Abstract
Seagrass species in the genus Halophila are usually distributed in tropical or subtropical areas, but a Halophila species identified as H. nipponica was first observed in temperate coastal regions of Korea in 2007. Since this species mainly occurs in warm temperate regions influenced by warm currents, we hypothesized that H. nipponica may exhibit different growth patterns from those of other temperate seagrass species in Korea, instead showing similar growth dynamics to tropical/subtropical species. The growth and morphology of H. nipponica in relation to coincident measurements of environmental factors were investigated from July 2008 to September 2009 to examine the growth dynamics of this species. Water temperature at the study site ranged from 9.7°C in January to 25.1°C in August. Shoot density, biomass, and productivity exhibited significant seasonal variation, increasing during summer and decreasing during winter. Productivity was severely restricted to nearly ceasing at water temperatures less than 15°C, and winter minimum growth lasted until May. The optimal temperature for H. nipponica growth was approximately 25°C, which was the maximum water temperature at the study site, and no growth reduction in high summer water temperature was observed. Thus, H. nipponica on the temperate coast of Korea exhibited a distinctly different growth pattern from those of temperate seagrass species in Korea, which have shown great reductions in growth at water temperatures higher than 20°C. Higher below- to above-ground ratio and leaf burial into sediments with shorter leaf petioles during winter might be overwintering strategies in this species. The growth patterns of H. nipponica at the study site imply that this species still possess the tropical characteristics of the genus Halophila.
Similar content being viewed by others
References
Beer S, Waisel Y (1982) Effects of light and pressure on photosynthesis in two seagrasses. Aquat Bot 13:331–337
Beer S, Mtolera M, Lyimo T, Björk M (2006) The photosynthetic performance of the tropical seagrass Halophila ovalis in the upper intertidal. Aquat Bot 84:367–371
Brian JA, Paul EK, Colin GNT (1999) Plants in action: adaptation in nature. Performance in cultivation. Macmillan, Melbourne
Brouns JJWM (1987a) Growth patterns in some Indo-West-Pacific seagrasses. Aquat Bot 28:39–61
Brouns JJWM (1987b) Quantitative and dynamic aspects of mixed seagrass meadow in Papua New Guinea. Aquat Bot 29:33–47
Bulthuis DA (1983) Effects of temperature on the photosynthesis-irradiance curve of the Australian seagrass, Heterozostera tasmanica. Mar Biol Lett 4:47–57
Cho Y-K, Kim T-W, You K-W, Park L-H, Moon H-T, Lee S-H, Youn Y-H (2005) Temporal and spatial variabilities in the sediment temperature on the Baeksu tidal flat, Korea. Estuarine Coastal Shelf Sci 65:302–308
Connell EL, Walker DI (2001) Nutrient cycling associated with the seagrass Halophila ovalis in the Swan-Canning Estuary based on seasonal variations in biomass and tissue nutrients. Hydrol Process 15:2401–2409
den Hartog C, Kuo J (2006) Taxonomy and biogeography of seagrasses. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 1–23
Dennison WC (1987) Effects of light on seagrass photosynthesis, growth and depth distribution. Aquat Bot 27:15–26
Dennison WC, Orth RJ, Moore KA, Stevenson JC, Carter V, Kollar S, Bergstrom PW, Batiuk RA (1993) Assessing water quality with submersed aquatic vegetation. Bioscience 43(2):86–94
Duarte CM (1991) Seagrass depth limits. Aquat Bot 40:363–373
Erftemeijer PLA, Stapel J (1999) Primary productivity of deep-water Halophila ovalis meadows. Aquat Bot 65:71–82
Evans AS, Webb KL, Penhale PA (1986) Photosynthetic temperature acclimation in two coexisting seagrass, Zostera marina L. and Ruppia maritima L. Aquat Bot 24:185–197
Goldstein G, Meinzer F (1983) Influence of insulating dead leaves and low temperatures on water balance in an Andean giant rosette phase. Plant Cell Environ 6:649–656
Green EP, Short FT (2003) World atlas of seagrasses. University of California Press, Berkeley
Hammerstrom KK, Kenworthy WJ, Fonseca MS, Whitfield PE (2006) Seed bank, biomass, and productivity of Halophila decipiens, a deep water seagrass on the west Florida continental shelf. Aquat Bot 84:110–120
Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber SC, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241
Herbert DA (1986) The growth dynamics of Halophila hawaiiana. Aquat Bot 23:351–360
Herzka SZ, Dunton KH (1998) Light and carbon balance in the seagrass Thalassia testudinum: evaluation of current production models. Mar Biol 132:711–721
Hillman K, McComb AJ, Walker DI (1995) The distribution, biomass and primary productivity of the seagrass Halophila ovalis in the Swan/Canning Estuary, Western Australia. Aquat Bot 51:1–54
Hulings NC (1979) The ecology, biometery and biomass of the seagrass Halophila stipulacea along the Jordanian coast of the Gulf of Aqaba. Bot Mar 22:425–430
Huong TTL, Vermaat JE, Terados J, Tien NV, Duarte CM, Borum J, Tri NH (2003) Seasonality and depth zonation of intertidal Halophila ovalis and Zostera japonica in Ha Long Bay (northern Vietnam). Aquat Bot 75:147–157
Josselyn M, Fonseca M, Niesen T, Larson R (1986) Biomass, productivity and decomposition of a deep water seagrass, Halophila decipiens Ostenf. Aquat Bot 25:47–61
Jupp BP, Durako MJ, Kenworthy WJ, Thayer GW, Schillak L (1996) Distribution, abundance, and species composition of seagrasses at several sites in Oman. Aquat Bot 53:199–213
Kaldy JE, Dunton KH (2000) Above- and below-ground production, biomass and reproductive ecology of Thalassia testudinum (turtle grass) in a subtropical coastal lagoon. Mar Ecol Progress Ser 193:271–283
Kaldy JE, Lee K-S (2007) Factor controlling Zostera marina L. growth in the eastern and western Pacific Ocean: Comparisons between Korea and Oregon, USA. Aquat Bot 87:116–126
Karagatzides JD, Huthinson I (1991) Intraspecific comparisons of biomass dynamics in Scirpus americanus and Scirpus maritimus on the Fraser river delta. J Ecol 79:459–476
Kenworthy WJ, Zieman JC, Thayer GW (1982) Evidence for the influence of seagrasses on the benthic nitrogen cycle in a coastal plain estuary near Beaufort, North Carolina (USA). Oecologia 54:152–158
Kenworthy WJ, Currin CA, Fonseca MS, Smith G (1989) Productivity, decomposition, and heterotrophic utilization of the seagrass Halophila decipiens in a submarine canyon. Mar Ecol Progress Ser 51:277–290
Kenworthy WJ, Durako MJ, Fatemy SMR, Valavi H, Thayer GW (1993) Ecology of seagrasses in northeastern Saudi Arabia one year after the Gulf War oil spill. Mar Pollut Bull 27:213–222
Kim JB, Park J-I, Jung C-S, Lee P-Y, Lee K-S (2009) Distributional range extension of the seagrass Halophila nipponica into coastal waters off the Korean peninsula. Aquat Bot 90:269–272
Kowalski JL, DeYoe HR, Allison TC (2009) Seasonal production and biomass of the seagrass, Halodule wrightii Aschers. (shoal grass), in a subtropical Texas lagoon. Estuar Coast 32:467–482
Kuo J, Kirkman H (1995) Halophila decipiens Ostenfield in estuaries of southwestern Australia. Aquat Bot 51:335–340
Kuo J, Kanamoto Z, Iizumi H, Aio K, Mukai H (2006a) Seagrassess from the Nansei Islands, Southern Japanese Archipelago: species composition, distribution and biogeography. Mar Ecol 27:290–298
Kuo J, Kanamoto Z, Iizumi H, Aio K, Mukai H (2006b) Seagrasses of the genus Halophila Thouars (Hydrocharitaceae) from Japan. Acta Phytotax Geobot 57(2):129–154
Lee K-S, Dunton KH (1996) Productivity and carbon reserve dynamics of the seagrass Thalassia testudinum in corpus Christi Bay, Texas, USA. Mar Ecol Progress Ser 143:201–210
Lee K-S, Lee SY (2003) The seagrasses of the Republic of Korea. In: Green EP, Short FT, Spalding MD (eds) World atlas of seagrasses: present status and future conservation. University of California Press, Berkeley, pp 193–198
Lee K-S, Park SR, Kim J-B (2005) Productivity dynamics of the eelgrass, Zostera marina in two bay systems on the south coast of the Korean peninsula. Mar Biol 147:1091–1108
Lee K-S, Park SR, Kim YK (2007) Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. J Exp Mar Biol Ecol 350:144–175
Lipkin Y (1979) Quantitative aspects of seagrass communities particularly those dominated by Halophila stipulacea, in Sinai (northern Red Sea). Aquat Bot 7:119–128
Marsh JA Jr, Dennison WC, Alberte RS (1986) Effects of temperature on photosynthesis and respiration in eelgrass (Zostera marina L.). J Exp Mar Biol Ecol 350:144–175
McMillan C (1979) Differentiation in response to chilling temperatures among populations of three marine spermatophytes, Thalassia testudinum, Syringodium filiforme and Halodule wrightii. Am J Bot 66(7):810–819
Nakaoka M, Aioi K (1999) Growth of seagrass Halophila ovalis at dugong trails compared to existing within-patch variation in a Thailand intertidal flat. Mar Ecol Progress Ser 184:97–103
Occhipinti-Ambrogi A (2007) Global change and marine communities: alien species and climate change. Mar Pollut Bull 55:342–352
Ogden JC, Ogden NB (1982) A preliminary study of two representative seagrass communities in Palau, West Caroline Islands (Micronesia). Aquat Bot 12:229–244
Park J-I, Lee K-S (2009) Peculiar growth dynamics of the surfgrass Phyllospadix japonicus on the southeastern coast of Korea. Mar Biol 156:2221–2233
Park SR, Kim J-H, Kang C-K, An S, Chung IK, Kim JH, Lee K-S (2009) Current status and ecological roles of Zostera marina after recovery from large-scale reclamation in the Nakdong River estuary, Korea. Estuarine Coastal Shelf Sci 81:38–48
Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergammon Press, New York
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915
Phillips RC, McMillan C, Bridges KW (1983) Phenology of eelgrass, Zostera marina L., along latitudinal gradients on North America. Aquat Bot 15:145–156
Precht WF, Aronson RB (2004) Climate flickers and range shifts of reef corals. Front Ecol Environ 2:307–314
Preen A (1995) Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Mar Ecol Progress Ser 124:201–213
Santamaría-Gallegos NA, Riosmena-Rodríguez R, Sánchez-Lizaso JL (2006) Occurrence and seasonality of Halophila decipiens Ostenfeld in the Gulf of California. Aquat Bot 84:363–366
Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196
Short FT, Fernandez E, Vernon A, Gaeckle JL (2006) Occurrence of Halophila baillonii meadows in Belize, Central America. Aquat Bot 85:249–251
Short FT, Carruthers T, Dennison W, Waycott M (2007) Global seagrass distribution and diversity: a bioregional model. J Exp Mar Biol Ecol 350:3–20
Uchimura M, Faye EJ, Shimada S, Arai S, Inoue T, Nakamura Y (2008) A reassessment of Halophila species (Hydrocharitaceae) diversity with special reference to Japanese representatives. Bot Mar 51:258–268
Vermaat JE, Agawin NSR, Duarte CM, Fortes MD, Marba N, Uri JS (1995) Meadow maintenance, growth and productivity of a mixed Philippine seagrass bed. Mar Ecol Progress Ser 124:215–225
Virnstein RW, Hall LM (2009) Northern range extension of the seagrass Halophila johnsonii and Halophila decipiens along the east coast of Florida, USA. Aquat Bot 90:89–92
Walker DI, Prince RT (1987) Distribution and biogeography of seagrass species on the northwest coast of Australia. Aquat Bot 29:19–32
Willette DA, Ambrose RF (2009) The distribution and expansion of the invasive seagrass Halophila stipulacea in Dominica, West Indies, with a preliminary report from St. Lucia. Aquat Bot 91:137–142
Williams S (2007) Introduced species in seagrass ecosystems: status and concerns. J Exp Mar Biol Ecol 350:89–110
Wilson B (1988) A review of evidence on the control of shoot:root ratio, in relation to models. Ann Bot 61:433–449
Yamano H, Sugihara, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys Res Lett. doi:10.1029/2010GL046474
Zacherl D, Gaines SD, Lonhart SI (2003) The limits to biogeographical distributions: insights from the northward range extension of the marine snail, Kelletia kelletia (Forbes, 1985). J Biogeogr 30:913–924
Acknowledgments
We thank JH Kim, JW Kim, and JI Park for their countless hours of field and laboratory assistances. This work was supported by the Korea Research Foundation Grant funded by the Korean Government (KRF-2008-314-C00318) and the Ministry of Land, Transport and Maritime Affairs, Korea (Project title: Long-term change of structure and function in marine ecosystems of Korea).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Bulleri.
Rights and permissions
About this article
Cite this article
Kim, S.H., Kim, Y.K., Park, S.R. et al. Growth dynamics of the seagrass Halophila nipponica, recently discovered in temperate coastal waters of the Korean peninsula. Mar Biol 159, 255–267 (2012). https://doi.org/10.1007/s00227-011-1804-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-011-1804-6