Introduction

Over the past four decades, considerable attention was given to the red seaweed, Kappaphycus alvarezii (Doty) Doty (Rhodophyta, Gigartinales, Areschougiaceae), an industrially important carrageenophyte. Reports state that the farming of this seaweed started in southern Mindanao in latter half of the 1960s in the Philippines using the local varieties selected from the wild (Doty 1973, 1978; Parker 1974). The farming has further expanded to other parts of the world, e.g., Indonesia, Fiji, Micronesia, Vietnam, China, South Africa and is well reviewed and documented by Ask et al. (2001). It is reported that the commercial cultivation of K. alvarezii was developed jointly by Marine Colloids Corporation (purchased by FMC Corporation in 1977, now part of BioPolymer; Ask et al. 2001) and by Dr Maxwell Doty of the University of Hawaii Botany Department (Parker 1974). Realizing the potential for commercial extraction of carrageenan, K. alvarezii was introduced to many countries for research, development, and commercialization by researchers and phycocolloid companies. The present paper is an attempt to compile and review the different aspects of global Kappaphycus farming introductions and environmental concerns. Reports of regional farming introductions and/or development after Ask et al. (2001) are cited in this review. As farming operations expanded, growing apprehensions over the impact of the introduction of exotic species to new environments, their interactions with endemic species, and its effect on biodiversity were also reported (Russell 1983; Woo 2000; Smith et al. 2002; Conklin and Smith 2005; Pereira and Verlecar 2005; Anon 2006; Vijayalakshmi 2007; Chandrasekaran et al. 2008). However, after four decades of introductions resulting in Kappaphycus being the most widely cultivated commercial eucheumoid, there are only a few Environmental Impact Assessment (EIA) studies addressing the ecological impacts of K. alvarezii on the environment (Tewari et al. 2006; Tewari 2006), even though recommendations for EIA studies have been suggested by researchers (Woo et al. 1989; Mesia and Mapelamao 2006) and organizations (National Academy of Agricultural Sciences, India 2003).

Global Kappaphycus introductions

Kappaphycus has been introduced to more than twenty countries in the past 35 years for the development of farming efforts. The state of the Kappaphycus introductions was last reviewed by Ask et al. (2001) and subsequently new information relating to its introduction, farming, and ecological interactions has been reported. This review attempts to highlight new Kappaphycus farming initiatives by Asian, African, and Pacific Island nations post Ask et al. (2001), some of which include multitrophic aquaculture (polyculture) strategies. Additionally, efforts include cultivar enhancement programs utilizing molecular techniques to: increase productivity, resist disease, herbivory, and epiphytism (Cheney et al. 1997, 1998; de Paula et al. 2001; Lombardi et al. 2001, 2006; Yarish et al. 2001; Wu et al. 2003; Msuya and Salum 2006; Zuccarello et al. 2006; Hayashi et al. 2007a, b, Hayashi et al. 2008a, b; Hurtado and Biter 2007; Rodrigueza and Montano 2007; Yano et al. 2007). Considering the environmental importance of Kappaphycus, available reports on the ecological interactions of this species with local environments have been covered by Woo (2000); Smith et al. (2002); Oliveira and Paula (2003); Smith (2003); Barrios (2005); Conklin and Smith (2005); Pereira and Verlecar (2005); Vijayalakshmi (2007); Chandrasekaran et al. (2008).

Pacific Island countries

Commercial Pacific Island Kappaphycus cultivation was initiated in the mid 1970s. Pickering and Forbes (2002), Mate et al. (2003), Teitelbaum (2003), Ponia (2005), Namudu and Pickering (2006), Mesia and Mapelamao (2006), and Pickering (2006) highlighted the importance of this species to various Pacific Islands as a means of income generation and coastal community economic development. Pickering and Forbes (2002) pointed out that Kappaphycus ventures in Fiji are regarded as a consolidation and diversification of its aquaculture industry after an earlier false start. The report advocated for legislative amendments strengthening government oversight of aquaculture via the collection of statistics. Additionally, the aquaculture industry association was encouraged to represent private sector interests, contribute to policy development, and adopt specific training requirements. Simultaneously, Teitelbaum (2003) published a manual that assists Pacific Island seaweed farmers in the farming of K. alvarezii. The manual describes different aspects of Kappaphycus farming including: site selection, seedling selection, relevant tools and equipment, methods of rope and raffia knot-tying, hanging of lines, harvesting, construction of drying frames, drying techniques, cleaning, processing and sale of the seaweed. The manual highlights the cause, effect, and solutions to commonly encountered problems, such as territorial grazing by herbivores, epiphytic algae, and ice-ice disease. Mate et al. (2003) reported the significance of the Fijian government workshop on farming K. alvarezii held in 2003. The report includes Fijian government policies for seaweed farming and the role of extension officers, and a brief summary of research findings on Fijian seaweed farming. Suggestions for environmental safeguards, profitability and stock replenishment of Kappaphycus farming in Pacific islands was offered by Ponia (2005). The success of southwest Pacific regional commercial seaweed aquaculture was reported for two species, K. alvarezii in Kiribati, Fiji, and Solomon Islands and Cladosiphon sp. in Tonga (Pickering 2006). The report states that the southwest Pacific region is environmentally ideal for seaweed aquaculture, overcoming the challenges of distance from main markets, vulnerability to world price fluctuations, and socio-economic issues. The report concluded that regional seaweed farming could make a useful contribution to income supplementation and a significant economic boost for isolated outer islands where few alternative income-generating opportunities exist. Cultivation initiative assessments focus on social factors as compared to technical issues in determining the success of rural development projects. A survey has been developed enabling the determination of community suitability for seaweed cultivation; Namudu and Pickering (2006) reported the results of social survey techniques carried out among eight communities within Fiji. Though developed for Fijian case studies, the survey can be applied to other rural Asia/Pacific localities (Namudu and Pickering 2006). Secretariat of the Pacific Community in 2006 gave an overview of Papua New Guinea aquaculture and the governmental interest in piloting Kappaphycus and sea cucumber multitrophic aquaculture. Kappaphycus and black lip pearl multitrophic aquaculture farms participated in a regional initiative aimed at identifying the root causes of coastal area and watershed degradation and to promote sustainable coastal fisheries by creating marine protected areas in the western province of the Solomon Islands (Mesia and Mapelamao 2006). The authors suggest the sustainable development of marine resources can only be achieved through the establishment of resource management plans in partnership with the local communities.

African countries

The farming of Eucheuma and Kappaphycus developed rapidly during the mid-1980s in Tanzania and commercial production began along the east coast of Zanzibar and Pemba Islands in 1989 and expanded rapidly throughout the 1990s (Ask 2001). Lundsor (2001) developed an alternative method for the commercial cultivation of E. denticulatum and K. alvarezii outside Paje on the east coast of Unguja Island, Zanzibar, Tanzania, termed the “broadcast system” (independent of tidal cycles resulting in greater yields) consisting of rectangular pens instead of lines. Mtorela (2003) investigated the potential effects of seagrass coverage on algal productivity by comparing the productivity of E. denticulatum and K. alvarezii in Paje (low seagrass cover) and Uroa (high seagrass cover), Zanzibar. The growth rate of E. denticulatum in Paje was 20–75% lower than in Uroa and was seasonal. Zanzibar E. denticulatum and K. alvarezii exhibited different growth rates as a function of stocking densities and culture duration (Msuya and Salum 2006). However, increasing production of K. alvarezii has been hampered in recent years by disease and predation (Rice and Savoie 2005). The total annual production of carrageenophytes in Tanzania, including Zanzibar, Pemba, and Mafia Islands, as well as the 1,400 km-long mainland coast exceeded 7,000 dried metric tons in 2002, making Tanzania the world’s sixth largest producer with a farm gate value of US$ 1.4 million. Production has been reduced to Pemba and Unguja Islands producing ~5,000 tons of E. denticulatum from each area in 2008 (E. Ask, per comm.). The seaweed farm gate production value represents over 99% of Tanzania’s aquaculture industrial output.

As a means of improving the local village livelihoods, off-bottom rope cultivation of commercial eucheumoids was investigated at three sites on the southern Kenyan coast, (Wakibia et al. 2006). E. denticulatum and K. alvarezii relative growth rates were highest at a mangrove system’s sandy flat (Gazi; 5.6% d−1), lowest in an intertidal reef flat (Kibuyuni; 3.2% d−1) and intermediate in a lagoon (Mkwiro; 4.8% d−1). Results suggest that commercial cultivation of eucheumoids in Kenya is feasible.

Recommendations to improve African K. alvarezii cultivation include: adoption of the Indonesian-style deep water, logline cultivation method with predator-excluding perimeter netting, submerging seed stock to deeper saline waters during the rainy season, and to capture and culture rabbit fish Siganus spp. as an adjunct to seaweed farming serving a dual function of removing key seaweed predators from cultivation sites and providing an alternative cash crop to seaweeds (Rice and Savoie 2005). Bryceson (2001) reported several thousand farmers, mostly women, engaged in the production and the sale of seaweeds, providing much needed income. Environmental effects appear minimal; in fact some herbivorous fishes actually gain an extra source of food when they graze on the farmed seaweed. Conflicts with other users of the coast appear manageable when zoning is applied to fishing boats and tourist activities. A significant challenge experienced is the extremely low price paid to farmers compared to the very high prices fetched for phycocolloid products by the pharmaceutical and food industries—the enormous profits made by transnational corporations raise important ethical questions in this era of globalization (Bryceson 2001).

Asian countries

Kappaphycus alvarezii constitutes 80% of the Philippine seaweed export, which is sold as both fresh and dried forms; although dried seaweed has a greater demand, fresh seaweed are highly valued in restaurants (Hurtado 2003). The Philippines has the largest carrageenan refinery in Asia supporting the introduction to other Asian countries, e.g. Indonesia, Malaysia, Japan, China, India, and Vietnam. Farming introductions continue to new localities. Indian K. alvarezii mariculture, located in Okha on the west coast, was initiated in the mid 1990s for kappa carrageenan production (Mairh et al. 1995). Subsequent Kappaphycus commercial cultivation was established in Mandapam, southeast coast of India, during 1995–1997. Initially, bag and net cultivation were practiced; later fishermen and women of Self Help Groups introduced the raft method for commercial cultivation. They adopted the Kudumpam model cultivation system with the cooperation of industries and nationalized banks (Eswaran and Jha 2006). Eswaran et al. (2002) evaluated the field and laboratory Mandapam K. alvarezii biomass yields and growth rates were much higher (nearly 3% per day) in December through February. The report indicated the potential for further large-scale cultivation efforts in Mandapam region. Highlighting the far-reaching societal impacts of this development, His Excellency Dr. A P J Abdul Kalam, then the President of India, encouraged the Kappaphycus seaweed cultivation for the livelihood support as a mission mode project of the coastal poor (Technology Empowers the Nation—address by the Honorable president of India at New Delhi on 11 May 2006, Technology Day). Subsequently, Kappaphycus experimental and field cultivation was initiated in several Indian coastal areas and results indicate the possibility of large-scale Kappaphycus commercial cultivation in Indian waters as a means of income generation (Sakthivel 1999; Subba Rao et al. 2004, 2008; Abhiram 2006; Bindu 2006, 2007, 2009; Bindu and Kumaraswamy Achary 2006; Reeta 2006; Sahoo 2006).

Dung and Nhan (2001) report the successful experimental cultivation of K. alvarezii in Haiquan Lagoon and Cat Ba Bay, Vietnam utilizing floating rafts and hanging-on plastic lines. The growth rates realized from the open sea are higher than those achieved in sheltered bays and ranged from 5.18–9.82% d–1 and 5.25–7.90% d–1, respectively. Kappaphycus alvarezii is considered a highly efficient cultivar generating jobs and supplemental income for the poor in Vietnam coastal areas (Nang 2005). Additionally, significant contributions to ecological balance and the bioremediation of coastal area nutrient enrichment are realized through the use of cultivation frames set on the bottom of shallow areas during the cool season with rapid water circulation, high wind, and waves, hot and sunny season with limited water circulation, minimal wind, and wave energies. Reductions in the concentration of ammonia, nitrite, nitrate, phosphate, and phosphorus content in the water ranged from 10–80% (Nang 2005). Quality of Vietnamese cultivated Eucheuma is high, meeting the required standards for sustainable commercial Eucheuma cultivation, particularly in the southern Vietnamese waters. Yarish et al. (2001) reported a prototype model that may illustrate the importance of integrating seaweed cultivation activities in the maintenance and health of coastal embayments, a model being explored for Xincun Bay, southeastern Hainan Province, China. The annual nitrogen and phosphorus removal capacity of Kappaphycus in Xincun Bay are 53.8 and 3.7 t, respectively, during the 1999–2000 growing season. Reports are also available on the cultivation of Eucheuma and Kappaphycus in Sabah, Malaysia where two factories for production of semi-refined carrageenan have been established and the inventory of Malaysian seaweeds continues (Phang 2006).

American countries

There are few reports on K. alvarezii introduction and commercial cultivation from the western hemisphere and most efforts concentrate on strain improvement and genetic manipulation through the use of modern biotechnological techniques (Ask and Azanza 2002). However, bioinvasive reports from Hawaii (Woo et al. 1989; Rodgers and Cox 1999; Smith 2003; Conklin and Smith 2005) and Venezuela (Barrios 2005) have focused on the ecological effects of eucheumoid introductions on local communities.

de Paula et al. (2002) reported on K. alvarezii commercial cultivation as technically feasible practice for Ubatuba Bay, Sao Paulo State, Brazil using floating raft cultivation technologies. Laboratory-grown branches of K. alvarezii, with mean weights ranging from 2.97 to 4.25 g, were successfully developed to produce thalli for monthly out-planting in Ubatuba Bay (see also Hiyashi et al. 2007a, b). Branch transplantation produced in unialgal cultures, avoids the risk of unwanted species introduction (de Paula et al. 2002). Ask et al. (2001) recommended research priorities including: replacement of “tie–tie system”, use of spores/sporelings in cultivation, multifactorial experiments considering nutrients, salinity, light, etc. to meet seasonality challenges, mitigation of pests, herbivores and diseases, strain improvement and transgenic development, and increasing the quality of extract through superior post-harvest handling methods. Recommendations for exploring, publicizing and utilizing practical and effective quarantine procedures for commercial eucheumoids introductions are also discussed. Three color strains of K. alvarezii were cultivated in Dzilam, Yucatan, Mexico using the fixed off-bottom monoline cultivation method to determine the technical viability of commercially producing this seaweed in the Yucatan peninsula’s tropical waters (Munoz et al. 2004). The study illustrated that K. alvarezii can be grown during the dry and part of the wet season, and concluded that seaweed farming could be attempted as an alternative activity in the area. Bulboa and de Paula (2005) compared the growth rates of K. alvarezii and K. striatum, in vitro under different light and temperature regimes in the sea off the southeastern coast of Ubatuba, São Paulo, Brazil. Kappaphycus alvarezii is physiologically distinct and grows faster than K. striatum. Additionally, as the risk of uncontrolled Kappaphycus propagation is of great concern, K. striatum field production was discontinued after monitoring efforts revealed the production of viable tetraspores. K. alvarezii was determined to be the more profitable and ecologically safer species for local cultivation programs.

Polyculture and multitrophic aquaculture

The solution to conflicting demands between development of intensive mariculture and protection of a marine environment may rely on multitrophic aquaculture (polyculture) interaction between primary producers and consumers (Wu et al. 2003). A number of reports point out the potential of K. alvarezii as a candidate species for viable multitrophic aquaculture (polyculture) practices (Lombardi et al. 2006; Namudu and Pickering 2006). Wu et al. (2003) discuss the effects of premium quality pearl yields from polycultured oysters cultivated and raised with K. alvarezii as compared to monocultured oysters. Mesia and Mapelamao (2006) report on Kappaphycus and black lip pearl farms in the western province of the Solomon Islands. Similarly, floating cages seeded with Pacific white marine shrimp, Litopenaeus vannamei, and K. alvarezii in open marine waters were deployed by the Aquaculture Research Center, State Fishery Institute in Ubatuba, Sao Paulo, Brazil (Lombardi et al. 2001) and the results supported using floating polyculture cages as a viable alternative. Algae:shrimp polyculture provides shelter, shade, and a bed for additional organisms, which could improve natural food, supply for the shrimp. A recent report (Lombardi et al. 2006) indicated Pacific white shrimp Litopenaeus vannamei production rates as high as 3.23 kg m2 y-1 and K. alvarezii production rates of 23.70 kg m2 y-1 utilizing experimental grow-out cages with polyester/PVC mesh fixed in PVC floating frames in Brazilian cultivation trials.

Molecular genetics and manipulation

Attempts to produce new strains of commercial eucheumoids through somatic hybridization and mutagenesis for field cultivation with improved growth rates and biochemical characteristics were reported by Cheney et al. (1997, 1998). As a result of advancements in protoplast fusion techniques and cell–cell fusion, new strains of E. denticulatum and K. alvarezii, demonstrated significantly faster growth rates (up to 14% per day) in extensive field trials. Using cell–cell fusion technique, a hybrid between E. denticulatum and K. alvarezii was produced which exhibits a novel carrageenan composition (Cheney et al. 1998). The report also describes several new techniques developed at the Seaweed Biotechnology Laboratory of Northeastern University, which have made the production of genetically improved cultivars of red seaweeds not only possible but also practical. K. alvarezii strain enhancement utilizing tissue culture and micropropagation was developed for the optimization of in vitro culture (Hayashi et al. 2008a, b). A series of cultivars and life history forms were tested (brown, green, red tetrasporophytes, brown female gametophyte, and germinated tetraspores). The germinated tetraspore samples exhibited the highest percentage of callus forming explants and regeneration potential in Von Stosch’s 50% solution, indicating a high micropropagation potential. Indole-3-acetic acid and benzylaminopurine stimulated the regeneration process and colchicine produced high regeneration potential explants.

Kappaphycus and Eucheuma (Areschougiaceae) systematics and taxonomy is complicated by their morphological plasticity, lack of adequate specific identification characters, and commercial names of convenience. Genetic variation and taxonomic relations of commercial, wild, and herbarium samples were determined utilizing a variety of molecular tools (Giuseppe et al. 2006). Mitochondrial cox2-3 and plastidal RuBisCo spacers were sequenced and clear genetic distinctions between K. alvarezii (“cottonii”) and K. striatum (“sacol”) were revealed. Hawaiian and African K. alvarezii were also found to be genetically distinct. Giuseppe et al. (2006) reported all currently cultivated K. alvarezii have similar mitochondrial haplotype. African samples of Eucheuma denticulatum (“spinosum”) appear to be genetically distinct. Data suggest that currently cultivated E. denticulatum may have been “domesticated” several times, whereas cultivated K. alvarezii have not. Kimberly et al. (2009) used three molecular markers (partial nuclear 28S rRNA, partial plastid 23S rRNA, and mitochondrial 5′ COI), and followed a DNA barcoding-like approach to identify Hawaiian Eucheuma and Kappaphycus samples. Neighbor-joining analyses were congruent in their separation of Eucheuma and Kappaphycus, and the resulting clusters were consistent with those revealed for global comparisons with the mitochondrial cox2-3 spacer and GenBank data.

Ecological interactions and bioinvasive reports

The global introduction of K. alvarezii to new ecosystems has created concerns over its non-endemic nature, affect on biodiversity, and alteration of local ecological community health and balance. The introduction of commercial invasive cultivars is gathering attention and is being considered as one of the potential challenges to algal cultivation as an economic development engine for coastal fishing communities. The ecological interactions of this species were first reported from the Hawaiian Islands (Woo et al. 1989) and subsequent reports of Rodgers and Cox (1999), Smith (2003), Barrios (2005), and Chandrasekaran et al. (2008) branded it as an ‘invasive species’. Apparently, there are practically no reports from countries where it has been introduced for cultivation purposes (Ask et al. 2001) and the cultivation practices are still going on providing income for thousands of families.

Woo et al. (1989) determined the role of herbivory (grazing) on K. striatum abundance and concluded grazing intensity is low and unable to affect algal biomass. Conversely, recent conversations with Indian Kappaphycus fishermen indicate that approximately 30% of the algal biomass is lost to herbivory. Woo et al. (1989) called for additional studies to assess the ability of the alga to reproduce vegetatively, as well as a qualitative assessment of the possible impact of algal overgrowth on live coral, to estimate further spread, habitat alteration, and ecological impact. Spread of K. alvarezii, K. striatum, and Gracilaria salicornia was measured on barrier reef, patch reef, and fringing reef in Kaneohe Bay, Oahu, Hawaii by Rodgers and Cox (1999). The report assessed the extent of these algae in the bay to determine their rate of spread with a manta tow board survey. The abundance of these species was determined by detailed reef transects in the central bay and reported the establishment of these species. Smith (2003) presented some of the first quantified evidence of significant negative impacts of Non Indigenous Marine Algae in tropical waters. Interactions between K. alvarezii and coral abundance were examined using photoquadrats and results indicate that the invader is causing coral death as a result of overgrowth and shading. Conklin and Smith (2005) conducted a study to quantify Kappaphycus spp. abundance both spatially and temporally, and to investigate control options including manual removal and the use of biocontrol agents in Kaneohe Bay, Hawaii, USA and recommended that rapid management action should be taken to prevent further damage and spread to other Hawaiian coral reefs.

Barrios (2005) reported K. alvarezii vegetative tissues were borne as a crust of small cells radially arranged with a large-cell central medulla with rhizoidal filaments. The lack of K. alvarezii limiting structures preventing thalli dispersal when farmed in open waters constitutes a risk of algal dissemination into the surrounding environment. High growth rates, asexual reproduction capacity via fragmentation, resistance to grazing and colonization by fouling organisms make Kappaphycus a potential invader to new environments. Chandrasekaran et al. (2008) reported the bioinvasion of K. alvarezii onto branching corals (Acropora sp.) in Kurusadai Island, the Gulf of Mannar Marine Biosphere Reserve, South India. The report quantifies the invasion and establishment of K. alvarezii on live and dead corals, corral rubble and pavements, resulting in significant shadowing and smothering of the coral colonies.

Environmental impact assessment studies

Although concerns of the transfer and introduction of K. alvarezii are increasing, Environmental Impact Assessment studies to address the issue are meager. EIA carried out on Indian Kappaphycus commercial cultivation is discussed with reference to a global scenario by Tewari et al. (2006a, b). Controversial issues include uncontrolled algal growth, invasion via spores and fragmentation, coral damage, and nutrient depletion. The Indian environmental impact assessment study has shown that Kappaphycus commercial cultivation has many positive impacts and a few negative environmental impacts. Planned scientific farming, including regular monitoring of the environment, could mitigate negative impacts. Impacts of Kappaphycus farming will differ from environment to environment; therefore, the negative impact experienced by one environment may not necessarily be experienced in another. Commercial cultivation of Indian K. alvarezii is not considered harmful to the environment. Alternatively, Pereira and Verlecar (2005) reported K. alvarezii on the verge of becoming invasive in southern India and its spread in the Gulf of Mannar. National Academy of Agricultural Sciences, India seaweed cultivation and utilization policy paper (2003) developed marine macroaglal commercial cultivation and processing recommendations and declared it as a national priority. Indian research and development priorities include: creation of baseline seaweed taxonomic database; formation of germplasm and herbaria library; classical and molecular strain improvement programs; diversification of algal products; and ecological and EIA studies pertaining to the introduction of exotic species.

In the light of available literature and verified reports, the present review concludes that the introduction of Kappaphycus cultivation to new localities will continue for the foreseeable future in tropical countries due to the high production values realized, coastal villages searching for alternative livelihoods, and the increased global industrial demand for carrageenan.