Surprising widespread Cymodocea nodosa occurrence along Israel’s Mediterranean coast and Implications for Seagrass Conservation in a hotspot of climate change


ORI HEPNER UCKΟ
EDUARDO ARLÉ
SHAHAR MALAMUD
GIDON WINTERS
JONATHAN BELMAKER
Аннотация

Cymodocea nodosa is a temperate seagrass that grows in shallow and sheltered waters of the Mediterranean Sea. Although it is found in both the western and eastern basins, it was thought to be absent from the extremely warm and salty waters along the Israeli coastline, the most eastern part of the Mediterranean. We conducted methodical, seasonal, towed-diver surveys along the Mediterranean coast of Israel, recording position, depth, presence/absence of C. nodosa, seabed characteristics, and habitat complexity. We used general additive models (GAMs) to understand how the combination of depth, latitude (space), and season (time), explained the distribution of local meadows. We then compared the habitat affinity of these Israeli meadows with other sites in the Eastern Mediterranean by conducting a systematic literature review and using Species Distribution Models (SDMs). Underwater surveys unveiled the extensive distribution of C. nodosa over a narrow depth range of 8-21m (with peak occurrence at 14m) in exposed habitats. These locations are distinct from other Eastern Mediterranean populations, in which C. nodosa is found in shallower and sheltered habitats. SDMs confirmed the increase in the geographical range also reflects an increase in realized niche breadth into higher values of temperatures, salinity, and current velocity. Considering that the eastern tip of the Mediterranean is a climate change hotspot, finding C. nodosa populations surviving these harsh conditions holds implications for seagrass conservation and restoration in the entire Mediterranean. However, the low density of observed meadows suggests that these populations require careful monitoring to prevent local extirpation.

Article Details
  • Раздел
  • Research Article
Скачивания
Данные скачивания пока недоступны.
Библиографические ссылки
Alberto, F., Massa, S., Manent, P., Diaz‐Almela, E., Arnaud‐ Haond, S. et al., 2008. Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean–Atlantic transition region. Journal of Biogeography, 35 (7).
Almagor, G., Gill, D., Perath, I., 2000. Marine sand resources offshore Israel. Marine Georesources & Geotechnology, 18 (1), 1-42.
Araújo, M.B., New, M., 2007. Ensemble forecasting of species distributions. Trends in Ecology and Evolution, 22 (1), 42-47.
Barbet-Massin, M., Jiguet, F., Albert, C.H., Thuiller, W., 2012. Selecting pseudo-absences for species distribution models: how, where and how many? Methods in Ecology and Evolution, 3 (2), 327-338.
Beca-Carretero, P., Teichberg, M., Winters, G., Procaccini, G., Reuter, H., 2020. Projected rapid habitat expansion of tropical seagrass species in the mediterranean sea as climate change progresses. Frontiers in Plant Science, 11, 555376.
Beca-Carretero, P., Winters, G., Teichberg, M., Procaccini, G., Schneekloth, F. et al., 2024. Climate change and the presence of invasive species will threaten the persistence of the Mediterranean seagrass community. Science of the Total Environment, 910, 168675.
Beer, S., Vilenkin, B., Weil, A., Veste, M., Susel, L. et al.,1998. Measuring photosynthetic rates in seagrasses by pulse amplitude modulated (PAM) fluorometry. Marine Ecology Progress Series, 174, 293-300.
Binzer, T., Borum, J., Pedersen, O., 2005. Flow velocity affects internal oxygen conditions in the seagrass Cymodocea nodosa. Aquatic Botany, 83 (3), 239-247.
Booth, T.H., 2017. Assessing species climatic requirements beyond the realized niche: some lessons mainly from tree species distribution modelling. Climatic Change, 145 (3- 4), 259-271.
Cebrián, J., Duarte, C.M., Marbà, N., 1996. Herbivory on the seagrass Cymodocea nodosa (Ucria) Ascherson in contrasting Spanish Mediterranean habitats. Journal of Experimental Marine Biology and Ecology. 204 (1-2), 103-111.
Chaikin, S., Belmaker, J., 2023. Fish depth redistributions do not allow maintenance of abundance in a region of rapid change. Oikos, 2023 (8), e09650.
Chaikin, S., Dubiner, S., Belmaker, J., 2022. Cold-water species deepen to escape warm water temperatures. Global Ecology and Biogeography, 31 (1), 75-88.
Chefaoui, R.M., Assis, J., Duarte, C.M., Serrão, E.A., 2016. Large-Scale Prediction of Seagrass Distribution Integrating Landscape Metrics and Environmental Factors: The Case of Cymodocea nodosa (Mediterranean–Atlantic). Estuaries and Coasts, 39 (1), 123-137.
Dennison, W.C., 1987. Effects of light on seagrass photosynthesis, growth and depth distribution. Aquatic Botany, 27 (1), 15-26.
Duffy, J.E., 2006. Biodiversity and the functioning of seagrass ecosystems. Marine Ecology Progress Series, 311, 233-250.
Edelist, D., Rilov, G., Golani, D., Carlton, J.T., Spanier, E., 2013. Restructuring the Sea: profound shifts in the world’s most invaded marine ecosystem. Diversity and Distributions, 19, 69-77.
El-Din, N.G.S., El-Sherif, Z.M., 2013. Nutritional value of Cymodocea nodosa and Posidonia oceanica along the western Egyptian Mediterranean coast. Egyptian Journal of Aquatic Research, 39, 153-165.
Fakiris, E., Giannakopoulos, V., Leftheriotis, G., Dimas, A., Papatheodorou, G., 2023. Predictive Mapping of Mediterranean Seagrasses-Exploring the Influence of Seafloor Light and Wave Energy on Their Fine-Scale Spatial Variability. Remote Sensing,15, 2943.
Fourqurean, J.W., Duarte, C.M., Kennedy, H., Marbà, N., Holmer, M. et al., 2012. Seagrass ecosystems as a globally significant carbon stock. Nature Geoscience, 5 (7), 505-509.
Galil, B., 2007. Seeing Red: Alien species along the Mediterranean coast of Israel. Aquatic Invasions, 2, 281-312.
Green, E.P, Short, F.T., 2003. World atlas of seagrasses. University of California, Berkeley, Los Angeles & London, 298 pp.
den Hartog, C., 1970 The sea-grasses of the world. North-Holland Publishing Company, Amsterdam, 275 pp.
Iturbide, M., Bedia, J., Gutiérrez, J.M., 2018. Background sampling and transferability of species distribution model ensembles under climate change. Global and Planetary Change, 166, 19-29.
Koch, E.W., 1994. Hydrodynamics, diffusion-boundary layers and photosynthesis of the seagrasses Thalassia testudinum and Cymodocea nodosa. Marine Biology, 118, 767-776.
Konstantinidis, I., Gkafas, G.A., Papathanasiou, V., Orfanidis, S., Küpper, F.C. et al., 2022. Biogeography pattern of the marine angiosperm Cymodocea nodosa in the eastern Mediterranean Sea related to the quaternary climatic changes. Ecology and Evolution, 12 (5), e8911.
Laffoley, D.d’A., Grimsditch, G. (Eds). 2009. The management of natural coastal carbon sinks. IUCN, Gland, Switzerland. 53 pp.
Lino K., Asher J., Ferguson M., Gray A., McCoy K. et al., 2018. Ecosystem Sciences Division standard operating procedures: data collection for towed-diver benthic and fish surveys. Pacific Islands Fisheries Science Center, National Marine Fisheries Service, Administration Report H; 18-02, 76 pp.
Lipkin, Y., Beer, S., and Zakai, D., 2003. The Eastern Mediterranean and Red Sea. p. 65–73 in: World Atlas of Seagrasses. Green, E. P., Short, F. T. (Eds). Berkeley, California: University of California Press.
Lobo, J.M., Jiménez-Valverde, A., Real, R., 2008. AUC: a misleading measure of the performance of predictive distribution models. Global Ecology and Biogeography, 17, 145-151.
Marbà, N., Duarte, C.M., Cebrián, J., Gallegos, M.E., Olesen, B. et al., 1996a. Growth and population dynamics of Posidonia oceanica on the Spanish Mediterranean coast: elucidating seagrass decline. Marine Ecology Progress Series, 137, 203-213.
Marbà, N., Cebrián, J., Enríquez, S., Duarte, C.M., 1996b. Growth patterns of Western Mediterranean seagrasses:species- specific responses to seasonal forcing. Marine Ecology Progress Series, 133, 203-215.
Masucci, A.P., Arnaud-Haond, S., Eguíluz, V.M., Hernández- García, E., Serrão, E.A., 2012. Genetic flow directionality and geographical segregation in a Cymodocea nodosa genetic diversity network. EPJ Data Science, 1, 11.
Maxwell, P.S., Eklöf, J.S., van Katwijk, M.M., O’Brien, K.R., de la Torre-Castro, M. et al., 2017. The fundamental role of ecological feedback mechanisms for the adaptive management of seagrass ecosystems - a review. Biological Reviews, 92, 1521-1538.
Mazarrasa, I., Marbà, N., Lovelock, C.E., Serrano, O., Lavery, P.S. et al., 2015. Seagrass meadows as a globally significant carbonate reservoir. Biogeosciences, 12 (16), 4993-5003.
Miller, I.R., Jonker, M.J., Coleman, G., 2009. Crown-of-thorns starfish and coral surveys using the manta tow and SCUBA search techniques. Australian Institute of Marine Science, Long-term monitoring of the Great Barrier Reef standard operation procedure number 9, edn 3, 74pp.
Millot, C., Candela, J., Fuda, J.L., Tber, Y., 2006. Large warming and salinification of the Mediterranean outflow due to changes in its composition. Deep Sea Research Part I: Oceanographic Research Papers, 53, 656-666.
Mutlu, E., Olguner, C., Özvarol, Y., Gökoğlu, M., 2022. Spatiotemporal biometrics of Cymodocea nodosa in a western Turkish Mediterranean coast. Biologia, 77 (3), 649-670.
Najdek, M., Korlević, M., Paliaga, P., Markovski, M., Ivančić, I. et al., 2020. Dynamics of environmental conditions during the decline of a Cymodocea nodosa meadow. Biogeosciences, 17, 3299-3315.
Nguyen, H.M., Ralph, P.J., Marín-Guirao, L., Pernice, M., Procaccini, G., 2021. Seagrasses in an era of ocean warming: a review. Biological Reviews, 96, 2009-2030.
Nordlund, L.M., Koch, E.W., Barbier, E.B., Creed, J.C., 2016. Seagrass Ecosystem Services and Their Variability across Genera and Geographical Regions. PLoS ONE, 11, e0163091.
Nordlund, L.M., Unsworth, R.K.F., Gullström, M., Cullen-Unsworth, L.C., 2017. Global significance of seagrass fishery activity. Fish and Fisheries, 19, 399-412.
Ohayon, S., Homma, H., Malamud, S., Ostrovsky, I., Yahel, R. et al., 2023. Consistent edge effect patterns revealed using continuous surveys across an Eastern Mediterranean no-take marine protected area. ICES Journal of Marine Sciences, 80 (6), 1594-1605.
Orfanidis, S., Panayotidis, P., Siakavara, A., 2005. Benthic macrophytes: main trends in diversity and distribution. P. 226- 235. In: State of the Hellenic Environment, Papathanassiou, E., Zenetos, A., (Eds). HCMR Publication, Athens.
Orfanidis, S., Papathanasiou, V., Gounaris, S., Theodosiou T., 2010. Size distribution approaches for monitoring and conservation of coastal Cymodocea habitats. Aquatic Conservation Marine and Freshwater Ecosystems, 20 (2), 177-188.
Ozer, T., Gertman, I., Kress, N., Silverman, J., Herut, B., 2017. Interannual thermohaline (1979–2014) and nutrient (2002– 2014) dynamics in the Levantine surface and intermediate water masses, SE Mediterranean Sea. Global and Planetary Change, 151, 60-67.
Ozer, T., Gertman, I., Gildor, H., Herut, B., 2022. Thermohaline Temporal Variability of the SE Mediterranean Coastal Waters (Israel) – Long-Term Trends, Seasonality, and Connectivity. Frontiers in Marine Science, 8:799457.
Pedersen, E.J., Miller, D.L., Simpson, G.L., Ross, N., 2019. Hierarchical generalized additive models in ecology: an introduction with mgcv. PeerJ, 7, e6876.
Pérez, M., Romero, J., 1992. Photosynthetic response to light and temperature of the seagrass Cymodocea nodosa and the prediction of its seasonality. Aquatic Botany, 43, 51-62.
Pickholtz, R.S.M., Kiflawi, M., Friedlander, A.M., Belmaker, J., 2018. Habitat utilization by an invasive herbivorous fish (Siganus rivulatus) in its native and invaded range. Biological Invasions, 20, 3499-3512.
Polunin, N.V.C., Roberts, C.M., 1993. Greater biomass and value of target coral-reef fishes in two small Caribbean marine reserves. Marine Ecology Progress Series, 100, 167-176.
Potouroglou, M., Bull, J.C., Krauss, K.W., Kennedy, H.A., Fusi, M. et al., 2017. Measuring the role of seagrasses in regulating sediment surface elevation. Scientific Reports, 7, 11917.
van Rijn, I., Kiflawi, M., Belmaker, J., 2020. Alien species stabilize local fisheries catch in a highly invaded ecosystem. Canadian Journal of Fisheries and Aquatic Sciences, 77, 752-761.
Sala, E., Kizilkaya, Z., Yildirim, D., Ballesteros, E., 2011. Alien marine fishes deplete algal biomass in the Eastern Mediterranean. PLoS ONE, 6, e17356.
Schröder, K., Gasparini, G.P., Tangherlini, M., Astraldi, M., 2006. Deep and intermediate water in the western Mediterranean under the influence of the Eastern Mediterranean Transient. Geophysical Research Letters, 33 (21).
Sghaier, Y.R., Limam, A., Samaha, L., Bitar, G., Khalaf, G. et al., 2014. Cymodocea nodosa distribution along the Lebanese coast. p. 248-249. In: Proceedings of the 5th Mediterranean Symposium on Marine Vegetation, Portoroz, Slovenia, 27-28 October 2014. UNEP-MAP-RAC/SPA, Tunis.
Short, F.T., Short, C.A., Novak, A.B., 2016. Seagrasses.p. 1-19. in: The Wetland Book: II: Distribution, Description and Conservation. Finlayson, C.M., Milton, G.R., Prentice, R.C., Davidson, N.C. (Eds.). Springer Netherlands, Dordrecht.
Spanier, E., Zviely, D., 2023. Key Environmental Impacts along the Mediterranean Coast of Israel in the Last 100 Years. Journal of Marine Science and Engineering, 11, 2.
Swets, J.A., 1988. Measuring the accuracy of diagnostic systems. Science, 240, 1285-1293.
Todd, P.A., Heery, E.C., Loke, L.H.L., Thurstan, R.H., Kotze, D.J. et al., 2019. Towards an urban marine ecology: characterizing the drivers, patterns and processes of marine ecosystems in coastal cities. Oikos, 128, 1215-1242.
Tsioli, S., Orfanidis, S., Papathanasiou, V., Katsaros, C., Exadactylos, A., 2019. Effects of salinity and temperature on the performance of Cymodocea nodosa and Ruppia cirrhosa: A medium-term laboratory study. Botanica Marina, 62, 97-108.
Tsioli, S., Papathanasiou, V., Rizouli, A., Kosmidou, M., Katsaros, C. et al., 2021. Diversity and composition of algal epiphytes on the Mediterranean seagrass Cymodocea nodosa : a scale-based study. Botanica Marina, 64, 101-118.
Turner, J.A., Babcock, R.C., Kendrick, G.A., Hovey, R.K., 2019. How does spatial resolution affect model performance? A case for ensemble approaches for marine benthic mesophotic communities. Journal of Biogeography, 46, 1249-1259.
Tuya, F., 2006. Seasonal cycle of a Cymodocea nodosa seagrass meadow and of the associated ichthyofauna at Playa Dorada (Lanzarote, Canary Islands, eastern Atlantic). Ciencias Marinas, 32, 695-704.
Tuya, F., Ribeiro-Leite, L., Arto-Cuesta, N., Coca, J., Haroun, R. et al., 2014. Decadal changes in the structure of Cymodocea nodosa seagrass meadows: Natural vs. human influences. Estuarine, Coastal and Shelf Science, 137, 41-49.
Unsworth, R.K.F., Nordlund, L.M., Cullen-Unsworth, L.C., 2018. Seagrass meadows support global fisheries production. Conservation Letters, e12566.
Vergés, A., Tomas, F., Cebrian, E., Ballesteros, E., Kizilkaya, Z. et al., 2014. Tropical rabbitfish and the deforestation of a warming temperate sea. Journal of Ecology, 102, 1518-1527.
Vizzini, S., 2009. Analysis of the trophic role of Mediterranean seagrasses in marine coastal ecosystems: a review. Botanica Marina, 52, 383-393.
Winters, G., Beer, S., Willette, D.A., Viana, I.G., Chiquillo, K.L. et al., 2020. The Tropical Seagrass Halophila stipulacea: Reviewing What We Know From Its Native and Invasive Habitats, Alongside Identifying Knowledge Gaps. Frontiers in Marine Science, 7:300.
Wood, S.N., 2017. “GAMs in Practice: mgcv.” Generalized additive models: an introduction with R. 2nd ed. New York: Chapman and Hall/CRC. 80pp.
Yeruham, E., Shpigel, M., Abelson, A., Rilov, G., 2020. Ocean warming and tropical invaders erode the performance of a key herbivore. Ecology,101, e02925.
Zhang, L., Liu, S., Sun, P., Wang, T., Wang, G. et al., 2015. Consensus forecasting of species distributions: the effects of niche model performance and niche properties. PLoS ONE, 10, e0120056.
Наиболее читаемые статьи этого автора (авторов)