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Eelgrass fairy rings: sulfide as inhibiting agent

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Abstract

Distinct ‘fairy rings’ consisting of narrow fringes of eelgrass (Zostera marina L.) expand radially over a bottom of chalk plates outside the calcium carbonate cliffs of the island of Møn, Denmark. We conducted a survey to evaluate possible explanations for the formation of the rings and, more specifically, for the apparent die-off of eelgrass shoots on the inner side of the rings. The fairy rings were up to 15 m in diameter consisting of 0.3- to 1-m-wide zones of sea grass shoots at densities of up to 1,200 shoots m−2 and rooted in an up to 10-cm-thick sediment layer. On the outer side, shoots expanded over the bare chalk plates. On the inner side, shoots were smaller, had lower absolute and specific leaf growth, shoot density was lower and the sediment eroded leaving the bare chalk with scattered boulders behind. Sediment organic matter and nutrients and tissue nutrient contents were not different among positions. Sediment pools of acid volatile sulfides and chromium-reducible sulfur increased from outer to the middle positions of the rings, and so did total sulfur content of eelgrass tissues, while tissue δ34S isotope ratios, regardless of position in the fringes, were low reflecting substantial invasion of sulfide from the sediment. Neither the clonal growth pattern of eelgrass, sediment burial of shoots, hydrodynamic forcing nor nutrient limitation could explain the ring-shaped pattern. We conclude that the most likely explanation must be found in invasion of eelgrass shoots by toxic sulfide accumulating in the sediment due to low iron availability in the carbonate-rich environment.

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References

  • Albrecht CF, Joubert JJ, De Rycke PH (2001) Origin of the enigmatic, circular, barren patches (‘Fairy Rings’) of the pro-Namib. S Afr J Sci 97:23–27

    Google Scholar 

  • Andersen JM (1976) Ignition method for determination of total phosphorus in lake sediments. Water Res 10:329–331

    Article  CAS  Google Scholar 

  • Barko JW, Smart RM (1983) Effects of organic matter additions to sediment on the growth of aquatic plants. J Ecol 71:161–175

    Article  CAS  Google Scholar 

  • Blenis PV, Chow PS, Duncan I, Knowles NR (2004) Cyanide levels near fairy rings affect the growth of grass and fungi. Can J Bot 82:1324–1329

    Article  CAS  Google Scholar 

  • Borum J, Pedersen O, Greve TM, Frankovich TA, Zieman JC, Fourqurean JW, Madden C (2005) The potential role of plant oxygen and sulfide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. J Ecol 93:148–158

    Article  CAS  Google Scholar 

  • Castellanos EM, Figueroa ME, Davy AJ (1994) Nucleation and facilitation in saltmarsh succession: interactions between Spartina maritima and Arthrocnemum perenne. J Ecol 82:239–248

    Article  Google Scholar 

  • Chambers RM, Fourqurean JW, Macko SA, Hoppenot R (2001) Biogeochemical effects of iron availability on primary producers in a shallow marine carbonate environment. Limnol Oceanogr 46:1278–1286

    Article  CAS  Google Scholar 

  • Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458

    Article  CAS  Google Scholar 

  • Dooley FD, Wyllie-Echeverria S, Roth MB, Ward PD (2013) Tolerance and response of Zostera marina seedlings to hydrogen sulfide. Aquat Bot 105:7–10

    Article  CAS  Google Scholar 

  • Duarte CM (1990) Seagrass nutrient content. Mar Ecol Prog Ser 67:201–207

    Article  Google Scholar 

  • Eaton A, Clesceri L, Greenberg A (1995) Standard methods for the examination of water and wastewater. American Public Health Association, Washington DC

    Google Scholar 

  • Fonseca MS, Kenworthy WJ (1987) Effects of current on photosynthesis and distribution of seagrasses. Aquat Bot 27:59–78

    Article  Google Scholar 

  • Fossing H, Jørgensen BB (1989) Measurement of bacterial sulphate reduction in sediments: evaluation of a single-step chromium reduction method. Biogeochemistry 8:205–222

    Article  CAS  Google Scholar 

  • Frederiksen MS, Holmer M, Borum J, Kennedy H (2006) Temporal and spatial variation in sulfide invasion in eelgrass (Zostera marina L.) as reflected by its sulfur isotopic composition. Limnol Oceanogr 51:2308–2318

    Article  CAS  Google Scholar 

  • Garcias-Bonet N, Marbà N, Holmer M, Duarte CM (2008) Effects of sulfides on seagrass Posidonia oceanica meristematic activity. Mar Ecol Prog Ser 372:1–6

    Article  CAS  Google Scholar 

  • Greve TM, Borum J, Pedersen O (2003) Meristematic oxygen variability in eelgrass (Zostera marina L.). Limnol Oceanogr 48:210–216

    Article  Google Scholar 

  • Holmer M (2009) Productivity and biogeochemical cycling in seagrass ecosystems. In: Perillo GME, Wolanski E, Cahoon DR, Brinson MM (eds) Coastal wetlands: an integrated ecosystem approach. Elsevier Science, Amsterdam, pp 375–401

    Google Scholar 

  • Holmer M, Duarte CM, Marbá N (2005a) Iron additions reduce sulfate reduction rates and improve seagrass growth on organic-enriched carbonate sediments. Ecosystems 8:721–730

    Article  CAS  Google Scholar 

  • Holmer M, Frederiksen MS, Møllegaard H (2005b) Sulfur accumulation in eelgrass (Zostera marina L.) and effect of sulfur on eelgrass growth. Aquat Bot 81:367–379

    Article  CAS  Google Scholar 

  • Jensen HS, McGlathery KJ, Marino R, Howarth RW (1998) Forms and availability of sediment phosphorus in carbonate sand of Bermuda seagrass beds. Limnol Oceanogr 43:799–810

    Article  CAS  Google Scholar 

  • Koch EW (1999) Sediment resuspension in a shallow Thalassia testudinum banks ex König bed. Aquat Bot 65:269–280

    Article  Google Scholar 

  • Koch MS, Erskine JM (2001) Sulfide as a phytotoxin to the tropical seagrass Thalassia testudinum: interactions with light, salinity and temperature. J Exp Mar Biol Ecol 266:81–95

    Article  CAS  Google Scholar 

  • Olesen B, Sand-Jensen K (1994) Patch dynamics of eelgrass, Zostera marina. Mar Ecol Prog Ser 106:144–156

    Article  Google Scholar 

  • Pedersen O, Binzer T, Borum J (2004) Sulphide intrusion in eelgrass (Zostera marina L.). Plant Cell Environ 27:595–602

    Article  CAS  Google Scholar 

  • Peter M (2006) Ectomycorrhizal fungi—fairy rings and the wood-wide web. New Phytol 171:685–687

    Article  Google Scholar 

  • Pulido C, Borum J (2010) Eelgrass (Zostera marina) tolerance to anoxia. J Exp Mar Biol Ecol 385:8–13

    Article  Google Scholar 

  • Raun AL, Borum J, Sand-Jensen K (2010) Influence of sediment organic enrichment and water alkalinity on growth of aquatic isoetid and elodeid plants. Freshw Biol 55:1891–1904

    Article  Google Scholar 

  • Sand-Jensen K, Pedersen O, Binzer T, Borum J (2005) Contrasting oxygen dynamics in the freshwater isoetid Lobelia dortmanna and the marine seagrass Zostera marina. Ann Bot 96:613–623

    Article  Google Scholar 

  • Sheffer E, Yizhag H, Gilad E, Shachak M, Meron E (2007) Why do plants in resource-deprived environments form rings? Ecol Complex 4:192–200

    Article  Google Scholar 

  • Sintes T, Marbà N, Duarte CM (2006) Modeling nonlinear seagrass clonal growth: assessing the efficiency of space occupation across the seagrass flora. Estuaries Coast 29:72–80

    Google Scholar 

  • Snowden RED, Wheeler BD (1993) Iron toxicity to fen plant species. J Ecol 81:35–46

    Article  CAS  Google Scholar 

  • Solórzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceangr 14:799–801

    Article  Google Scholar 

  • Stone EL, Thorp L (1971) Lycopodium fairy rings: effects on soil nutrient release. Soil Sci Soc Am Proc 35:991–997

    Article  CAS  Google Scholar 

  • van der Heide T, Bouma TJ, van Nes EH, van de Koppel J, Scheffer M, Roelofs JGM, van Katwijk MM, Smolders AJP (2010) Spatial self-organized patterning in seagrasses along a depth gradient of an intertidal ecosystem. Ecology 91:362–369

    Article  Google Scholar 

  • van Rooyen MW, Theron GK, van Rooyen N, Jankowitz WJ, Matthews WS (2004) Mysterious circles in the Namib Desert: review of hypotheses on their origin. J Arid Environ 57:467–485

    Article  Google Scholar 

  • van Wijck C, de Groot C-J, Grillas P (1992) The effect of anaerobic sediment on the growth of Potamogeton pectinatus L.: the role of organic matter, sulphide and ferrous iron. Aquat Bot 44:31–49

    Article  Google Scholar 

  • Zieman JC (1974) Methods for the study of the growth and production of the turtle grass, Thalassia testudinum König. Aquaculture 4:139–143

    Article  Google Scholar 

  • Zopfi J, Kjær T, Nielsen LP, Jørgensen BB (2001) Ecology of Thioplaca spp.: nitrate and sulfur storage in relation to chemical microgradients and influence of Thioplaca spp. on the sedimentary nitrogen cycle. App Environ Microbiol 67:5530–5537

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank LVSE Petersen and B. Kjøller for technical assistance, and we are grateful for the logistic support provided by Geocenter Møns Klint. We also thank Jacob Topsøe Johansen for his permission to use the photo of the rings. The study was funded by the Danish Strategic Science Foundation through grant DSF 09-063190.

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Authors and Affiliations

  1. Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, Universitetsparken 4, 2100, Copenhagen Ø, Denmark

    Jens Borum, Ane Løvendahl Raun & Ole Pedersen

  2. Institute of Biology, University of Southern Denmark, Campusvej 55, 5230, Odense M, Denmark

    Harald Hasler-Sheetal, Mia Østergaard Pedersen & Marianne Holmer

  3. Institute of Advanced Studies, University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Ole Pedersen

Authors
  1. Jens Borum
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  2. Ane Løvendahl Raun
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  3. Harald Hasler-Sheetal
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  4. Mia Østergaard Pedersen
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  5. Ole Pedersen
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  6. Marianne Holmer
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Corresponding author

Correspondence to Jens Borum.

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Communicated by K. Bischof.

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Borum, J., Raun, A.L., Hasler-Sheetal, H. et al. Eelgrass fairy rings: sulfide as inhibiting agent. Mar Biol 161, 351–358 (2014). https://doi.org/10.1007/s00227-013-2340-3

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  • DOI: https://doi.org/10.1007/s00227-013-2340-3

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