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Quantifying Variation in Zostera marina Seed Size and Composition at the Species’ Southern Limit in the Western Atlantic: Implications for Eelgrass Population Resilience

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Abstract

At the southern limit of Zostera marina in the Western Atlantic, sexual reproduction has provided a mechanism of recovery following thermal stress–related interannual losses. To understand the natural variability in seed quality in eelgrass meadows, flowering shoots were collected weekly to bi-weekly during the 2018 flowering season (March–June) from three sites in Topsail Sound, North Carolina (NC). Seeds were also collected during the period of maximum flowering (May) and examined for changes in seed composition (carbohydrates and proteins) and viability across seed sizes and between sites. The results of the present study show that while eelgrass phenology is following recognized temperature patterns, flowers matured 2–4 weeks earlier in the year than was previously documented. NC eelgrass populations also produced smaller seeds at greater densities than more northern perennial North American populations. In addition, viability did not differ across seed sizes suggesting that seed weight at the time of seed release may not be a reliable measure of seed quality. However, absolute carbohydrate and protein content did increase with seed size. More energy resources in larger compared with smaller seeds may result in better seed germination success. There was also site-based variation in seed length, width, area, and carbohydrate content despite similar temperature environments across the sites, indicating that local-scale factors may affect Z. marina seed size and composition. Information on variations in phenology, seed production, seed size, and seed composition across the species’ geographic range is necessary to better predict eelgrass response to biophysical disturbances and climate change.

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References

  • Beltrán-Peña, E., A. Ortíz-López, and E. Sánchez de Jiménez. 1995. Synthesis of ribosomal proteins from stored mRNAs early in seed germination. Plant Molecular Biology 28 (2): 327–336.

    Google Scholar 

  • Bewley, J.D. 1997. Seed germination and dormancy. The Plant Cell Online 9: 1055–1066.

    CAS  Google Scholar 

  • Blok, S.E., B. Olesen, and D. Krause-Jensen. 2018. Life history events of eelgrass Zostera marina L. populations across gradients of latitude and temperature. Marine Ecology Progress Series 590: 79–93.

    Google Scholar 

  • Bolker B. and R Development Core Team. 2020. bbmle: tools for general maximum likelihood estimation. R package version 1.0.23.1. https://CRAN.R-project.org/package=bbmle. Accessed 21 Jan 2020.

  • Cabaço, S., and R. Santos. 2012. Seagrass reproductive effort as an ecological indicator of disturbance. Ecological Indicators 23: 116–122.

    Google Scholar 

  • Cao, Y., Y. Xiao, H. Huang, J. Xu, W. Hu, and N. Wang. 2016. Simulated warming shifts the flowering phenology and sexual reproduction of Cardamine hirsuta under different planting densities. Scientific Reports 6 (1): 27835.

    CAS  Google Scholar 

  • Churchill, A.C. 1983. Field studies on seed germination and seedling development in Zostera marina L. Aquatic Botany 16: 21–29.

    Google Scholar 

  • Churchill, A.C., and M.I. Riner. 1978. Anthesis and seed production in Zostera marina L. from Great South Bay, New York, U.S.A. Aquatic Botany 4: 83–93.

    Google Scholar 

  • Conacher, C., I. Poiner, J. Butler, S. Pun, and D. Tree. 1994. Germination, storage and viability testing of Zostera capricorni Aschers. from a tropical bay in Australia. Aquatic Botany 491: 47–58.

    Google Scholar 

  • Cribario-Neto, F., and A. Zeileis. 2010. Beta regression in R. Journal of Statistical Software 342: 1–24. http://www.jstatsoft.org/v34/i02/. Accessed 21 Jan 2020.

  • De Cock, A.W.A.M. 1980. Flowering, pollination and fruiting in Zostera marina L. Aquatic Botany 9: 201–220.

    Google Scholar 

  • Delefosse, M., K. Povidisa, D. Poncet, E. Kristensen, and B. Olesen. 2016. Variation in size and chemical composition of seeds from the seagrass Zostera marina—ecological implications. Aquatic Botany 131: 7–14.

    Google Scholar 

  • den Hartog, C. 1970. The sea-grasses of the world. Amsterdam: North Holland Publishing Co..

    Google Scholar 

  • 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 submersed aquatic vegetation. BioScience 43 (2): 86–94.

    Google Scholar 

  • Dillon C (1971) A comparative study of the primary productivity of estuarine phytoplankton and macrobenthic plants. 112 Chapel Hill, NC: Univ. of North Carolina. Ph.D. thesis.

  • Dooley, F.D., S. Wyllie-Echeverria, and E. Van Volkenburgh. 2013. Long-term seed storage and viability of Zostera marina. Aquatic Botany 111: 130–134.

    Google Scholar 

  • Duarte, C.M., J. Terrados, N.S. Agawin, and M.D. Fortes. 2000. An experimental test of the occurrence of competitive interactions among SE Asian seagrasses. Marine Ecology Progress Series 197: 231–240.

    Google Scholar 

  • Dulekgurgen, E. 2004. Total carbohydrates protocol. Campaign: University of Illinois at Urbana-Champaign (UIUC).

    Google Scholar 

  • Felger, R.S., and C.P. McRoy. 1975. Seagrasses as potential food plants. In: G. Fred Somers (Editor), Seed bearing halophytes as food plants. Proceedings of a Conference at the University of Delaware. NOAA Office of Seagrant, Dept. of Commerce (Grant No. 2-35223).

  • Fenner, M. 1983. Relationships between seed weight, ash content and seedling growth in twenty-four species of Compositae. New Phytologist 954: 697–706.

    Google Scholar 

  • Feussner, I., C. Wasternack, H. Kindl, and H. Kühn. 1995. Lipoxygenase-catalyzed oxygenation of storage lipids is implicated in lipid mobilization during germination. Proceedings of the National Academy of Sciences 92 (25): 11849–11853.

    CAS  Google Scholar 

  • Fox, J., and S. Weisberg. 2019. An {R} companion to applied regression. third ed. Thousand Oaks CA: Sage URL: https://socialsciences.mcmaster.ca/jfox/Books/Companion/.

    Google Scholar 

  • Green, E., and F. Short. 2003. World atlas of seagrasses. Berkeley: University of California Press.

  • Harper, J.L., P.H. Lovell, and K.G. Moore. 1970. The shapes and sizes of seeds. Annual Review of Ecology and Systematics 1 (1): 327–356.

    Google Scholar 

  • Harrison, P.G. 1991. Mechanisms of seed dormancy in an annual population of Zostera marina eelgrass from The Netherlands. Canadian Journal of Botany 699: 1972–1976.

    Google Scholar 

  • Infantes, E., L. Eriander, and P.O. Moksnes. 2016. Eelgrass Zostera marina restoration on the west coast of Sweden using seeds. Marine Ecology Progress Series 546: 31–45.

    Google Scholar 

  • Inglis, G.J. 2000. Disturbance-related heterogeneity in the seed banks of a marine angiosperm. Journal of Ecology 881: 88–99.

    Google Scholar 

  • Irving, D.W., V.A. Breda, R. Becker, and R.M. Saunders. 1988. Anatomy and composition of Zostera marina L.—a potential new crop. Ecology of Food and Nutrition 20 (4): 263–274.

    Google Scholar 

  • Jacobs, R., and E. Pierson. 1981. Phenology of reproductive shoots of eelgrass, Zostera marina L., at Roscoff France. Aquatic Botany 10: 45–60.

    Google Scholar 

  • Jarvis, J.C., and K.A. Moore. 2010. The role of seedlings and seed bank viability in the recovery of Chesapeake Bay, USA, Zostera marina populations following a large-scale decline. Hydrobiologia 649 (1): 55–68.

    Google Scholar 

  • Jarvis, J.C., and K.A. Moore. 2015. Effects of seed source, sediment type and burial depth on mixed-annual and perennial Zostera marina L. seed germination and seedling establishment. Estuaries and Coasts 383: 964–978.

    Google Scholar 

  • 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.

    Google Scholar 

  • Jarvis, J.C., M.J. Brush, and K.A. Moore. 2014. Modeling loss and recovery of Zostera marina beds in the Chesapeake Bay: the role of seedlings and seed-bank viability. Aquatic Botany 113: 32–45.

    Google Scholar 

  • Johnson, A.J., R.J. Orth, and K.A. Moore. 2020. The role of sexual reproduction in the maintenance of established Zostera marina meadows. Journal of Ecology 108 (3): 945–957.

    Google Scholar 

  • Jørgensen, M.S., R. Labouriau, and B. Olesen. 2019. Seed size and burial depth influence Zostera marina L. (eelgrass) seed survival, seedling emergence and initial seedling biomass development. PLoS ONE 14 (4).

  • Keddy, C. 1987. Reproduction of annual eelgrass: variation among habitats and comparison with perennial eelgrass (Zostera marina L.). Aquatic Botany 27 (3): 243–256.

    Google Scholar 

  • Kendrick, G.A., M. Waycott, T.J.B. Carruthers, M.L. Cambridge, R. Hovey, S.L. Krauss, P.S. Lavery, D.H. Lee, R.J. Lowe, O.L.M. Vidal, J.L.S. Ooi, R.J. Orth, D.O. Rivers, L. Ruiz-Montoya, E.A. Sinclair, J. Statton, J. Kornelis, and J.L. Verduin. 2012. The central role of dispersal in the maintenance and persistence of seagrass populations. BioScience 621: 56–65.

    Google Scholar 

  • Kenworthy, W.J. 1981. The interrelationship between seagrass Zostera marina and Halodule wrightii, and the physical and chemical properties of sediments in a mid-Atlantic coastal plain estuary near Beaufort, North Carolina. MSc Thesis, Univ. of VA.

  • Kenworthy, W.J., J.C. Zieman, and G.W. Thayer. 1982. Evidence for the influence of seagrass on the benthic nitrogen cycle in a coastal plain estuary near Neaufort, North Carolina (USA). Oecologia 54: 152–158.

    Google Scholar 

  • Koch, E.W. 2001. Beyond light: geological and geochemical parameters as possible submersed aquatic vegetation habitat requirements. Estuaries 24: 1–17.

  • Koch, E.W., M.S. Ailstock, D.M. Booth, D.J. Shafer, and A.D. Magoun. 2010. The role of currents and waves in the dispersal of submersed angiosperms, seeds, and seedlings. Restoration Ecology 18: 584–595.

    Google Scholar 

  • Kowalski, J., H. DeYoe, and T. Allison. 2009. Seasonal production and biomass of the seagrass, Halodule wrightii Aschers. (shoal grass), in a subtropical Texas lagoon. Estuaries and Coasts 32 (3): 467–482.

    Google Scholar 

  • Lakon, G. 1949. The topographical tetrazolium method for determining the germinating capacity of seeds. Plant Physiology 24 (3): 389–394.

    CAS  Google Scholar 

  • Lee, K.S., S.R. Park, and Y.K. Kim. 2007. Effects of irradiance, temperature and nutrients on growth dynamics of seagrasses: a review. Journal of Experimental Marine Biology and Ecology 350 (1-2): 144–175.

    Google Scholar 

  • Lefcheck, J.S., R.J. Orth, W.C. Dennison, D.J. Wilcox, R.R. Murphy, J. Keisman, C. Gurbisz, M. Hannam, J.B. Landry, K.A. Moore, and C.J. Patrick. 2018. Long-term nutrient reductions lead to the unprecedented recovery of a temperate coastal region. Proceedings of the National Academy of Sciences 115 (14): 3658–3662.

    Google Scholar 

  • Lenth, R.V. 2016. Least-squares means: the R package lsmeans. Journal of Statistical Software 69 (1): 1–33. https://doi.org/10.18637/jss.v069.i01.

    Article  Google Scholar 

  • Livernois, M.C., J.H. Grabowski, A.K. Poray, T.C. Gouhier, A.R. Hughes, K.F. O’Brien, L.A. Yeager, and F.J. Fodrie. 2017. Effects of habitat fragmentation on Zostera marina seed distribution. Aquatic Botany 142: 1–9.

    Google Scholar 

  • Luckenbach, M.L., and R.J. Orth. 1999. Effects of a deposit-feeding invertebrate on the entrapment of Zostera marina L. seeds. Aquatic Botany 62 (4): 235–247.

    Google Scholar 

  • Marion, S.R., and R.J. Orth. 2010. Innovative techniques for large-scale seagrass restoration using Zostera marina eelgrass seeds. Restoration Ecology 184: 514–526.

    Google Scholar 

  • Micheli, F., M.J. Bishop, C.H. Peterson, and J. River. 2008. Alteration of seagrass species composition and function over two decades. Ecological Monographs 78 (2): 225–244.

    Google Scholar 

  • Molès, A.T., and M. Westoby. 2004. Seedling survival and seed size: a synthesis of the literature. Journal of Ecology 923: 372–383.

    Google Scholar 

  • Moore, K.A., and J.C. Jarvis. 2008. Environmental factors affecting recent eelgrass diebacks in the lower Chesapeake Bay: are these southern Atlantic populations responding to global warming events? Journal of Coastal Research 55: 135–147.

    Google Scholar 

  • Moore, K.A., and F.T. Short. 2006. Zostera: biology, ecology, and management. In Seagrasses: biology, ecology and conservation, ed. A.W. Larkum, R.J. Orth, and C.M. Durate, 361–386. Dordrecht: Springer.

    Google Scholar 

  • Morita, T., H. Okumura, M. Abe, A. Kurashima, and M. Maegawa. 2007. Density and distribution of seeds in bottom sediments in Zostera marina beds in Ago Bay, central Japan. Aquatic Botany 87: 38–42.

    Google Scholar 

  • National Oceanic and Atmospheric Association (NOAA) (2014, September). Chart 11539: New River Inlet to Cape Fear. https://www.charts.noaa.gov/OnLineViewer/11539.shtml. Accessed Feb 19 2019.

  • Niu, S., P. Zhang, J. Liu, D. Guo, and X. Zhang. 2012. The effect of temperature on the survival, growth, photosynthesis, and respiration of young seedlings of eelgrass Zostera marina L. Aquaculture 350–353: 98–108.

    Google Scholar 

  • Orth, R.J., M. Luckenbach, and K.A. Moore. 1994. Seed dispersal in a marine macrophyte: implications for colonization and restoration. Ecology 75 (7): 1927–1939.

    Google Scholar 

  • Orth, R.J., T.C. Carruthers, W. Dennison, C.M. Duarte, J.W. Fourqurean, K.L. Heck Jr., and S.L. Williams. 2006. A global crisis for seagrass ecosystems. BioScience 56: 987–996.

    Google Scholar 

  • Orth, R.J., W.C. Dennison, J.S. Lefcheck, C. Gurbisz, M. Hannam, J. Keisman, J.B. Landry, K.A. Moore, R.R. Murphy, C.J. Patrick, J. Testa, D.E. Weller, and D.J. Wilcox. 2017. Submersed aquatic vegetation in Chesapeake Bay: sentinel species in a changing world. BioScience 67: 698–712.

    Google Scholar 

  • Phillips, R.C. 1960. Observations on the ecology and distribution of the Florida seagrasses. Professional Paper Series No. 2. Florida State Board Conserv Mar Lab, St. Petersburg, FL.

  • 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 (1): 85–90.

    Google Scholar 

  • Phillips, R.C., C. McMillan, and K.W. Bridges. 1983. Phenology of eelgrass, Zostera marina L., along latitudinal gradients in North America. Aquatic Botany 152: 145–156.

    Google Scholar 

  • Primack, R.B. 1987. Relationships among flowers, fruits, and seeds. Annual review of ecology and systematics 18 (1): 409–430.

    Google Scholar 

  • Qin, L.Z., W.T. Li, X.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 (6): 671–682.

    Google Scholar 

  • R Core Team 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

  • Reynolds, L.K., M. Waycott, and K.J. McGlathery. 2013. Restoration recovers population structure and landscape genetic connectivity in a dispersal-limited ecosystem. Journal of Ecology 101: 1288–1297.

  • Richardson, J.P., J.S. Lefcheck, and R.J. Orth. 2018. Warming temperatures alter the relative abundance and distribution of two co-occurring foundational seagrasses in Chesapeake Bay, USA. Marine Ecology Progress Series 599: 65–74.

    Google Scholar 

  • Rosa, M., M. Hilal, J.A. González, and F.E. Prado. 2004. Changes in soluble carbohydrates and related enzymes induced by low temperature during early developmental stages of quinoa Chenopodium quinoa seedlings. Journal of Plant Physiology 161 (6): 683–689.

  • Ruiz-Montoya, L., R.J. Lowe, K.P. Van Niel, and G.A. Kendrick. 2012. The role of hydrodynamics on seed dispersal in seagrasses. Limnology and Oceanography 575: 1257–1265.

    Google Scholar 

  • Salisbury, E.J. 1942. The reproductive capacity of plants: studies in quantitative biology. London: G. Bell and Sons Ltd..

    Google Scholar 

  • 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 (4): 329–339.

    Google Scholar 

  • Setchell, W.A. 1929. Morphological and phenological notes on Zostera marina L. University of California Publications in Botany 14: 389–452.

    Google Scholar 

  • Shewry, P.R., J.A. Napier, and A.S. Tatham. 1995. Seed storage proteins: structures and biosynthesis. The Plant Cell 77: 945–956.

    Google Scholar 

  • Shields, E.C., D. Parrish, and K.A. Moore. 2019. Short-term temperature stress results in seagrass community shift in a temperate estuary. Estuaries and Coasts 42 (3): 755–764.

    Google Scholar 

  • Short, F., T. Carruthers, W. Dennison, and M. Waycott. 2007. Global seagrass distribution and diversity: a bioregional model. Journal of Experimental Marine Biology and Ecology 350: 76–20.

    Google Scholar 

  • Silberhorn, G.M., R.J. Orth, and K.A. Moore. 1983. Anthesis and seed production in Zostera marina L. eelgrass from the Chesapeake Bay. Aquatic Botany 152: 133–144.

    Google Scholar 

  • Spencer, D. 1984. The physiological role of storage proteins in seeds. Philosophical Transactions of the Royal Society London, B 304: 275–285.

    CAS  Google Scholar 

  • Tanner, C.E., and T. Parham. 2010. Growing Zostera marina eelgrass from seeds in land-based culture systems for use in restoration projects. Restoration Ecology 18: 527–537.

    Google Scholar 

  • Taylor, A. 1957. Studies of the development of Zostera marina L.: the embryo and seed. Canadian Journal of Botany 35: 477–499.

    Google Scholar 

  • Thayer, G.W., W.J. Kenworthy, and M.S. Fonseca. 1984. The ecology of eelgrass meadows of the Atlantic Coast: a community profile. Silver Spring (MD): National Oceanographic and Atmosphereic Administration (NOAA) Coastal Ocean Office. NOAA Coastal Ocean Program Decision Analysis Series no. 12.

  • Tomlinson, P.B. 1974. Vegetative morphology and meristem dependence—the foundation of productivity in seagrasses. Aquaculture 4: 107–130.

    Google Scholar 

  • Touchette, B.W., and J.M. Burkholder. 2000. Review of nitrogen and phosphorus metabolism in seagrass. Journal of Experimental Marine Biology and Ecology 2501: 133–167.

    Google Scholar 

  • Unsworth, R.K.F., C.J. Collier, M. Waycott, L.J. Mckenzie, and L.C. Cullen-Unsworth. 2015. A framework for the resilience of seagrass ecosystems. Marine Pollution Bulletin 100 (1): 34–46.

    CAS  Google Scholar 

  • van Katwijk, M.M., A.R. Bos, P. Kennis, and R. de Vries. 2010. Vulnerability to eutrophication of a semi-annual life history: a lesson learnt from an extinct eelgrass Zostera marina population. Biological Conservation 1431: 248–254.

    Google Scholar 

  • 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 (1): 59–75.

    Google Scholar 

  • Viles, F.J., and L. Silverman. 1949. Determination of starch and cellulose with anthrone. Analytical Chemistry 21 (8): 950–953.

    CAS  Google Scholar 

  • Waycott, M., C.M. Duarte, T.J. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, and G.A. Kendrick. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106: 12377–12381.

    CAS  Google Scholar 

  • Wigand, C., and C. Churchill. 1988. Laboratory studies on eelgrass seed and seedling predation. Estuaries 11: 180–183.

    Google Scholar 

  • Williams, S.L., R. Ambo-Rappe, C. Sur, J.M. Abbott, and S.R. Limbong. 2017. Species richness accelerates marine ecosystem restoration in the Coral Triangle. Proceedings of the National Academy of Sciences 114 (45): 11986–11991.

    CAS  Google Scholar 

  • Wilson, K., and H. Lotze. 2019. Projected range shift of eelgrass Zostera marina in the Northwest Atlantic with climate change. Marine Ecology Progress Series 62: 47–62.

    Google Scholar 

  • Wyllie-Echeverria, S., P. Cox, A. Churchill, J. Brotherson, and T. Wyllie-Echeverria. 2003. Seed size variation within Zostera marina L. Zosteraceae. Botanical Journal of the Linnean Society 142: 281–288.

    Google Scholar 

  • Xu, S., P. Wang, Y. Zhou, X. Zhang, R. Gu, X. Liu, B. Liu, X. Song, S. Xu, and S. Yue. 2018. New insights into different reproductive effort and sexual recruitment contribution between two geographic Zostera marina L. populations in temperate China. Frontiers in. Plant Science 9: 15.

    Google Scholar 

  • Yemm, E.W., and A.J. Willis. 1954. The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57-3: 508–514.

    Google Scholar 

  • Yuan, K., and J. Wysocka-Diller. 2006. Phytohormone signalling pathways interact with sugars during seed germination and seedling development. Journal of Experimental Botany 57 (12): 3359–3367.

    CAS  Google Scholar 

  • Zhang, D. 2020. rsq: R-Squared and related measures. R package version 2.0. https://CRAN.R-project.org/package=rsq. Accessed 21 Jan 2020.

  • Zuur, A.F., G.M. Smith, and E.N. Ieno. 2007. Analysing ecological data. New York: Springer-Verlag.

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Acknowledgments

The authors would like to thank the University of North Carolina Wilmington and the North Carolina Division of Marine Fisheries Coastal Recreational Fisheries program for financial support. Special thanks to Ariel Potter, Nicole Taylor, Amy Bartenfelder, and Evan Heit for help with field and laboratory assistance.

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Combs, A.R., Jarvis, J.C. & Kenworthy, W.J. Quantifying Variation in Zostera marina Seed Size and Composition at the Species’ Southern Limit in the Western Atlantic: Implications for Eelgrass Population Resilience. Estuaries and Coasts 44, 367–382 (2021). https://doi.org/10.1007/s12237-020-00839-5

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