Depauperate seed banks in urban tropical seagrass meadows
Glendon Hong Ming Ong A , Samantha Lai B , Siti Maryam Yaakub C D and Peter Todd BA NTU Food Technology Centre, 50 Nanyang Avenue, N1.2-B3-27, Singapore 639798, Republic of Singapore.
B Experimental Marine Ecology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Block S3, Level 2, Singapore 117543, Republic of Singapore.
C Ecological Habitats and Processes Department, DHI Water & Environment (S) Pte Ltd, 2 Venture Drive, #18–18, Vision Exchange, Singapore 608526, Republic of Singapore.
D Corresponding author. Email: smj@dhigroup.com
Marine and Freshwater Research 71(8) 935-941 https://doi.org/10.1071/MF19204
Submitted: 2 June 2019 Accepted: 21 May 2020 Published: 17 July 2020
Abstract
Seagrasses need to be resilient if they are to persist in the long term. Being able to build up a dormant seed bank in sediments is a key strategy that some species employ to regenerate from large-scale degradation. Much of the research on seed banks has focussed on temperate species, and little is known regarding the status of seed banks in tropical meadows. In the present study, we examined the seed bank status of three common seagrass species at six sites in Singapore and attempted to identify potential drivers of seed abundance. Our results indicated depauperate seed banks with few species setting viable seed and low seed densities. Halophila ovalis seeds were found at four sites and Halodule uninervis seeds at two sites, but Cymodocea rotundata seeds were absent from all six sites. Whereas H. ovalis seed viability ranged from 20% to 68.8%, none of the H. uninervis seeds was viable. Halophila ovalis seed densities (33–334 m–2) were much higher than those of H. uninervis (9–21 m–2). Of the variables examined, only H. ovalis cover was positively correlated with the number of seeds. Our study has highlighted the vulnerability of seagrass meadows in Singapore’s urban waters to future disturbances.
Additional keywords: Cymodocea rotundata, dispersal, germination, Halodule uninervis, Halophila ovalis, sexual reproduction.
References
Balestri, E., and Cinelli, F. (2003). Sexual reproductive success in Posidonia oceanica. Aquatic Botany 75, 21–32.| Sexual reproductive success in Posidonia oceanica.Crossref | GoogleScholarGoogle Scholar |
Baskin, C. C., and Baskin, J. M. (1998). ‘Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination.’ (Academic Press: New York, NY, USA.)
Bell, S. S., Fonseca, M. S., and Kenworthy, W. J. (2008). Dynamics of a subtropical seagrass landscape: links between disturbance and mobile seed banks. Landscape Ecology 23, 67–74.
| Dynamics of a subtropical seagrass landscape: links between disturbance and mobile seed banks.Crossref | GoogleScholarGoogle Scholar |
Cullen-Unsworth, L., and Unsworth, R. (2013). Seagrass meadows, ecosystem services, and sustainability. Environment 55, 14–28.
| Seagrass meadows, ecosystem services, and sustainability.Crossref | GoogleScholarGoogle Scholar |
Durako, M. J., and Moffler, M. D. (1987). Factors affecting the reproductive ecology of Thalassia testudinum (Hydrocharitaceae). Aquatic Botany 27, 79–95.
| Factors affecting the reproductive ecology of Thalassia testudinum (Hydrocharitaceae).Crossref | GoogleScholarGoogle Scholar |
Erftemeijer, P. L. A., and Robin Lewis, R. R. (2006). Environmental impacts of dredging on seagrasses: a review. Marine Pollution Bulletin 52, 1553–1572.
| Environmental impacts of dredging on seagrasses: a review.Crossref | GoogleScholarGoogle Scholar |
Fishman, J. R., and Orth, R. J. (1996). Effects of predation on Zostera marina L. seed abundance. Journal of Experimental Marine Biology and Ecology 198, 11–26.
| Effects of predation on Zostera marina L. seed abundance.Crossref | GoogleScholarGoogle Scholar |
Gallegos, M. E., Merino, M., Marbá, N., and Duarte, C. M. (1992). Flowering of Thalassia testudinum banks ex König in the Mexican Caribbean: age-dependence and interannual variability. Aquatic Botany 43, 249–255.
| Flowering of Thalassia testudinum banks ex König in the Mexican Caribbean: age-dependence and interannual variability.Crossref | GoogleScholarGoogle Scholar |
Hammerstrom, K. K., and Kenworthy, W. J. (2003). A new method for estimation of Halophila decipiens Ostenfeld seed banks using density separation. Aquatic Botany 76, 79–86.
| A new method for estimation of Halophila decipiens Ostenfeld seed banks using density separation.Crossref | GoogleScholarGoogle Scholar |
Holbrook, S. J., Hansen, K., Reed, D. C., and Blanchette, C. A. (2000). Spatial and temporal patterns of predation on seeds of the surfgrass Phyllospadix torreyi. Marine Biology 136, 739–747.
| Spatial and temporal patterns of predation on seeds of the surfgrass Phyllospadix torreyi.Crossref | GoogleScholarGoogle Scholar |
Inglis, G. J. (2000). Disturbance-related heterogeneity in the seed banks of a marine angiosperm. Journal of Ecology 88, 88–99.
| Disturbance-related heterogeneity in the seed banks of a marine angiosperm.Crossref | GoogleScholarGoogle Scholar |
Inglis, G. J., and Waycott, M. (2001). Methods for assessing seagrass seed ecology and population genetics. In ‘Global Seagrass Research Methods’. (Eds F. T. Short and R. G. Coles.) pp. 123–141. (Elsevier Science: Amsterdam, Netherlands.)
Jarvis, J. C., Brush, M. J., and Moore, K. A. (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.
| Modeling loss and recovery of Zostera marina beds in the Chesapeake Bay: the role of seedlings and seed-bank viability.Crossref | GoogleScholarGoogle Scholar |
Kuo, J., and Kirkman, H. (1992). Fruits, seeds and germination in the seagrass Halophila ovalis (Hydrocharitaceae). Botanica Marina 35, 197–204.
| Fruits, seeds and germination in the seagrass Halophila ovalis (Hydrocharitaceae).Crossref | GoogleScholarGoogle Scholar |
Lai, S., Loke, L. H. L., Hilton, M. J., Bouma, T. J., and Todd, P. A. (2015). The effects of urbanisation on coastal habitats and the potential for ecological engineering: a Singapore case study. Ocean and Coastal Management 103, 78–85.
| The effects of urbanisation on coastal habitats and the potential for ecological engineering: a Singapore case study.Crossref | GoogleScholarGoogle Scholar |
Lai, S., Yaakub, S. M., Poh, T. S. M., Bouma, T. J., and Todd, P. A. (2018). Unlikely nomads: settlement, stablishment, and dislodgement processes of vegetative seagrass fragments. Frontiers in Plant Science 9, 160.
| Unlikely nomads: settlement, stablishment, and dislodgement processes of vegetative seagrass fragments.Crossref | GoogleScholarGoogle Scholar | 29491880PubMed |
Leck, M. A. (1989). Wetland seed banks. In ‘Ecology of Soil Seed Banks’. (Eds M. A. Leck, V. T. Parker, and R. C. Simpson.) pp. 283–308. (Academic Press: San Diego, CA, USA.)
McMahon, K., van Dijk, K. J., Ruiz-Montoya, L., Kendrick, G. A., Krauss, S. L., Waycott, M., Verduin, J., Lowe, R., Statton, J., Brown, E., and Duarte, C. (2014). The movement ecology of seagrasses. Proceedings of the Royal Society B: Biological Sciences 281, 20140878.
| The movement ecology of seagrasses.Crossref | GoogleScholarGoogle Scholar | 25297859PubMed |
McMillan, C. (1991). The longevity of seagrass seeds. Aquatic Botany 40, 195–198.
| The longevity of seagrass seeds.Crossref | GoogleScholarGoogle Scholar |
McMillan, C., Bridges, K. W., Logan Kock, R., and Falanruw, M. (1982). Fruit and seedlings of Cymodocea rotundata in Yap, Micronesia. Aquatic Botany 14, 99–105.
| Fruit and seedlings of Cymodocea rotundata in Yap, Micronesia.Crossref | GoogleScholarGoogle Scholar |
Murdoch, A. J., and Ellis, R. H. (1992). Dormancy, viability and longevity. In ‘Seeds: The Ecology of Regeneration and Plant Communities’. (Ed. M. Fenner.) pp. 183–214. (CAB International: Wallingford, UK.)
Orth, R. J., Luckenbach, M., and Moore, K. A. (1994). Seed dispersal in a marine macrophyte: implications for colonization and restoration. Ecology 75, 1927–1939.
| Seed dispersal in a marine macrophyte: implications for colonization and restoration.Crossref | GoogleScholarGoogle Scholar |
Orth, R. J., Harwell, M. C., and Inglis, G. J. (2006). Ecology of seagrass seeds and seagrass dispersal processes. In ‘Seagrasses: Biology, Ecology and Conservation’. (Eds A. W. D. Larkum, R. J. Orth, and C. M. Duarte.) pp. 111–133. (Springer: Dordrecht, Netherlands.)
Orth, R. J., Kendrick, G. A., and Marion, S. R. (2007). Posidonia australis seed predation in seagrass habitats of Two Peoples Bay, Western Australia. Aquatic Botany 86, 83–85.
| Posidonia australis seed predation in seagrass habitats of Two Peoples Bay, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Patil, V. N., and Dadlani, M. (2009). Tetrazolium test for seed viability and vigour. In ‘Handbook of Seed Testing’. (Eds J. Renugadevi, P. Srimathi, R. R. Renganayaki, and V. Manonmani.) pp. 209–241. (Agrobios: New Delhi, India.)
Piazzi, L., Balestri, E., and Cinelli, F. (2000). Grazing of inflorescences of the seagrass Posidonia oceanica (L.) Delile. Botanica Marina 43, 581–584.
| Grazing of inflorescences of the seagrass Posidonia oceanica (L.) Delile.Crossref | GoogleScholarGoogle Scholar |
Rasheed, M. A. (2004). Recovery and succession in a multi-species tropical seagrass meadow following experimental disturbance: the role of sexual and asexual reproduction. Journal of Experimental Marine Biology and Ecology 310, 13–45.
| Recovery and succession in a multi-species tropical seagrass meadow following experimental disturbance: the role of sexual and asexual reproduction.Crossref | GoogleScholarGoogle Scholar |
Sculthorpe, C. D. (1967). ‘The Biology of Aquatic Vascular Plants.’ (Edward Arnold: London, UK.)
Silander, J. A. J. (1985). Microevolution in clonal plants. In ‘Population Biology and Evolution of Clonal Organisms’. (Eds J. B. C. Jackson, L. W. Buss, and R. E. Cook.) pp. 107–152. (Yale University Press: New Haven, CT, USA.)
Skaug, H., Fournier, D., Nielsen, A., Magnusson, A. and Bolker, B. (2013). Generalized Linear Mixed Models using AD Model Builder. R package version 0.7.5, Vienna, Austria.
Thompson, K., and Grime, J. P. (1979). Seasonal variation in the seed banks of herbaceous species in 10 contrasting habitats. Journal of Ecology 67, 893–921.
| Seasonal variation in the seed banks of herbaceous species in 10 contrasting habitats.Crossref | GoogleScholarGoogle Scholar |
Tol, S. J., Jarvis, J. C., York, P. H., Grech, A., Congdon, B. C., and Coles, R. G. (2017). Long distance biotic dispersal of tropical seagrass seeds by marine mega-herbivores. Scientific Reports 7, 4458.
| Long distance biotic dispersal of tropical seagrass seeds by marine mega-herbivores.Crossref | GoogleScholarGoogle Scholar | 28667257PubMed |
Tomlinson, P. B. (1974). Vegetative morphology and meristem dependence: the foundation of productivity in seagrasses. Aquaculture 4, 107–130.
| Vegetative morphology and meristem dependence: the foundation of productivity in seagrasses.Crossref | GoogleScholarGoogle Scholar |
Unsworth, R. K. F., Collier, C. J., Waycott, M., Mckenzie, L. J., and Cullen-Unsworth, L. C. (2015). A framework for the resilience of seagrass ecosystems. Marine Pollution Bulletin 100, 34–46.
| A framework for the resilience of seagrass ecosystems.Crossref | GoogleScholarGoogle Scholar |
Waycott, M., Duarte, C. M., Carruthers, T. J. B., Orth, R. J., Dennison, W. C., Olyarnik, S., Calladine, A., Fourqurean, J. W., Heck Jr, K. L., Hughes, A. R., Kendrick, G. A., Kenworthy, W. J., Short, F. T., and Williams, S. L. (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.
| Accelerating loss of seagrasses across the globe threatens coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 19587236PubMed |
Weatherall, E. J., Jackson, E. L., Hendry, R. A., and Campbell, M. L. (2016). Quantifying the dispersal potential of seagrass vegetative fragments: a comparison of multiple subtropical species. Estuarine, Coastal and Shelf Science 169, 207–215.
| Quantifying the dispersal potential of seagrass vegetative fragments: a comparison of multiple subtropical species.Crossref | GoogleScholarGoogle Scholar |
Yaakub, S. M., Lim, R. L. F., Lim, W. L., and Todd, P. A. (2013). The diversity and distribution of seagrass in Singapore. Nature in Singapore 6, 105–111.
Yaakub, S. M., McKenzie, L. J., Erftemeijer, P. L. A., Bouma, T., and Todd, P. A. (2014). Courage under fire: Seagrass persistence adjacent to a highly urbanised city-state. Marine Pollution Bulletin 83, 417–424.
| Courage under fire: Seagrass persistence adjacent to a highly urbanised city-state.Crossref | GoogleScholarGoogle Scholar | 24508045PubMed |