Skip to main content
SpringerLink
Log in

Ecological risk assessment of the introduction of exotic carrageenophytes in the tropical Western Atlantic

  • IV Latin American Congress of Algae Biotechnology (CLABA) and IV Redealgas Workshop
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The potential risks of cultivating carrageenophyte genera for commercial purposes in the circumtropical belt are debated. However, species introductions of two such genera, Kappaphycus Doty and Eucheuma J. Agardh, have been reported in 30 different locations in this region over the last 30 years. On several occasions, these introductions did not adequately evaluate potential environmental risks or were conducted without approval from local regulatory bodies. In the present paper, a working protocol is proposed for the quarantine and assessment of the possible effects of the introduction of Kappaphycus alvarezii and Kappaphycus striatus to shallow marine ecosystems of the tropical Western Atlantic. This protocol is based on field data following from the introduction of eucheumoids onto the Cuban shelf in the early 1990s. It was demonstrated that the propagation of either carrageenophyte in oligotrophic waters of the Cuban Archipelago did not pose a potential risk to the region’s biodiversity due to the synergic combination of high herbivory and low rates of growth. Physical features of the substrate and depth were the most important regulators of grazing. These environmental conditions restrict potential cultivation sites in the Cuban Archipelago to a few small regions where nutrient pulses are well established. In these areas, when the canopy of cultivated carrageenophytes is sufficiently high, a significant effect on benthic communities is observed. In consideration of the need to protect places with high intrinsic value, this fact should be considered during site selection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alcolado PM, Herrera A (1987) Efectos de la contaminación sobre las comunidades de esponjas en el litoral de La Habana, Cuba. Rep Investig (Cuba), 68: 17 p

  • Araújo PG, Miranda GEC, Barros-Barreto M, Fujii MT (2013) Molecular identification of the exotic lineage of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) cultivated in the tropical region of Brazil. Phytotaxa 109:17–26

    Article  Google Scholar 

  • Areces AJ (1995) Cultivo comercial de carragenófitas del género Kappaphycus Doty. In: Alveal K, Ferrario ME, Oliveira EC, Sar E (eds) Manual de métodos ficológicos. Universidad de Concepción, Concepción, pp 529–550

    Google Scholar 

  • Areces, AJ [Ed] (2002) Hábitats bentónicos presentes en los fondos marinos someros de Cuba. In Ecorregionalización y clasificación de hábitats marinos en la plataforma Cubana. Resultados. Workshop sponsored by Instituto de Oceanologia, WWF-Canada, Environmental Defense-USA and Centro Nacional de Áreas Protegidas (Cuba), Havana, May 20–23, 2002, Mimeo. 83 pp

  • Areces AJ, Céspedes N (1992) Potencialidad productiva de algunas carragenófitas del Indopacífico en aguas del Caribe. Bol Red Acuic (Colombia) 6:13–16

    Google Scholar 

  • Areces AJ, Martínez JC (1992) Dinámica, estacionalidad y efectos de la epifauna colonizadora sobre el cultivo de la agarófita Bryothamnion triquetrum (Gmelin) Howe. Avicennia (Cuba) 0:43–59

    Google Scholar 

  • Areces AJ, del Valle R, Ibarzábal D, Pol J, Hernández L (1992) Características generales de la fauna asociada a cuatro especies de macroalgas del mesolitoral rocoso cubano. Cienc Biol (Cuba) 25:117–131

    Google Scholar 

  • Ask E, Batisbaga A, Zertuche-González JA, de San M (2003) Three decades of Kappaphycus alvarezii (Rhodophyta) introduction to non-endemic locations. In: Chapman AR, Anderson ORJ, Vreeland VJ, Davison IR (eds) Proceeding of 17th International Seaweed Symposium, pp 49–57

  • Bagla P (2008) Seaweed invader elicits angst in India. Science 320:1271

    Article  PubMed  CAS  Google Scholar 

  • Barbaroux O, Perez R, Dreno JP (1984) L'algue rouge Eucheumaspinosum possibilities d'exploitation et de culture aux Antilles. Sci Pêche 348:9

  • Barrios JE (2005) Dispersión del alga exótica Kappaphycus alvarezii (Gigartinales: Rhodophyta) en la región Nororiental de Venezuela. Bol Inst Oceanogr Venez Univ Oriente 44:29–34

    Google Scholar 

  • Batista de Vega G, Shields C, Yee R, González J (2008) Seaweeds farms on the Caribbean coast of Panamá. En: Romero RR, García-Jiménez P, Batista de Vega G Cultivo Ecosostenible de Algas Marinas (Seaweed ecofriendly aquaculture, SEApanamá). Manuales de Laboratorio, Memoria PCI C 5054/06, Universidad Las Palmas, Gran Canaria y Universidad Panamá, pp 250–254

  • Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38

    Article  PubMed  CAS  Google Scholar 

  • Brown MB, Forsythe AB (1974) Robust tests for equality of variances. J Am Stat Assoc 69:364–367

    Article  Google Scholar 

  • Bulboa CRB, Paula EJ (2005) Introduction of nonnative species of Kappaphycus (Rhodophyta, Gigartinales) in subtropical waters: comparative analysis of growth rates of Kappaphycus alvarezii and Kappaphycus striatum in vitro and in the sea in south-eastern Brazil. Phycol Res 53:183–188

    Article  Google Scholar 

  • Bulboa CRB, Paula EJ, Chow F (2008) Germination and survival of tetraspores of Kappaphycus alvarezii var. alvarezii (Solieriaceae, Rhodophyta) introduced in subtropical waters of Brazil. Phycol Res 56:39–45

    Article  Google Scholar 

  • Castelar B, Perpetuo-Reis R, Bastos M (2009) Contribuição ao protocolo de monitoramento ambiental da maricultura de Kappaphycus alvarezii (Doty) Doty ex P.C. Silva (Areschougiaceae-Rhodophyta) na baía de Sepetiba, RJ, Brasil. Acta Bot Bras 23:613–617

    Article  Google Scholar 

  • Chandrasekaran S, ArunNagendran N, Pandiaraja D, Krishnankutty N, Kamalakannan B (2008) Bioinvasion of Kappaphycus alvarezii on corals in the Gulf of Mannar, India. Curr Sci 94:1167–1172

    Google Scholar 

  • del Valle R, Espinosa J, del Castillo N (1992) Efectos de la contaminación sobre las comunidades de moluscos del litoral rocoso al W de la Bahía de La Habana. Rep Investig (Cuba) 5:8

    Google Scholar 

  • García-Vásquez A, Pardo-Castro PV (2002) Observaciones de la adaptación de Kappaphycus alvarezii (Doty, 1988) y las variaciones de su tasa de crecimiento en el Acuario Mundo Marino. Seminario de Investigación. Facultad de Biología Marina, Universidad de Bogotá Jorge Tadeo Lozano

  • Gómez-Quintero MJ, Areces AJ (1976) Algunas consideraciones hidroquímicas sobre el río Quibú y áreas litorales limítrofes. Inédito, Archivo CientíficoInstituto de Oceanología, Cuba

  • Hay ME (1981) Spatial patterns of grazing intensity on a Caribbean barrier reef: herbivory and algal distribution. Aquat Bot 11:97–109

    Article  Google Scholar 

  • Herrera A, Martínez N (1987) Efectos de la contaminación sobre las comunidades de corales escleractíneos al oeste de la bahía de La Habana. Rep Investig (Cuba) 62:29

    Google Scholar 

  • Herrera-Moreno A, Alcolado PM (1983) Efectos de la contaminación sobre las comunidades de gorgonáceos al Oeste de la Bahía de La Habana. Cienc Biol (Cuba) 10:69–85

    Google Scholar 

  • Kamalakanna B, Jeevamani JJJ, Nagendran NA, Pandiaraja DN, KrishnanKutty N, Chandrasekaran S (2010) Turbinaria sp. as victims to Kappaphycus alvarezii in reefs of Gulf of Mannar, India. Coral Reefs 29:1077

  • Lang JC (2003) Status of coral reefs in the Western Atlantic: results of initial surveys, Atlantic and Gulf Rapid Reef Assessment (AGRRA) program. Atoll Res Bull 496:1–630

    Article  Google Scholar 

  • Lemus Castro AJ (1999) Macroalgas exóticas y su presencia em mares venezolanos. Acta Cient Venez 50:11–14

    Google Scholar 

  • Lluis M (1974) Estudios hidrológicos de un área semicerrada y de las aguas adyacentes en la costa Norte de la provincia de La Habana. Serie Oceanol 19:5–45

    Google Scholar 

  • Luckhurst BE, Luckhurst K (1978) Analysis of the influence of substrate variables on coral reef fish communities. Mar Biol 49:317–323

  • Lugioyo M, Rodríguez F (1988) Aislamiento e identificación de bacterias del sedimento de la costa Norte de C. de La Habana, Cuba. Rep Investig (Cuba) 4:9

    Google Scholar 

  • Mack R, Simberloff D, Lonsdale M, Evans H, Clout M, Bazzaz F (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • MARINALG International (2012) A protocol for introducing non-indigenous seaweeds, Kappaphycus and Eucheuma, into a new farming area with minimum intrusive environmental impact. http://www.marinalg.org/wp-content/uploads/2012/09/Protocol-for-introducing-non-indigeous-seaweed.pdf. Accessed 12 July 2012

  • Mooney HA, Hobbs RJ (2000) Invasive species in a changing world. Island Press, Washington, D.C

    Google Scholar 

  • Muñoz J, Freile-Pelegrín Y, Robledo D (2004) Mariculture of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) color strains in tropical waters of Yucatán, México. Aquaculture 239:161–177

    Article  Google Scholar 

  • Oliveira EC (2005) Considerações sobre o impacto ambiental do cultivo da alga Kappaphycus alvarezii na costa sudeste do Brasil. Bol Ficol Ano 24

  • Osman R, Shirley T (2007) Proceedings and final report of the Gulf of Mexico and Caribbean marine invasive species workshop. Harte Research Institute for Gulf of Mexico Studies. Texas A&M University–Corpus Christi, Corpus Christi

    Google Scholar 

  • Paula EJ, Pereira RTL, Ostini S (1998) Introdução de espécies exóticas de Eucheuma e Kappaphycus (Gigartinales, Rhodophyta) para fins de maricultura no litoral brasileiro: abordagem teórica e experimental. In: Paula EJ, Cordeiro-Marino M, Pupo Santos D, Fujii M, Plastino EM, Yokoya N (eds) IV Congresso Latino Americano de Ficologia, II Reunião Ibero-Americana de Ficologia e VII Reunião Brasileira de Ficologia. Sociedade Brasileira de Ficologia, São Paulo, pp 340–357

    Google Scholar 

  • Paula EJ, Pereira RTL, Ohno M (2002) Growth rate of the carragenophyte Kappaphycus alvarezii (Rhodophyta, Gigartinales) introduced in subtropical waters of São Paulo State, Brazil. Phycol Res 50:1–9

    Article  Google Scholar 

  • Perpetuo Reis R, Bastos M, Geromel Góes H (2007) Cultivo do Kappaphycus alvarezii no litoral do Rio de Janeiro: subsídios ao monitoramento da produção em escala industrial. Panor Aquic 9:42–47

    Google Scholar 

  • Pickering TD, Skelton P, Sulu RJ (2007) Intentional introductions of commercially harvested alien seaweeds. Bot Mar 50:338–350

    Article  Google Scholar 

  • Pirani Ghilardi N, Hayashi L, Berchez F, Sumie Yokoya N, de Oliveira EC (2008) An alternative environmental monitoring approach to nonindigenous species introduced for maricultural purposes: the case of Kappaphycus alvarezii (Rhodophyta, Solieriacea) cultivation in Brazil. Oecol Bras 12:270–274

    Google Scholar 

  • Rincones RE, Gallo HM (2004) Programa de Capacitación en el cultivo de algas marinas “Jimoula” a las comunidades del Cabo de la Vela, Península de La Guajira. Proyecto IBAvH/FAO TCP/COL/2901Fortalecimiento para el Desarrollo de Empresas Rurales a partir de Productos de la Biodiversidad enel Cabo de la Vela, Departamento de La Guajira. Bogotá D.C. Informe Final

  • Rincones RE, Rubio JN (1999) Introduction and commercial cultivation of the red alga Eucheuma in Venezuela for the production of phycocolloids. World Aquac Mag 30:57–61

    Google Scholar 

  • Risk MJ (1972) Fish diversity on a coral reef in the Virgin Islands. Atoll Res Bull 153:1–6

    Article  Google Scholar 

  • Rodgers K, Cox EF (1999) The distributions of the introduced rhodophytes Kappaphycus alvarezii, Kappaphycus striatum and Gracilaria salicornia in relation to various physical and biological factors in Kane’ohe Bay, O’ahu, Hawai’i. Pac Sci 53:232–241

    Google Scholar 

  • Russell DJ (1983) Ecology of the red imported seaweed Kappaphycus striatum on Coconut Island, Oahu, Hawai’i. Pac Sci 37:87–107

    Google Scholar 

  • Serpa Madrigal A, Areces AJ (1995) Selección del refugio por juveniles de la langosta espinosa (Panulirus argus Latreille): influencia de la naturaleza, morfología y tamaño del sustrato algal. Rev Cuba Investig Pesq 19:27–31

    Google Scholar 

  • Serpa-Madrigal A, Areces AJ (1998) Influencia de algunos factores fitotécnicos en la actividad de los herbívoros sobre el cultivo de Kappaphycus Doty (Gigartinales: Rhodophyta) en el ecosistema arrecifal caribeño. Bol Inst Oceanogr Venez Univ Oriente 37:63–68

  • Serpa-Madrigal A, Areces AJ, Cano M, Bustamante G (1997) Depredación sobre las carragenófitas comerciales Kappaphycus alvarezii y K. striatum. Rev Inv Mar (Cuba) 18:65–69

    Google Scholar 

  • Siegel S (1975) Estadística no paramétrica. Ediciones Trillas, México, 346 p

    Google Scholar 

  • Simberloff D (2000) Nonindigenous species: a global threat to biodiversity and stability. In: Raven P, Williams T (eds) Nature and Human Society: the Quest for a Sustainable World. National Academy Press, Washington, DC, pp 325–334

    Google Scholar 

  • Sulu R, Kumar L, Hay C, Pickering T (2004) Kappaphycus seaweed in the Pacific: review of introductions and field testing proposed quarantine protocols. Secretariat of the Pacific Community, Noumea

    Google Scholar 

  • Trespoey A, Daessle J, Batista G, Bleicher-Lhonneur G, Critchley AT (2008) Preliminary analysis of the impact of cultivation conditions on carrageenan yield and quality from a newly established farming area in Panama. In: Romero RR, García-Jiménez P, Batista de Vega G (eds) Cultivo Ecosostenible de Algas Marinas (Seaweed Ecofriendly Aquaculture, SEA Panamá). Manuales de Laboratorio, Memoria PCI C 5054/06, Universidad Las Palmas, Gran Canaria y Universidad de Panamá, pp 267–281

  • Trowbridge CD (2006) A global proliferation of non-native marine and brackish macroalgae. In: Critchley AT, Ohno M, Largo D (eds) Seaweed resources. Expert Centre for Taxonomic Identification (ETI), University of Amsterdam (CD ROM series)

  • Valdés-Muñoz E, Garrido OH (1987) Distribución de los peces en un arrecife costero del litoral habanero. Rep Investig (Cuba) 61:16

    Google Scholar 

  • Verlecar XN, Pereira N (2006) Is Kappaphycus alvarezii heading marine bioinvasion? Curr Sci 90:619–620

    Google Scholar 

  • Vinogradova LA (1974) Ciclo anual del desarrollo de la micro y macroflora en un área semicerrada y en aguas adyacentes de la plataforma Cubana. Serie Oceanol (Cuba) 19:47–60

    Google Scholar 

  • Wallentinus I (2002) Introduced marine algae and vascular plants in European aquatic environments. In: Leppakoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts, and management. Kluwer, Amsterdam, pp 27–52

    Chapter  Google Scholar 

  • Woo M (2000) Ecological impacts and interactions of the introduced red alga Kappaphycus striatum in Kane’ohe Bay, O’ahu. Master’s thesis, University of Hawai’i

  • Woo M, Smith C, Smith W (2000) Ecological interactions and impacts of invasive Kappaphycus striatum in Kane’ohe Bay, a tropical reef. In: Pedersen J (ed) Marine bioinvasions. Massachusetts Institute of Technology, Sea Grant College Program, pp 186–192

Download references

Acknowledgments

This research was conducted as part of research projects financed by the Institute of Marine Science and the Center of Fishing Research from the Ministry of Science, Technology and the Environment and the Ministry of Fishing of Cuba. This research was a multidisciplinary endeavor involving numerous researchers, technicians and students. We thank Michael Wynne for his suggestions. Thanks are particularly due to Mercedes Cano, Alejandro Serpa, Olga Valdés, Rafael Rubio, Nancy Céspedes and Francisco González Agramonte

Author information

Authors and Affiliations

  1. Laboratório de Macroalgas, Departamento de Oceanografia, Universidade Federal de Pernambuco, Av. Professor Moraes Rego, 1235 Cidade Universitária, Recife, 50670-901, PE, Brazil

    Arsenio José Areces Mallea & Juliane Bernardi

  2. Centro de Energia Nuclear na Agricultura (CENA), Universidade de São Paulo, Piracicaba, 13400-970, São Paulo, Brazil

    Felipe Carlos Alvarez Villanueva

  3. Departamento de Ingeniería Agricola, Universidad de Costa Rica, San Pedro, Montes de Oca, 2060, Costa Rica

    Ruben Cabrera

Authors
  1. Arsenio José Areces Mallea
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felipe Carlos Alvarez Villanueva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juliane Bernardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ruben Cabrera
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Felipe Carlos Alvarez Villanueva.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mallea, A.J.A., Villanueva, F.C.A., Bernardi, J. et al. Ecological risk assessment of the introduction of exotic carrageenophytes in the tropical Western Atlantic. J Appl Phycol 26, 2055–2063 (2014). https://doi.org/10.1007/s10811-014-0385-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-014-0385-4

Keywords

Search

Navigation