Abstract
When two ecosystem engineers share the same natural environment, the outcome of their interaction will be unclear if they have contrasting habitat-modifying effects (e.g., sediment stabilization vs. sediment destabilization). The outcome of the interaction may depend on local environmental conditions such as season or sediment type, which may affect the extent and type of habitat modification by the ecosystem engineers involved. We mechanistically studied the interaction between the sediment-stabilizing seagrass Zostera noltii and the bioturbating and sediment-destabilizing lugworm Arenicola marina, which sometimes co-occur for prolonged periods. We investigated (1) if the negative sediment destabilization effect of A. marina on Z. noltii might be counteracted by positive biogeochemical effects of bioirrigation (burrow flushing) by A. marina in sulfide-rich sediments, and (2) if previously observed nutrient release by A. marina bioirrigation could affect seagrasses. We tested the individual and combined effects of A. marina presence and high porewater sulfide concentrations (induced by organic matter addition) on seagrass biomass in a full factorial lab experiment. Contrary to our expectations, we did not find an effect of A. marina on porewater sulfide concentrations. A. marina activities affected the seagrass physically as well as by pumping nutrients, mainly ammonium and phosphate, from the porewater to the surface water, which promoted epiphyte growth on seagrass leaves in our experimental set-up. We conclude that A. marina bioirrigation did not alleviate sulfide stress to seagrasses. Instead, we found synergistic negative effects of the presence of A. marina and high sediment sulfide levels on seagrass biomass.
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References
Andersen FO, Kristensen E (1992) The importance of benthic macrofauna in decomposition of microalgae in a coastal marine sediment. Limnol Oceanogr 37:1392–1403
Ashforth EJ, Olive PJW, Ward AC (2011) Phylogenetic characterisation of bacterial assemblages and the role of sulphur-cycle bacteria in an Arenicola marina bioturbated mesocosm. Mar Ecol Prog Ser 439:19–30
Asmus H, Asmus RM (1998) The role of macrobenthic communities for sediment-water material exchange in the Sylt-Rømø tidal basin. Senckenb Marit 29:111–119
Asmus RM, Jensen MH, Jensen KM, Kristensen E, Asmus H, Wille A (1998) The role of water movement and spatial scaling for measurement of dissolved inorganic nitrogen fluxes in intertidal sediments. Estuar Coast Shelf Sci 46:221–232
Banta GT, Holmer M, Jensen MH, Kristensen E (1999) Effects of two polychaete worms: Nereis diversicolor and Arenicola marina, on aerobic and anaerobic decomposition in a sandy marine sediment. Aquat Microb Ecol 19:189–204
Bertness MD, Leonard GH (1997) The role of positive interactions in communities: lessons from the intertidal habitats. Ecology 78:1976–1989
Borum J et al (2005) The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. J Ecol 93:148–158
Bos A, van Katwijk MM (2007) Planting density, hydrodynamic exposure and mussel beds affect survival of transplanted intertidal seagrass. Mar Ecol Prog Ser 336:121–129
Bos A, Bouma T, Dekort G, Vankatwijk M (2007) Ecosystem engineering by annual intertidal seagrass beds: sediment accretion and modification. Estuar Coast Shelf Sci 74:344–348
Bouma TJ et al (2005) Trade-offs related to ecosystem engineering: a case study on stiffness of emerging macrophytes. Ecology 86:2187–2199
Bouma TJ, Olenin S, Reise K, Ysebaert T (2009) Ecosystem engineering and biodiversity in coastal sediments: posing hypotheses. Helgol Mar Res 63:95–106
Brun FG, van Zetten E, Cacabelos E, Bouma TJ (2009) Role of two contrasting ecosystem engineers (Zostera noltii and Cymodocea nodosa) on the food intake rate of Cerastoderma edule. Helgol Mar Res 63:19–25
Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125
Cadée GC (1976) Sediment reworking by Arenicola marina on tidal flats in the Dutch Wadden Sea. Neth J Sea Res 10:440–460
Cadée GC (2001) Sediment dynamics by bioturbating organisms. In: Reise K (ed) Ecological comparisons of sedimentary shores. Springer, Berlin, pp 127–236
Calleja ML, Marba N, Duarte CM (2007) The relationship between seagrass (Posidonia oceanica) decline and sulfide porewater concentration in carbonate sediments. Estuar Coast Shelf Sci 73:583–588
Christianen MJA et al (2013) Low-canopy seagrass beds still provide important coastal protection services. Plos One 8:e62413
Crain CM, Bertness MD (2006) Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211–218
Dean RB, Dixon WJ (1951) Simplified statistics for small numbers of observations. Anal Chem 23:636–638
Eklof JS, van der Heide T, Donadi S, van der Zee EM, O’Hara R, Eriksson BK (2011) Habitat-mediated facilitation and counteracting ecosystem engineering interactively influence ecosystem responses to disturbance. Plos One 6:e23229
Eriksson BK, van der Heide T, van de Koppel J, Piersma T, van der Veer HW, Olff H (2010) Major changes in the ecology of the Wadden Sea: human impacts, ecosystem engineering and sediment dynamics. Ecosystems 13:752–764
Flach EC, Beukeman JJ (1994) Density-governing mechanisms in populations of the lugworm Arenicola marina on tidal flats. Mar Ecol Prog Ser 115:139–149
Fonseca M (1989) Sediment stabilization by Halophila decipiens in comparison to other seagrasses. Estuar Coast Shelf Sci 29:501–507
Fonseca MS, Cahalan JA (1992) A preliminary evaluation of wave attenuation by 4 species of seagrass. Estuar Coast Shelf Sci 35:565–576
Govers et al (in revision) Toxic constraints for seagrass patch survival and expansion
Granata TC, Serra T, Colomer J, Casamitjana X, Duarte CM, Gacia E (2001) Flow and particle distributions in a nearshore seagrass meadow before and after a storm. Mar Ecol Prog Ser 218:95–106
Grilo TF, Cardoso PG, Pardal MA (2012) Implications of Zostera noltii recolonization on Hydrobia ulvae population structure success. Mar Environ Res 73:78–84
Grossmann S, Reichardt W (1991) Impact of Arenicola marina on bacteria in intertidal sediments. Mar Ecol Prog Ser 77:85–93
Hansen K, King GM, Kristensen E (1996) Impact of the soft-shell clam Mya arenaria on sulfate reduction in an intertidal sediment. Aquat Microb Ecol 10:181–194
Hines ME, Jones GE (1985) Microbial biogeochemistry and bioturbation in the sediments of Great Bay, New Hampshire. Estuar Coast Shelf Sci 20:729–742
Holmer M, Nielsen SL (1997) Sediment sulfur dynamics related to biomass-density patterns in Zostera marina (eelgrass) beds. Mar Ecol Prog Ser 146:163–171
Hylleberg J (1975) Influence of the lugworm Arenicola marina on porewater nutrient profiles of sandflat sediments. Mar Ecol Prog Ser 62:241–248
Isaksen MF, Finster K (1996) Sulphate reduction in the root zone of the seagrass Zostera noltii on the intertidal flats of a coastal lagoon (Arcachon, France). Mar Ecol Prog Ser 137:187–194
Jacobs R, Hegger HH, Raswillems A (1983) Seasonal variations in the structure of a Zostera community in tidal flats in the SW Netherlands, with special reference to the benthic fauna. Proc K Ned Akad Wetensch Ser C Biol Med Sci 86:347–375
Jones CG, Lawton JH, Shackak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Jørgensen BB (1982) Mineralization of organic matter in the sea bed—the role of sulphate reduction. Nature 296:643–645
Koch EW et al (2009) Non-linearity in ecosystem-services: temporal and spatial variability in coastal protection. Front Ecol Environ 7:29–37
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
Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser 446:285–302
Lamers LPM, Tomassen HBM, Roelofs JGM (1998) Sulfate-induced eutrophication and phytotoxicity in freshwater wetlands. Environ Sci Technol 32:199–205
Lamers LP et al (2013) Sulfide as a soil phytotoxin—a review. Front Plant Sci 4:268
Mascaró O, Valdemarsen T, Holmer M, Pérez M, Romero J (2009) Experimental manipulation of sediment organic content and water column aeration reduces Zostera marina (eelgrass) growth and survival. J Exp Mar Biol Ecol 373:26–34
Meysman FJ, Middelburg JJ, Heip CH (2006) Bioturbation: a fresh look at Darwin’s last idea. Trends Ecol Evol 21:688–695
Nielsen OI, Kristensen E, Holmer M (2003) Impact of Arenicola marina (Polychaeta) on sediment sulfur dynamics. Aquat Microb Ecol 33:95–105
Papaspyrou S, Kristensen E, 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
Passarelli C, Olivier F, Paterson DM, Meziane T, Hubas C (2013) Organisms as cooperative ecosystem engineers in intertidal flats. J Sea Res. doi:10.1016/j.seares.2013.07.010
Peralta G, Bouma TJ, van Soelen J, Perez-Llorens JL, Hernandez I (2003) On the use of sediment fertilization for seagrass restoration: a mesocosm study on Zostera marina L. Aquat Bot 75:95–110
Peralta G, van Duren LA, Morris EP, Bouma TJ (2008) Consequences of shoot density and stiffness for ecosystem engineering by benthic macrophytes in flow dominated areas: a hydrodynamic flume study. Mar Ecol Prog Ser 368:103–115
Peterson CH, Luettich RA, Micheli F, Skilleter GA (2004) Attenuation of water flow inside seagrass canopies of differing structure. Mar Ecol Prog Ser 268:81–92
Philippart CJM (1994) Interactions between Arenicola marina and Zostera noltii on a tidal flat in the Wadden Sea. Mar Ecol Prog Ser 111:251–257
Reise K (2002) Sediment mediated species interactions in coastal waters. J Sea Res 48:127–141
Reise K, Kohlus J (2007) Seagrass recovery in the Northern Wadden Sea? Helgol Mar Res 62:77–84
Reise K, Herre E, Sturm M (2008) Mudflat biota since the 1930s: change beyond return? Helgol Mar Res 62:13–22
Rijken M (1979) Food and food uptake in Arenicola marina. Neth J Sea Res 13:406–421
Romero J, Lee K, Perez M, Mateo MA, Alcoverro T (2006) Nutrient dynamics in seagrass ecosystems. In: Larkum AWD, Orth RJ, Duarte AC (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht
Sand-Jensen K (1977) Effects of epiphytes on eelgrass photo-synthesis. Aquat Bot 3:55–63
Suykerbuyk W et al (2012) Suppressing antagonistic bioengineering feedbacks doubles restoration success. Ecol Appl 22:1224-1231
Timmermann K, Banta GT, Glud RN (2006) Linking Arenicola marina irrigation behavior to oxygen transport and dynamics in sandy sediments. J Mar Res 64:915–938
Tomasko DA, Lapointe BE (1991) Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Mar Ecol Prog Ser 75:9–17
Valdemarsen T, Kristensen E, Holmer M (2010) Sulfur, carbon, and nitrogen cycling in faunated marine sediments impacted by repeated organic enrichment. Mar Ecol Prog Ser 400:37–53
Valdemarsen T, Wendelboe K, Egelund JT, Kristensen E, Flindt MR (2011) Burial of seeds and seedlings by the lugworm Arenicola marina hampers eelgrass (Zostera marina) recovery. J Exp Mar Biol Ecol 410:45–52
Valentine JF, Heck KL, Harper P, Beck M (1994) Effects of bioturbation in controlling turtlegrass (Thalassia testudinum Banks ex König) abundance: evidence from field enclosures and observations in the Northern Gulf of Mexico. J Exp Mar Biol Ecol 178:181–192
Van Beusekom JEE (2005) A historic perspective on Wadden Sea eutrophication. Helgol Mar Res 59:45–54
Van der Heide T, Van Nes EH, Van Katwijk MM, Olff H, Smolders AJP (2011) Positive feedbacks in seagrass ecosystems—evidence from large-scale empirical data. Plos One 6:e16504
Van der Heide T et al (2012) A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336:1432–1434
Van Katwijk MM, Bos AR, De Jonge VN, Hanssen LSAM, Hermus DCR, De Jong DJ (2009) Guidelines for seagrass restoration: importance of habitat selection and donor population, spreading of risks, and ecosystem engineering effects. Mar Pollut Bull 58:179–188
Van Wesenbeeck BK, Van de Koppel J, Herman PMJ, Bakker JP, Bouma TJ (2007) Biomechanical warfare in ecology; negative interactions between species by habitat modification. Oikos 116:742–750
Vermaat JE, Verhagen FCA (1996) Seasonal variation in the intertidal seagrass Zostera noltii Hornem.: coupling demographic and physiological patterns. Aquat Bot 52:259–281
Volkenborn N, Reise K (2006) Lugworm exclusion experiment: responses by deposit feeding worms to biogenic habitat transformations. J Exp Mar Biol Ecol 330:169–179
Volkenborn N, Hedtkamp SIC, van Beusekom JEE, Reise K (2007) Effects of bioturbation and bioirrigation by lugworms (Arenicola marina) on physical and chemical sediment properties and implications for intertidal habitat succession. Estuar Coast Shelf Sci 74:331–343
Wendelboe K, Egelund JT, Flindt MR, 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
Wood ED, Armstron FA, Richards FA (1967) Determination of nitrate in sea water by Cadmium-Copper reduction to nitrite. J Mar Biol Assoc UK 47:23
Acknowledgments
We are grateful to Niki de Lange for helping out during the experiment, to Germa Verheggen and Martin Versteeg for their technical support, to Jelle Eygensteyn for his help with the analyses, and to the people at the NIOZ Yerseke nutrient lab for their help with the nutrient analyses. We also thank three anonymous referees for their suggestions to improve the quality of our manuscript.
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Communicated by Ulrich Sommer.
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Govers, L.L., Pieck, T., Bouma, T.J. et al. Seagrasses are negatively affected by organic matter loading and Arenicola marina activity in a laboratory experiment. Oecologia 175, 677–685 (2014). https://doi.org/10.1007/s00442-014-2916-8
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DOI: https://doi.org/10.1007/s00442-014-2916-8