems" between transitional and coastal waters. J. Coast. Conserv. 15, 369-392. doi: 10.1007/s11852-010-0095-2
64. Petersen, J. D., Rask, N., Madsen, H. B., Jørgensen, O. T., Petersen, S. E., Nielsen, S. V. K., et al. (2009). Odense Pilot River Basin: implementation of the EU Water Framework Directive in a shallow eutrophic estuary (Odense Fjord, Denmark) and its upstream catchment. Hydrobiologia 629, 71-89. doi: 10.1007/s10750-009-9774-0
65. Petersen, J. K., Hansen, J. W., Laursen, M. B., Clausen, P., Carstensen, J., and Conley, D. J. (2008). Regime shift in a coastal marine ecosystem. Ecol. Appl. 18, 497-510. doi: 10.1890/07-0752.1
66. Pischedda, L., Cuny, P., Esteves, J. L., Poggiale, J.-C., and Gilbert, F. (2012). Spatial oxygen heterogeneity in a Hediste diversicolor irrigated burrow. Hydrobiologia 680, 109-124. doi: 10.1007/s10750-011-0907-x
67. Quintana, C. O., Hansen, T., Delefosse, M., Banta, G. T., and Kristensen, E. (2011). Burrow ventilation and associated porewater irrigation by the polychaete Marenzelleria viridis. J. Exp. Mar. Biol. Ecol. 397, 179-187. doi: 10.1016/j.jembe.2010.12.006
68. Quintana, C. O., Kristensen, E., and Valdemarsen, T. (2013). Impact of the invasive polychaete Marenzelleria viridis on the biogeochemistry of sandy marine sediments. Biogeochemistry 115, 95-109. doi: 10.1007/s10533-012-9820-2
69. Rasmussen, B., and Josefson, A. B. (2002). Consistent estimates for the residence time of micro-tidal estuaries. Estuar. Cost. Shelf Sci. 54, 65-73. doi: 10.1006/ecss.2001.0836
70. Reise, K., Olenin, S., and Thieltges, D. W. (2006). Are aliens threatening European aquatic coastal ecosystems? Helgol. Mar. Res. 60, 77-83. doi: 10.1007/s10152-006-0024-9
71. Reitze, M., and Schöttler, U. (1989). The time dependence of adaptation to reduced salinity in the lugworm Arenicola marina L. (Annelida: Polychaeta). Comp. Biochem. Physiol. 93A, 549-559. doi: 10.1016/0300-9629(89)90009-1
72. Riisgård, H. U. (1991). Suspension feeding in the polychaete Nereis diversicolor. Mar. Ecol. Prog. Ser. 70, 29-37. doi: 10.3354/meps070029
73. Riisgård, H. U., and Banta, G. T. (1998). Irrigation and deposit feeding by the lugworm Arenicola marina, characteristics and secondary effects on the environment. A review of current knowledge. Vie Milieu 48, 243-257
74. Riisgård, H. U., Berntsen, I., and Tarp, B. (1996). The lugworm (Arenicola marina) pump: characteristics, modeling and energy cost. Mar. Ecol. Prog. Ser. 138, 149-156. doi: 10.3354/meps138149
75. Riisgård, H. U., Jensen, M. H., and Rask, N. (2008). "Odense fjord and kerteminde fjord/kertinge nor, " in Ecology of Baltic Coastal Waters. Ecological Studies 197, ed U. Schiewer (Berlin: Springer), 361-394. doi: 10.1007/978-3-540-73524-3_16
76. Riisgård, H. U., and Larsen, P. S. (2005). Water pumping and analysis of flow in burrowing zoobenthos: an overview. Aquat. Ecol. 39, 237-258. doi: 10.1007/s10452-004-1916-x
77. Scheffer, M., and Carpenter, S. R. (2003). Catastrophic shifts in ecosystems: linking theory and observation. Trends Ecol. Evol. 18, 648-656. doi: 10.1016/j.tree.2003.09.002
78. Shull, D. H., Benoit, J. M., Wojcik, C., and Senning, J. R. (2009). Infaunal burrow ventilation and pore-water transport in muddy sediments. Estuar. Coast. Shelf Sci. 83, 277-286. doi: 10.1016/j.ecss.2009.04.005
79. Shumway, S. A., and Davenport, J. (1977). Some aspects of the physiology of Arenicola marina (Polychaeta) exposed to fluctuating salinities. J. Mar. Biol. Ass. U.K. 57, 907-924. doi: 10.1017/S0025315400026011
80. Solan, M., Raffaelli, D. G., Paterson, D. M., White, P. C. L., and Pierce, G. J. (2006). Introduction. Mar. Ecol. Prog. Ser. 311, 175-178. doi: 10.3354/meps311175
81. Spencer, M., Birchenough, S. N. R., Mieszkowska, N., Robinson, L. A., Simpson, S. D., Burrows, M. T., et al. (2010). Temporal change in UK marine communities: trends or regime shifts? Mar. Ecol. 32, 10-24. doi: 10.1111/j.1439-0485.2010.00422.x
82. Stief, P. (2013). Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10, 7829-7846. doi: 10.5194/bg-10-7829-2013
83. Suess, E. (1980). Particulate organic carbon flux in the oceans-surface productivity and oxygen utilization. Nature 288, 260-263. doi: 10.1038/288260a0
84. Sun, M.-Y., Lee, C., and Aller, R. C. (1993). Laboratory studies of oxic and anoxic degradation of chlorophyll-a in Long Island Sound sediments. Geochim. Cosmochim. Acta 57, 147-157. doi: 10.1016/0016-7037(93)90475-C
85. Teixeira, I. G., Crespo, B. G., Nielsen, T. G., and Figueiras, F. G. (2014). Stratification-mixing cycles and plankton dynamics in a shallow estuary (Limfjord, Denmark). J. Plankton Res. 36, 475-489. doi: 10.1093/plankt/fbt107
86. Thrush, S. F., Hewitt, J. E., Gibbs, M., Lundquist, C., and Norkko, A. (2006). Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9, 1029-1040. doi: 10.1007/s10021-005-0068-8
87. Valdemarsen, T., and Kristensen, E. (2010). Degradation of dissolved organic monomers and short-chain fatty acids in sandy marine sediment by fermentation and sulfate reduction. Geochim. Cosmochim. Acta 74, 1593-1605. doi: 10.1016/j.gca.2009.12.009
88. Valdemarsen, T., Quintana, C. O., Kristensen, E., and Flindt, M. R. (2014). Recovery of organic-enriched sediments through microbial degradation: implications for eutrophic estuaries. Mar. Ecol. Prog. Ser. 503, 41-58. doi: 10.3354/meps10747
89. Valdemarsen, T., Wendelboe, K., Egelund, J. T., Kristensen, E., and Flindt, M. R. (2011). Burial of seeds and seedlings by the lugworm Arenicola marina hampers eelgrass (Zostera marina) recovery. J. Exp. Mar. Biol. Ecol. 410, 45-52. doi: 10.1016/j.jembe.2011.10.006
90. van Nes, E. H., Amaro, T., Scheffer, M., and Duineveld, G. C. A. (2007). Possible mechanisms for a marine benthic regime shift in the North Sea. Mar. Ecol. Prog. Ser. 330, 39-47. doi: 10.3354/meps330039
91. Viitasalo-Frösén, S., Laine, A. O., and Lehtiniemi, M. (2009). Habitat modification mediated by motile surface stirrers versus semi-motile burrowers: potential for a positive feedback mechanism in a eutrophied ecosystem. Mar. Ecol. Prog. Ser. 376, 21-32. doi: 10.3354/meps07788
92. Volkenborn, N., and Reise, K. (2006). Lugworm exclusion experiment: Responses by deposit feeding worms to biogenic habitat transformations. J. Exp. Mar. Biol. Ecol. 330, 169-179. doi: 10.1016/j.jembe.2005.12.025
93. Wendelboe, K., Egelund, J. T., Flindt, M. R., and Valdemarsen, T. (2013). Impact of lugworms (Arenicola marina) on mobilization and transport of fine particles and organic matter in marine sediments. J. Sea Res. 76, 31-38. doi: 10.1016/j.seares.2012.10.013
94. 2 dynamics: effects of fauna activity. Limnol. Oceanogr. 49, 1471-1481. doi: 10.4319/lo.2004.49.5.1471
95. Ysebaert, T., Fettweis, M., Meire, P., and Sas, M. (2005). Benthic variability in intertidal soft-sediments in the mesohaline part of the Schelde estuary. Hydrobiologia 540, 197-216. doi: 10.1007/s10750-004-7144-5
96. Zipperle, A., and Reise, K. (2005). Freshwater springs on intertidal sand flats cause a switch in dominance among polychaete worms. J. Sea Res. 54, 143-150. doi: 10.1016/j.seares.2005.01.003