Estuaries and Coasts

, Volume 40, Issue 2, pp 553–563 | Cite as

Depth-Related Changes in Reproductive Strategy of a Cold-Temperate Zostera marina Meadow

  • Birgit OlesenEmail author
  • Dorte Krause-Jensen
  • Peter Bondo Christensen


Biomass allocation and demographic characteristics of a Danish Zostera marina population were determined along a depth gradient of light and exposure to evaluate the reproductive strategy for meadow maintenance and recovery. From May to September, biomass, shoot growth and reproductive allocation were measured monthly at three depths (1.8, 4 and 6 m). Also, seedling survival along the deep edge (6.2 m) of the studied meadow was followed over a 12-month period. Shoot density and biomass showed pronounced differences among depths with up to 12-fold lower shoot density and 6-fold lower biomass at deep compared to shallow sites. Comparatively, little variation was found in leaf formation rates and rhizome elongation rates among depths. However, new shoots formed through vegetative reproduction and surviving until September constituted a significantly higher fraction of total shoot density in shallow water (45.7 %) than in deep water (17.3–21.1 %). Conversely, allocation to sexual reproduction was highest at intermediate and high water depths where the proportion of reproductive shoots to total shoot density at time of maximum density was 21.1 and 10.6 %, respectively, and only 3.9 % at the shallow depth. Seed production was also higher at intermediate depth (1970 seeds m−2) than at the upper (1230 seeds m−2) and lower (760 seeds m−2) distribution limit. Seedling recruitment within the meadow took place at all sampling depths but no seedlings persisted throughout the summer period, whereas 8 % of the seedlings established in bare areas along the deep meadow edge (0.43 seedlings m−2) survived their first year. Overall, the results suggest that the shallow edge of the meadow is primarily maintained by vegetative recruitment whereas the deep edge to larger extent relies on sexual recruitment. The intermediate depth zone may act as a buffer zone supporting the maintenance of shallower and deeper eelgrass through seed supply and vegetative expansion, thereby stabilizing the meadow by increasing its resilience towards disturbances and its recovery potential upon disturbances.


Seagrass Eelgrass Depth gradient Clonal growth Sexual recruitment Biomass allocation 



The study received financial support from the “NOVAGRASS” project funded by the Danish Council for Strategic Research.


  1. Abal, E.G., N. Loneragan, P. Bowen, C.J. Perry, J.W. Udy, and W.C. Dennison. 1994. Physiological and morphological responses of the seagrass Zostera capricorni Aschers to light intensity. Journal of Experimental Marine Biology and Ecology 178: 113–129.CrossRefGoogle Scholar
  2. Biber, P.D., W.J. Kenworthy, and H.W. Paerl. 2009. Experimental analysis of the response and recovery of Zostera marina (L.) and Halodule wrightii (Ascher.) to repeated light-limitation stress. Journal of Experimental Marine Biology and Ecology 369: 110–117.CrossRefGoogle Scholar
  3. Bintz, J.C., and S.W. Nixon. 2001. Responses of eelgrass Zostera marina seedlings to reduced light. Marine Ecology Progress Series 223: 133–141.CrossRefGoogle Scholar
  4. Boese, B.L., J.E. Kaldy, P.J. Clinton, P.M. Eldridge, and C.L. Folger. 2009. Recolonization of intertidal Zostera marina L. (eelgrass) following experimental shoot removal. Journal of Experimental Marine Biology and Ecology 374: 69–77.CrossRefGoogle Scholar
  5. Brown, J.H., J.F. Gillooly, A.P. Allen, V.M. Savage, and G.B. West. 2004. Toward a metabolic theory of ecology. Ecology 85: 1771–1789. doi: 10.1890/03-9000.CrossRefGoogle Scholar
  6. Cabaco, S., and R. Santos. 2012. Seagrass reproductive effort as an ecological indicator of disturbance. Ecological Indicators 23: 116–122.CrossRefGoogle Scholar
  7. Cabello-Pasini, A., C. Lara-Turrent, and R.C. Zimmerman. 2002. Effect of storms on photosynthesis, carbohydrate content and survival of eelgrass populations from a coastal lagoon and the adjacent open ocean. Aquatic Botany 74: 149–164.CrossRefGoogle Scholar
  8. Collier, C.J., P.S. Lavery, R. Masini, and P.J. Ralph. 2007. Morphological, growth and meadow characteristics of the seagrass Posidoniasinuosa along a depth-related gradient of light availability. Marine Ecology Progress Series. 337: 103–115.CrossRefGoogle Scholar
  9. Cook, R.E. 1985. Growth and development in clonal plant populations. In Population biology of clonal organisms, eds. J.B.C. Jackson, L.W. Buss, and R.E. Cook, 259–296. New Haven Connecticut: Yale University Press.Google Scholar
  10. Dennison, W.C. 1987. Effects of light on seagrass photosynthesis, growth and depth distribution. Aquatic Botany 27: 15–26.CrossRefGoogle Scholar
  11. Dennison, W.C., and R.S. Alberte. 1982. Photosynthetic responses of Zostera marina L. (eelgrass) to in situ manipulations of light intensity. Oecologia 55: 137–144.CrossRefGoogle Scholar
  12. Dennison, W.C., R.J. Orth, K.A. Moore, J.C. Stevenson, V. Carter, S. Kollar, P.W. Bergstrom, and R.A. Batiuk. 1993. Assessing water quality with submerged aquatic vegetation. Bioscience 43: 86–94.CrossRefGoogle Scholar
  13. Duarte, C.M. 1991. Seagrass depth limits. Aquatic Botany 40: 363–377.CrossRefGoogle Scholar
  14. Duarte, C.M., J.W. Fouqurean, D. Krause-Jensen, and B. Olesen. 2006. Dynamics of seagrass stability and change. In Seagrasses: biology, ecology and conservation, eds. A.W.D. Larkum, R.J. Orth, and C.M. Duarte, 271–294. Dortrecht: Springer.Google Scholar
  15. Duarte, C.M., N. Marbà, D. Krause-Jensen, and M. Sánchez-Camacho. 2007. Testing the predictive power of seagrass depth limit models. Estuaries and Coasts 30: 652–656.CrossRefGoogle Scholar
  16. Fonseca, M.S., J.C. Zieman, G.W. Thayer, and J.S. Fisher. 1983. The role of current velocity in structuring eelgrass (Zostera marina L.) meadows. Estuarine, Coastal and Shelf Science 17: 367–380.CrossRefGoogle Scholar
  17. Fyns Amt. 2002. Kystvande 2001. (in Danish). Vandmiljøovervågning. Natur- og Vandmiljøafdelingen, Fyns Amt.Google Scholar
  18. Greve, T.M., and D. Krause-Jensen. 2005. Stability of eelgrass (Zostera marina L.) depth limits: influence of habitat type. Marine Biology 147: 803–812.CrossRefGoogle Scholar
  19. Greve, T.M., D. Krause-Jensen, M.B. Rasmussen, and P.B. Christensen. 2005. Means of rapid eelgrass (Zostera marina L.) recolonisation in former dieback areas. Aquatic Botany 82: 143–156.CrossRefGoogle Scholar
  20. Holmer, M., and E.J. Bondgaard. 2001. Photosynthetic and growth response of eelgrass to low oxygen and high sulfide concentrations during hypoxic events. Aquatic Botany 70: 29–38.CrossRefGoogle Scholar
  21. Inglis, G.J. 2000. Variation in the recruitment behaviour of seagrass seeds: implications for populations dynamics and resource management. Pacific Conservation Biology 5: 251–259.CrossRefGoogle Scholar
  22. Jarvis, J.C., K.A. Moore, and W.J. Kenworthy. 2012. Characterization and ecological implication of eelgrass life history strategies near the species’ southern limit in the western North Atlantic. Marine Ecology Progress Series 444: 43–56.CrossRefGoogle Scholar
  23. Kenworthy, W.J., C.L. Gallegos, C. Costello, D. Field, and G. di Carlo. 2014. Dependence of eelgrass (Zostera marina) light requirements on sediment organic matter in Massachusetts coastal bays: implications for remediation and restoration. Marine Pollution Bulletin 83: 446–457.CrossRefGoogle Scholar
  24. Kim, S.H., J.-H. Kim, S.R. Park, and K.-S. Lee. 2014. Annual and perennial life history strategies of Zostera marina populations under different light regimes. Marine Ecology Progress Series 509: 1–13.CrossRefGoogle Scholar
  25. Kim, Y.K., S.H. Kim, and K.S. Lee. 2015. Seasonal growth responses of the seagrass Zostera marina under severely diminished light conditions. Estuaries and Coasts 38: 558–568.CrossRefGoogle Scholar
  26. Krause-Jensen, D., A.L. Middelboe, K. Sand-Jensen, and P.B. Christensen. 2000. Eelgrass, Zostera marina, growth along depth gradients: upper boundaries of the variation as a powerful predictive tool. Oikos 91: 233–244.CrossRefGoogle Scholar
  27. Krause-Jensen, D., M.F. Pedersen, and C. Jensen. 2003. Regulation of eelgrass (Zostera marina) cover along depth gradients in Danish coastal waters. Estuaries and Coasts 26: 866–877.CrossRefGoogle Scholar
  28. Krause-Jensen, D., J. Carstensen, S.L. Nielsen, T. Dalsgaard, P.B. Christensen, H. Fossing, and M.B. Rasmussen. 2011. Sea bottom characteristics affect depth limits of eelgrass (Zostera marina L. Marine Ecology Progress Series 425: 91–102. doi: 10.3354/meps09026.CrossRefGoogle Scholar
  29. Lee, K.-S., J.-I. Park, Y.K. Kim, S.R. Park, and J.-H. Kim. 2007. Recolonization of Zostera marina following destruction caused by a red tide algal bloom: the role of new shoot recruitment from seed banks. Marine Ecology Progress Series 342: 105–115.CrossRefGoogle Scholar
  30. Lotze, H.K., H.S. Lenihan, B.J. Bourque, R.H. Bradbury, R.G. Cooke, M.C. Kay, S.M. Kidwell, M.X. Kirby, C.H. Peterson, and J.B.C. Jackson. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312: 1806–1809.CrossRefGoogle Scholar
  31. Munkes, B. 2005. Eutrophication, phase shift, the delay and the potential return in the Greifswalder Bodden, Baltic Sea. Aquatic Sciences 67: 372–381.CrossRefGoogle Scholar
  32. Ochieng, C.A., F.T. Short, and D.I. Walker. 2010. Photosynthetic and morphological responses of eelgrass (Zostera marina L.) to a gradient of light conditions. Journal of Marine Biology and. Ecology 382: 117–124.Google Scholar
  33. Olesen, B. 1999. Reproduction in Danish eelgrass (Zostera marina L.) stands: size-dependence and biomass partitioning. Aquatic Botany 65: 209–219.CrossRefGoogle Scholar
  34. Olesen, B., and K. Sand-Jensen. 1993. Seasonal acclimatization of eelgrass Zostera marina growth to light. Marine Ecology Progress Series 94: 91–99.CrossRefGoogle Scholar
  35. Olesen, B., and K. Sand-Jensen. 1994. Demography of shallow eelgrass (Zostera marina) populations—shoot dynamics and biomass development. Journal of Ecology 82: 379–390.CrossRefGoogle Scholar
  36. Olesen, B., S. Enríquez, C.M. Duarte, and K. Sand-Jensen. 2002. Depth-acclimation of photosynthesis, morphology and demography of Posidonia oceanica and Cymodocea nodosa in the Spanish Mediterranean Sea. Marine Ecology Progress Series 236: 89–97.CrossRefGoogle Scholar
  37. Olesen, B., D. Krause-Jensen, N. Marbà, and P.B. Christensen. 2015. Eelgrass (Zostera marina L) in subarctic Greenland: dense meadows with slow biomass turnover in cold waters. Marine Ecology Progress Series 518: 107–121. doi: 10.3354/meps11087.CrossRefGoogle Scholar
  38. Orth, R.J., T.J.B. Carruthers, W.C. Dennison, C.M. Duarte, J.W. Fourqurean, K.L. Heck Jr., A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, S. Olyarnik, F.T. Short, M. Waycott, and S.L. Williams. 2006. A global crisis for seagrass ecosystems. Bioscience 56: 987–996.CrossRefGoogle Scholar
  39. Peralta, G., J.L. Pérez-Lloréns, I. Hernández, and J.J. Vergara. 2002. Effects of light availability on growth, architecture and nutrient content of the seagrass Zostera noltii Hornem. Journal of Experimental Marine Biology and Ecology 269: 9–26.CrossRefGoogle Scholar
  40. Phillips, R.C., and T.W. Backman. 1983. Phenology and reproductive biology of eelgrass (Zostera marina L.) at Bahia Kino, sea of Cortez, Mexico. Aquatic Botany 17: 85–90.CrossRefGoogle Scholar
  41. Plus, M., J.M. Deslous-Paoli, and F. Dagault. 2003. Seagrass (Zostera marina L.) bed recolonisation after anoxia induced full mortality. Aquatic Botany 77: 121–134.CrossRefGoogle Scholar
  42. Qin, L.-Z., W.-T. Li, Z.-M. Zhang, M. Nie, and Y. Li. 2014. Sexual reproduction and seed dispersal pattern of annual and perennial Zostera marina in a heterogeneous habitat. Wetlands Ecology and Management 22: 671–682.CrossRefGoogle Scholar
  43. Riemann, B., J. Carstensen, K. Dahl, H. Fossing, J.W. Hansen, H.H. Jakobsen, A.B. Josefson, D. Krause-Jensen, S. Markager, P.A. Stæhr, K. Timmermann, J. Windolf, and J.H. Andersen. 2016. Recovery of Danish coastal ecosystems after reductions in nutrient loading: a holistic ecosystem approach. Estuaries and Coasts 39: 82–97.CrossRefGoogle Scholar
  44. Robertson, A.I., and K.H. Mann. 1984. Disturbance by ice and life-history adaptations of the seagrass Zostera marina. Marine Biology 80: 131–141.CrossRefGoogle Scholar
  45. Rueda, J.L., C. Salas, and P. Marina. 2008. Seasonal variation in a deep subtidal Zostera marina L. Bed in southern Spain (western Mediterranean Sea. Botanica Marina 51: 92–102.CrossRefGoogle Scholar
  46. Ruiz, J.M., and J. Romero. 2001. Effects of in situ experimental shading on the Mediterranean seagrass Posidonia oceanica. Marine Ecology Progress Series 215: 107–120.CrossRefGoogle Scholar
  47. Sand-Jensen, K. 1975. Biomass, net production and growth dynamics in an eelgrass (Zostera marina L.) population in Vellerup Vig, Denmark. Ophelia 14: 185–201.CrossRefGoogle Scholar
  48. Santamaría-Gallegos, N.A., J.L. Sánchez-Lizaso, and E.F. Félix-Pico. 2000. Phenology and growth cycle of annual subtidal eelgrass in a subtropical locality. Aquatic Botany 66: 329–339.CrossRefGoogle Scholar
  49. Short, F.T., and C.M. Duarte. 2001. Methods for the measurement of seagrass growth and production. In Global seagrass research methods, eds. F.T. Short, and R.G. Coles, 155–182. Amsterdam: Elsevier 482 pages.CrossRefGoogle Scholar
  50. Short, F.T., and S. Wyllie-Echeverria. 1996. Natural and human-induced disturbance of seagrasses. Environmental Conservation 23: 17–27.CrossRefGoogle Scholar
  51. Terrados, J., C.M. Duarte, L. Kamp-Nielsen, N.R.S. Agawin, E. Gacia, C.D.A. Lacap, M.D. Fortes, J. Borum, M. Lubanski, and T. Greve. 1999. Are seagrass growth and survival constrained by the reducing conditions of the sediment? Aquatic Botany 65: 175–197.CrossRefGoogle Scholar
  52. Terrados, J., M. Grau-Castella, D. Piñol-Santiñà, and P. Riera-Fernández. 2006. Biomass and primary production of a 8–11 m depth meadow versus <3 m depth meadows of the seagrass Cymodocea Nodosa (Ucria) Ascherson. Aquatic Botany 84: 324–332.CrossRefGoogle Scholar
  53. Tomlinson, P.B. 1974. Vegetative morphology and meristem dependence—the foundation of productivity in seagrasses. Aquaculture 4: 107–130.CrossRefGoogle Scholar
  54. van Lent, F., and J.M. Verschuure. 1994. Intraspecific variability of Zostera marina L. (eelgrass) in the estuaries and lagoons of the southwestern Netherlands. II. Relation with environmental factors. Aquatic Botany 48: 59–75.CrossRefGoogle Scholar
  55. Waycott, M., C.M. Duarte, T.J.B. Cattuthers, R.J. Orth, W.C. Dennison, S. Olayarnik, A. Calladine, J.W. Fourqurean, K.L. Heck, A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106: 12377–12381.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2016

Authors and Affiliations

  1. 1.Department of BioscienceAarhus UniversityAarhus CDenmark
  2. 2.Department of BioscienceAarhus UniversitySilkeborgDenmark

Personalised recommendations