Philippine Journal of Science 148 (4): 803-811, December 2019 ISSN 0031 - 7683 Date Received: 27 Aug 2019

Edible Seaweeds Sold in the Local Public Markets in Tawi-Tawi,

Richard V. Dumilag*

Institute of Oceanography and Environmental Science Mindanao State University – Tawi-Tawi College of Technology and Oceanography Boheh Sallang, Sanga-Sanga, , Tawi-Tawi 7500 Philippines

Documenting local knowledge regarding the identity and use of wild resources in rural communities is a pressing concern because such knowledge is likely disappearing into oblivion. As easily perceived, the large crowds in public markets provide opportunities for the exchange of local resources. Tawi-Tawi is one of the rural areas in the Philippines for which a list of seaweed species sold in the local marketplace has not been reported to date. Here, a survey of Tawi-Tawi public markets resulted in a list of seven commercialized seaweed species – namely Caulerpa lentillifera, Caulerpa cf. macrodisca ecad corynephora, Caulerpa cf. racemosa, Eucheuma denticulatum, alvarezii, Kappaphycus striatus, and Solieria robusta. The local name, description, and other key trade information for each seaweed ethnotaxon were provided. This study contributes to filling in data gaps in ethnophycological literature in the Philippines and its value placed on it by various stakeholders.

Keywords: bioprospecting, ethnophycology, Philippine local knowledge, resource management, seaweed taxonomy

INTRODUCTION key nexuses for knowledge generation (McMillian 2002, Delgado 2004, Cetina 2006). For example, many fields Ethnophycology is a branch of ethnobiology that deals with in social sciences identify market studies as a goldmine the study of interrelationships between humans and of historical and cultural epistemology (Tangires 2008, (Arenas 2016), with seaweeds as relatively the most studied Brown and Miller 2008, Morales 2009, Silalahi et al. group. One hundred forty-seven (147) species of seaweed 2015) while scientists ferret out various resources sold worldwide are believed to be edible, of which many are from local markets for food development, drug discovery, also known to have other commercial surpluses (Pereira bioprospecting, among others (e.g., Albuquerque et al. 2007, 2016). The fact that seaweeds are a lucrative source of Lee et al. 2008, Monteiro et al. 2010, Randriamiharisoa et natural products, whose uses are still being explored, has al. 2015, Lima et al. 2016). Notwithstanding the long and made several reviews covering their chemistry and biology intimate association of humans to seaweeds, the range of works in progress (e.g., Smit 2004, Stengel et al. 2011, ethnophycological studies involving local markets in the Pérez et al. 2016, Makkar et al. 2016, Cikoš et al. 2019). Philippines remains limited. Public markets are places where buying and selling take Seaweed is an important food source commodity in the place between resident consumers and traders. More than Philippines. Its domestication in the islands of Tawi- points of a product exchange, these areas are becoming Tawi, southern Mindanao has been one of the largest *Corresponding Author: [email protected] producing areas in the Philippines (Romero 2002, Hurtado

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2013). Of the seaweed species domestically grown, Tawi are only a few (Trono 1972, Puig-Shariff 2015, Tahil eucheumatoids – particularly Kappaphycus alvarezii – and Liao 2019). While Tawi-Tawi has become the “site- are the most widely commercialized. Eucheumatoids of-choice” for various studies involving eucheumatoids, are the world’s main sources of carrageenan (Doty the area has received a disproportionate share of scholarly and Norris 1985) – a hydrocolloid used as thickener, attention concerning other edible seaweeds locally utilized emulsifier, or binder to various food products (Necas in the area. The present paper, therefore, focuses attention and Bartosikova 2013). Remarkably, the commercial on a fundamental question on the identity of the common cultivation of eucheumatoids in Tawi-Tawi goes far seaweed species sold in Tawi-Tawi public markets. beyond the livelihood it offers. The advent of seaweed commercialization across the Archipelago (Doty 1973, Parker 1974) has historically impacted the ebb and flow of human migration in Tawi-Tawi (Nimmo 1986). MATERIALS AND METHODS In Islands, the southernmost border boundary of Tawi-Tawi, seaweed farming has entrenched women Study Site to make a vital contribution to the economy of their farms Tawi-Tawi (Figure 1) is located at the tip of the southwest to the communities in which they live (Aming 2004). In area of of Mindanao. The province covers more recent years, commercial seaweeds of Tawi-Tawi a land area of 1,087.40 km2. The expanse of to its became a trope in local festivities (known as the Agal- north, the Sabah Sea to its west, and the North Kalimantan agal festival), which celebrates the rich seaweed bounty. Sea from western and southern borders geographically divide It is said that such a festival promotes solidarity among the region from the Sulu province, Malaysia, and Indonesia, its local peoples as well as boosts tourism activities in respectively. Politically, Tawi-Tawi also includes the Tawi-Tawi (Sali and Gonzales 2017, Romero et al. 2017). Is. (formerly Cagayan de Tawi-Tawi) and the Turtle Islands Aside from eucheumatoids, other seaweeds produced in whose geographic locations are nearer to Sabah, Malaysia Tawi-Tawi have had long found elemental to the daily (about 20 km) than that of most islands of Tawi-Tawi. diets of its local people. It is highly likely that the first Tabuh (Figure 2) is the local market in Tawi-Tawi. In this settlers of Tawi-Tawi, the Sama Dilaut (Badjao), had study, two major tabuh were visited: the Bongao Public the earliest and widest seaweed resource use. Any exact Wet Market (5°04’11.2’’N 119°53’02.0’’E) in Bongao and date on the origin of this practice would perhaps be pure the Batu-Batu Public Market (5°04'11.2"N 119°53'02.0"E) conjecture; however, seaweed trades in Tawi-Tawi prior situated at the Municipal Fish Port. In to its domestication could be traced back to as early as the terms of size and number of traders and buyers, these two 1700s (Fry 1970). Studies on seaweed diversity in Tawi- marketplaces are the largest in Tawi-Tawi.

Figure 1. Maps showing the location of Tawi-Tawi in the Philippines and respective study areas.

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Confirmation of Seaweed Source Origin After the interview, one of the seaweed source areas – Belatan Is. (Pondohan Tiyadtad, 5°03'57"N 120°01'02"E) – was also visited to confirm the presence of each of the species identified in this study. Underwater photographs of habit specimens were taken using a Canon PowerShot D30 (Canon Inc., Tokyo, Japan) camera.

RESULTS

Market Ambiance The Bongao Public Wet Market (Figure 2A) operates daily from 06:00 AM to 05:00 PM. The present market structure was built adjacent to the Chinese Pier, the central hub for vessel transportation in the entirety of Tawi-Tawi. The area was covered by a concrete base. There are 24 tiled tabletops inside, mainly occupied by regular vendors (magdagang-dagang) who exclusively sell fish and other marine merchandise. Sellers hawk their goods in loud voices. Peak hours start from 01:00 PM to 05:00 PM. There were only six vendors (both survey months) who permanently sell seaweeds. All of Figure 2. Vendors selling edible seaweeds in public market (tabuh) them participated in the interview. They were situated in (A) Bongao Public Wet Market and (B) Batu-Batu, inside the marketplace proper. Seaweed stockpiles are Panglima Sugala in Tawi-Tawi. Stockpiles of seaweeds commonly placed inside karut (sack) or pastan (basin). placed inside (C) tiklis and (D) tambusâ. All vendors were female. Batu-Batu Public Market (Figure 2B) is a periodic type Interview of market and operates every Friday only, with high foot Samples of morphologically different species of seaweeds traffic at 02:00 PM onwards but – beginning 24 Aug 2019 were purchased, which were subsequently used for – the operation was moved every Saturday from 08:00 voucher preparation. Information on seaweed merchandise AM onwards. During peak hours, the number of vendors from target marketplaces was obtained via an unstructured was comparably two-fold than that of the Bongao Public interview with vendors as the respondents. Following Tito Market. Goods consisted of both wet and dry merchandise. and Liao (2000), the information was directly extracted: Vendors hawk their produce in loud voices. On the first (1) local name of the seaweed, (2) source, (3) seasonality, survey, a total of 20 vendors sell seaweed produce in the (4) price, and (5) usage. The interview was done twice i.e., area, of which 12 (60%) respondents participated; on July and August 2019. A total of 38 vendors participated the next visit, 20 (62.5%) of the 32 vendors joined the in this study, representing six and 32 respondents from interview. There were seven respondents who consistently Bongao and Batu-Batu Public Markets, respectively. joined both surveys. In the open-air were the seaweed produce displayed over Species Identification karut. Seaweed stockpiles were placed inside karut, tiklis Species identification in situ was done based on (bamboo basket) (Figure 2C), or tambusâ (Figure 2D), a morphological criteria. Key phenotypic features were traditional bag made up of weaved coconut leaves. All examined, documented, and used the most recent literature vendors were female. Magsaliyu or barter transaction (Ganzon-Fortes et al. 2005, Tan et al. 2013, Belton et al. was still a common practice, especially between farmers 2015, Huisman 2015, Pattarach et al. 2019) to identify and fishers. Magsaliyu is characterized as an innovative each taxon down to species level. Voucher specimens were negotiable transaction between traders. For example, da prepared using the protocol of Trono and Ganzon-Fortes tumpuk (a handful heap) of seaweed can be exchanged for (1988) but untreated with formalin. Exsiccatae were lodged pieces of panggi bagun (sweet potato), sayul (vegetables), in Mindanao State University (MSU) Herbarium at the MSU or buah-buah (fruits). – Tawi-Tawi College of Technology and Oceanography in Boheh Sallang, Sanga-Sanga, Bongao, Tawi-Tawi.

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Seaweed Source Area The Pondohan Tiyadtad is part of the Belatan group of islands. A pondohan is a small community of seaweed farmers residing in stilt houses amidst the sea. The Pondohan Tiyadtad is characterized as a wide seagrass bed ranged from small patches to large meadows. The substrate of the area is primarily sandy with several coral bommies and large stones scattered here and there. Indications of seagrass destruction were observed, most probably due to human activities such as seaweed farming and boat anchoring and transport.

Seaweed Species A total of seven seaweed species (three chlorophytes and four rhodophytes) are offered for sale in the local markets of Tawi-Tawi. They were chiefly known locally as agal- agal, latoh (gamay in Tausug), and gulaman, and were confirmed to occur at least in Belatan Is. (one of seaweed area sources). All species can be harvested year-round but vendors in Bongao Public Market consistently claimed that gulaman can be unavailable for some months (the vendors did not specify). The prices of seaweed goods, regardless of species, were the same per marketplace. The prices were fixed. Seaweed vendors from Batu-Batu Public Market offered Php 10.00 (around USD 0.15–0.20) per heap but doubled its price in the Bongao Public Wet Market. Vendors believe that their seaweeds are beneficial to the welfare of the whole community; however, no respondent provided any specific health benefits. According to the vendors, buyers prepare seaweeds as a salad commonly Figure 3. Caulerpa species sold at public markets in Tawi-Tawi, Philippines. (A) Caulerpa lentillifera in situ habit mixed with onions, tomatoes, and vinegar. Table 1 shows and (B) a photo showing its erect assimilators with the summary information extracted from the seaweed densely covered subspherical ramuli. (C) Caulerpa vendors from the study sites. cf. macrodisca ecad corynephora in situ habit and (D) a photo illustrating its assimilator bearing oppositely Latoh. Also locally referred to as gamay in Tausug, arranged turbinate ramuli. (E) Caulerpa cf. racemosa in latoh constitutes the species of Caulerpa. They are found situ habit and (F) a photo showing its typical spherical to abundantly growing in seagrass meadows characterized by clavate ramuli. All scale bars measure 2 mm. sandy substrates. Three species were recognized: Caulerpa lentillifera (Figure 3A), Caulerpa cf. macrodisca ecad

Table 1. Seaweed species sold in local markets in Tawi-Tawi, Philippines, including local names and source. Voucher Local Species Source* specimen name Balimbing Proper, Belatan Is., 1. Caulerpa lentillifera MSU-00011 Latoh, Gamay Tongbangkaw, Tandubas Is. 2. Caulerpa cf. macrodisca ecad corynephora MSU-00012 Latoh, Gamay Belatan Is., Tongbangkaw, Tandubas Is. 3. Caulerpa cf. racemosa MSU-00013 Latoh, Gamay Belatan Is., Tongbangkaw, Tandubas Is. 4. Eucheuma denticulatum MSU-00014 Agal-agal, Spinosum Belatan Is., Tongbangkaw, Tandubas Is. 5. Kappaphycus alvarezii MSU-00015 Agal-agal, Tambalang Belatan Is., Tongbangkaw, Tandubas Is. 6. Kappaphycus striatus MSU-00016 Agal-agal, Katunay Belatan Is., Tongbangkaw, Tandubas Is. 7. Solieria robusta MSU-00017 Gulaman Belatan Is., Tongbangkaw, Tandubas Is. *For this study, the only source origin was confirmed in Pondohan Tiyadtad, Belatan Is.

806 Philippine Journal of Science Dumilag: Edible Seaweeds in Tawi-Tawi Markets Vol. 148 No. 4, December 2019 corynephora (Figure 3B), and Caulerpa cf. racemosa striatus. These are the most common seaweed species (Figure 3C). Characteristic to Caulerpa species sold in in Tawi-Tawi public markets. Locals can tell them apart the public markets in Tawi-Tawi were their bottle green as spinosum, tambalang, and katunay, respectively. The colored thalli with assimilators bearing succulent ramuli color of agal-agal ranged from yellow and pale brown to that come in various shapes. C. lentillifera differed grass green or a mixture thereof. The thalli of agal-agal sharply from other congeneric produce by having erect were cartilaginous and sympodial, axes were cylindrical. assimilators densely covered by subspherical ramuli. E. denticulatum differed from K. alvarezii and K. striatus Both C. macrodisca ecad corynephora and C. racemosa by having relatively thinner axes (< 1 cm diameter) developed assimilators with oppositely arranged ramuli. beset with regular whorls of spines to entirely smooth The former species distinctively bear clavate to turbinate on some portions. Both K. alvarezii and K. striatus had ramuli, while the shape of the latter species ranged from smooth axes with dichotomous to irregular branching clavate to mostly spherical. pattern. K. striatus formed bushier branches near tips. The dichotomous branching is generally more consistent Agal-agal. Agal-agal is the local name given for three in K. striatus than in K. alvarezii. species – namely Eucheuma denticulatum (Figures 4A–B), Kappaphycus alvarezii (Figures 4C-D), and K. Gulaman. Gulaman is identified as Solieria robusta striatus (Figures 4E–F). In Pondohan Tiyadtad, Belatan (Figures G–H). The species was found growing on rock Is., E. denticulatum was found growing in the wild near entangled with Laurencia sp. Distinct to this species was seaweed farm areas consisting of K. alvarezii and K. its yellow, smooth cylindrical, soft gel-filled branches. Its axes spanned up to 4 mm and appeared as radially and distichously branched. Its axes gradually reduced in width upward to pointed apices. Probably during harvest and transportation and in part due to its delicate thallus, gulaman often vend as a fragment of branches on heaps, thus obscuring its overall distichous branching pattern.

DISCUSSION Seaweeds are important in the traditional diet of the local people of Tawi-Tawi. Public markets in Tawi-Tawi constitute strong seaweed entrepreneurship virtually participated in by local women. Dubbed as the “food basket of Tawi-Tawi” (Mercado 2008), the public concourse of seaweed traders and possible buyers in Batu-Batu was found significantly larger (i.e., a larger difference in terms of the number of respondents) than that of Bongao. Although the majority of local seaweed occupations involve domestication of eucheumatoids, the local people of Tawi-Tawi also gather substantial amounts of wild seaweeds for trade. Here, on the basis of morphology, seven species were identified. It appears that the number of seaweed ethnotaxa elsewhere in the Philippines, particularly the northern region of the country (Dumilag 2018), is higher than what is so far known in Tawi-Tawi. Probably, such a list for Tawi-Tawi will be increased once the research is conducted involving non- trade taxa (i.e., those that are gathered exclusive for food Figure 4. Species of Euchuema, Kappaphycus, and Solieria sold at public markets in Tawi-Tawi, Philippines. (A) sustenance and other commercial purposes) at wider Underwater photo of a wild Eucheuma denticulatum sampling site coverage. attached on rock and (B) its habit, scale = 4 cm. (C) Kappaphycus alvarezii grown on a rope and (D) its habit, Except for S. robusta, all identified species are widely scale = 3 cm. (E) Kappaphycus striatus grown on a rope known marketed in a much wider area in the Philippines and (F) its habit, scale = 4 cm. (G) Underwater photo of (Zaneveld 1959; Moreland 1979; Hurtado-Ponce 1983, Solieria robusta and (H) its habit, scale = 3 cm. 1992; Marcos-Agngarayngay 1983; Tungpalan 1983;

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Cordero 1987). Only S. robusta (known as tajuk bau’no) Tariq et al. 2001, Yen et al. 2004). is also found on sale in the local public markets in Zamboanga (Tito and Liao 2000), a province 300 km off Ethnophycological studies involving identification of north Tawi-Tawi. The same species locally referred to as local resources must begin to place greater worth more lumitamana has also been reported to have commercial than ever (Turner 2014), particularly in this modern value in Suva and Nausori markets in Fiji (South 1993). time where many of the recent societal challenges can Many taxa in the genus Caulerpa, in particular within be resolved using identified specimens (Soltis 2007, the Caulerpa racemosa complex, are difficult to identify Upton et al. 2019). Accordingly, the present study is due to morphological variability (Sauvage et al. 2013, offered as a contribution to Philippine ethnophycology Belton et al. 2014) brought by environmental factors whose attention is little, yet many of its aspects – once (Peterson 1972, Gacia et al. 1996). Those identified unraveled – can certainly aid address various problems Caulerpa species sold in Tawi-Tawi markets belong to that the Philippine society faces today. this complex; therefore, the use of a more reliable tool (molecular approaches) to validate species identification for this group is strongly suggested. ACKNOWLEDGMENTS The total production and other relevant data on the The author would like to thank A. M. Diansuy, A. B. distribution and source availability of wild edible Hadjirul, S. K. Kalimuddin, A. A. Juaini, A. Sanuddin, seaweed resources in Tawi-Tawi are hitherto unknown. N. Sanuddin, S. Z. B. Halun, and K. J. B. Serag for their Attempts to domesticate other seaweed species, aside valuable help during the conduct of the study. S. U. from eucheumatoids, are yet to be realized in the area. Damsik and A. L. Recto are acknowledged for thoughtful However, their potential to contribute to food security conversations on the topic. Two anonymous reviewers and sustainable aquaculture has long been harnessed in are thanked for their insightful comments on further other areas in the Philippines, e.g., Caulerpa farming in developing this manuscript. Batangas (Trono and Denila 1987), Cebu (Trono 1988, Romano 1999), and Palawan (Mundo et al. 2002). The same holds true for Tawi-Tawi, the market supply of S. robusta in Zamboanga (Tito and Liao 2000), which REFERENCES remains widely dependent on wild stocks. ALBUQUERQUE UP, MONTEIRO JM, RAMOS Market knowledge is particularly relevant for local MA, AMORIM EL. 2007. Medicinal and magic seaweed resources demanded by various stakeholders. plants from a public market in northeastern Brazil. J Cataloging species names in any given region remain as a Ethnopharmacol 110: 76–91. fundamental reference for seaweed conservation planners and resource managers. Without basic information on AMING N. 2004. Participation of Filipino Muslim the identity of these resources, it would be difficult to women in seaweed farming in Sitangkai, Tawi-Tawi, evaluate their status and implement proposed conservation Philippines [Ph.D. Dissertation]. University of the measures. The negative impacts of the changing climate Philippines, Los Baños. 129p. to seaweed communities are undoubtedly of no exception ARA J, SULTANA V, QASIM R, AHMAD VU. 2002. (Harley et al. 2012). Many seaweed communities in the Hypolipidaemic activity of seaweed from Karachi Philippines in their natural stock have also been suggested coast. Phytotheraphy Res 16: 479–483. to be highly vulnerable to anthropogenic pressures, including overharvesting and habitat degradation (Largo ARENAS PM. 2016. Ethnophycology. In: Introduction 2002). The list of seaweed species presented in this to Ethnobiology. Albuquerque UP, Alves R ed. study serves as an important resource tool for future Switzerland: Springer International Publishing. p. bioprospecting in Tawi-Tawi. Natural products from 47–52. seaweeds have long been fertile sources of nutrient and BELTON GS, PRUD’HOMME VAN REINE WF, bioactive compounds. For example, various Caulerpa and HUISMAN JM, DRAISMA SGA, GURGEL CFD. eucheumatoid species contain high nutrient and bioactive 2014. Resolving phenotypic plasticity and species compounds (e.g., Smit 2004, Gaillande et al. 2016). S. designation in the morphologically challenging robusta is also a potential source of carrageenan (Chiovitti Caulerpa racemosa-peltata complex (Caulerpaceae, et al. 1999) but its domestication has yet to be realized. Chlorophyta). J Phycol 50: 32–54. Studies have found that S. robusta possesses significant antifungal (Khanzada et al. 2007), hypolipidaemic (Ara BELTON GS, HUISMAN JM, GURGEL CFD. 2015. et al. 2002), and anticancer properties (Hori et al. 1988, Caulerpaceae. In: Algae of Australia: Marine benthic algae of north-western Australia. 1. Green and brown

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