1-s2.0-S0044848601007244-main

Advances in cultivation technology of commercial

eucheumatoid species: a review with suggestions

for future research

Erick I. Ask a, Rhodora V. Azanza b,*

aFMC BioPolymer, 1735 Market St., Philadelphia, PA 19103, USAbMarine Science Institute, University of the Philippines, 1101 Diliman, Quezon City, Philippines

Received 16 December 2000; received in revised form 9 May 2001; accepted 19 June 2001

Abstract

An ‘‘advance’’ is defined as any technology that leads to an increase in production of

Kappaphycus alvarezii (Doty) Doty, K. striatum Schmitz and Eucheuma denticulatum (Burman)

Collins et Harvey (commercial eucheumatoid species) per unit time, effort, area and cost in more

than one cultivation area. The present review has shown that no true advances have taken place in

commercial eucheumatoid farming in over a decade. These species have remained the primary

source of carrageenan through expansion of cultivation area and increase in the number of farmers

since farmer productivity has not increased through time. Priority should be given to researches that

could replace ‘‘tie– tie system’’ currently being used in the vegetative propagation of the crops and

the possible use of spores/sporelings in cultivation as in other economic seaweeds. Multifactorial

experiments considering nutrients, salinity and light especially, need to be done to meet seasonality

problems in growth/production of the crops. Understanding and developing the capability to mitigate

or eliminate pests, herbivores and diseases need to be addressed more closely. Strains should be

developed through a continuous selection of wild varieties, breeding programs and genetic

manipulation or transgenic production/development. Increasing the quality of extract through

superior post-harvest handling and strain improvement should be achieved. Practical and effective

quarantine procedures should be explored, publicized and utilized for introduction of crops to new

areas. D 2002 Elsevier Science B.V. All rights reserved.

Keywords: Kappaphycus alvarezii; Kappaphycus striatum; Eucheuma denticulatum; Cultivation technology;

Seaweed; Carrageenan

0044-8486/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved.

PII: S0044 -8486 (01 )00724 -4

* Corresponding author. Tel./fax: +63-2-921-5967.

E-mail address: [email protected] (R.V. Azanza).

www.elsevier.com/locate/aqua-online

Aquaculture 206 (2002) 257–277

1. Introduction

Wild and farmed crops of Eucheuma denticulatum (Collins et Harvey), Kappaphycus

alvarezii (Doty) Doty and K. striatum (Doty) are primary sources of the commercially

valuable hydrocolloid carrageenan. The annual value of the crop has been estimated to be

about US$200 million (Bixler, 1995). ‘‘Spinosum’’ is the trade name for farmed E.

denticulatum, which produces iota-carrageenan while ‘‘cottonii’’ is the commercial name

for the two farmed Kappaphycus species that produce kappa carrageenan. These three

species are the ‘‘Eucheuma of commerce’’ (Santos, 1989).

Cultivation efforts were begun by Dr. Maxwell Doty of the University of Hawaii in

conjunction with Marine Colloids (purchased by FMC in 1977) in the mid-1960s and

included the Philippines’ Bureau of Fisheries and Aquatic Resources in the early 1970s

(Ronquillo and Gabral-Llana, 1989). Production of commercial Eucheuma has increased

sharply since the inception of cultivation in 1971 from less than 1000 dryweight Mt (Doty

and Alvarez, 1975) to approximate worldwide production of over 100,000 Mt at present

(Fig. 1). In addition, the number of countries producing commercial quantities of

eucheumatoid species, ‘‘cotton’’ and ‘‘spinosum’’ (Table 1) and the number of regions

within the countries have increased in the Philippines (Lim and Porse, 1981; Velosos,

1989) and Indonesia. Cottonii production estimates in the Philippines indicate that

productivity remained at less than 6 Mt per farmer per year (Alih, 1990; Dawes and

Koch, 1991). Commercial eucheumatoid suppliers from the Philippines, Indonesia and

Kiribati indicate that these production numbers are roughly true today.

From 1971 to 1989, there have been reports of improvements of farm systems and

agronomic practices which led to huge increases in per farmer productivity: 6272 dry kg

ha�1 year�1 in 1978 to 36,036 dry kg ha�1 year�1 in 1988 (Padilla and Lampe, 1989).

Actual production numbers from the same site during the same period, however, do not

support these assertions (Alih, 1990).

Fig. 1. Production trend of cultivated cottonii in the Philippines (data courtesy of Seaweed Industry Association of

the Philippines).

E.I. Ask, R.V. Azanza / Aquaculture 206 (2002) 257–277258

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Table 1

Countries where commercial eucheumatoids have been introduced for cultivation or experimental purposes and where commercial quantities are currently being produced for the carrageenan

industry

Country Year introduced or

experiments begun

Commercial

cultivation

Citation

Fiji mid-1970s, 1984 Prakash (1990), Luxton et al. (1987), Doty (1985a)

Philippines 1971 � Doty and Alvarez (1973), Doty (1973), Parker (1974)

USA

(Hawaii) 1971, 1985 Doty (1985a,b)

(California) 1985 lab use only Doty (1985a)

(Florida) 1988 lab use only Dawes (1989)

Djiboiti 1973 Braud et al. (1974), Braud and Perez (1978), Perez and Braud (1978)

Kiribati (Christmas Island,

Tarawa Island)

1977, 1981 � Russell (1982), Tanaka (1990), Luxton and Luxton (1999), Robertson (1989)

Tuvalu 1977 Gentle (1990)

Samoa Previous to 1978 Doty (1978a)

Malaysia 1978 � Doty (1980)

French Antilles 1978 � Barbaroux et al. (1984)

Tonga 1982 Doty (1985a), Tanaka (1990), Fa’anunu (1990)

Japan 1983 Mairh et al. (1986)

Indonesia 1985 � Soerjodinoto (1969), Adnan and Porse (1987)

Federal States of

Micronesia (Ponape)

Previous to 1985 Doty (1985a)

French Polynesia Previous to 1985 Doty (1985a)

Guam Previous to 1985 Doty (1985a)

China 1985 � Wu et al. (1988)

Maldives 1986 de Reviers (1989)

Solomon Islands 1987 Tanaka (1990), Smith (1990)

Tanzania 1989 � Lirasan and Twide (1993)

India 1989 Mairh et al. (1995)

Cuba 1991 Serpa-Madrigal et al. (1997)

Vietnam 1993 Ohno et al. (1995, 1996)

Brazil 1995 de Paula et al. (1998, 1999)

Venezuela 1996 Rincones and Rubio (1999)

Kenya 1996 J. Wakibia, personal communication

Madagascar 1998 Ask et al., in preparation

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It appears that global production increases are due to increased number of farmers, not

an increase in per farmer production as brought about by technological advances. An

‘‘advance’’ in commercial eucheumatoid technology is defined as anything that leads to

one or more of the following increases to individual farmer productivity: (1) increase in

production per unit time; (2) increase in production per unit effort; (3) increase in

production per unit area; (4) increase in production per unit cost.

This paper reviews the current cultivation practices and knowledge of commercial

eucheumatoid species and suggests future research to improve per farmer productivity and

raw material quality. The review covers: Seaweed Biology (Life Cycle and Reproduction,

Fundamental Physiology); Farm Systems; Farm Ecology and Crop Improvement.

2. Biology of K. alvarezii and E. denticulatum

Species of Eucheuma and Kappaphycus occur throughout the Indo-Pacific region from

East Africa to Guam, in waters of China and Japan and mostly in algal reef areas of islands

in Southeast Asia (Doty, 1987). Although Philippine K. alvarezii and E. denticulatum are

the most commonly farmed carrageenophytes throughout the world, some local strains

have been farmed in Indonesia, Malaysia and Tanzania.

Taxonomic descriptions of the commercial species of Eucheuma and Kappaphycus are

in detailed Doty (1988) and Trono (1992, 1997).

During the late 1960s, various iota and kappa carrageenan producing eucheumatoid

species were all placed in the genus Eucheuma, e.g. E. spinosum, E. cottonii, E. striatum.

Later, the tribe Eucheumatodeae and the genus Kappaphycus were created (Doty, 1985a,b,

1988), which renamed a few of the species (Table 2). E. spinosum is the synonym of E.

denticulatum and E. cottonii is the synonym of K. alvarezii.

2.1. Life cycle and reproduction

The life cycle of Eucheuma spp. and Kappaphycus spp. are triphasic consisting of the

carposporophyte (2N), tetrasporophyte (2N) and gametophyte (N) phases. The vegetative

and reproductive structures of tetrasporic and gametophytic populations and their

occurrence in farming sites in the Philippines have been described (Azanza-Corrales,

1990; Azanza-Corrales et al., 1992).

Table 2

Previous and current names of the commercial eucheumatoids

Previous name Present name

E. denticulatum (L. Burman)

Collins et Harvey

E. denticulatum (trade name= spinosum)

E. alvarezii Doty K. alvarezii (Doty) Doty (trade name = cottonii)

E. striatum Schmitz K. striatum (Schmitz) Doty (trade name = cottonii)

E. cottonii Weber-van Bosse K. cottonii (Weber-van Bosse) Doty


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E. denticulatum and K. alvarezii produce zonate tetraspores (Doty, 1987; Okuda and

Neushul, 1983; Yokuchi, 1983) and tetrasporophytes occur in K. alvarezii cultured

species (Azanza-Corrales, 1990). Tetrasporophytes dominate natural beds near farms in

Tawi-Tawi, Philippines (Azanza-Corrales et al., 1996), while in Danajon Reef,

Philippines, only K. striatum var. ‘‘dichotomous’’ (or ‘‘sakol’’) and E. denticulatum

from farms were found to have tetrasporophytes predominating (Azanza-Corrales et al.,

1992). Male gametophytes and structures are rare to unknown in these genera as

reported by Cheney and Dawes (1981) and Dawes et al. (1974). The male sori have

been found on thallus sections (Azanza-Corrales, 1990; Doty, 1985a). Female repro-

ductive structures of Eucheuma and Kappaphycus and resulting cystocarps are visible

as sub-spherical to spherical, sessile to pedicelled bodies. Within the cystocarp, a

central fusion cell is found from which gonimoblast filaments and carpospores radiate.

Diploid carpospores when released germinate to form the tetrasporophytes (Azanza-

Corrales, 1990).

In vitro cystocarp formation, carpospore release, germination and development have

been described (Doty, 1987; Mairh et al., 1986; Azanza-Corrales and Aliaza, 1999) as well

as the recruitment of carpospores in the sea/farm (Azanza-Corrales et al., 1996). The clone

cultivation is presently very useful; further research, however, should include the use of

sporelings for culture as in other economically important seaweeds like Porphyra and

Laminaria. Sporeling cultivation would provide the possibility of greater farming

manipulations.

2.2. Ecophysiology

2.2.1. Light response

Field studies on Eucheuma (Glenn and Doty, 1981; Zertuche-Gonzalez, 1988) have

shown the damaging effects of excessive light. This can be offset by decreasing the

distances between lines and cuttings attached to lines (Trono, 1994). Further, photo-

synthetic rates vary for tissue types in E. striatum var. tambalang with tissue nearer the tip

having higher rates (Glenn and Doty, 1981). In addition, a UV-absorbing compounds in E.

striatum that absorbs at 333 nm, and increases in quantity with exposure to higher levels of

UV. The photopigment is destroyed when exposed to two times the level of UV found in

the natural environment (Wood, 1989).

Numerous light response curves have been developed for the commercial eucheu-

matoid (Glenn and Doty, 1981; Dawes, 1984, 1989). A study important for strain se-

lection showed that the different color types of E. denticulatum and K. alvarezii (Dawes,

1992) had different photosynthetic responses. Ecotypic differentiation and variation in

photosynthetic efficiency were shown between E. denticulatum color types red, brown

and green which were not exhibited by K. alvarezii when nitrogen limitation was

raised.

Photosynthesis in E. striatum follows a diurnal pattern, with a peak before noon,

when cultivated in natural light (Glenn and Doty, 1981). Mairh et al. (1986) found for

the same species (E. striatum) that the maximum growth rates was achieved with a

12:12 L/D cycle at 6000 lx. This growth rate dropped, though not significantly, at

10,000 lx. More field studies considering light as a single factor or its interaction with

E.I. Ask, R.V. Azanza / Aquaculture 206 (2002) 257–277 261

other factors are, however, needed to help increase per farmer productivity especially in

relation to seasonality in production and light should be recorded in SI units.

2.2.2. Temperature response

Temperature responses of commercial eucheumatoids have been well studied both in

field and laboratory. E. striatum (var. tambalang and elkhorn) and E. denticulatum have

maximum photosynthetic rates at 30 �C with inhibition at 35–40 �C (Glenn and Doty,

1981). An optimum photosynthetic rate was obtained between 30 and 35 �C for E.

denticulatum by Dawes (1979). Dawes (1989) looked at the temperature response with

acclimation from 22 to 25 �C for K. alvarezii and reported no acclimation to 18 �C either

through gradual or abrupt transfers.

In Japan, Mairh et al. (1986) cultivated E. striatum in the field over a temperature

range of 14.3–31.2 �C, with highest growth rates recorded at 21–31 �C. Optimum

temperature was between 24 and 31 �C in laboratory plants, and they could not be

sustained at 17 �C or lower. Later, in India, Mairh et al. (1995) reported that in outdoor

chambers, K. striatum showed high growth rates between 23 and 30 �C with growth

declining above 30 �C and below 20 �C. Observing the growth of K. alvarezii in the

field for over a year, Ohno et al. (1994) found that commercial growth rates could not

be obtained below 20 �C and the optimum temperature range was 25–28 �C. In

tropical farm areas, however, Trono and Ohno (1989) reported that rapid growth and

high biomass production by Kappaphycus and Eucheuma occur during months

characterized by warmer temperature, i.e. 25–30 �C.

2.2.3. Salinity response

Little work has been done on the growth or photosynthetic response of commercial

eucheumatoids in relation to salinity. Other species therefore are included in this account.

E. isiforme has been found to have a broad respirometric maximum at about 30–40xwhile E. uncinatum and E. denticulatum had a maximum at 30x(Dawes, 1979, 1984).

For E. isiforme, Mathieson and Dawes (1974) had earlier reported a photosynthetic

maxima at 30–40xdepending on temperature. Mairh et al. (1986) likewise reported that

in laboratory cultivated E. striatum, plants did not survive beyond 7–14 days in less than

24xor above 45x.

Single and interactive effects of salinity with other factors on the commercial

cultivation of Eucheuma and K. alvarezii should be further studied. On shallow floating

forms or off bottom farms exposed at low tide, commercial eucheumatoids can be exposed

to rapid decreases in salinity during tropical downpours. This is often associated with

noticeable drops in temperature and light levels as well. In addition, plants located in the

intertidal can experience rapid changes in salinity from freshwater runoff.

2.2.4. Nutrients and water motion

Using an NH4 nutrient dip of 10 mM for 1 h every 3 days and cultivating K. alvarezii in

tanks and open sea, Li et al. (1990) noted a doubling of growth rates of the plants

compared to the control. Carbon/nitrogen ratios, carrageenan yield and gel strength were

also recorded and indicated beneficial impacts from the treatment. Mairh et al. (1995) also


found that K. striatum had increased growth rates with nutrient enrichment as opposed to

ambient seawater.

Schramm et al. (1984) summarized the nutrient dynamics on a eucheumatoid farm in

central Philippines with the goal of developing protocols to boost farm production. There

were very real diurnal and seasonal fluctuations in nutrient patterns (nitrate, nitrite,

ammonium, phosphate and total phosphorus) and sediment nutrients were much lower

in a farmed area (where the off-bottom method was used) than a non-farmed area, perhaps

explaining observed production declines after 2–3 years of farming. Overall, urea was a

poor source of nitrogen. Nitrogen applications were carried out in the farm by dips in

tanks, clod cards and clay pots, with the last supporting highest growth rate.

In a field experiment on a reef flat in Hawaii, Glenn and Doty (1992) determined that

growth of K. alvarezii, K. striatum and E. denticulatum was significantly correlated to

water flow. Growth response to water motion by K. alvarezii was higher in summer than in

winter.

Multifactorial experiments on effects of nutrients and water motion for both K. alvarezii

and E. denticulatum strains are recommended for future work. Results may allow creation

of color charts to determine nutrient status within propagules on farms. Improved site

selection protocols and results of nutrient uptake studies can indicate the potential of farms

as nutrient sinks benefiting reef communities and fish culture systems.

3. Farm systems

Of the numerous systems developed from field and laboratory experiments, only one

type, the tie–tie system (Doty and Alvarez, 1975) manifested in three basic forms: fixed

off-bottom, floating long line and rafts (Trono, 1989) has survived. The system pre-

dominated primarily because (1) it was simple, (2) farm materials were readily available

and inexpensive, and (3) plants grew well (Trono, 1989; Ask, 1999). Bag nets (R.

Barraca, personal communication) and tube nets (GEM, 1999) are in use today, but only

on a small-scale basis. All farm systems that have been developed over the years are listed

in Table 3.

Tying individual propagules to lines, the basis of the ‘‘tie–tie’’ system, appears to be a

major bottleneck to increasing per farmer productivity because it is laborious and time-

consuming. Other systems that do not require tying, such as tube nets, have not been

adopted on a commercial scale for one or more of the following reasons: (a) slower growth

than those with ‘‘tie–tie’’, (b) higher capital cost, (c) unavailability of suitable farm area

for the system, and (d) higher incidence of problems such as pest weeds.

There is a need to replace the ‘‘tie–tie’’ system with a less labor-intensive method as

well as an increase in efficiency in handling, planting, maintaining and harvesting. Any

new system, however, must be developed with the environment and users in mind. It is

noteworthy that new farm systems intended for family farmers should be simpler and with

a low capital and operating costs. A corporate plantation would require higher capital costs

and must be able to handle large volumes of the crop efficiently.

Polyculture systems might offer an advance to commercial eucheumatoid cultivation if

they can spread overhead and labor costs, thereby lowering production costs and/or


Table 3

Farm systems that have been tried since cultivation was developed in 1971

Farm system Description Used today? Citation

Horizontal nets off-bottom Large mesh gill nets with propagules tied at knots

suspended at four corners by mangrove stakes

No Parker (1974), BFAR (1974),

Ricohermoso and Deveau (1979)

Horizontal nets (floating) Same as above but floating and anchored with rocks No BFAR (1974)

Sewn tubular nets Nylon nets sewn around PVC pipe with propagules

seed through pipe

No BFAR (1974)

Broadcast Propagules tied to rock and broadcast on reef flat No BFAR (1974)

Lawn planting PVC coated wire net on reef with planting stuck

underneath, sandwiched to bottom

No Doty (1978a,b)

Hollow planting Loose plants placed in hollows on reef flat No Doty (1978a,b)

Pen planting Pens on reef flats where loose plants are placed No Doty (1978a,b)

Raceways Cement ponds with flow through water No Doty (1980)

Solid tubular nets Like sewn tubular nets but PVC pipe used for

harvesting as well

No Perez (1992)

Pond broadcast and off-bottom Plants cultivated in abandoned prawn ponds Experimental Ohno et al. (1995, 1996)

Monoline/off-bottom lines Single lines (monofilament or twisted nylon)

with cuttings attached with nylon straw (tie-tie)

Yes Ricohermoso and Deveau (1979)

Floating lines Same as above but floated Yes Trono (1990)

Floating rafts Same as monoline, but attached to floating raft Yes Trono (1990)

Bag nets Net bags holding 1kg, placed on floating long lines Yes R. Barracca, personal communication

Tubular nets from extruded HDPE Same as tubular nets above but net is one piece of

extruded HDPE

Experimental GEM (1999) (started by FMC in 1995)

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increase production (growth rates) due to benefits derived from co-cultivation, e.g.

shading and increased nutrient supply. Possibilities for eucheumatoid polyculture are

with giant clam, abalone and lobster (Gomez and Azanza-Corrales, 1988; Solis-Duran and

Inocencio, 1990; Manzano and Manzano, 1992).

Polyculture has been tried with the grouper Lates calcarifer (Hurtado-Ponce, 1992)

near Iloilo, Philippines, the pearl oyster Pinctada martensi (Qian et al., 1996) in China.

None of these systems are currently operating on a commercial scale. Other possibilities

for polyculture include sponges, corals, sea cucumbers, green snails and Trochus. Neish

and Ask (1995) suggested that expert systems could be developed for such integrated

mariculture projects.

Agronomic protocols refer to all the activities (site selection, planting, maintenance,

harvesting, culling and drying) which must be conducted in order to increase production

per unit time, effort, area and cost. Once a superior protocol has been proposed,

disseminating the technology and/or information to the farmers is critical and a more

difficult task. Standard agronomic protocols and criteria for site selection were developed

early, i.e. from the initial research effort to develop cultivation (Doty and Alvarez, 1973;

BFAR, 1974) and trial and error by a number of farmers (I. Neish’s comments in Doty,

1980). The importance of maintenance, still overlooked by most new farmers, was

recognized early on in cultivation development (Parker, 1974). These standard protocols

have changed little in the past 10 years. Most recent descriptions of these standard

procedures are those of Trono and Ganzon-Fortes (1989), Trono (1992) and Ask (1999).

Blakemore (1990) and Ask (1999) covered post-harvest handling (drying) in depth.

3.1. Site selection

Papers cited under the sections on biology, especially fundamental physiology

describing optimal light, temperature, salinity, nutrient and water motion requirements

are certainly important to consider in site selection. In addition, Mairh et al. (1986) looked

at water depth and found no significant difference in growth rate between E. striatum

grown at 0.25–2 m depth and those cultivated from 2.25 to 3.5 m. Exposure studies

indicated that K. alvarezii and E. denticulatum grew less when exposed at low tide than

those continuously submerged in similar environment in Tawi-Tawi, Philippines (Baltazar,

1992).

Non-biological criteria of shipping cost, politics, socio-economics, logistics, infra-

structure and demographics are also important to site selection (Ask, 1999) and hence,

need to be studied. Some of these factors directly related to farming are considered here.

3.2. Transport and introduction of commercial eucheumatoids

Commercial eucheumatoids will remain healthy at least 2 days if packed properly for

transport. A packing system in which commercial eucheumatoids arrived mostly

undamaged has been described (Azanza-Corrales and Dawes, 1989). Commercial

eucheumatoids could therefore be considered as hardy and will recover from stress of

transfer (Glenn and Doty, 1981). de Reviers (1989) reported the successful acclimatiza-

tion of K. alvarezii thalli from the Philippines to the Maldive Islands where 5 kg were


introduced and grew to 150 tons (fresh weight) within 12 months. Transport and intro-

duction was similarly successful in Indonesia (Adnan and Porse, 1987) and Tanzania

(Lirasan and Twide, 1993).

As Table 1 indicates, the commercial eucheumatoids have been introduced to numerous

locations in the world. Impacts of introduction were recorded by Russell (1983) in

Christmas Island, Kiribati and in Hawaii (Doty, 1978a). K. alvarezii and Gracilaria

salicornia were introduced to specific sites in Kane’ohe Bay in the 1970s and their

distributions have increased. Distributions have not been uniform and abundance of

Kappaphycus spp. has been highest on patch reefs. K. alvarezii and K. striatum have

spread 6 km from their points of introduction in 1974, an average rate of spread of

approximately 250 m/year (Rodgers and Cox, 1999). One of two scenarios usually unfold

with introduction, then abandonment of cultivation. In the first scenario, the plants

completely disappear, as has been the case in the Solomon Islands, Samoa and parts of

Fiji and the Kingdom of Tonga. Plants disappeared from certain lagoons and islands in

Tonga. Some continued to exist on the southern island of Tonga Tapu but not in the north,

where it was introduced for cultivation. Due, however, to herbivore pressure and other trial

farming problems, success has not been achieved. In the second, the plants go wild, never

attaching but tumbling around the local subtidal until lodged between rocks or coral or

settling into sandy ‘‘holes’’, where they can grow. In the latter case, in Fiji, the plants never

covered more than 5% of the subtidal in the local area of the previous farming activity and

were never found 500 m from the point of introduction (Ask et al., 2001).

In only two cases that the authors know of, the Solomon Islands (Smith, 1990) and

Brazil (de Paula et al., 1998) were proper introduction procedures developed and followed.

For most introductions, no quarantine or introduction procedures were used, e.g. Indonesia

(Adnan and Porse, 1987), Tanzania (Lirasan and Twide, 1993) and the Maldives (de

Reviers, 1989). Though no known catastrophic impacts have been recorded, Ask et al.

(2001) have created a practical and effective quarantine procedure which should publi-

cized and utilized for further introductions.

3.3. Culling and tying

Eucheuma thalli have large diameters, in excess of 2 cm, and can be cut and tied to

monolines individually, hence, these plants have been propagated vegetatively for many

years. E. denticulatum tends to be brittle and when handled in bulk, large numbers can be

damaged hence, proper handling is important (Ask, 1999). Cutting propagules of new

tissue from large harvested plants is necessary (Ask, 1999) and cultivation handbooks

(Juanich, 1988; Trono and Ganzon-Fortes, 1989) proposed slicing the plants perpendicular

to the thallus with clean, stainless steel blade. K. striatum fragments (1.0-cm diameter) cut

obliquely have been found to have higher growth rates than transversely cut apices and

that apical tissue grew faster than basal and median fragments (Mairh et al., 1995)

implying that well branched propagules with numerous tips would be superior for

replanting. Eucheuma alvarezii can completely recover from wound, healing in 22 days

in the laboratory, but must be faster in the field (Azanza-Corrales and Dawes, 1989).

Introduced in 1971, the monoline method is now ubiquitous and involves tying the

propagules loosely since rigidly/closely attached propagules have been found to have


poorer growth response (Glenn and Doty, 1992). Loosely held plants are able to move and

orient with the water current. Cultivation techniques, specifically stocking density,

propagule size, line spacing, maintenance and seedstock preparation and selection have

also improved from early efforts (Padilla and Lampe, 1989).

Though there are certainly hard and fast rules to cultivating eucheumatoids, it is also

very important to remember that most protocols, such as spacing, grow out period,

propagule size, planting depth, and line spacing are site- and season-specific. For every

site and season, a round of agronomic experiments should be carried out to determine

appropriate agronomic protocols to maintain high production throughout the year for that

area (Ask, 1999).

4. Farm ecology

4.1. Seasonality

Since cultivation of the commercial eucheumatoids began, seasonal patterns to growth

have been noted (Doty and Alvarez, 1975). The ability to mitigate or completely

eliminate the negative effects of seasonal growth patterns so that year round growth

rates and carrageenan quality could be maintained at high levels would be considered an

advance.

To understand the seasonal patterns, one must first implement a crop log program,

where both eucheumatoid plant parameters (e.g., growth rate, incidence of ice–ice and

plant loss) and environmental parameters (e.g., temperature, water motion and salinity) are

monitored for at least 1 year. A classic example is the 55-week study of Glenn and Doty

(1990) that noted wind direction as the primary factor correlating to growth. In similar

studies, Ohno et al. (1994) found that temperature was crucial to growth of K. alvarezii,

while Trono and Lluisma (1992) reported the seasonal patterns of growth and carrageenan

yields but no correlations of these data were made with environmental changes. All three

studies found different factors, or no recorded factors, as influencing the so-called

eucheumatoid or plant parameters. Since such factors are site-specific, a few of the

primary factors that decrease production substantially can be deemed seasonal, and will be

discussed in the succeeding sections.

The physical and chemical factors affecting the growth of these plants have been

discussed earlier in relation to the crop’s physiology. As in other types of aquaculture/

agriculture, monsoons or seasonal events can exert major environmental changes on a

farming site. If the plants exhibit poor performance during certain months of the year due

to extreme changes of environmental factors as salinity, temperature and nutrient

availability, and very little or nothing can be done, a relocation of the farming site should

be considered.

Maintaining test plots at various locations will allow the farmer to know where to move

the farm (Ask, 1999). Other options include harvesting and selling before the unfavorable

environmental condition set in and leaving some thalli in a relatively ‘‘safe’’ environment

to wait for a favorable season for planting (Ask, 1999). Crop logging is crucial to

developing the ‘‘pro-active’’ techniques described here.


4.2. Epiphytes

Pest weeds were noted as a serious problem since cultivation of Eucheuma spp. began

(Parker, 1974). During 25 years, not only has little work been done to alleviate this

problem, but also the problem has not been thoroughly described or studied. Fletcher

(1995) provides a useful and related review on the impacts of pest weeds on Gracilaria

cultivation. Two types of pest weeds can be recognized: large algae/seaweeds that grow

over the farmed plants and epiphytic filamentous algae (EFA), which as the name implies,

grow attached to the crops (Ask, 1999).

Understanding the factors that drive the seasonality of pest weed blooms and under-

standing the interaction between them and commercial eucheumatoids could lead to novel

and effective management protocols. Current protocols (Ask, 1999) for managing pest

weeds are to note the seasonal patterns and when they appear, remove them manually as

quickly as possible before they reproduce and spread. Removed pest weeds should be

taken to land and could even be used as compost material.

EFAs constitute numerous species of filamentous algae that attach to the cortical layer

of the host thalli. They can leave the eucheumatoids stunted, rough and poorly branched

(Ask, 1999). At the moment, the only management scheme is to harvest infested

propagules of commercial eucheumatoids and replace them with propagules from another

location that are uninfested (Ask, 1999).

4.3. Herbivory

Like pest weeds, herbivory was noted as a major problem for farmers since the

beginning of eucheumatoid cultivation (Doty, 1973; Parker, 1974; Doty and Alvarez,

1981). Though the problem has been mentioned over the years, published information

describing the problem and detailed studies to combat the problem are limited.

Fish selectively graze smaller branches of commercial eucheumatoids (Russell, 1983;

Uy et al., 1998). Juvenile scarids and acanthurids have been observed to consume as much

as 50–80% of the Eucheuma population at 0.5 and 2.0 m depth, resulting a loss of 10–20

tons/month in the farm (Russell, 1983). Bags of 100 g of para-dichlorobenzene can be tied

at intervals on the farm to deter fish grazing (Doty, 1978b). Also, the impact of the urchins

Diadema setosum and Tripneustes gratilla could be lessened by either killing them

outright or releasing a heavy cloud of lime in a line or band at the up stream edge of a

planting area (Doty, 1978b). Doty (1978a) also noted that in areas heavily fished, there

was little problem with the grazing turtle Chelonia midas.

Ask (1999) has categorized the herbivores into four groups based on type of damage:

(1) ‘‘tip nippers’’, which are various fish, including adult siganids, that eat the thalli tips;

(2) ‘‘pigment pickers’’, which are solely juvenile siganids and eat the outer pigmented

layer of cells; (3) ‘‘thalli planers’’, which are particular sea urchins, especially T. gratilla;

and (4) if the entire propagule is missing, except for a bit around the tie–tie, one can

suspect the green turtle, C. midas.

Over the years, a few studies described counter measures (Mtolera et al., 1996; Ohno

et al., 1994). More thorough studies identifying the perpetrators, their seasonal popula-

tion patterns, biology and feeding habits would be more helpful. Studies on the impact of


herbivory as percentage crop loss and work on anti-herbivory devices are likewise needed.

A few methods that could possibly be developed to lessen or eliminate the impact of

herbivores are listed in Table 4.

4.4. Diseases

‘‘Ice–ice’’ has been identified as a major problem for eucheumatoid farmers (Doty and

Alvarez, 1975; Uyenco et al., 1981). The term ‘‘ice–ice’’ was coined by Filipino farmers

by using the English term ‘‘ice’’ to describe the senescent tissue devoid of pigment that

causes healthy branches to break off.

Early on, stress was identified as the major factor promoting ice–ice and Doty (1978b)

also noted that there is a direct correlation between its occurrence and those of epiphytes.

Uyenco et al. (1981) noted high populations of bacteria found on propagules with ice–ice

but that they were secondary to the problem. Doty (1987) also noted that the occurrence of

ice–ice in commercial eucheumatoids is seasonal and possibly correlates with changes in

monsoon wind patterns (Doty and Alvarez, 1975).

Largo et al. (1995b) showed that certain bacteria appeared capable of inducing ‘‘ice–

ice’’, especially in stressed propagules. Largo et al. (1995a) showed that light intensity of

less than 50 mmol photon m�2 s and salinity of 20 ppt or less induces ‘‘ice–ice’’

development in K. alvarezii transplanted from Danajon Reef, Philippines to the sub-

tropical waters of southern Japan. Moreover, wide-scale whitening leading to complete

damage of the branches was caused by temperature of up to 33–35 �C. Thus, theseexperiments have shown that abiotic factors can induce ‘‘ice–ice’’ development.

E. denticulatum has been observed to produce volatile halocarbons (VHC) under high

light and CO2 deficient environments (Mtolera et al., 1996). High quantities of VHC

can become toxic to plants and produce diseases as in G. cornea (Pedersen et al., 1996),

thus ice–ice is a result of stress and prevention must focus on stress reduction in the

form of superior site selection and following proper farm protocols as outlined by Ask

(1999).

As emphasized in this paper, crop logging programs can help elucidate seasonal growth

patterns and correlate that to all recorded environmental parameters including possible

interaction between them, e.g. role of pest weeds, herbivores and ‘‘ice–ice’’ as causes of

Table 4

Possible methods for combating herbivory

Category Description

Avoidance Plant outside herbivores’ natural habitat, e.g. float to avoid urchins and bottom

dwelling fish, away from coral heads to avoid reef bound herbivorous fish

Barriers Gill nets, cages, barrier nets

Auditory Underwater noise makers to frighten fish

Visual Scare lines or plastic/wood models of predators

Electrical Electrical signals emulating predators

Chemical Compounds that deter herbivores such as those produced by algae that are not

susceptible to herbivores


seasonal growth. Another possible method to combat stress and disease is to develop

strains (either through breeding programs or transgenic methods) that are hardier.

5. Crop improvement: genetics and strain selection

It has been noted that since the inception of cultivation in 1970, there has been a

decrease in hardiness and carrageenan quality of the cultivated varieties (Trono and Ohno,

1989; Trono and Lluisma, 1992). In this regard, hardier, faster growing and higher yielding

strains could result in a 2% increase in growth rates per day and would triple the net yield

over a 6-week grow out period. Strain improvement in eucheumatoid cultivation focuses

on two goals—higher yields of high quality carrageenan and higher and sustained seasonal

growth rates year round. The latter goal could be manifested as resistance to herbivory,

pest weeds and stress-induced senescence. Strains could be developed through selection of

wild varieties, breeding programs and genetic manipulation or transgenic production/

development.

Of the three species covered in this paper, K. alvarezii var. tambalang is the most

widely cultivated crop (Ask, 1999). It has been described as tough, fast growing and high

yielding and was developed through a strain selection program of wild plants (Doty and

Alvarez, 1975; Doty, 1987). Similar programs have been conducted on K. striatum

(Mollion and Braud, 1993) and E. denticulatum (Adnan and Porse, 1987; Lirasan and

Twide, 1993).

K. alvarezii and E. denticulatum have formed variants of green, red and brown forms

(Trono and Lluisma, 1992; Dawes, 1992) but little is known about possible causes of color

differences. For. K. alvarezii, Azanza-Corrales (1990) noted that the colors are retained by

the brown, green and red strains and that the shades probably vary with the season or

ambient light. Studies on seasonal growth rate and carrageenan yields have been

conducted on the color varieties of K. alvarezii and E. denticulatum (Azanza-Corrales

and Sa-a, 1990; Trono and Lluisma, 1992; Dawes et al., 1994).

In addition to color, varieties based on branch appearance have been noted for K.

alvarezii (Doty, 1985a, 1988) and E. denticulatum (Doty, 1985b) and tested for cultivation.

Examples of varieties of K. alvarezii and K striatum currently cultivated today are

alvarezii, tambalang, elkhorn, dichotomous variety (a.k.a. ‘‘sakol’’). Cultivated varieties

of K. alvarezii, K. striatum and E. denticulatum have been developed in Madagascar,

Tanzania and Indonesia as well as the Philippines.

Techniques for branch culture, micropropagation and callus production of K. alvarezii

and E. denticulatum have been developed (Dawes and Koch, 1991; Dawes et al., 1993)

and would probably be necessary for a low-cost breeding and selection program. Practical

applications of these techniques for maintenance and disbursement have, however, not

been developed.

No transgenetic work has been done that has produced improved strains in eucheu-

matoids with respect to growth and/or carrageenan. Nicholl (1996) pointed out that

‘‘successful genetic manipulation’’ of plants requires: (i) methods for introducing genes

into plants, and (ii) a detailed knowledge of the molecular genetics of the system that is

being manipulated. However, protoplast fusion techniques have been developed for both


E. denticulatum and K. alvarezii. Cheney et al. (1998) claim to have created new strains of

both species with superior growth rates, up to 14% per day at the laboratory.

Kapraun and Lopez-Bautista (1997), realizing the need for knowledge of the genetics,

have studied the karyology and begun quantifying and characterizing the nuclear genome

of K. alvarezii, K. striatum and E. denticulatum. Based on tetraspore mother cells during

diakinesis, aceto-carmine stain revealed that both K. alvarezii and E. denticulatum have a

chromosome number of N = 100. No recent results have been presented on genetic strain

selection/development programs for the commercial eucheumatoids. de Paula et al. (1999),

however, has shown that tetraspore progeny can be used for strain selection in K. alvarezii.

The fields of horticulture and agronomy have successfully utilized genetic engineering

techniques to develop transgenic varieties and this may prove to be a valuable model for

eucheumatoid cultivation. However, concerns over genetically modified organisms for

human consumption will probably preclude this. The Porphyra cultivation industry,

pursuing a selective breeding program, has been quite successful at developing numerous

improved strains (Van Der Meer, 1990), and this provides guidance for commercial

eucheumatoids.

6. Recommendation

The people involved in developing commercial eucheumatoid farming in the late 1960s

probably had no idea how successful this industry would become, with well over 100,000

Mt dry of commercial eucheumatoids produced annually from five nations and with

perhaps 50,000 families employed. In addition, by cultivating commercial eucheumatoids,

the carrageenan business was revolutionized with a steady supply of relatively uniform raw

material. However, 30 years on, the carrageenan industry is still faced with raw material

problems relating to quality, supply and volumes. It is time to make concerted efforts to

assure a continuing prosperous future for the cultivation industry and hence the carra-

geenan industry. Demand for raw material continuous to grow as new market develops.

There has been little support from the industry since only a number of companies has

been engaged in research and development for raw material development. It is important

that research be done in vital areas, namely: increasing per farmer production (decreasing

labor costs and sustaining high growth rates year-round) and increasing quality of extract

through superior post-harvest handling and strain improvement. Only this will ensure a

bright future for the carrageenan industry including the tens of thousands of farmers

throughout the world and the nations that have come to depend on the numerous benefits

derived from commercial eucheumatoid cultivation.

Acknowledgements

Support for the Eucheuma/Kappaphycus researches of the second author has been

provided by the International Foundation for Science (IFS), the University of the

Philippines Diliman and the Department of Science and Technology’s Philippine Council

for Aquatic and Marine Research and Development (DOST-PCAMRD). The assistance of


Lilibeth N. Miranda and Marites T. Barrientos in typing the manuscript is gratefully

acknowledged. Help extended by seaweed farmers in the countries (Philippines, Indonesia,

etc.) we have worked in is also acknowledged. We are thankful to Dr. Clinton Dawes for

suggestions on the improvement of the paper.

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