Acknowledgement
The present work formed part of the first author's PhD thesis 'Macroalgal biodiversity of Kuwait, with special emphasis on the vicinity of desalination plants'. We acknowledge Dr. Hedda Weitz (University of Aberdeen) for providing help in the laboratory and from Ioanna Kosma (University of the Aegean) and Andreas Henkel (Kuwait University) for diving and logistics support during the expedition to Kuwait. We acknowledge the funding received to support this work from the Marine Alliance for Science and Technology (grant reference HR09011) to FCK and Kuwait Foundation for the Advancement of Science (KFAS; grant number PR17125L18) to DA. To Mr. Yusuf Buhadi from the department of Marine Sciences at Kuwait University for his help in the field work and to Mrs. Nisha V. S. Vadakkhancheril for photography.
References
- Al-Adilah, H., Al-Bader, D., Elktob, M., Kosma, I., Kumari, P. & Kupper,F. C. 2021. Trace element concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes. Bot. Mar. 64:327-338. https://doi.org/10.1515/bot-2021-0027
- Al-Adilah, H., Peters, A. F., Al-Bader, D., Raab, A., Akhdhar, A., Feldmann, J. & Kupper, F. C. 2020. Iodine and fluorine concentrations in seaweeds of the Arabian Gulf identified by morphology and DNA barcodes. Bot. Mar. 63:509-519. https://doi.org/10.1515/bot-2020-0049
- Alghunaim, A., Taqi, A., Al-Kandari, M. & Al-Said, T. 2019. Distribution and nature of Sargassum species in the Kuwait waters. J. Geosci. Environ. Prot. 7:53-59.
- Al-Hasan, R. H. & Jones, W. E. 1989. Marine algal flora and sea grasses of the coast of Kuwait. J. Univ. Kuwait Sci. 16:289-341.
- Al-Mutairi, N., Abahussain, A. & Al-Battay, A. 2014. Environmental assessment of water quality in Kuwait Bay. Int. J. Environ. Sci. Dev. 5:527-532. https://doi.org/10.7763/IJESD.2014.V5.539
- Al-Said, T., Al-Ghunaim, A., Subba Rao, D. V., Al-Yamani, F., Al-Rifaie, K. & Al-Baz, A. 2017. Salinity-driven decadal changes in phytoplankton community in the NW Arabian Gulf of Kuwait. Environ. Monit. Assess. 189:268.
- Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. https://doi.org/10.1093/nar/25.17.3389
- Al-Yamani, F. Y., Bishop, J., Ramadhan, E., Al-Husain, M. & Al-Ghadban, A. N. 2004. Oceanographic atlas of Kuwait waters. Kuwait Institute for Scientfic Research, Kuwait, 203 pp.
- Al-Yamani, F. Y., Polikarpov, I., Al-Ghunaim, A. & Mikhaylova, T. 2014. Field guide of marine macroalgae (Chlorophyta, Rhodophyta, Phaeophyceae) of Kuwait. Kuwait Institute for Scientific Research, Kuwait, 190 pp.
- Bartolo, A. G., Zammit, G., Peters, A. F. & Kupper, F. C. 2020. The current state of DNA barcoding of marcroalgae in the Mediterranean Sea: presently lacking but urgently required. Bot. Mar. 63:253-272. https://doi.org/10.1515/bot-2019-0041
- Bolton, J. J. 1983. Ecoclinal variation in Ectocarpus siliculosus (Phaeophyceae) with respect to temperature growth optima and survival limits. Mar. Biol. 73:131-138. https://doi.org/10.1007/BF00406880
- Broom, J. E. S., Nelson, W. A., Farr, T. J., Phillips, L. E. & Clayton, M. 2010. Relationships of the Porphyra (Bangiales, Rhodophyta) flora of the Falkland Islands: a molecular survey using rbcL and nSSU sequence data. Aust. Syst. Bot. 23:27-37. https://doi.org/10.1071/SB09033
- Coelho, S. M., Scornet, D., Rousvoal, S., Peters, N. T., Dartevelle, L., Peters, A. F. & Cock, J. M. 2012. Ectocarpus: a model organism for the brown algae. Cold Spring Harb. Protoc. 2012:193-198. https://doi.org/10.1101/pdb.emo065821
- Destombe, C. & Douglas, S. E. 1991. Rubisco spacer sequence divergence in the rhodophyte alga Gracilaria verrucosa and closely related species. Curr. Genet. 19:395-398. https://doi.org/10.1007/BF00309601
- De Vargas, C., Audic, S., Henry, N., Decelle, J., Mahe, F., Logares, R., Lara, E., Berney, C., Le Bescot, N., Probert, I., Carmichael, M., Poulain, J., Romac, S., Colin, S., Aury, J.-M., Bittner, L., Chaffron, S., Dunthorn, M., Engelen, S., Flegontova, O., Guidi, L., Horak, A., Jaillon, O., Lima-Mendez, G., Lukes, J., Malviya, S., Morard, R., Mulot, M., Scalco, E., Siano, R., Vincent, F., Zingone, A., Dimier, C., Picheral, M., Searson, S., Kandels-Lewis, S., Tara Oceans Coordinators, Acinas, S. G., Bork, P., Bowler, C., Gorsky, G., Grimsley, N., Hingamp, P., Iudicone, D., Not, F., Ogata, H., Pesant, S., Raes, J., Sieracki, M. E., Speich, S., Stemmann, L., Sunagawa, S., Weissenbach, J., Wincker, P. & Karsenti, E. 2015. Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605. https://doi.org/10.1126/science.1261605
- Dittami, S. M., Corre, E., Brillet-Gueguen, L., Lipinska, A. P., Pontoizeau, N., Aite, M., Avia, K., Caron, C., Cho, C. H., Collen, J., Cormier, A., Delage, L., Doubleau, S., Frioux, C., Gobet, A., Gonzalez-Navarrete, I., Groisillier, A., Herv, C., Jollivet, D., KleinJan, H., Leblanc, C., Liu, X., Marie, D., Markov, G V., Minoche, A. E., Monsoor, M., Pericard, P., Perrineau, M. M., Peters, A. F., Siegel, A., Simeon, A., Trottier, C., Yoon, H. S., Himmelbauer, H., Boyen, C. & Tonon, T. 2020a. The genome of Ectocarpus subulatus: a highly stress-tolerant brown alga. Mar. Genomics 52:100740. https://doi.org/10.1016/j.margen.2020.100740
- Dittami, S. M., Peters, A. F., West, J. A., Cariou, T., KleinJan, H., Burgunter-Delamare, B., Prechoux, A., Egan, E. & Boyen, C. 2020b. Revisiting Australian Ectocarpus subulatus (Phaeophyceae) from the Hopkins River: distribution, abiotic environment, and associated microbiota. J. Phycol. 56:719-729. https://doi.org/10.1111/jpy.12970
- Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. https://doi.org/10.1093/nar/gkh340
- Fama, P., Wysor, B., Kooistra, W. H. C. F. & Zuccarello, G. C. 2002. Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. J. Phycol. 38:1040-1050. https://doi.org/10.1046/j.1529-8817.2002.t01-1-01237.x
- Fatemi, S. M. R., Ghavam Mostafavi, P., Rafiee, F. & Saeed Taheri, M. 2012. The study of seaweeds biomass from intertidal rocky shores of Qeshm Island, Persian Gulf. Int. J. Mar. Sci. Environ. 2:101-106.
- Gachon, C. M. M., Strittmatter, M., Muller, D. G., Kleinteich, J. & Kupper, F. C. 2009. Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: not all algae are equal. Appl. Environ. Microbiol. 75:322-328. https://doi.org/10.1128/AEM.01885-08
- Hall, J. D., Fucikov, K., Lo, C., Lewis, L. A. & Karol, K. G. 2010. An assessment of proposed DNA barcodes in freshwater green algae. Cryptogam. Algol. 31:529-555.
- Han, K. Y., Graf, L., Reyes, C. P., Melkonian, B., Andersen, R. A., Yoon, H. S. & Melkonian, M. 2018. A re-investigation of Sarcinochrysis marina (Sarcinochrysidales, Pelagophyceae) from its type locality and the descriptions of Arachnochrysis, Pelagospilus, Sargassococcus and Sungminbooa genera nov. Protist 169:79-106. https://doi.org/10.1016/j.protis.2017.12.004
- Hasan, A. H., Van der Aa, P., Kupper, F. C., Al-Bader, D. & Peters, A. F. 2022. Kuwaitiella rubra gen. et sp. nov. (Bangiales, Rhodophyta), a new filamentous genus and species from the north-western Indian Ocean. Phycol. Res. 70:192-202. https://doi.org/10.1111/pre.12498
- Hodge, F. J., Buchanan, J. & Zuccarello, G. C. 2010. Hybridization between the endemic brown algae Carpophyllum maschalocarpum and Carpophyllum angustifolium (Fucales): genetic and morphological evidence. Phycol. Res. 58:239-247. https://doi.org/10.1111/j.1440-1835.2010.00583.x
- Hoffmann, A. J. & Santelices, B. 1991. Banks of algal microscopic forms: hypotheses on their functioning and comparisons with seed banks. Mar. Ecol. Prog. Ser. 79:185-194. https://doi.org/10.3354/meps079185
- John, D. M. 2012. Marine algae (seaweeds) associated with coral reefs of the Gulf. In Riegl, B. M. & Purkis, S. J. (Eds.) Coral Reefs of the Gulfs: Adaptation to Climate Extremes. Coral Reefs of the World, Vol. 3. Springer, Dordrecht, pp. 170-186.
- John, D. M. & Al-Thani, R. F. 2014. Benthic marine algae of the Arabian Gulf: a critical review and analysis of distribution and diversity patterns. Nova Hedwigia 98:341-392. https://doi.org/10.1127/0029-5035/2014/0156
- Jones, D. 1986. A field guide to the seashores of Kuwait and the Arabian Gulf. University of Kuwait, Kuwait, 193 pp.
- Kawai, H., Hanyuda, T., Draisma, S. G. A. & Muller, D. G. 2007. Molecular phylogeny of Discosporangium mesarthrocarpum (Phaeophyceae) with a reinstatement of the order discosporangiales. J. Phycol. 43:186-194. https://doi.org/10.1111/j.1529-8817.2006.00308.x
- Kirkendale, L., Saunders, G. W. & Winberg, P. 2013. A molecular survey of Ulva (Chlorophyta) in temperate Australia reveals enhanced levels of cosmopolitanism. J. Phycol. 49:69-81. https://doi.org/10.1111/jpy.12016
- Kokabi, M. & Yousefzadi, M. 2015. Checklist of the marine macroalgae of Iran. Bot. Mar. 58:307-320. https://doi.org/10.1515/bot-2015-0001
- Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547-1549. https://doi.org/10.1093/molbev/msy096
- Kunimoto, M., Kito, H., Kaminishi, Y., Mizukami, Y. & Murase, N. 1999. Molecular divergence of the SSU rRNA gene and internal transcribed spacer 1 in Porphyra yezoensis (Rhodophyta). J. Appl. Phycol. 11:211-216. https://doi.org/10.1023/A:1008023525847
- Kupper, F. C., Peters, A. F., Shewring, D. M., Sayer, M. D. J., Mystikou, A., Brown, H., Azzopardi, E., Dargent, O., Strittmatter, M., Brennan, D., Asensi, A. O., van West, P. & Wilce, R. T. 2016. Arctic marine phytobenthos of northern Baffin Island. J. Phycol. 52:532-549. https://doi.org/10.1111/jpy.12417
- Lane, C. E., Mayes, C., Druehl, L. D. & Saunders, G. W. 2006. A multi-gene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. J. Phycol. 42:493-512. https://doi.org/10.1111/j.1529-8817.2006.00204.x
- Lawton, R. J., Mata, L., de Nys, R. & Paul, N. A. 2013. Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PLoS ONE 8:e77344.
- Lewin, J. 1966. Silicon metabolism in diatoms. V. Germanium dioide, a specific inhibitor of diatom growth. Phycologia 6:1-12. https://doi.org/10.2216/i0031-8884-6-1-1.1
- Macreadie, P. I., Jarvis, J., Trevathan-Tackett, S. M. & Bellgrove, A. 2017. Seagrasses and macroalgae: importance, vulnerability and impacts. In Phillips, B. F. & Perez-Ramirez, M. (Eds.) Climate Change Impacts on Fisheries and Aquaculture: A Global Analysis. Wiley-Blackwell, Oxford, pp. 729-770.
- Martinez, B., Pato, L. S. & Rico, J. M. 2012. Nutrient uptake and growth responses of three intertidal macroalgae with perennial, opportunistic and summer-annual strategies. Aquat. Bot. 96:14-22. https://doi.org/10.1016/j.aquabot.2011.09.004
- 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. Bull. Natl. Mus. Nat. Sci. Ser. B Bot. 40:1-13.
- Mayakun, J. & Prathep, A. 2005. Seasonal variations in diversity and abundance of macroalgae at Samui Island, Surat Thani Province, Thailand. Songklanakarin J. Sci. Technol. 27:653-663.
- Muller, D. G. & Ramirez, M. E. 1994. Filamentous brown algae from the Juan Fernandez Archipelago (Chile): contribution of laboratory culture techniques to a phytogeographic survey. Bot. Mar. 37:205-211. https://doi.org/10.1515/botm.1994.37.3.205
- Nishihara, G. N. & Terada, R. 2010. Spatial variations in nutrient supply to the red algae Eucheuma serra (J. Agardh) J. Agardh. Phycol. Res. 58:29-34. https://doi.org/10.1111/j.1440-1835.2009.00555.x
- Nybakken, J. W. 1993. Marine biology an ecological approach. Harper Collins College Publishers, NY, 10022 pp.
- Pedersen, M. F., Borum, J. & Fotel, F. L. 2010. Phosphorus dynamics and limitation of fast- and slow-growing temperate seaweeds in Oslofjord, Norway. Mar. Ecol. Prog. Ser. 399:103-115. https://doi.org/10.3354/meps08350
- Peters, A. F., Couceiro, L., Tsiamis, K., Kupper, F. C. & Valero, M. 2015. Barcoding of cryptic stages of marine brown algae isolated from incubated substratum reveals high diversity in Acinetosporaceae (Ectocarpales, Phaeophyceae). Cryptogam. Algol. 36:3-29. https://doi.org/10.7872/crya.v36.iss1.2015.3
- Peters, A. F. & Ramirez, M. E. 2001. Molecular phylogeny of small brown algae, with special reference to the systematic position of Caepidium antarcticum (Adenocystaceae, Ectocarpales). Cryptogam. Algol. 22:187-200. https://doi.org/10.1016/S0181-1568(01)01062-5
- Peters, A. F., Scornet, D., Muller, D. G., Kloareg, B. & Cock, J. M. 2004. Inheritance of organelles in artificial hybrids of the isogamous multicellular chromist alga Ectocarpus siliculosus (Phaeophyceae). Eur. J. Phycol. 39:235-242. https://doi.org/10.1080/09670260410001683241
- Phillips, J. C. & Hurd, C. L. 2003. Nitrogen ecophysiology of intertidal seaweeds from New Zealand: N uptake, storage and utilisation in relation to shore position and season. Mar. Ecol. Prog. Ser. 264:31-48. https://doi.org/10.3354/meps264031
- Pirian, K., Piri, K., Sohrabipour, J., Jahromi, S. T. & Blomster, J. 2016. Molecular and morphological characterisation of Ulva chaugulii, U. paschima and U. ohnoi (Ulvophyceae) from the Persian Gulf, Iran. Bot. Mar. 59:147-158. https://doi.org/10.1515/bot-2016-0009
- Pokavanich, T. & Alosairi, Y. 2014. Summer flushing characteristics of Kuwait Bay. J. Coast. Res. 30:1066-1073. https://doi.org/10.2112/JCOASTRES-D-13-00188.1
- Prathep, A., Wichachucherd, B. & Thongroy, P. 2007. Spatial and temporal variation in density and thallus morphology of Turbinaria ornata in Thailand. Aquat. Bot. 86:132-138. https://doi.org/10.1016/j.aquabot.2006.09.011
- Price, A. R. G., Vincent, L. P. A., Venkatachalam, A. J., Bolton, J. J. & Basson, P. W. 2006. Concordance between different measures of biodiversity in Indian Ocean macroalgae. Mar. Ecol. Prog. Ser. 319:85-91. https://doi.org/10.3354/meps319085
- Provasoli, L. 1966. Media and prospects for the cultivation of marine algae. In Watanabe, A. & Hattori, A. (Eds.) Cult. Collect. Algae: Proc. US-Japan Conf. Japan Society of Plant Physiology, Hakone, pp. 63-75.
- Ramirez, M. E. & Muller, D. G. 1991. New records of benthic marine algae from Easter Island. Bot. Mar. 34:133-137. https://doi.org/10.1515/botm.1991.34.2.133
- Rizouli, A., Kupper, F. C., Louizidou, P., Mogg, A. O. M., Azzopardi, E., Sayer, M. D. J., Kawai, H., Hanyuda, T. & Peters, A. F. 2020. The minute alga Schizocladia ischiensis (Schizocladiophyceaase, Ochrophyta) isolated by germling emergence from 24 m depth of Rhodes (Greece). Diversity 12:102.
- Santianez, W. J. E., Al-Bader, D., West, J. A., Bolton, J. J. & Kogame, K. 2020. Status, morphology, and phylogenetic relationships of Iyengaria (Scytosiphonaceae, Phaeophyceae), a brown algal genus with a disjunct distribution in the Indian Ocean. Phycol. Res. 68:323-331. https://doi.org/10.1111/pre.12438
- Saunders, G. W. 2005. Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:1879-1888. https://doi.org/10.1098/rstb.2005.1719
- Saunders, G. W. & Kucera, H. 2010. An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogam. Algol. 31:487-528.
- Saunders, G. W. & McDevit, D. C. 2013. DNA barcoding unmasks overlooked diversity improving knowledge on the composition and origins of the Churchill algal flora. BMC Ecol. 13:9.
- Schoenrock, K. M., McHugh, T. A. & Krueger-Hadfield, S. A. 2021. Revisiting the 'bank of microscopic forms' in macroalgal-dominated ecosystems. J. Phycol. 57:14-29. https://doi.org/10.1111/jpy.13092
- Siemer, B. L., Stam, W. T., Olsen, T. J. & Pedersen, P. M. 1998. Phylogenetic relationships of the brown algal orders Ectocarpales, Chordariales, Dictyosiphonales, and Tilopteridales (Phaeophyceae) based on RUBISCO large subunit and spacer sequences. J. Phycol. 34:1038-1048. https://doi.org/10.1046/j.1529-8817.1998.341038.x
- Silva, P. C., Basson, P. W. & Moe, R. L. 1996. Catalogue of the benthic marine algae of the Indian Ocean. Vol. 79. University California Press, Berkeley, CA, 1259 pp.
- Starr, R. C. & Zeikus, J. A. 1993. UTEX: the culture collection of algae at the University of Texas at Austin. 1993 List of cultures. J. Phycol. 29:1-106. https://doi.org/10.1111/j.0022-3646.1993.00001.x
- Tanaka, A., Uwai, S., Nelson, W. & Kawai, H. 2010. Phaeophysema gen. nov. and Vimineoleathesia gen. nov., new brown algal genera for the minute Japanese members of the genus Leathesia. Eur. J. Phycol. 45:107-115. https://doi.org/10.1080/09670260903383271
- Tarakhovskaya, E. R., Kang, E. J., Kim, K. Y. & Garbary, D. J. 2012. Effect of GeO2 on embryo development and photosynthesis in Fucus vesiculosus (Phaeophyceae). Algae 27:125-134. https://doi.org/10.4490/algae.2012.27.2.125
- Uddin, S., Al Ghadban, A. N. & Khabbaz, A. 2011. Localized hyper saline waters in Arabian Gulf from desalination activity: an example from South Kuwait. Environ. Monit. Asses. 181:587-594. https://doi.org/10.1007/s10661-010-1853-1
- West, J. A., Loiseaux-De Goer, S. & Zuccarello, G. C. 2012. Upright Erythropeltidales (Rhodophyta) in Brittany, France and description of a new species, Erythrotrichia longistipitata. Cah. Biol. Mar. 53:255-270.
- White, T. J., Bruns, T., Lee, S. & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (Eds.) PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, CA, pp. 315-322.
- Wolf, M. 2012. Molecular and morphological investigations on seaweed biodiversity and alien introductions in the Adriatic Sea (Mediterranean, Italy). Ph.D. dissertation, Universit Degli Studi Di padova Dipartimento Di Biologia, Padova, Italy, 183 pp.
- Wynne, M. J., Kamiya, M., West, J. A., Loiseaux-de Goer, S., Lim, P.-E., Sade, A., Russell, H. & Kupper, F. C. 2020. Morphological and molecular evidence for the recognition of Hypoglossum sabahense sp. nov. (Delesseriaceae, Rhodophyta) from Sabah, Malaysia. Algae 35:157-165. https://doi.org/10.4490/algae.2020.35.5.31
- Yoon, H. S., Hackett, J. D. & Bhattacharya, D. 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. U. S. A. 99:11724-11729. https://doi.org/10.1073/pnas.172234799
- Zuccarello, G. C., Yoon, H. S., Kim, H., Sun, L., de Gor, S. & West, J. A. 2011. Molecular phylogeny of the upright erythropeltidales (Compsopogonophyceae, Rhodophyta): multiple cryptic lineages of Erythrotrichia carnea. J. Phycol. 47:627-637. https://doi.org/10.1111/j.1529-8817.2011.00985.x