Kappaphycus alvarezii , a red macroalgal species native to South-East Asia, has been introduced for commercial purposes to more than 20 tropical countries. In 2000, Panama became the first Central American country to develop its cultivation following a pilot-commercial approach. Twelve years after his introduction to Panama, the species was found to the south Caribbean coast. In the present study, we report the first record of K. alvarezii collected in Costa Rican waters. Genetic identification of the sample was performed with the mitochondrial marker cox2-cox3 intergenic spacer, and phylogenetic analyses showed that the sample collected grouped into a monophyletic clade with GenBank sequences from Vietnam, Indonesia, the Philippines, Brazil and Venezuela. Here we provide further description of its position with respect to other strains of K. alvarezii collected globally . Its possible route of entry to the Caribbean coast of Costa Rica is discussed. To date, it is possible to locate K . alvarezii in different areas away from the production fields which show its dispersion, and that the species is expanding; but more studies are needed to know the phase of colonization in which it is located because it is a combination of natural factors and human exploitation that determines the invasive potential of the species.
Atmadja, W.S. (2001) Kappaphycus alvarezii (Doty) Doty ex Silva. In: Prud’homme van Reine, W.F. and Trono, G.C., Eds., Plant Resources of South-East Asia Cryptogams: Algae, Backhuys Publishers, Leiden, The Netherlands, 215-219.
Areces, A.J., Alvarez, F.A., Bernardi, J. and Cabrera, R. (2014) Ecological Risk Assessment of the Introduction of Exotic Carrageenophytes in the Tropical Western Atlantic. Journal of Applied Phycology, 26, 2055-2063. https://doi.org/10.1007/s10811-014-0385-4
Ask, E.I., Batibasaga, A., Zertuche-González, J.A. and De San, M. (2003) Three Decades of Kappaphycus alvarezii (Rhodophyta) Introduction to Non-Endemic locations. In: Chapman, A.R.O., Anderson, R.J., Vreeland, V.J., Davison, I.R., Eds., Proceedings of the 17th International Seaweed Symposium, Cape Town, South Africa, 49-57.
Ask, E.I. and Azanza, R.V. (2002) Advances in Cultivation Technology of Commercial Eucheumatoid Species: A Review with Suggestions for Future Research. Aquaculture, 206, 257-277. https://doi.org/10.1016/S0044-8486(01)00724-4
Conklin, E.J. and Smith, J.E. (2005) Abundance and Spread of the Invasive Red Algae, Kappaphycus spp., in Kane’ohe Bay, Hawai and an Experimental Assessment of Management Options. Biological Invasions, 7, 1029-1039. https://doi.org/10.1007/s10530-004-3125-x
McHugh, D.J. (2003) A Guide to the Seaweed Industry. FAO Fisheries Technical Paper, No 441, Rome.
Barrios, J. (2005) Scattering of the Exotic Seaweed Kappaphycus alvarezii (Gigartinales: Rhodophyta) in the Northeastern Region of Venezuela. Boletín del Instituto Oceanográfico de Venezuela, 44, 29-34.
Gavino, C. and Trono, J. (1992) Eucheuma and Kappaphycus: Taxonomy and Cultivation. Bulletin Marine Science, 12, 51-65.
Areces, A.J. (1995) Commercial Cultivation of Carrageenans of the Genus Kappaphycus alvarezii Doty. In: Alveal, K., Ferrario, M.E., Oliveira, E.C. and Sar, E., Eds., Manual de Métodos Ficológicos, Universidad de Concepción, Concepcion, Chile, 529-549.
Azanza-Corrales, R., Mamauag, S.S., Alfiler, E. and Orolfo, M.J. (1992) Reproduction in Eucheuma denticulatum (Burman) Collins and Hervey and Kappaphycus alvarezii (Doty) Doty Farmed in Danjon Reef, Philippines. Aquaculture, 103, 29-34. https://doi.org/10.1016/0044-8486(92)90275-P
Castelar, B., Perpetuo-Reis, R., Moura, A.L. and Kirk, R. (2009) Invasive Potential of Kappaphycus alvarezii of the South Coast of Rio de Janeiro State, Brazil: A Contribution to Environmentally Secure Cultivation in the Tropics. Botanica Marina, 52, 283-289. https://doi.org/10.1515/BOT.2009.002
Araújo, P.G., Miranda, G.E.C., Barros-Barreto, M.B. and Fujii, M.T. (2013) Molecular Identification of the Exotic Lineage of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) Cultivated in the Tropical Region of Brazil. Phytotaxa, 109, 17-26. https://doi.org/10.11646/phytotaxa.109.1.2
Sellers, A.J., Saltonstall, K. and Davidson, T.M. (2015) The Introduced Alga Kappaphycus alvarezii (Doty ex P.C. Silva, 1996) in Abandoned Cultivation Sites in Bocas del Toro, Panama. BioInvasions Records, 4, 1-7. https://doi.org/10.3391/bir.2015.4.1.01
Schaffelke, B., Smith, J.E. and Hewitt, C.L. (2006) Introduced Macroalgae—A Growing Concern. Journal of Applied Phycology, 18, 529-554. https://doi.org/10.1007/s10811-006-9074-2
Gribben, P.E. and Wright, J.T. (2006) Invasive Seaweed Enhances Recruitment of a Native Bivalve: Roles of Refuge from Predation and the Habitat Choice of Recruits. Marine Ecology Progress Series, 318, 177-185. https://doi.org/10.3354/meps318177
Wright, J.T., Byers, J.E., DeVore, J.L. and Sotka, E.E. (2014) Engineering or Food? Mechanisms of Facilitation by a Habitat-Forming Invasive Seaweed. Ecology, 95, 2699-2706. https://doi.org/10.1890/14-0127.1
Dijkstra, J.A., Harris, L.G., Mello, K., Litterer, A., Wells, C. and Ware, C. (2017) Invasive Seaweeds Transform Habitat Structure and Increase Biodiversity of Associated Species. Journal of Ecology, 105, 1668-1678. https://doi.org/10.1111/1365-2745.12775
Rodgers, S. and Cox, E.F. (1999) Rate of Spread of Introduced Rhodophytes Kappaphycus alvarezii, Kappaphycus striatum, and Gracilaria salicornia and Their Current Distribution in Kane’ohe Bay, O’ahu Hawai’i. Pacific Science, 53, 232-241.
Woo, M., Smith, C. and Smith, W. (1999) Ecological Interactions and Impacts of Invasive Kappaphycus striatum in Kaneohe Bay, a Tropical Reef. In: Pederson, J., Ed., Proceedings of the First National Conference on Marine Bioinvaders, Cambridge, UK, 186-192.
Kamalakannan, B., Jeevamani, J.J., Nagendran, N.A., Pandiaraja, D. and Chandrasekaran, S. (2014) Impact of Removal of Invasive Species Kappaphycus alvarezii from Coral Reef Ecosystem in Gulf of Mannar, India. Current Science, 106, 1401-1408.
Batista de Vega, G., Contreras, A. and Shields, C. (2002) Experimental Farms of Gracilaria sp and Eucheuma cottoni in the Panamanian Caribbean. VI Congreso Latinoamericano de Ficología y IV Reunión Iberoamericana de Ficología, Ponce, Puerto Rico.
Radulovich, R., Umanzor, S., Cabrera, R. and Mata, R. (2015) Tropical Seaweeds for Human Food, Their Cultivation and Its Effect on Biodiversity Enrichment. Aquaculture, 436, 40-46. https://doi.org/10.1016/j.aquaculture.2014.10.032
Araújo, P.G., Schmidt, E.C., Kreusch, M.G., Kano, C.H., Guimaraes, S.M.P.B., Bouzon, Z.L., Fujii, M.T. and Yokoya, N.S. (2014) Ultrastructural, Morphological, and Molecular Characterization of Colaconema infestans (Colaconematales, Rhodophyta) and Its Host Kappaphycus alvarezii (Gigartinales, Rhodophyta) Cultivated in the Brazilian Tropical Region. Journal of Applied Phycology, 26, 1953-1961. https://doi.org/10.1007/s10811-014-0348-9
Liu, C., Huang, X. and Liu, J. (2013) Assessment of Introduced Kappaphycus (Solieriaceae, Rhodophyta) Species Relationships in China with Molecular Markers. Acta Oceanologica Sinica, 32, 59-65. https://doi.org/10.1007/s13131-013-0277-5
Dumilag, R.V. and Lluisma, A.O. (2014) Resolving the Phylogenetic Affinities of Kappaphycus inermis within the Genus Kappaphycus (Gigartinales, Solieriaceae) Using Mitochondrial and Plastid Markers. Phytotaxa, 162, 223-231. https://doi.org/10.11646/phytotaxa.162.4.5
Dumilag, R.V., Salvador, R.C. and Hallin, C. (2016) Genotype Introduction Affects Population Composition of Native Philippine Kappaphycus (Gigartinales, Rhodophyta). Conservation Genetics Resources, 8, 439-441. https://doi.org/10.1007/s12686-016-0591-2
Dumilag, R.V., Fredmoore, L., Orosco, A. and Lluisma, O. (2016) Genetic Diversity of Kappaphycus Species (Gigartinales, Rhodophyta) in the Philippines. Systematics and Biodiversity, 14, 441-451. https://doi.org/10.1080/14772000.2016.1157643
Hung, L.D., Hirayama, M., Lya, B.M. and Hori, K. (2015) Biological Activity, cDNA Cloning and Primary Structure of lectin KSA-2 from the Cultivated Red Alga Kappaphycus striatum (Schmitz) Doty ex Silva. Phytochemistry Letters, 14, 99-105. https://doi.org/10.1016/j.phytol.2015.09.012
Li, Y., Liu, N., Wang, X., Tang, X., Zhang, L., Meinita, M.D.N., Wang, G., Yin, H., Jin,Y., Wang, H., Liu, C., Chil, S., Liu, T. and Zhang. J. (2018) Comparative Genomics and Systematics of Betaphycus, Eucheuma, and Kappaphycus (Solieriaceae: Rhodophyta) Based on Mitochondrial Genome. Journal of Applied Phycology, 30, 3435-3443. https://doi.org/10.1007/s10811-018-1450-1
Lim, P.E., Tan, J., Phang, S.M., Nikmatullah, A., Hong, D.D., Sunarpi, H. and Hurtado, A.Q. (2014) Genetic Diversity of Kappaphycus Doty and Eucheuma J. Agardh (Solieriaceae, Rhodophyta) in Southeast Asia. Journal of Applied Phycology, 26, 1253-1272. https://doi.org/10.1007/s10811-013-0197-y
Lim, P-E., Yang, L.E., Tan, L., Maggs, C.A. and Brodie, J. (2017) Advancing the Taxonomy of Economically Important Red Seaweeds (Rhodophyta). European Journal of Phycology, 52, 438-451. https://doi.org/10.1080/09670262.2017.1365174
Syafitri, E., Prayitno, S.B., Ma’ruf, W.F. and Radjasa, O.K. (2017) Genetic Diversity of the Causative Agent of Ice-Ice Disease of the Seaweed Kappaphycus alvarezii from Karimunjawa Island, Indonesia. IOP Conference Series Earth and Environmental Science, 55, Article No. 012044. https://doi.org/10.1088/1755-1315/55/1/012044
Tan, J., Lim, P.E., Phang, S.M., Hong, D.D., Sunarpi, H. and Hurtado, A.Q. (2012) Assessment of Four Molecular Markers as Potential DNA Barcodes for Red Algae Kappaphycus Doty and Eucheuma J. Agardh (Solieriaceae, Rhodophyta). PLoS ONE, 7, e52905. https://doi.org/10.1371/journal.pone.0052905
Tan, J., Lim, P.E. and Phang, S.M. (2013) Phylogenetic Relationship of Kappaphycus Doty and Eucheuma J. Agardh (Solieriaceae, Rhodophyta) in Malaysia. Journal of Applied Phycology, 25, 13-29. https://doi.org/10.1007/s10811-012-9833-1
Tan, J., Lim, P.E., Siew, M.P., Adibi, R., Aluh, N., Sunarpi, H. and Hurtado, A.Q. (2014) Kappaphycus malesianus sp. Nov.: A New Species of Kappaphycus (Gigartinales, Rhodophyta) from Southeast Asia. Journal of Applied Phycology, 26, 1273-1285. https://doi.org/10.1007/s10811-013-0155-8
Thien, V.Y., Wilson, T., Yong, L. and Chin, W.G.J.L. (2016) Morphological and Molecular Studies of Undescribed Kappaphycus Species. International Journal of Marine Science, 6, 1-7. https://doi.org/10.5376/ijms.2016.06.0033
Yong, W.T.L., Chin, W.G.J.L. and Rodrigues, K.F. (2016) Genetic Identification and Mass Propagation of Economically Important Seaweeds. In: Thajuddin, N. and Dhanasekaran, D., Eds., Algae-Organisms for Imminent Biotechnology, IntechOpen, London. https://doi.org/10.5772/62802
Zuccarello, G.C., Critchley, A.T., Smith, J.E., Sieber, V., Lhonneur, G.B. and West, J.A. (2006) Systematics and Genetic Variation in Commercial Kappaphycus and Eucheuma (Solieriaceae, Rhodophyta). Journal of Applied Phycology, 18, 643-651. https://doi.org/10.1007/s10811-006-9066-2
Barros-Barreto, M.B., Marinho, L.C., Reis, R.P., Mata, C.S. and Ferreira, P.C.G. (2013) Kappaphycus alvarezii (Gigartinales, Rhodophyta) Cultivated in Brazil: Is It Only One Species? Journal of Applied Phycology, 25, 1143-1149. https://doi.org/10.1007/s10811-012-9952-8
Halling, C., Wikstrom, S.A., Lillieskold-Sjoo, G., Mork, E., Lundsor, E. and Zuccarello, G.C. (2013) Introduction of Asian Strains and Low Genetic Variation in Farmed Seaweeds: Indications for New Management Practices. Journal of Applied Phycology, 25, 89-95. https://doi.org/10.1007/s10811-012-9842-0
Cortes, J., Jimenez, C.E., Fonseca, A.C. and Alvarado, J.J. (2010) Status and Conservation of Coral Reefs in Costa Rica. Revista Biologia Tropical, 58, 33-50. https://doi.org/10.15517/rbt.v58i1.20022
Fonseca, A.C., Nielsen, V. and Cortes, J. (2007) Monitoring of Seagrasses in Río Perezoso, Cahuita, Costa Rica (CARICOMP Site). Revista de Biologia Tropical, 55, 55-66.
Zuccarello, G., Burger, G., West, J. and King, J.R. (1999) A Mitochondrial Marker for Red Algal Intraspecific Relationships. Molecular Ecology, 8, 1443-1447. https://doi.org/10.1046/j.1365-294x.1999.00710.x
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.
Huelsenbeck, J.P. and Ronquist, F. (2001) MRBAYES: Bayesian Inference of Phylogeny. Bioinformatics, 17, 754-755. https://doi.org/10.1093/bioinformatics/17.8.754
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution, 28, 2731-2739. https://doi.org/10.1093/molbev/msr121
Doty, M.S. (1985) Eucheuma alvarezii sp. nov. (Gigartinales, Rhodophyta) from Malaysia. In: Abbott, I.A. and Norris, J.N., Eds., Taxonomy of Economic Seaweeds with Reference to Some Pacific and Caribbean Species, California Sea Grant College Program, La Jolla, CA, 37-45.
Bernecker, A. (2009) Marine Benthic Algae. In: Wehrtmann, I.S. and Cortés, J., Eds., Marine Biodiversity of Costa Rica, Central America, Springer Science + Business Media B.V., Berlin, Germany, 109-117. https://doi.org/10.1007/978-1-4020-8278-8_5
Abbott, I.A. (1996) Ethnobotany of Seaweeds: Clues to Uses of Seaweeds. Hydrobiologia, 326, 15-20. https://doi.org/10.1007/BF00047782
Bindu, M.S. and Levine, I.A. (2011) The Commercial Red Seaweed Kappaphycus alvarezii—An Overview on Farming and Environment. Journal of Applied Phycology, 23, 789-796. https://doi.org/10.1007/s10811-010-9570-2
Valderrama, D., Cai, J., Hishamunda, N., Ridler, N., Neish, I.C., Hurtado, A.Q., Msuya, F.E., Krisnan, M., Narayanakumar, R., Kronen, M., Robledo, D., Gasca-Leyva, E. and Fraga, J. (2015) The Economics of Kappaphycus Seaweed Cultivation in Developing Countries: A Comparative Analysis of Farming Systems. Aquaculture Economics and Management, 19, 251-277. https://doi.org/10.1080/13657305.2015.1024348
Serpa-Madriga, A., Areces, A.J., Cano, M. and Bustamante, G. (1997) Depredación sobre las carragenofitas comerciales Kappaphycus alvarezii (Doty) Doty y Kappaphycus striatum (Schmitz) Doty (Rhodophyta, Gigartinales) Introducidas en Cuba. Revista de Investigaciones Marinas, 18, 65-69.
Chandrasekaran, S., Nagendran, N.A., Pandiaraja, D., and Krishnankutty, N. (2008) Bioinvasion of Kappaphycus alvarezii on Corals in the Gulf of Mannar, India. Current Science, 94, 1167-1172.
Oliveira, E.C., Bouzon, Z.L., et al. (2011) Kappaphycus alvarezii (Rhodophyta, Areschougiaceae) Cultivated in Subtropical Waters in Southern Brazil. Journal of Applied Phycology, 23, 337-343. https://doi.org/10.1007/s10811-010-9543-5
Paula, E.J., Pereira, R.T.L. and Ohno, M. (1999) Strain Selection in Kappaphycus alvarezii var. alvarezii (Soliericeae, Rhodophyta) Using Tetrasporesprogeny. Journal of Applied Phycology, 11, 111-121. https://doi.org/10.1023/A:1008085614360
Bulboa, C.R. and Paula, E.J. (2005) Introduction of Non-Native Species of Kappaphycus alvarezii (Rhodophyta, Gigartinales) in Subtropical Waters: Comparative Analyses of Growth Rates of Kappaphycus alvarezii and Kappaphycus striatum in Vitro and in the Sea in Southeastern Brazil. Phycological Research, 53, 183-188.
Bulboa, C.R., Paula, E.J. and Chow, F. (2008) Germination and Survival of Tetraspores of Kappaphycus alvarezii (Solieriaceae, Rhodophyta) Introduced in Subtropical Waters of Brazil. Phycological Research, 56, 39-45. https://doi.org/10.1111/j.1440-1835.2008.00483.x
Dumilag, R.V., Gallardo, W.G.M., Garcia, C.P.C., You, Y., Chaves, A.K.G. and Agahan, L. (2017) Phenotypic and mtDNA Variation in Philippine Kappaphycus cottonii (Gigartinales, Rhodophyta). Mitochondrial DNA Part A, 29, 951-963. https://doi.org/10.1080/24701394.2017.1398745
Tan, J., Phaik-Eem, L., Siew-Moi, P. and Hurtado, A.Q. (2017) Biodiversity, Biogeography and Molecular Genetics of the Commercially Important Genera Kappaphycus and Eucheuma. In: Hurtado, A.Q., Critchley, A.T. and Neish, I.C., Eds., Tropical Seaweed Farming Trends, Problems and Opportunities, Developments in Applied Phycology, Springer, Cham, 29-43. https://doi.org/10.1007/978-3-319-63498-2_2
Chopin, T., Buschmann, A.H., Halling, C., Troell, M., Kautsky, N., Neori, A., Kraemer, G.P., Zertuche-González, J.A., Yarish, C. and Neefus, C. (2001) Integrating Seaweeds into Marine Aquaculture Systems: A Key toward Sustainability. Journal of Phycology, 37, 975-986. https://doi.org/10.1046/j.1529-8817.2001.01137.x
Thiel, M. and Gutow, L. (2004) The Ecology of Rafting in the Marine Environment. I. The Floating Substrata. Oceanography and Marine Biology: An Annual Review, 42, 181-263.
Hoek, C. (1987) The Possible Significance of Long-Range Dispersal for the Biogeography of Seaweeds. Helgolander Meeresuntersuchungen, 41, 261-272. https://doi.org/10.1007/BF02366191
Woelkerling, W.J. (1975) On the Epiphytic and Pelagic Chlorophyceae, Phaeophyceae, and Rhodophyceae of the Western Sargasso Sea. Rhodora, 77, 1-40.
Aliani, S. and Molcard, A. (2003) Hitch-Hiking on Floating Marine Debris: Macrobenthic Species in the Western Mediterranean Sea. Hydrobiologia, 503, 59-67. https://doi.org/10.1023/B:HYDR.0000008480.95045.26
Winston, J.E., Gregory, M.R. and Stevens, L.M. (1997) Encrusters, Epibionts, and Other Biota Associated with Pelagic Plastics: A Review of Biogeographical, Environmental, and Conservation Issues. In: Coe, J.M. and Rogers, D.B., Eds., Marine Debris Sources, Impacts, and Solution, Springer, New York, 81-97. https://doi.org/10.1007/978-1-4613-8486-1_9
Boo, G.H., Mansilla, A., Nelson, W., Bellgrove, A. and Boo, S.M. (2014) Genetic Connectivity between Trans-Oceanic Populations of Capreolia implexa (Gelidiales, Rhodophyta) in Cool Temperate Waters of Australasia and Chile. Aquatic Botany, 119, 73-79. https://doi.org/10.1016/j.aquabot.2014.08.004
Fraser, C.I., Zuccarello, G.C., Spencer, H.G., Salvatore. L.C. and García, G.R. (2013) Genetic Affinities between Trans-Oceanic Populations of Non-Buoyant Macroalgae in the High Latitudes of the Southern Hemisphere. PLoS ONE, 8, 69-138. https://doi.org/10.1371/journal.pone.0069138
Guillemin, M.L., Valero, M., Faugeron, S., Nelson, W. and Destombe, C. (2014) Tracing the Trans-Pacific Evolutionary History of a Domesticated Seaweed (Gracilaria chilensis) with Archaeological and Genetic Data. PLoS ONE, 9, 1-17. https://doi.org/10.1371/journal.pone.0114039