Synchronized sexual reproduction of the seagrass <i>Syringodium filiforme</i> (Cymodoceaceae) in a tropical reef lagoon on the Caribbean coast of Costa Rica

Keywords: flowering, manatee grass, marine angiosperms, phenology, reproductive cymes


There has been an increasing effort to understand the mechanisms of sexual reproduction in seagrasses, which is usually synchronized. Synchronization is caused by environmental cues, such as temperature and light availability, and most likely occurs to maximize pollination success. At higher latitudes where seagrass reproductive seasons are clearly marked, intraannual variability of environmental triggers is significant. Our aim was to identify the period and frequency of sexual reproduction for the manatee grass Syringodium filiforme in a tropical coral reef lagoon, where the above-mentioned environmental triggers are homogenous all year round. The reproductive state and frequency and shoot length of S. filiforme were measured non-destructively in a monospecific patch on the tropical Caribbean coast of Costa Rica. The meadow was surveyed at 1 to 4-month intervals between May 2010 and May 2012. Water turbidity, temperature, and salinity were measured in situ. During the surveyed period, sexual reproduction of S. filiforme was detected in February and May, while seagrass shoot length showed no variation. The moment of seagrass sexual reproduction was not fully explained by the environmental parameters studied. Regardless of the limited environmental variability compared to previous studies at higher latitudes, synchronization of seagrass sexual reproduction at this tropical location is interesting and requires further studies on mechanisms and its possible adaptive advantage.


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Author Biographies

Jimena Samper-Villarreal, Universidad de Costa Rica

Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación

Margarita Loría-Naranjo, Universidad de Costa Rica

Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación

Brigitta Ine van Tussenbroek, Universidad Nacional Autónoma de México

Unidad Académica Sistemas Arrecifales-Puerto Morelos, Instituto de Ciencias del Mar y Limnología

Jorge Cortés, Universidad de Costa Rica

Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación, Escuela de Biología


Ackerman, J. D. (2006). Sexual reproduction of seagrasses: pollination in the marine context. In A. Larkum, R. Orth & C. Duarte (Eds.), Seagrasses: Biology, Ecology and Conservation (pp. 89-109). The Netherlands: Springer.

Barber, B. J. & Behrens, P. J. (1985). Effects of elevated temperature on seasonal in situ leaf productivity of Thalassia testudinum Banks ex König and Syringodium filiforme Kützing. Aquat. Bot., 22(1), 61-69.

Bates, D., Maechler, M. & Bolker, B. (2012). lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0.

Bijak, A. L., Van Dijk, K. & Waycott, M. (2018). Population structure and gene flow of the tropical seagrass, Syringodium filiforme, in the Florida Keys and subtropical Atlantic region. PloS ONE, 13(9), e0203644.

Bowman, H. H. M. (1918). Botanical ecology of the Dry Tortugas. Pap. Mar. Biol. Carnegie Inst. Wash., 12, 111-137.

Cortés, J. (2016). The Caribbean coastal and marine ecosystems. In M. Kappelle (Ed.), Costa Rican Ecosystems (pp. 591-617). Chicago: University of Chicago Press.

Cortés, J., Fonseca, A. C., Nivia-Ruiz, J., Nielsen-Muñoz, V., Samper-Villarreal, J., Salas, E…. & Zamora-Trejos, P. (2010). Monitoring coral reefs, seagrasses and mangroves in Costa Rica (CARICOMP). Rev. Biol. Trop., 58(Suppl. 3), 1-22.

Cortés, J. & Risk, M. J. (1985). A reef under siltation stress: Cahuita, Costa Rica. Bull. Mar. Sci., 36(2), 339-356.

Crawley, M. J. (2007). The R book. England: John Wiley & Sons.

Den Hartog, C. (1970). The Sea-Grasses of the World. The Netherlands and England: North-Holland Publishing Company.

Fonseca, A. C., Nielsen, V. & Cortés, J. (2007). Monitoreo de pastos marinos en Perezoso, Cahuita, Costa Rica (sitio CARICOMP). Rev. Biol. Trop., 55(1), 55-66.

Fry, B. & Virnstein, R. W. (1988). Leaf production and export of the seagrass Syringodium filiforme Kütz. in Indian River Lagoon, Florida. Aquat. Bot., 30(3), 261-266.

Gilbert, S. & Clark, K. B. (1981). Seasonal variation in standing crop of the seagrass Syringodium filiforme and associated macrophytes in the Northern Indian River, Florida. Estuaries, 4(3), 223-225.

James, R. K., Silva, R., Van Tussenbroek, B. I., Escudero-Castillo, M., Mariño-Tapia, I., Dijkstra, H. A…. & Bouma, T. J. (2019). Maintaining tropical beaches with seagrass and algae: a promising alternative to engineering solutions. BioScience, 69(2), 136-142.

Johnson, A. J., Moore, K. A. & Orth, R. J. (2017). The influence of resource availability on flowering intensity in Zostera marina (L.). J. Exp. Mar. Biol. Ecol., 490, 13-22.

Johnson, E. A. & Williams, S. (1982). Sexual reproduction in seagrasses: reports for five Caribbean species with details for Halodule wrightii Aschers and Syringodium filiforme Kütz. Carib. J. Sci., 18(1-4), 61-70.

Kendrick, G. A., Duarte, C. M. & Marbà, N. (2005). Clonality in seagrasses, emergent properties and seagrass landscapes. Mar. Ecol. Prog. Ser., 290, 291-296.

Kendrick, G. A., Waycott, M., Carruthers, T. J., Cambridge, M. L., Hovey, R., Krauss, S. L. … & i Vidal, O. M. (2012). The central role of dispersal in the maintenance and persistence of seagrass populations. BioScience, 62(1), 56-65.

Kjerfve, B. (1981). Tides of the Caribbean Sea. J. Geophys. Res. 86(C5), 4243-4247.

Lizano, O. G. (2006). Algunas características de las mareas en la costa Pacífica y Caribe de Centroamérica. Ciencia y Tecnología, 24(1), 51-64.

Loría-Naranjo, M., Samper-Villarreal, J., Sandoval-Siles, M. & Cortés, J. (2018). Intra- and inter-annual variation in a seagrass meadow on the Caribbean coast of Costa Rica: 2009-2015. Rev. Biol. Trop., 66(3), 1149-1161.

Marbà, N. & Walker, D. I. (1999). Growth, flowering, and population dynamics of temperate Western Australian seagrasses. Mar. Ecol. Prog. Ser., 184, 105-118.

McMahon, K., Van Dijk, J. K., Ruiz-Montoya, L., Kendrick, G. A., Krauss, S. L., Waycott, M.… & Duarte, C. (2014). The movement ecology of seagrasses. Proc. R. Soc. London, Ser. B, 281, 20140878.

McMillan, C. (1976). Experimental studies on flowering and reproduction in seagrasses. Aquat. Bot., 2, 87-92.

McMillan, C. (1980). Reproductive physiology in the seagrass, Syringodium filiforme, from the Gulf of Mexico and the Caribbean. Am. J. Bot., 67(1), 104-110.

McMillan, C. (1981). Seed reserves and seed germination for two seagrasses, Halodule wrightii and Syringodium filiforme, from the western Atlantic. Aquat. Bot., 11, 279-296.

McMillan, C. (1982). Reproductive physiology of tropical seagrasses. Aquat. Bot., 14, 245-258.

Nielsen-Muñoz, V. & Cortés, J. (2008). Abundancia, biomasa y floración de Thalassia testudinum (Hydrocharitaceae) en el Caribe de Costa Rica. Rev. Biol. Trop., 56(Suppl. 4), 175-189.

Nordlund, L. M., Jackson, E. L., Nakaoka, M., Samper-Villarreal, J., Beca-Carretero, P. & Creed, J. C. (2018). Seagrass ecosystem services - what’s next? Mar. Pollut. Bull, 134, 145-151.

O’Brien, K. R., Adams, M. P., Ferguson, A. J., Samper-Villarreal, J., Maxwell, P. S., Baird, M. E. & Collier, C. (2018a). Seagrass resistance to light deprivation: Implications for resilience. In A. W. D. Larkum, G. A. Kendrick & P. J. Ralph (Eds.), Seagrasses of Australia (pp. 287-311). The Netherlands: Springer.

O’Brien, K. R., Waycott, M., Maxwell, P., Kendrick, G. A., Udy, J. W., Ferguson, A. J. … & Dennison, W. C. (2018b). Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance. Mar. Pollut. Bull,, 134, 166-176.

Orth, R. J., Carruthers, T. J. B., Dennison, W. C., Duarte, C. M., Fourqurean, J. W. … & Olyarnik, S. (2006a). A global crisis for seagrass ecosystems. BioScience, 56(12), 987-996.[987:AGCFSE]2.0.CO;2

Orth, R. J., Harwell, M. C. & Inglis, G. J. (2006b). Ecology of seagrass seeds and seagrass dispersal processes. In A. Larkum, R. Orth & Duarte, C. (Eds.), Seagrasses: Biology, Ecology and Conservation (pp. 111-133). The Netherlands: Springer.

R Development Core Team. (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Retrieved from

Rasheed, M. A., McKenna, S. A., Carter, A. B. & Coles, R. G. (2014). Contrasting recovery of shallow and deep water seagrass communities following climate associated losses in tropical north Queensland, Australia. Mar. Pollut. Bull., 83, 491-499.

Samper-Villarreal, J., Van Tussenbroek, B. I. & Cortés, J. (2018). Seagrasses of Costa Rica: from the mighty Caribbean to the dynamic meadows of the Eastern Tropical Pacific. Rev. Biol. Trop., 66(Suppl. 1), S53-S65.

Short, F. T., Carruthers, T. J. R., van Tussenbroek, B. & Zieman, J. (2010). Syringodium filiforme. The IUCN Red List of Threatened Species. e.T173378A7003203.

Short, F. T., Montgomery, J., Zimmermann, C. & Short, C. (1993). Production and nutrient dynamics of a Syringodium filiforme Kütz. Seagrass bed in Indian River Lagoon, Florida. Estuaries, 16(2), 323-334.

Taylor, W. R. (1928). The marine algae of Florida with special reference to the Dry Tortugas. USA: Carnegie Institution of Washington.

Tomlinson, P. B. & Posluszny, U. (1978). Aspects of floral morphology and development in the seagrass Syringodium filiforme (Cymodoceaceae). Bot. Gaz., 139(3), 333-345.

Valentine, J. F. & Duffy, J. E. (2006). The central role of grazing in seagrass ecology. In A. Larkum, R. Orth & C. Duarte (Eds.), Seagrasses: Biology, Ecology and Conservation (pp. 463-501). The Netherlands: Springer.

Van Tussenbroek, B. I. (1994). Spatial and seasonal variability in biomass and leaf morphology of the manatee grass, Syringodium filiforme in a tropical coral reef lagoon, Mexico. An. Inst. Cienc. Mar Limnol. UNAM, 1-2, 1-13.

Van Tussenbroek, B. I., Cortés, J., Collin, R., Fonseca, A. C., Gayle, P. M. H., Guzmán, H. M.… & Weil, E. (2014). Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse. PLoS ONE, 9(3), e90600.

Van Tussenbroek, B. I., Márquez-Guzman, J. & Wong, R. (2009). Phenology of marine angiosperms (seagrasses): reproductive synchrony in the sea. In A. Gamboa-deBuen, A. Orozco-Segovia & F. Cruz-García (Eds.), Functional Diversity of Plant Reproduction (pp. 17-46). India: Research Singpost.

Van Tussenbroek, B. I., Monroy-Velazquez, L. V. & Solis-Weiss, V. (2012). Meso-fauna foraging on seagrass pollen may serve in marine zoophilous pollination. Mar. Ecol. Prog. Ser., 469, 1-6.

Van Tussenbroek, B. I. & Muhlia-Montero, M. (2013). Can floral consumption by fish shape traits of seagrass flowers? Evol. Ecol., 27(2), 269-284.

Van Tussenbroek, B. I., Soissons, L. M., Bouma, T. J., Asmus, R., Auby, I., Brun, F. G.… & Ganthy, F. (2016a). Pollen limitation may be a common Allee effect in marine hydrophilous plants: implications for decline and recovery in seagrasses. Oecologia, 182(2), 595-609.

Van Tussenbroek, B. I., Villamil, N., Márquez-Guzmán, J., Wong, R., Monroy-Velázquez, L. V. & Solis-Weiss, V. (2016b). Experimental evidence of pollination in marine flowers by invertebrate fauna. Nat. Commun., 7, 12980.

Van Tussenbroek, B. I., Wong, J. R. & Márquez-Guzman, J. (2008). Synchronized anthesis and predation on pollen in the marine angiosperm Thalassia testudinum (Hydrocharitaceae). Mar. Ecol. Prog. Ser., 354, 119-124.

Villalobos-Flores, R. & Rojas-Morales, N. (2016). Descripción del Clima Cantón de Limón. Costa Rica: Instituto Meteorológico Nacional (IMN), Ministerio Nacional del Ambiente y Energía (MINAE) de Costa Rica.

Walker, D. I., Olesen, B. & Phillips, R. C. (2001). Reproduction and phenology in seagrasses. In F. Short & R. Coles (Eds.), Global Seagrass Research Methods (Vol. 33, pp. 59-78). The Netherlands: Elsevier Science B.V.

Waycott, M., Duarte, C. M., Carruthers, T. J. B., Orth, R. J., Dennison, W. C., Olyarnik, S.… & Hughes, A. R. (2009). Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. U.S.A., 106(30), 12377-12381.

Waycott, M., Procaccini, G., Les, D. H. & Reusch, T. B. (2006). Seagrass evolution, ecology and conservation: a genetic perspective. In A. Larkum, R. Orth & C. Duarte (Eds.), Seagrasses: Biology, Ecology and Conservation (pp. 25-50). The Netherlands: Springer.

Zimmerman, M. S. & Livingston, R. J. (1976). Seasonality and physico-chemical ranges of benthic macrophytes from a north Florida estuary (Apalachee Bay). Contrib. Mar. Sci., 20, 33-45.

How to Cite
Samper-Villarreal, J., Loría-Naranjo, M., van Tussenbroek, B., & Cortés, J. (2020). Synchronized sexual reproduction of the seagrass <i>Syringodium filiforme</i&gt; (Cymodoceaceae) in a tropical reef lagoon on the Caribbean coast of Costa Rica. Journal of Marine and Coastal Sciences, 12(1), 49-68.
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