Introduction

Commercial carrageenophyte farming in the Philippines has grown significantly for the past four decades (Doty 1973; 1978; Parker 1974; Dakay 2010). It has satisfied the global demand for the carrageenan industry that was left void in the 1960s by the decline of the natural stocks of Chondrus crispus (also known as Irish moss) from temperate coastal waters, such as in Canada, Ireland, and Portugal (Hishamunda and Valderrama, 2012).

A number of papers have been written regarding the state of Philippine red seaweed farming and its importance (Trono 1992; Guerrero 2001; Hurtado and Cheney 2003; Bindu and Levine 2011), including suggestions for its sustainability (Ask 2003; Ask and Azanza 2002; Hayashi et al. 2010).

Since then, these carrageenophytes that are endemic to the Philippines, particularly Kappaphycus alvarezii (Doty) Doty ex P. Silva (“cottonii” of commerce) and Eucheuma denticulatum (Burman) Collins and Harvey (“spinosum” of commerce), have been introduced to more than 20 countries (Ask et al. 2003; Bindu and Levine 2011). K. alvarezii has been successfully introduced even in the subtropical waters of southern Brazil (Hayashi et al. 2010). The state of farming of non-endemic cultivars has been reviewed by Ask et al. (2003) and subsequently, more environmental concerns are being presented regarding this practice (Bindu and Levine 2011).

Despite the global growth in the cultivation of carrageenophytes in many maritime countries, the Philippines is still one of the top-ranking carrageenophyte producers (Fig. 1). It has experienced a decline in production in the past 4 years starting in 2008. However, it is still the leading producer of carrageenan globally (Fig. 2). Hence, this paper aims to assess the current carrageenophyte farming industry and put together the factors that will help bring back the industry to its usual high productivity.

Fig. 1
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Top producers of carrageenophytes (“cottonii” and “spinosum” combined), 2002–2009 (Dakay 2010)

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Fig. 2
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World producers of carrageenan (t), 2009 (Dakay 2010)

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History and development of carrageenophyte farming

Prior to the development of the red seaweed farming industry in the Philippines, the only sources of carrageenan were the red algae, Chondrus and Gigartina species from the cold waters of the Atlantic coasts of Canada and Europe. However, in the 1960s, wild stock of C. crispus declined in Canada (Chopin 1998), leading to an active search for alternative sources of carrageenophytes. Finally, wild stocks of red seaweeds belonging to K. alvarezii and E. denticulatum were identified in the Philippines by MS Doty (Doty 1973; 1978; Parker 1974). Initial culture trials were conducted in Siasi, Sulu in the mid-1960s. It is reported that the commercial cultivation of K. alvarezii was developed jointly by Marine Colloids Corporation (purchased in 1977 by FMC Corporation, now part of BioPolymer; Ask 2003), Dr. Maxwell Doty of the Department of Botany, University of Hawaii (Parker 1974), the Bureau of Fisheries and Aquatic Resources and the Marine Science Institute, University of the Philippines. The industry made its first export of 500 MT of farmed carrageenophytes in 1973 (Doty and Alvarez 1981). Since then, the Philippines has been the leading supplier of “cottonii” seaweed until 2007. In 2008–2009, the production of carrageenophytes declined by 10 and 25 %, respectively, compared to the 2007 harvest (Bixler and Porse 2011). For its part, the harvest in Indonesia increased by 7 and 15 % in 2008 and 2009, respectively, compared to the harvest in 2007. The increase in Indonesian production stems primarily from a greater number of farmers opening up new areas for farming (Bixler and Porse 2011). The downward trend in Philippine production was brought about primarily by the deteriorating quality of propagules and the perennial occurrence of “ice-ice” and harmful endophytes caused by environmental stresses due to unfavorable weather conditions. Moreover, the peace and order problem in the major producing areas like Maguindanao, South Cotabato, Basilan, and Sulu also causes a decline in the carrageenophyte harvest. However, the production of carrageenan has been rising steadily since 1979. Of the total production of 84,700 t in 2009, approximately 41 % was from the Philippines (Dakay 2010). This is probably due to a number of local carrageenan processors that are operational (Hurtado 2012) plus outsourcing for raw materials outside the country.

The carrageenophytes

There are four genera of carrageenophytes found in the Philippines. They include eight species and 24 morphotypes or cultivars (Table 1). They belong to Family Solieriaceae. Included in the group are the two most commonly cultivated species for commercial purposes, K. alvarezii (“cottonii”, of commerce) and E. denticulatum (“spinosum”, of commerce) (Fig. 3a–c). The biggest number of morphotypes or cultivars are those belonging to Kappaphycus (Fig. 4).

Table 1 Carrageenophytes in the Philippines (modified from Trono 1992)
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Fig. 3
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a–c Habit of the green and brown forms of a Kappaphycus alvarezii “cottonii”, b K. striatum, and c Eucheuma denticulatum, “spinosum”. (Photos by AQ Hurtado; bar = 1 cm)

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Fig. 4
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Different commercial varieties of Kappaphycus (Hurtado et al. 2008)

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These various kinds of red seaweeds could have any of the three different types of carrageenan. These types include the kappa, iota, and lambda types, which have different uses in the industry. The kappa type, that yields the brittle gel, is usually obtained from the farmed Kappaphycus spp., while the elastic gel-forming iota is from farmed E. denticulatum (Bixler and Porse 2011). For its part, the non-gelling lambda type is not yet obtained from commercially available seaweeds, although Acanthophora spicifera may have this type of carrageenan.

There are approximately 16 morphotypes or commercial varieties of Kappaphycus (Fig. 4). These different kinds could be ecotypes or may be genetically different from one another. They could have also come from neighboring islands' sporelings or seaweeds, especially near the islands in Tawi-Tawi. Of these different kinds, different places have different preferences of algal materials. For example, in Zamboanga City (Mindanao), they prefer to farm the slow-growing types like K. striatum var. sacol and K. alvarezii var. adik-adik, while in Zamboanga Sibugay, they farm the fast-growing type of K. alvarezii var. tambalang (Hurtado 2010). In fact, in the handbook on “Primer on farming and strain selection of Kappaphycus and Eucheuma in the Philippines”, Trono et al. (2000) recommends different morphotypes in different places because they noted the site and season specificity of the seaweeds (Table 2).

Table 2 Recommended seedstock production months and farming months of different carrageenophyte morphotypes (cultivars) in Danahon Reef, Bohol (Visayas) (modified from Trono et al. 2000)
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Farming sites

The Philippines is an archipelago comprising several thousand islands that are grouped into three major subdivisions, i.e., Luzon, Visayas, and Mindanao. It has one of the longest combined coastlines in the world with a total of 36,289 km. These coastlines are rich with algae. One of the places where tropical seaweeds grow abundantly and robustly is in Mindanao, at the southern part of the country, which includes places like Sitangkai, Tawi-Tawi (Autonomous Region of Muslim Mindanao, ARMM,). This area is also least frequented by typhoons or tropical storms, being situated within the tenth parallel latitude (Fig. 5). In fact, it was around this area where the first trials of seaweed farming were done by Dr. Maxwell Doty (Doty 1973; 1978; Parker 1974), and it now holds the largest area being farmed with Kappaphycus in the country, at approximately 23,600 ha in 2008 (Hurtado 2012). In addition to this, there is approximately 20,500 ha more for expansion for mariculture purposes (Table 3). Aside from the ARMM, there are three more areas identified to have a high production of red seaweeds in 2008, i.e., Regions: IV-B (Palawan, Luzon), IX (Western Mindanao), and VII (Bohol, Central Visayas), in decreasing order of production (Hurtado 2010). Table 3 shows that these four productive areas had a total of 34,640 ha farmed in 2008. There was approximately 515 % or a six-fold increase in hectares farmed over a period of 9 years (1999–2009) in the four productive areas (1999–2008). Moreover, there is still a potential of 43,000 ha that can still be farmed or an average of 50 % more areas that could be planted (Hurtado 2012). Table 4 shows that the productivity of these four sites increased 20-fold times over a period of 9 years. Therefore, the increase in the productivity of these areas could not only be accounted for by the increase in area farmed in 2008, but more importantly, by the kind of seedstock, type of farming system, or other technologies newly introduced in these places. Figure 5 shows that carrageenophyte farming has moved northward over time, from Sulu and Tawi-Tawi (Mindanao) (in 1972) up to the Ilocos provinces (Luzon) (at present). However, with the exception of Mindanao and Palawan (Luzon), farming production is usually seasonal, and, therefore not sustainable. The geographical location of the Sulu archipelago within the 10°N of the equator corresponds with the most productive areas for “cottonii” and “spinosum” in the Philippines.

Fig. 5
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Sites of carrageenophyte farming and highly productive areas in the Philippines. (Modified from Hurtado et al. 2008)

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Table 3 Farmed carrageenophytes (hectares) in 1999 and 2008 and potential areas for expansion (as of 2008) in the four places of the Philippines (Guerrero 2001; Hurtado 2012)
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Table 4 Carrageenophyte production (t ha−1 year−1, fresh wt.) in 1999 and in 2008 in four places of the Philippines (Guerrero 2001; Hurtado 2012)
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Farming techniques

There are essentially two types of farming techniques used in cultivating the carrageenophytes, (1) the fixed-off bottom line and (2) the raft or floating method. The fixed-bottom-line method is commonly used in shallow waters, where the water depth, at the lowest tide, is between 0.25 and 0.5 m (Hurtado et al. 2008; Trono 1990). Hence, this is usually used near the coastline. This is considered cheap and easy to install. In fact, the monoline fixed-off bottom technique is the first type of farming technique that was used by the farmers. The floating method is recommended in sites with mild wave action. It is established farther away from the coastline, where the water depth, at the lowest tide, is from 1 m to greater than 5 m. The advantages of this method are: (1) grazing by bottom animals, including zooplankters are minimized or eliminated because the algae are raised way out of reach of the grazers, and (2) the algae, being the near the surface of the water column, are exposed to more moderate water movement caused by the wave action, hence the faster in growth rate (Trono 1990).

Over time, there have been modifications from these two types based on the topography of the place, the strength of the water current, the wind direction on the farming site, and stocking density. For example, in the fixed bottom-line technique, there evolved the monoline and the net system of cultivation. Another type of fixed-bottom method is the hanging long line that was used in Tawi-Tawi (Mindanao) (Hurtado et al. 2008). Cages are also grouped under this type. The support structure may be made of ropes or split bamboo that could be in vertical lines or clustered in a horizontal manner (Hurtado et al. 2001). There have been many modifications in the floating method; thus, this is further subdivided into the hanging long line (HLL) floating and the raft type. The HLL is usually employed when the water depth, at the lowest tide, is >10 m. This includes the single-spring, single-free swing, triangular, vertical, and spider web methods, while the raft method is used in places with a water depth of 1–5 m at the lowest tide. Among the types in the latter are the single raft, multiple raft long line, multiple floating, and multiple submerged methods (Hurtado et al. 2008).

With the different farming techniques that have evolved, the farmers have many selections to choose from to maximize their production. For example, in Tawi-Tawi, they used different farming techniques in different months of the year with different commercial varieties of K. alvarezii or K. striatum. In this case, the seaweed farmers in Tawi-Tawi grow the fast-growing type of K. alvarezii var. tambalang with the floating type of faming technique, while in the fixed-off bottom of farming, they usually farm the slow-growing type of K. striatum var. sacol (Hurtado 2012). The seasonality of farming either K. alvarezii or K. striatum variants is primarily due to resistance to “ice-ice” symptoms and/or Neosiphonia infestation (Hurtado 2012).

The culturing of the seaweed has always been monospecies, but in some cases, they practice multiple species of farming (Trono and Lluisma 1992) or the seaweed is cultured with fishes (Hurtado-Ponce 1994). The culture period is usually for 3 months. Table 5 shows that the daily growth rates of K. alvarezii may have a maximum value of 5.7 % day−1. Polyculture seems to yield a high growth rate, whether the seaweed is combined with fish (Hurtado-Ponce 1994) or with oyster (6.1 % day−1; in China) (Qian et al. 1996). Hence, this is a culture technique that can be further encouraged among farmers to obtain higher yields, aside from getting another protein source. Integrated Multi Trophic Aquaculture (IMTA) is now successfully practiced in Israel, Canada, Denmark, and other countries (Neori et al. 2004), and the Philippines could adapt it to maximize the farming areas and consequently increase productivity. Of the various techniques, the most commonly used is the fixed-off bottom line, probably because this is easier and cheaper to put up.

Table 5 Daily growth rates (% day−1) of Kappaphycus alvarezii using different farming techniques in different sites of the Philippines (modified from Hayashi et al. 2010)
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Source of “seed stocks”

Cultivation of the carrageenophytes has been done mainly by vegetative propagation since the 1970s (Doty 1973; 1978; Trono 1974). Likewise, the source of seedstocks is usually from these vegetatively propagated seaweeds. Such a seedstock source is usually unreliable due to seasonality in production (Trono et al. 2000; Trono and Lluisma 1992). Besides, it is established that vegetatively propagated organisms are less flexible and less vigorous than genetically propagated organisms. Attempts have been made in academic and research institutions to propagate calluses and tissues of these carrageenophytes in the laboratory (Azanza-Corrales and Dawes 1989; Azanza-Corrales et al. 1994; Dawes et al. 1994; Hurtado and Cheney 2003; Hurtado and Biter 2007; Hurtado et al. 2009; Yunque et al. 2011). New strains of eucheumatoids (E. denticulatum and K. alvarezii) have been reported through somatic hybridization and mutagenesis with improved growth rates and biochemical characteristics (Cheney et al. 1998). Recently, a successful outplanting of young thalli generated from spores of wild K. striatum has been reported by Luhan and Sollesta (2010). Though these strains have been tested in the field, the propagules have not yet been commercialized. This is probably another undertaking that will ensure the sustainability of carrageenophyte farming industry in the country.

Other biological factors

The occurrence of epiphytes, like the Neosiphonia spp. and the “ice-ice” symptoms has been earlier addressed (Largo et al. 1995a–b), but the more recent reports of Loureiro et al. (2010), Borlongon et al. (2011), and Hurtado et al. (2012) showed promising results on the use of Acadian Marine Plant Extract Powder (AMPEP), a biostimulant, growth enhancer and reducer of “ice-ice” malaise and Neosiphonia infestation. However, more studies are to be pursued further to assess the impact of AMPEP on the molecular level of Kappaphycus, but in most cases, commercial farming of carrageenophytes is very dependent on the practical cultivation practices in a specific site. Foremost is the proper selection of cultivation site that is far away from domestic wastes and less siltation, with mild and constant water movement. The next factor to consider is the proper selection of healthy and robust seed stock adopted to the site.

Socio-economic factors

The positive effect of seaweed aquaculture in the Philippines can be greatly attributed to the fact that the main beneficiaries of the economic benefits are the seaweed farmers. For example, the estimated total production of carrageenophytes in 2004 was between 97,000 and 102,820 t, dry wt. (Dakay 2010; Bixler and Porse 2011). The price of the seaweed at that time was US$ 850 t−1 dry wt. (Bixler and Porse 2011). Therefore, the estimated cost of the seaweed for that year (2004) ranged from US$ 82.4 to 87.4 million. It is presumed that the main beneficiaries of this amount are the farmers. The marketing of seaweed usually starts at the shoreline (Hurtado 2010). The first stage of marketing is from the harvest of a group of families, called the “pondohan”, headed by a consolidator. The price of seaweeds is dependent on many factors, including the moisture content and impurities. Usually, the farmers sell their seaweed in fresh form, but this is usually the cheapest value they can get out of their raw material. Figure 6 shows seaweed production in Tawi-Tawi (Mindanao) in 2006–2008 for each quarter. There was higher production in the first quarter of the year (January–March), which coincided with lower water temperatures and less rains due to the northeast monsoon. The price of the seaweed in 2006–2007 was Php 4.00–5.00 kg−1 fresh wt. (=US$ 0.095–0.119 kg−1) and followed the law of supply and demand. Total farm gate revenues for Tawi-Tawi (Mindanao) during this period ranged from about Php 278,000 to 792,000 (=US$ 6,629–18,857). However, the seaweed price was much higher in 2008, reaching a maximum value that almost doubled the prices in 2006–2007. This price situation was also observed globally (Bixler and Porse 2011). For example, the prices of the seaweed for the whole Philippines in 2006 and 2007 were US$ 748 and US$ 947 t−1 dry wt., respectively (Bixler and Porse 2011), while in 2008, the price of the dry raw material almost doubled (US$ 2,342 t−1). The market situation was also true in Indonesia (Bixler and Porse 2011). An explanation given for this unusual situation in 2008 was the aggressive buying from new plants in China (because there are no substantial carrageenophytes growing in China) that raised prices to such a high level, a problem probably exacerbated by “campaign buying” (Bixler and Porse 2011). Therefore, the objective in the industry is to have more or less stable prices which can be achieved through reliable production statistics and relevant market intelligence available to farmers, traders, and processors in due time. The farmers should also have access not only to fair trade but also to market links through the help of the government, like the Department of Agriculture-Bureau of Fisheries and Aquatic Resources.

Fig. 6
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Seaweed production (metric tons fresh wt. quarter−1, 1–4) (a) and farm gate price of fresh seaweed (Php kg−1 quarter−1) (b), in Tawi-Tawi, Mindanao (2006–2008). (Modified from Hurtado 2012)

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The seaweed farming enterprise is patterned on small-scale, family operations, in contrast to corporate and other plantation-style farms, which favor the employment of families along the coastal areas of the country. These communities are usually found in remote areas with fewer economic opportunities besides fishing. However, coastal fisheries are currently being affected by overexploitation. In this case, the impact of seaweed farming goes beyond the economic benefits, as it reduces incentives for overfishing. Hurtado (2012) presented anecdotal evidence indicating the economic fortunes seaweed farming brought to villages. Many of these communities usually lived at or below poverty levels (Asia-Pacific poverty level of ≤US$ 1.35 day−1, ADB 2008) prior to engaging in seaweed farming, after which they experienced a substantial improvement in their standard of living, which allowed them to provide their children with proper schooling, improved their dwellings, enhanced their diet and increased their purchasing power for material goods. This observation is also substantiated by the comprehensive study done by Jain (2006). Furthermore, since this farming enterprise is usually engaged in by a family or a group of families (20–30 families), it gives another income-generating activity to the female members of the family (like wives or mothers) without neglecting their traditional household chores (Hurtado 2012).

However, the achievement of the farmers can be further improved if they have access to research and development (R & D) technologies and verification studies suitable to a particular farming site. Furthermore, opportunities should be available to them to further their education beyond the primary level, such as through adult education programs in a community.

Conclusions and recommendations

Seaweed farming is a profitable business uplifting the socio-economic conditions of families along the coastal communities of the Philippines. Its success for more than four decades is mainly due to the perseverance and dedication of the seaweed farmers to supplying the increasing demand for seaweed-carrageenan in the global market. Furthermore, seaweed farming provides a sanctuary for other forms of marine life, thus increasing biodiversity in the area and decreases destructive fishing malpractices. Despite the success of seaweed farming, its recent downturn in productivity may hopefully be reversed with the untiring assistance of scientists in research and academic institutions, support from the government, and the cooperation of non-government organizations and multinational companies (MNCs) based in the Philippines. Among these recommendations which are of equal improtance are: (1) expansion of farming areas, especially in the productive areas, with concomitant financial assistance from the government, (2) encouraging farming in non-traditional areas, and (3) access to research and development (R & D) technologies suitable to a particular farming site and season. Among the R & D technologies that need to be addressed immediately and seriously are: (1) establishment of cultivar “bank” with superior qualities in terms of growth performance, resistance to biotic and abiotic factors, (2) establishment of land-sea-based nurseries to maintain and sustain propagules, ultimately providing an access of superior quality of propagules to the farmers; and (3) access to free trade and market links.