Native, invasive and cryptogenic Ulva species from the Israeli Mediterranean Sea: risk and potential


NIMROD KRUPNIK
GUY PAZ
JACOB DOUEK
EFRAIM LEWINSOHN
ALVARO ISRAEL
NAVA CARMEL
FRÉDÉRIC MINEUR
CHRISTINE A. MAGGS
Resumen

The genus Ulva (Chlorophyta) is ubiquitous along Israeli Mediterranean shores where it has been studied extensively due to its important ecological role and potential value in biotechnology and aquaculture. Previous identifications of Ulva in Israel were based only on morphology. Here, we compare species found in 2002 and in 2014-2016. Analyses of ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL) and elongation factor 1-alpha (tufA) plastid genes (2014-2016 samples only), combined with morphological data, identified six Ulva species, three of which are new records for Israel and probably originate from the Indo-Pacific. Ulva compressa, rarely found in 2002, is now the most abundant species and exhibits two fairly distinct morphologies correlated with different haplotypes for both genes.  Ulva fasciata was found more commonly in 2002 than in 2014-16, whereas the morphologically similar, and closely related, invasive species U. ohnoi seemed more frequent in recent samples.  The finely branched tubular Ulva tepida was found in 2002 and 2015/16, and U. chaugulii and U. mediterranea were discovered for the first time in 2015/16.  The changing Ulva flora of the Israeli Mediterranean may be correlated with major environmental changes including 3°C increase in sea surface temperatures over the last two decades, as well as a generally increasing prevalence of non-native species.  The local Ulva species now found in Israel could be of value for various industrial uses.

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Alongi, A., Cormaci, M., Furnari, G. 2014. A nomenclatural reassessment of some of Bliding's Ulvaceae. Webbia: Journal of Plant Taxonomy and Geography, 69, 89-96.
Aragay, J., Vitales, D., Garreta, A.G., Siguan, M.R., Steen, F. et al., 2016. Phenological and molecular studies on the introduced seaweed Dictyota cyanoloma (Dictyotales, Phaeophyceae) along the Mediterranean coast of the Iberian Peninsula. Mediterranean Marine Science, 17, 766-776.
Awad, N.E, 2000. Biologically active steroid from the green alga Ulva lactuca. Phytotherapy Research, 14(8), 641-643.
Azaza, M.S., Mensi, F., Ksouri, J., Dhraief, M.N., Brini, B. et al., 2008. Growth of Nile tilapia (Oreochromis niloticus L.) fed with diets containing graded levels of green algae Ulva meal (Ulva rigida) reared in geothermal waters of southern Tunisia. Journal of Applied Ichthyology, 24, 202-207.
Bartoli M, Nizzoli D., Naldi M., Vezzulli L., Porrello S. et al., 2005. Inorganic nitrogen control in wastewater treatment ponds from a fish farm (Orbetello, Italy): denitrification versus Ulva uptake. Marine Pollution Bulletin, 50, 1386-1397.
Bast, F., John, A.A., Bhushan, S., 2014. Strong endemism of bloom-forming tubular Ulva in Indian west coast, with description of Ulva paschima sp. nov. (Ulvales, Chlorophyta). PLoS ONE, 9(10), e109295.
Beer, S., Israel, A., Drechsler, Z., Cohen, Y., 1990. Photosynthesis in Ulva fasciata V. Evidence for an inorganic carbon concentrating system, and ribulose-1, 5-bisphosphate carboxylase/oxygenase CO2 kinetics. Plant Physiology, 94, 1542-1546.
Beer, T., Israel, A., Helman, Y., Kaplan, A., 2008. Acidification and CO2 production in the boundary layer during photosynthesis in Ulva rigida (Chlorophyta) C. Agardh. Israel Journal of Plant Sciences, 56, 55-60.
Bliding, C., 1960. A preliminary report on some new Medtierranean green algae. Botaniska Notiser, 113, 172-184.
Bliding, C., 1963. A critical survey of European taxa in Ulvales, Part I. Capsosiphon, Percursaria, Blidingia, Enteromorpha. Botaniska Notiser, Supplement, 8, 1-160.
Blomster, J., Maggs, C.A., Stanhope M.J., 1998. Molecular and morphological analysis of Enteromorpha intestinalis and E. compressa (Chlorophyta) in the British Isles. Journal of Phycology, 34, 319-340.
Blomster, J., Back, S., Fewer, D.P., Kiirikki, M., Lehvo, A. et al., 2002. Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. American Journal of Botany, 89, 1756-1763.
Brito, L.O., Arantes, R., Magnotti, C., Derner, R., Pchara, F. et al., 2013. Water quality and growth of Pacific white shrimp Litopenaeus vannamei (Boone) in co-culture with green seaweed Ulva lactuca (Linaeus) in intensive system. Aquaculture International, 22, 497-508
Brodie, J., Maggs, C.A, John, D.M., 2007. Green seaweeds of Britain and Ireland. British Phycological Society, London. 242 pp.
Chemodanov, A., Jinjikhashvily, G., Habiby, O., Liberzon, A., Israel, A. et al., 2017. Net primary productivity, biofuel potential for biorefineries and climate change mitigation of Ulva (Chlorophyta) biomass in a coastal area of the Eastern Mediterranean. Energy Conversion and Management, 148, 1497-1507.
Coat, G., Dion, P., Noailles, M.C., De Reviers, B., Fontaine, J.M. et al., 1998. Ulva armoricana (Ulvales, Chlorophyta) from the coasts of Brittany (France). II. Nuclear rDNA ITS sequence analysis. European Journal of Phycology, 33, 81-86.
Cruz-Suarez, L.E., Leon, A., Pena-Rodriguez, A., Rodríguez-Peña, G., Moll, B. et al., 2010. Shrimp/Ulva co-culture: A sustainable alternative to diminish the need for artificial feed and improve shrimp quality. Aquaculture, 301, 64-68.
Delile, A.R., 1813. Description de l’Égypte (Tom. sec.) 3 (Florae Aegypticae Illustratio). Imprimerie Impériale, Paris.
Díez, I., Muguerza, N., Santolaria, A., Ganzedo, U., Gorostiaga, J.M., 2012. Seaweed assemblage changes in the eastern Cantabrian Sea and their potential relationship to climate change. Estuarine, Coastal and Shelf Science, 99, 108-120.
Einav, R., Israel, A., 2008. Checklist of seaweeds from the Israeli Mediterranean: Taxonomical and ecological approaches. Israel Journal of Plant Sciences, 56, 1-2, 127-191.
Einav, R., 2007. Seaweed of the eastern Mediterranean coast. A.R. Gantner Verlag, Ruggell.
Felsenstein, J. (2013) PHYLIP version 3.696. http://evolution.genetics.washington.edu/phylip.html
Figueroa, F.L., Martínez, B., Israel, A., Neori, A., Malta, E. et al., 2009. Acclimation of Red Sea macroalgae to solar radiation: photosynthesis and thallus absorptance. Aquatic Biology, 7, 159-172.
Flagella, M.M., Verlaque, M., Soria, A., Buia, M.C., 2007. Macroalgal survival in ballast water tanks. Marine Pollution Bulletin, 54, 1395-1401.
Flagella, M.M., Andreakis, N., Hiraoka, A., Verlaque, M., Buia, M.C., 2009. Identification of cryptic Ulva species (Chlorophyta, Ulvales) transported by ballast water. Journal of Biological Research, 13, 47-57.
Gertman, I., Goldman, R., Ozer, T., Zodiatis, G., 2013. Interannual changes in the thermohaline structure of the southeastern Mediterranean. Rapport du 40e Congrès du Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée, 40, 211.
Goren, M., Galil, B.S., Diamant, A., Stern, N., Levitt-Barmats, Y., 2016. Invading up the food web? Invasive fish in the southeastern Mediterranean Sea. Marine Biology 163, 180. DOI: 10.1007/s00227-016-2950-7.
Gouy, M., Guindon, S., Gascuel, O., 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221-224.
Guidone, M., Thornber, C., Wysor, B., O’Kelly, C.J., 2013. Molecular and morphological diversity of Narragansett Bay (RI, USA) Ulva (Ulvales, Chlorophyta) populations. Journal of Phycology, 49, 979- 995.
Guidone, M., Thornber, C.S., 2013. Examination of Ulva bloom species richness and relative abundance reveals two cryptically occurring bloom species in Narragansett Bay, Rhode Island. Harmful Algae, 24, 1-9.
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. et al., 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307-321.
Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
Hayden, H.S., Waaland, J.R., 2002. Phylogenetic systematics of the Ulvaceae (Ulvales, Ulvophyceae) using chloroplast and nuclear DNA sequences. Journal of Phycology, 38, 1200-1212.
Hayden, H.S., Blomster, J., Maggs, C.A., Silva, P.C., Stanhope, M.J. et al., 2003. Linaeus was right all along: Ulva and Enteromorpha are not distinct genera. European Journal of Phycology, 38, 277-294.
Higgins, D.G., Sharp, P.M., 1989. Fast and sensitive multiple sequence alignments on a microcomputer. Computer Applications in the Biosciences 5, 151-153.
Hiraoka, M., Shimada, S., Uenosono, M., Masuda, M., 2004. A new green-tide-forming alga, Ulva ohnoi Hiraoka et Shimada sp. nov. (Ulvales, Ulvophyceae) from Japan. Phycological Research, 51, 17-29.
Hiraoka, M., Ichihara, K., Zhu, W., Shimada, S., Oka, N. et al., 2017. Examination of species delimitation of ambiguous DNA-based Ulva (Ulvophyceae, Chlorophyta) clades by culturing and hybridisation. Phycologia, 56, 517-532.
Hoffman, R., Wynne, M.J., 2016. Tetrasporangial plants of Monosporus indicus (Ceramiales, Rhodophyta): a new alien in the Mediterranean Sea. European Journal of Phycology, 51, 461-468.
Israel, A., Einav, R., 2017. Alien seaweeds in the Levant basin (Eastern Mediterranean Sea), with special emphasis to the Israeli shores. Israel Journal of Plant Sciences DOI: 10.1080/07929978.2016.1257091).
Israel, A., Hophy, M., 2002. Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Global Change Biology 8, 831-840.
Joshi, H.V., Krishnamurthy, V., 1972. The species of Enteromorpha from India. Botanical Journal of the Linnean Society, 65, 119-128.
Katsanevakis, S., Crocetta, F., 2014. Pathways of introduction of marine alien species in European waters and the Mediterranean – a possible undetermined role of marine litter. CIESM Workshop Monograph, 61-68.
Kirkendale L., Saunders G.W., Winberg P., 2013. A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism. Journal of Phycology, 49, 69-81.
Korzen, L., Pulidindi, I.N., Israel, A., Abelson, A., Gedanken, A., 2015. Single step production of bioethanol from the seaweed Ulva rigida using sonication. RSC Advances, 5, 16223-16229.
Korzen, L., Abelson, A., Israel, A., 2016. Growth, protein and carbohydrate contents in Ulva rigida and Gracilaria bursa-pastoris integrated with an offshore fish farm. Journal of Applied Phycology, 28, 1835-1845.
Kraft, L.G.K, Kraft, G.T., Waller, R.F., 2010. Investigations into southern Australian Ulva (Ulvophyceae, Chlorophyta) taxonomy and molecular phylogeny indicate both cosmopolitanism and endemic cryptic species. Journal of Phycology, 46, 1257-1277.
Leskinen, E., Alstrom-Rapaport, C., Pamilo, P., 2004. Phylogeographical structure, distribution and genetic variation of the green algae Ulva intestinalis and U. compressa (Chlorophyta) in the Baltic Sea area. Molecular Ecology, 13, 2257- 2265.
Li, Y., Huang, H.J., Li, H., Liu, J., Yang, W., 2016. Genetic diversity of Ulva prolifera population in Qingdao coastal water during the green algal blooms revealed by microsatellite. Marine Pollution Bulletin, 111, 237-246.
Longstaff, B.J., Kildea, T., Runcie, J.W., Cheshire, A., Dennison, W.C. et al., 2002. An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynthesis Research, 74, 281-293.
Loughnane, C.J., McIvor, L.M., Rindi, F., Stengel, D.B., Guiry, M.D., 2008. Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia, 47, 416-429.
Maddison, W.P., Maddison, D.R., 1992. MacClade: analysis of phylogeny and character evolution. Evolution, PMBD, 185908476.
Malta, E.J., Draisma, S., Kamermans, P., 1999. Free-floating Ulva in the southwest Netherlands: species or morphotypes? A morphological, molecular and ecological comparison. European Journal of Phycology, 34, 443-454.
Mares J., Leskinen, E., Sitkowska, M., Skácelová, O., Blomster, J., 2011. True identity of the European freshwater Ulva (Chlorophyta, Ulvophyceae) revealed by a combined molecular and morphological approach. Journal of Phycology, 47, 1177-1192.
Masakiyo, Y., Shimada, S., 2014. Species diversity of the genus Ulva (Ulvophyceae, Chlorophyta) in Japanese waters, with special reference to Ulva tepida Masakiyo et S.Shimada sp. nov. Bulletin of the National Science Museum Series B (Botany), 40 (1): 1-13.
McNeill, J., Barrie, F.R., Buck, W.R., Demoulin, V., Greuter, W. et al. (eds.), 2012. International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Regnum Vegetabile, 154. A.R.G. Gantner Verlag.
Mineur, F., Arenas, F., Assis, J., Davies, A.J., Engelen, A.H. et al., 2015. European seaweeds under pressure: consequences for communities and ecosystem functioning. Journal of Sea Research, 98, 91-108.
Nunes, A.L, Katsanevakis, S, Zenetos, A., Cardoso, A.C., 2014. Gateways to alien invasions in the European seas. Aquatic Invasions, 9, 133–144.
Ogawa, T., Ohki, K., Kamiya, M., 2013. Differences of spatial distribution and seasonal succession among Ulva species (Ulvophyceae) across salinity grandients. Phycologia, 52, 637-651
Ozer, T., Gertman, I., Kress, N., Silverman, J., Herut, B., 2016. Interannual thermohaline (1979-2014) and nutrient (2002-2014) dynamics in the Levantine surface and intermediate water masses, SE Mediterranean Sea. Global and Planetary Change, 1-8. doi:10.1016/j.gloplacha.2016.04.001.
Phillips, J.A., Lawton, R.J., Denys, R., Paul, N.A., Carl, C., 2016. Ulva sapora sp. nov., an abundant tubular species of Ulva (Ulvales) from the tropical Pacific Ocean. Phycologia, 55, 55-64.
Pirian, K., Piri, K., Sohrabipour, J., Tamadoni Jahromi, S., Blomster, J., 2016. Molecular and morphological characterisation of Ulva chaugulii, U. paschima and U. ohnoi (Ulvophyceae) from the Persian Gulf, Iran. Botanica Marina, 59, 147-158.
Raveh, O., David, N., Rilov, G., Rahav, E., 2015. The temporal dynamics of coastal phytoplankton and bacterioplankton in the Eastern Mediterranean Sea. Plos ONE, 10, e0140690. doi:10.1371/journal.pone.0140690.
Rouxel, C., Bonnabeze, E., Daniel, A., Jerome, M., Etienne, M. et al., 2001. Identification by SDS PAGE of green seaweeds (Ulva and Enteromorpha) used in the food industry. Journal of Applied Phycology, 13, 215-219.
Saunders, G.W., Kucera, H., 2010. An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the green algae. Cryptogamie, Algologie, 31, 487-528.
Shaltout, M., Omstedt, A., 2014. Recent sea surface temperature trends and future scenarios for the Mediterranean Sea. Oceanologia, 56 (3), 411-443. doi:10.5697/oc.56-3.411.
Shefer, S., Israel, A., Golberg, A., Chudnovsky, A., 2017. Carbohydrate-based phenotyping of the green macroalga Ulva fasciata using near infrared spectrometry: potential implications to marine biorefinery. Botanica Marina, 60, 219-228.
Shimada, S., Hiraoka, M., Nabata, S., Iima, M., Masuda, M., 2003. Molecular phylogenetic analyses of the Japanese Ulva and Enteromorpha (Ulvales, Ulvophyceae), with special reference to the free floating Ulva. Phycological Research, 51, 99-108.
Singh, J., Gu, S., 2010. Commercialization potential of microalgae for biofuels production. Renewable and Sustainable Energy Reviews, 14, 2596-2610.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725-2729.
Tang, J., Tao, J., Urakawa, H., Corander, J., 2007. T-BAPS: a Bayesian statistical tool for comparison of microbial communities using terminal-restriction fragment length polymorphism (T-RFLP) data. Statistical Applications in Genetics and Molecular Biology, 6, 1-19.
Titelboim, D, Almogi-Labin, A., Herut, B., Kucera, M., Schmidt, C. et al., 2016. Selective responses of benthic foraminifera to thermal pollution. Marine Pollution Bulletin 105, 324-336.
Trivedi, N., Gupta, V., Reddy, C.R.K., Jha, B., 2013. Enzymatic hydrolysis and production of bioethanol from common macrophytic green alga Ulva fasciata Delile. Bioresource Technology, 150, 106-112.
Viera, M.D.P., Courtois de Viçose, G., Fernández‐Palacios, H., Izquierdo, M., 2016. Grow‐out culture of abalone Haliotis tuberculata coccinea Reeve, fed land‐based IMTA produced macroalgae, in a combined fish/abalone offshore mariculture system: effect of stocking density. Aquaculture Research, 47, 71-81.
Wolf, M.A., Sciuto, K., Andreoli, C., Moro, I., 2012. Ulva (Chlorophyta, Ulvales) biodiversity in the north Adriatic Sea (Mediterranean, Italy): cryptic species and new introductions. Journal of Phycology, 48, 1510-1521.
Zenetos, A., Cinar, M.E., Pancucci-Papadopoulou, M.A., Harmelin, J.G., Furnari, G. et al., 2005. Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterranean Marine Science, 6, 62-118.
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