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Growth of the seaweeds Kappaphycus alvarezii, K. striatum and Eucheuma denticulatum as affected by environment in Hawaii
84 (1990) 245-255 Elsevier Science Publishers B.V.. Amsterdam
245
Aquaculture,
-
Printed
in The Netherlands
Growth of the Seaweeds Kappaph ycus alvarezii, K. striatum and Eucheuma denticulatum as Affected by Environment in Hawaii EDWARD P. GLENN” and MAXWELL “Environmental bDepartment
(Accepted
Research of Botany,
Laboratory, University
S. DOTYb
2601 E. Airport
Drive, Tucson, AZ 85706 (U.S.A.)
of Hawaii at Manoa, Honolulu,
HI 96822 (U.S.A.)
27 June 1989)
ABSTRACT Glenn, E.P. and Doty, MS., 1990. Growth of the seaweeds Kappaphycus alvarezii, K. striatum and Eucheuma denticulatum as affected by environment in Hawaii. Aquaculture, 84: 245-255. Three commercial gel-producing seaweed species native to the Philippines were grown experimentally in pens on an algal reef-flat in Kaneohe Bay, Oahu, Hawaii. Growth rates and environmental conditions were measured for 55 consecutive weeks. The normal northeast trade winds created a flow of water through the 272-m’ farm, one side of which faced northeast. Upstream thalli of Kappaphycus alvarezii grew at an average relative growth rate of 5.06%/day, whereas K. striatum and Eucheuma denticulatum grew at 3.5O%/day. These growth rates and the overall productivity of 20.8 tonnes dry wt/ha per year were similar to those obtained on Philippine reefflat farms. Growth rates tended to be independent of season, and correlations between growth rates and environmental variables were low. The study suggested a range of conditions under which these eucheumatoids can be productive in a farm setting: temperature maxima of 24-30°C and minima of 21-22°C; nitrogen levels of 2-4 ,ug-atm/l; phosphate levels of 0.5-1.0 pg-atm/l; and high solar energy levels. The pH and salinity were near 8.0 and 32 ppt, respectively, throughout the study period. The degree of water motion per se was not correlated with growth rate but the direction of wind across the farm was important. Downstream thalli generally appeared unhealthy and grew at half the rate of upstream thalli. When the normal trade winds reversed, the (formerly) upstream thalli grew poorly. None of the measured environmental factors was correlated with the downstream growth reduction, and its cause remains unknown.
INTRODUCTION
The red algal genera Kuppuphycus and Eucheuma are farmed on tropical reef-flats for their polysaccharide, carrageenan. Cultivation of these red seaweeds started in The Philippines as an alternative to harvesting the wild crop (Doty, 1973; Parker, 1974). Test plantings of these eucheumatoids also have
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E.P.GLENNANDM.S.DOTY
been successful in Hawaii (Doty, 1977; Glenn and Doty, 1981; Russell, 1983), Indonesia (Braud and Perez, 1979; Adnan and Porse, 1987), China (Liu and Ping, 1984 ) , Fiji (Luxton et al., 1987 ), Florida (Dawes et al., 1976) and even in subtropical waters off Japan during warm seasons (Mairh et al., 1986). However, commercial farming has not spread far from its point of origin. Most farmed crop still comes from The Philippines (Doty, 1986)) with less coming from Indonesia and a little for internal use being grown in Hainan, China. One hindrance to farming these seaweeds has been the difficulty of finding productive farm sites. It is generally assumed that the species require warm sea temperature, high light levels, nutrient-enriched water, and a high degree of water motion driven by waves or tides. However, the attributes of a successful farm have not been satisfactorily quantified, and new farms are sited largely subjectively. The present study was designed to better define the range of environmental conditions under which three commercial seaweeds are productive in a farm setting. MATERIALS
AND METHODS
Kappaphycw aluarezii (Doty)Doty ( = E. striatum var. tambalang, Glenn and Doty, 1981; = E. striatum Schmitz, Russell, 1983), K. striatum (Schmitz) Doty ( = E. striatum var. elkhorn, Glenn and Doty, 1981) and E. denticulutum [ BurmanlCollins & Hervey ( = E. spinosum) (see Doty, 1988 for full taxonomit descriptions) were transplanted from The Philippines to an experimental seaweed farm in Kaneohe Bay, Oahu, Hawaii. In the following text these three species are referred to by their colloquial names, respectively, tambalang, elkhorn and spinosum. They were grown in pen culture on the north reef of Coconut Island, Oahu, near the Hawaii Institute of Marine Biology research station. The farm was sited over light-colored sand on a section of reef-flat covered with approximately 10 cm of water at the lowest tide and 1.5 m at the highest tide. The pens were made of plastic-coated 2.5 cm wire-mesh fence material 1 m high. Each pen was 3.3x3.3 m square. The farm was made up of 25 pens forming a square of 5 rows of 5 pens each, with the runs set on a northwest-tosoutheast axis, and occupied a total area of ca. 272 m2. The normal flow of water across the reef was driven to the southwest by northeast trade winds. Consequently, the row of pens on the northeast side was designated the upstream row while the opposite (southwest) side was designated as downstream. Under normal trade wind conditions water flowed into the seaweeds through the upstream pens. More detailed descriptions of the farm are given by Doty ( 1977) and Russell ( 1983 ). Loose thalli of all three seaweeds were grown within the pens. At irregular intervals the pens were partially harvested to allow room for regrowth. The three species were mixed together in each pen, and at each harvest some of
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
247
each was left behind as seedstock. The three middle rows of pens were allowed to become densely packed with algae before they were harvested. However, the upstream and downstream rows, where growth measurements were made, were tended on a weekly basis, to keep the test thalli free from shading and crowding. Thalli removed from these pens were combined with thalli in the middle rows of pens. Growth rates and environmental factors were measured for 55 consecutive weeks from 27 May 1976 to 15 June 1977. The measurements were taken the same day each week. Maintenance was done at sampling time and consisted of repairing the fences and removing epiphytes (mainly Enteromorpha) from the upstream row of pens. Enteromorpha grew profusely on the fence material but not on the seaweeds themselves. Growth of the seaweeds was measured by weighing individual tagged thalli of each species. The tagged thalli were secured by two methods. Thalli were either tied to a piece of fence material on the ground (lawn planting) or tied to a l-m length of string attached to the fence, which allowed some degree of movement of the thallus within the pen (pen planting). Since the two planting methods gave nearly identical average growth rates, the results were combined for all statistical analyses. The same thalli were generally weighed each week. If a thallus was lost or damaged, it was replaced with a new thallus from the loose seaweeds in the pen. The tagged thalli were kept in the range of 150 to 500 g wet weight by trimming them as necessary after they were weighed. After weighing and trimming, the tagged thalli were returned to their original positions. Ten tagged thalli of each species were in the upstream row of pens (two per pen) and ten were in the downstream pens (two per pen). The results were averaged so that each algal species was represented by two data points per week: upstream and downstream, with each datum the average of ten thalli. Relative growth rate was calculated using the formula RGR = (In final wt - In initial wt)/time and expressed as % growth per day. Water motion was measured with clod cards (Doty, 1971). Two clod cards were placed in an upstream pen and two in a downstream pen each week and collected 24 h later. The diffusion increase factor (DIF) was calculated by the ratio of weight lost compared to a clod card in still water. Oxygen was measured weekly for four samples taken from two upstream and two downstream pens; samples were fixed with permanganate solution in the field at the time of collection and titrated for oxygen content in the lab using the Winkler method (Strickland and Parsons, 1972 ). Four samples of water were collected weekly from two upstream and two downstream pens for determination of ammonia, nitrate and phosphate; these samples were delivered to the Hawaii Institute of Marine Biology analytical laboratory within 30 min of collection, where they were filtered immediately and frozen for later analyses using a Technicon Autoanalyzer.
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E.P. GLENN AND M.S. DOTY
Water temperature was measured using maximum-minimum thermometers at the upstream and downstream ends of the farm. Air temperature and wind velocity were recorded hourly at the Kaneohe Marine Corps Air Station, which operated a weather station nearby on Kaneohe Bay. The daily maximum and minimum temperatures were averaged to obtain weekly values. Wind direction and velocity were averaged by week and expressed as the north wind vector in knots per hour (velocity xcos 0, where 8 is the angle of the average wind velocity with respect to north). Transformation of the data produced a positive number for wind velocity when the normal trade winds were blowing and a negative number when the winds reversed and blew from the south. Light energy was measured in Honolulu, about 20 miles away, by the National Weather Service, Pacific Region, and was averaged by week. Salinity was measured with a hand-held refractometer (A/O Special Scale Model) accurate to 2 ppt. The pH was measured with a portable Beckman pH meter by placing the electrode in water in the upstream and downstream pens; the meter was accurate to 0.2 pH units. The total biomass production of the farm was estimated for the year by adding up the amount of seaweed harvested from the pens. The farm was partially harvested twice during the study and completely harvested (and dismantled) at the completion of the study. Statistical analyses were conducted using programs in MSTAT (Michigan State University, Lansing, MI). Differences between means were compared using Student’s t-test. Correlation coefficients were calculated using Pearson’s r. RESULTS
Appearance and growth rates of seaweeds Usually there was a striking difference in appearance of upstream and downstream thalli of all three species. Upstream thalli were large and darkly pigmented compared to downstream thalli, which were straw colored. Downstream thalli were also more fragmented than upstream thalli (a consequence of ice-ice, the necrosis of narrow bands of tissue which causes the thalli to break apart). The first three rows of pens contained healthy-appearing thalli whereas the last two (downstream) rows contained unhealthy-appearing thalli. When healthy-appearing thalli were placed in downstream pens, they lost their dark pigmentation by the following week. Table 1 gives means and standard deviations of growth rates averaged over the study. Downstream growth rates averaged only half the upstream rates and the differences were significant for all three species (P < 0.01). Upstream thalli of tambalang grew 45% faster than the other two species (PC 0.01). Seasonal fluctuations in growth rates were small compared to the week-toweek variations. However, tambalang grew approximately 15% faster in sum-
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GROWTH OF THREE SEAWEED SPECIES IN HAWAII
TABLE 1 Seaweed growth rates (% per day) and standard deviations (s.d.) for three species of algae obtained in Kaneohe Bay, Hawaii, during 55 consecutive weeks Species
Condition
Growth rate
s.d.
Tambalang Elkhorn Spinosum Tambalang Elkhorn Spinosum
Upstream Upstream Upstream Downstream Downstream Downstream
5.06 3.51 3.52 2.07** 1.43** 2.29**
1.34 1.05 1.36 1.05 0.71 1.21
**Significant
differences
between upstream
and downstream
growth rates at PC 0.01.
TABLE 2 Seasonal growth rates (% per day) and standard deviations (in parentheses) of seaweeds in Kaneohe Bay, Hawaii. Summer, 22 June to 21 September; fall, 22 September to 21 December; winter, 22 December to 21 March; and spring, 22 March to 21 June Species
Tambalang Tambalang Elkhorn Elkhorn Spinosum Spinosum *Significant
Condition
Growth rate
Upstream Downstream Upstream Downstream Upstream Downstream differences
Summer
Fall
Winter
Spring
6.23 (0.95) 1.94(1.23) 3.33 (0.98) l.OO(O.71) 4.05(1.33) 2.70(1.18)
4.41*(0.93) 2.43(0.92) 2.98(0.&j) 1.47(0.83) 3.52(1.17) 2.22(1.49)
4.15*(1.35) 2.27 (0.95) 3.76( 1.23) 1.75(0.65) 3.36( 1.57) 2.23(1.26)
5.25(1.24) 1.92(0.99) 3.95(1.16) 1.61(0.77) 3.05(1.24) 2.00(0.86)
between summer and the fall and winter values at P < 0.05.
TABLE 3 Correlation coefficients between growth rates of seaweeds grown at the upstream or downstream rows of the experimental seaweed farm in Kaneohe Bay, Hawaii, over 55 consecutive weeks Tambalang UP Tambalang Tambalang Elkhorn Elkhorn Spinosum *Significant
UP Down
Elkhorn Down
Up
Down
Up
Down
0.004
0.520** -
0.700* 0.182
0.461** 0.372** -
0.456** 0.300* 0.409**
UP Down UP at P < 0.05; **significant
Spinosum
at P< 0.01.
250
E.P. GLENN AND MS. DOTY
mer than in winter and fall (PcO.05) (Table 2). There was a moderate correlation among growth rates over the study (Table 3 ). A total of 3600 kg wet weight of seaweed was harvested from the farm, equivalent to an annual production of 130 tonnes/ha. The dry weight of the thalli averaged approximately 16% of the wet weight; hence the production was equivalent to 20.8 tonnes/ha per year of dry matter. The standing density of seaweeds in the pens at the terminal harvest was 7.5 kg/m*. The individual species were not separated when the pens were harvested, but elkhorn and spinosum thalli were noted to be much less abundant in the harvested material than tambalang thalli. Environmental parameters Table 4 gives means and standard deviations of upstream and downstream water quality factors, as well as maximum and minimum air temperatures, light energy, and the velocity of the northerly component of the wind. There were only two significant differences between upstream and downstream measurements: oxygen levels and degree of water motion. The oxygen level was 1 ppm higher in the downstream pens (PC 0.05), presumably due to the photosynthesizing mass of seaweeds in the intervening pens. Water motion was 20% lower downstream than upstream (PC 0.01 ), presumably due to the obstruction of the current by the mass of seaweeds in the pens. Water temperature closely paralleled air temperature. The max/min thermometers left in the water were occasionally lost, resulting in an incomplete data set. Hence, only the air temperatures were used in further statistical analyses. Oxygen content was the only water-quality factor that showed an obvious seasonal trend, being lowest in winter. Ammonia, nitrate and phosphate concentrations tended to have stable base levels punctuated by irregularly occurring very high levels. The pH and salinity were relatively constant over the study, within the range of accuracy of the instrument used for measurement; pH was 8.0 to 8.2 and salinity was 32 to 34 ppt upstream and downstream. The weekly mean maximum/minimum air temperature ranged from a low of 21 oC to a high of 27 QC with little seasonal fluctuation. Light energy showed a seasonal trend, with the winter minimum being half that of the summer maximum. The strength of the trade winds varied from week to week, but the north vector was strongly negative during only 6 weeks. The most prolonged period of southerly winds was during January and February. Correlations between growth rates and environmental factors A correlation matrix was calculated relating upstream and downstream growth rates of the three seaweeds to the environmental factors (Table 5). Eight of the correlation coefficients were statistically significant (P < 0.05 ) . However, the coefficients of determination (r’) were all low. No single envi-
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
251
TABLE 4 Environmental and water-quality factors measured at the upstream and downstream ends of the Kaneohe Bay, Hawaii, seaweed farm. Data could not be collected for some of the variables in some weeks, making the number of observations less than 55 for some variables Mean Nitrate (,ng-atm/l) Upstream Downstream Ammonia (pg-atm/l) Upstream Downstream Phosphate (pg-atm/l) Upstream Downstream Water motion (DIF)a Upstream Downstream Oxygen (mg/l) Upstream Downstream Air temperature ( ‘C ) Maximum Minimum Water temperature ( ‘C 1 Upstream max. Upstream min. Downstream max. Downstream min. Light energy (g Cal/cm* per day ) North wind velocity (knots/h) “DIF = diffusion increase factor. *-**Significant differences between **p
s.d.
Number
1.44 1.10
1.11 0.97
51 51
1.98 2.01
2.17 2.21
44 44
0.66 0.62
0.29 0.27
51 51
44.9 37.6* 7.22 8.25*
13.0 10.8
53 53
1.99 2.15
53 53
27.6 20.8
1.10 1.60
55 55
27.7 22.6 28.0 23.1 371 1.83
1.54 1.21 1.31 1.40 18 2.17
46 46 46 46 55 45
upstream
and downstream
measurements
at *PC 0.05 or
ronmental factor explained more than 20% of the variation in any seaweed growth rate. Upstream tambalang growth rate was positively correlated with light level and phosphate level, whereas upstream elkhorn growth rate was negatively correlated with maximum and minimum air temperature. Downstream tambalang growth rate was negatively correlated with ammonia and phosphate and positively correlated with water motion, whereas downstream elkhorn growth rate was negatively correlated with phosphate. None of the correlation coefficients for upstream or downstream spinosum was statistically significant. Stepwise multiple linear regression analyses did not significantly improve the correlation between growth rate and environmental variables for any species. None of the resulting equations could account for more than 25%
E.P. GLENN AND MS. DOTY
252 TABLE 5
Correlation coefficients between upstream and downstream growth rates and environmental rameters measured over 55 consecutive weeks in Kaneohe Bay, Hawaii
pa-
Growth rate Elkhorn
Tambalang
Light energy Max. air temp. Min. air temp. Water motion North wind Nitrate Ammonia Phosphate Dissolved oxygen *Significant
Spinosum
UP
Down
UP
Down
Up
Down
0.341** -0.193 0.208 - 0.047 0.283 - 0.043 - 0.038 0.476** -0.159
- 0.294 0.068 -0.031 0.318* 0.086 0.086 - 0.425** - 0.343 - 0.039
0.206 - 0.448** -0.317* 0.152 0.275 -0.132 0.029 0.111 0.040
-0.178 -0.181 - 0.264 0.123 - 0.082 0.048 -0.146 - 0.350* 0.253
- 0.055 0.002 0.084 - 0.026 0.130 0.216 -0.187 - 0.009 - 0.209
- 0.032 -0.114 0.177 -0.061 0.027 0.026 -0.277 0.030 0.071
at P < 0.05; **significant
at P < 0.01.
of the variation in growth rate regardless of which combination of independent variables was tried (data not shown). Growth rates and environmental factors during a period of prolonged wind reversal The differences in appearance of upstream and downstream thalli tended to reverse when the normal northeasterly trade winds failed and wind blew from the south. Normally the wind reversals last for only a few days, but one lasted for a month and was studied in detail with respect to algal growth rate and environmental factors. Data obtained during this period (weeks 32 to 34) were compared to data over the entire study (Table 6). The upstream growth rates of all three seaweeds were much lower than normal during the wind reversal and were depressed for several weeks after the trade winds returned. Downstream growth rates did not change significantly during the period of wind reversal, although by the end of the period the downstream tagged thalli had increased in pigmentation and looked healthier. North wind velocity during this period became negative but of the same magnitude as during the rest of the study. The flow of water through the pens reversed as a result of the wind reversal, but none of the water quality factors changed significantly. Downstream oxygen level remained higher than upstream level except for week 34, when the upstream measurement was 11.8 ppm and the downstream measurement was 8.8 ppm. Water motion was within
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
253
TABLE 6 Seaweed growth rates and environmental factors (standard deviations in parentheses) upstream and downstream in Kaneohe Bay, Hawaii, during the major period of wind reversal (5 January to 2 February 1977)
Growth rates (%/day) Tambalang Elkhorn Spinosum Water motion (DIF) Nitrate-N (pg-atm/l) Ammonia-N (pg-atm/l) Phosphate-P (p-atm/l) North wind (knots/h) PH Salinity (ppt) Oxygen (mg/l) **Values significantly
different
Upstream
Downstream
2.78 2.38 2.08 40.7 0.80 2.13 0.51 - 1.88 8.0 32 7.79
1.51 1.41 1.39 36.1 0.48 2.05 0.47 - 1.88 8.0 32 8.95
(0.44)** (0.54)** (1.25)** (17.4) (0.26) (1.42) (0.06) (2.38)** (0.2) (2) (2.28)
(0.62) (0.30) (0.78) (15.7) (0.11) (1.40) (0.10) (2.38) (0.2) (2) (0.72)
from mean values over the total study period at P-c0.01.
the normal range upstream and downstream throughout the period of southerly winds. DISCUSSION
Kaneohe Bay appears to be a fertile site for eucheumatoid cultivation. A growth rate of 3.5% per day is considered good in commercial cultivation (Parker, 1974; Braud and Perez, 1979; Liu and Ping, 1984; Adnan and Porse, 1987; Luxton et al., 1987). Upstream tambalang exceeded this target figure by 45% and upstream elkhorn and spinosum matched the target figure. The total biomass output from the farm exceeded that of commercial farms in The Philippines, which have been estimated to produce from 4.5 tonnes/ha dry weight (Miura, 1980) to 13 tonnes/ha (Parker, 1974; Doty, 1986). Much higher productivities have been extrapolated based on growth rate data not only for eucheumatoids (Doty, 1973; Parker, 1974) but Gracilmia and other red seaweeds (LaPointe and Ryther, 1978; DeBusk and Ryther, 1984; Hanisak, 1987) but yields as high as the present ones have rarely been achieved on farms or in large-scale culture (Hanisak, 1987). It is not known how many modules of the size tested here could be placed on a hectare of reef-flat and farmed productively, given the growth inhibition observed within the 25 pens at the downstream end of the farm. The production of these seaweeds is seasonal in many regions, but growth rates in Kaneohe Bay were high throughout the year, except when the trade
254
E.P. GLENN
AND
MS.
DOW
winds failed. There were approximately 45 days of lowered production due to wind reversal during the 55 weeks of this study. The results suggest a range of environmental values over which good eucheumatoid growth can be expected (although even better growth cannot be excluded outside this range of values). Ammonia and/or nitrate levels in the range of 1-2 p-atm/l were sufficient as nitrogen sources; 0.5-1.0 fi-atm/l of phosphate was sufficient as a phosphorus source. Even lower nutrient levels can support Eucheuma growth; Dawes et al. (1976) found a positive growth response to nitrogen but not phosphorus for what is now called E. isiforme var. denudatum at levels one tenth those measured in Kaneohe Bay. Diurnal minimum and maximum temperatures averaging 21°C and 28”C, respectively, supported high growth rates of these three species, and there was no evidence of growth limitation due to temperature at any time of year. Mairh et al. (1986) found that elkhorn did not grow at temperatures below 20°C in Japanese coastal waters, whereas we previously reported (Glenn and Doty, 1981) the photosynthetic temperature response of all three species increased up to 32 ‘C, then sharply declined. The correlation between light levels and growth of tambalang and its greater growth rate in summer and spring than in winter and fall suggest that light may become limiting for this species. Tambalang thalli tied to a line extending over the reef into deep water grew fastest just below the surface, and growth rate declined with depth and decreasing light intensity (Russell, 1983) as did photosynthetic capacity (Glenn and Doty, 1981). Water motion per se was not correlated with growth rate nor was the velocity of the wind, so long as it blew from the north or northeast. However, the direction of the wind appeared to be the most important factor in the growth of the seaweeds. Downstream growth rate was severely depressed compared to upstream during normal wind conditions, and when the winds reversed, upstream growth rate decreased rapidly to a low level. Presumably the wind affected the algae by reversing the direction of water flow through the pens. However, one of the measured water quality factors changed significantly during the wind reversal. The cause of the downstream growth inhibition was not discovered. There was no strong evidence for a nitrogen or phosphorus limitation. Dense seaweed cultures may become limited by the diffusion rate of carbon dioxide into the water (DeBusk and Ryther, 1984) but in this study pH, which is an indicator of carbon dioxide level, did not change appreciably and the oxygen content rose by only 1 ppm, on average, in the passage of water through the farm. Hence it is unlikely that carbon limitation was the cause of the downstream growth inhibition. It has been noticed by others that seaweeds grown in dense cultures exhibit autoinhibition of growth, due to the release of toxic or inhibitory substances into the water (Hanisak, 1987).
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
255
ACKNOWLEDGEMENTS
This work was partially supported by the Sea Grant College Program, No. NA 85AA-D-CG082 and the Aquaculture Development Program Hawaii State Department of Land and Natural Resources.
Grant of the
REFERENCES Adnan, H. and Porse, H., 1987. Culture of Eucheuma cottonii and Eucheuma spinosum in Indonesia. Hydrobiologia, 151/152: 355-358. Braud, J.P. and Perez, R., 1979. Farming on pilot scale of Eucheuma spinosum (Florideophyceae) in Djibouti waters. Proc. 9th Int. Seaweed Symp., pp. 533-539. Dawes, C.J., LaClaire, J.W. and Moon, R.E., 1976. Culture studies on Eucheuma nudum J. Agardh, a carrageenan producing red alga from Florida. Aquaculture, 7: l-10. DeBusk, T.A. and Ryther, J.H., 1984. Effects of seawater exchange, pH and carbon supply on the growth of Gracilaria tikuahiae in large scale cultures. Bot. Mar., 27: 357-362. Doty. M.S., 1971. Measurement of water movement in reference to benthic algal growth. Bot. Mar., 14: 32-35. Doty, M.S., 1973. Eucheuma Farming for Carrageenans. Sea Grant Advisory Report, UNIHISEAGRANT-AR-73-02,21 pp. Doty, M.S., 1977. Eucheuma - current marine agronomy. In: R.W. Krauss (Editor), The Marine Plant Biomass of the Pacific Northwest Coast. Oregon State University Press, Corvallis, OR, pp. 203-214. Doty, M.S., 1986. The production and uses of Eucheuma. FAO Fish. Tech. Pap. No. 281, pp. 123161. Doty, M.S., 1988. Prodromus ad Systematica Eucheumatoideorum: a tribe of commercial seaweeds related to Eucheuma (Solieroaceae, Gigartinales). In: LA. Abbott (Editor), Taxonomy of Economic Seaweeds. California Sea Grant No. T-CSGCP-018, pp. 159-208. Glenn, E.P. and Doty, M.S., 1981. Photosynthesis and respiration of the tropical red seaweeds, Eucheuma striatum (Tambalang and Elkhorn varieties) and E. denticulatum: Aquat. Bot., 10: 353-364. Hanisak, M.D., 1987. Cultivation of Gracilaria and other macroalgae in Florida for energy production. In: K.T. Bird and P.H. Benson (Editors), Seaweed Cultivation for Renewable Resources. Elsevier, Amsterdam, pp. 191-218. LaPointe, B.E. and Ryther, J.H., 1978. Some aspects of the growth and yield of Gracilaria tikuahiae in culture. Aquaculture, 15: 185-193. Liu, S. and Ping, Z., 1984. The commercial cultivation of Eucheuma in China. Proc. 11th Int. Seaweed Symp., pp. 243-245. Luxton, D.M., Robertson, M. and Kindley, M.J., 1987. Farming of Eucheuma in the South Pacific islands of Fiji. Hydrobiologia, 151/152: 359-362. Mairh, O.P., Soe-Htun, U. and Ohno, M., 1986. Culture of Eucheuma striatum (Rhodophyta, Solieriaceae) in subtropical waters of Shikoku, Japan. Bot. Mar., 29: 185-191. Miura, A., 1980. Seaweed cultivation: present practices and potentials. In: E.M. Borgese (Editor ), Ocean Yearbook 2. University of Chicago Press, Chicago, IL, pp. 57-68. Parker, H.S., 1974. The culture of the red algal genus Eucheuma in The Philippines. Aquaculture, 3: 425-439. Russell, D.J., 1983. Ecology of the imported red seaweed Eucheuma striatum Schmitz on Coconut Island, Oahu, Hawaii. Pacific Sci., 37: 87-107. Strickland, .J.D.H. and Parsons, T.R., 1972. A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada, Ottawa, Ont., Bull. No. 167,309 pp.
245
Aquaculture,
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Printed
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Growth of the Seaweeds Kappaph ycus alvarezii, K. striatum and Eucheuma denticulatum as Affected by Environment in Hawaii EDWARD P. GLENN” and MAXWELL “Environmental bDepartment
(Accepted
Research of Botany,
Laboratory, University
S. DOTYb
2601 E. Airport
Drive, Tucson, AZ 85706 (U.S.A.)
of Hawaii at Manoa, Honolulu,
HI 96822 (U.S.A.)
27 June 1989)
ABSTRACT Glenn, E.P. and Doty, MS., 1990. Growth of the seaweeds Kappaphycus alvarezii, K. striatum and Eucheuma denticulatum as affected by environment in Hawaii. Aquaculture, 84: 245-255. Three commercial gel-producing seaweed species native to the Philippines were grown experimentally in pens on an algal reef-flat in Kaneohe Bay, Oahu, Hawaii. Growth rates and environmental conditions were measured for 55 consecutive weeks. The normal northeast trade winds created a flow of water through the 272-m’ farm, one side of which faced northeast. Upstream thalli of Kappaphycus alvarezii grew at an average relative growth rate of 5.06%/day, whereas K. striatum and Eucheuma denticulatum grew at 3.5O%/day. These growth rates and the overall productivity of 20.8 tonnes dry wt/ha per year were similar to those obtained on Philippine reefflat farms. Growth rates tended to be independent of season, and correlations between growth rates and environmental variables were low. The study suggested a range of conditions under which these eucheumatoids can be productive in a farm setting: temperature maxima of 24-30°C and minima of 21-22°C; nitrogen levels of 2-4 ,ug-atm/l; phosphate levels of 0.5-1.0 pg-atm/l; and high solar energy levels. The pH and salinity were near 8.0 and 32 ppt, respectively, throughout the study period. The degree of water motion per se was not correlated with growth rate but the direction of wind across the farm was important. Downstream thalli generally appeared unhealthy and grew at half the rate of upstream thalli. When the normal trade winds reversed, the (formerly) upstream thalli grew poorly. None of the measured environmental factors was correlated with the downstream growth reduction, and its cause remains unknown.
INTRODUCTION
The red algal genera Kuppuphycus and Eucheuma are farmed on tropical reef-flats for their polysaccharide, carrageenan. Cultivation of these red seaweeds started in The Philippines as an alternative to harvesting the wild crop (Doty, 1973; Parker, 1974). Test plantings of these eucheumatoids also have
0044-8486/90/$03.50
0 1990 Elsevier Science Publishers
B.V.
‘46
E.P.GLENNANDM.S.DOTY
been successful in Hawaii (Doty, 1977; Glenn and Doty, 1981; Russell, 1983), Indonesia (Braud and Perez, 1979; Adnan and Porse, 1987), China (Liu and Ping, 1984 ) , Fiji (Luxton et al., 1987 ), Florida (Dawes et al., 1976) and even in subtropical waters off Japan during warm seasons (Mairh et al., 1986). However, commercial farming has not spread far from its point of origin. Most farmed crop still comes from The Philippines (Doty, 1986)) with less coming from Indonesia and a little for internal use being grown in Hainan, China. One hindrance to farming these seaweeds has been the difficulty of finding productive farm sites. It is generally assumed that the species require warm sea temperature, high light levels, nutrient-enriched water, and a high degree of water motion driven by waves or tides. However, the attributes of a successful farm have not been satisfactorily quantified, and new farms are sited largely subjectively. The present study was designed to better define the range of environmental conditions under which three commercial seaweeds are productive in a farm setting. MATERIALS
AND METHODS
Kappaphycw aluarezii (Doty)Doty ( = E. striatum var. tambalang, Glenn and Doty, 1981; = E. striatum Schmitz, Russell, 1983), K. striatum (Schmitz) Doty ( = E. striatum var. elkhorn, Glenn and Doty, 1981) and E. denticulutum [ BurmanlCollins & Hervey ( = E. spinosum) (see Doty, 1988 for full taxonomit descriptions) were transplanted from The Philippines to an experimental seaweed farm in Kaneohe Bay, Oahu, Hawaii. In the following text these three species are referred to by their colloquial names, respectively, tambalang, elkhorn and spinosum. They were grown in pen culture on the north reef of Coconut Island, Oahu, near the Hawaii Institute of Marine Biology research station. The farm was sited over light-colored sand on a section of reef-flat covered with approximately 10 cm of water at the lowest tide and 1.5 m at the highest tide. The pens were made of plastic-coated 2.5 cm wire-mesh fence material 1 m high. Each pen was 3.3x3.3 m square. The farm was made up of 25 pens forming a square of 5 rows of 5 pens each, with the runs set on a northwest-tosoutheast axis, and occupied a total area of ca. 272 m2. The normal flow of water across the reef was driven to the southwest by northeast trade winds. Consequently, the row of pens on the northeast side was designated the upstream row while the opposite (southwest) side was designated as downstream. Under normal trade wind conditions water flowed into the seaweeds through the upstream pens. More detailed descriptions of the farm are given by Doty ( 1977) and Russell ( 1983 ). Loose thalli of all three seaweeds were grown within the pens. At irregular intervals the pens were partially harvested to allow room for regrowth. The three species were mixed together in each pen, and at each harvest some of
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
247
each was left behind as seedstock. The three middle rows of pens were allowed to become densely packed with algae before they were harvested. However, the upstream and downstream rows, where growth measurements were made, were tended on a weekly basis, to keep the test thalli free from shading and crowding. Thalli removed from these pens were combined with thalli in the middle rows of pens. Growth rates and environmental factors were measured for 55 consecutive weeks from 27 May 1976 to 15 June 1977. The measurements were taken the same day each week. Maintenance was done at sampling time and consisted of repairing the fences and removing epiphytes (mainly Enteromorpha) from the upstream row of pens. Enteromorpha grew profusely on the fence material but not on the seaweeds themselves. Growth of the seaweeds was measured by weighing individual tagged thalli of each species. The tagged thalli were secured by two methods. Thalli were either tied to a piece of fence material on the ground (lawn planting) or tied to a l-m length of string attached to the fence, which allowed some degree of movement of the thallus within the pen (pen planting). Since the two planting methods gave nearly identical average growth rates, the results were combined for all statistical analyses. The same thalli were generally weighed each week. If a thallus was lost or damaged, it was replaced with a new thallus from the loose seaweeds in the pen. The tagged thalli were kept in the range of 150 to 500 g wet weight by trimming them as necessary after they were weighed. After weighing and trimming, the tagged thalli were returned to their original positions. Ten tagged thalli of each species were in the upstream row of pens (two per pen) and ten were in the downstream pens (two per pen). The results were averaged so that each algal species was represented by two data points per week: upstream and downstream, with each datum the average of ten thalli. Relative growth rate was calculated using the formula RGR = (In final wt - In initial wt)/time and expressed as % growth per day. Water motion was measured with clod cards (Doty, 1971). Two clod cards were placed in an upstream pen and two in a downstream pen each week and collected 24 h later. The diffusion increase factor (DIF) was calculated by the ratio of weight lost compared to a clod card in still water. Oxygen was measured weekly for four samples taken from two upstream and two downstream pens; samples were fixed with permanganate solution in the field at the time of collection and titrated for oxygen content in the lab using the Winkler method (Strickland and Parsons, 1972 ). Four samples of water were collected weekly from two upstream and two downstream pens for determination of ammonia, nitrate and phosphate; these samples were delivered to the Hawaii Institute of Marine Biology analytical laboratory within 30 min of collection, where they were filtered immediately and frozen for later analyses using a Technicon Autoanalyzer.
248
E.P. GLENN AND M.S. DOTY
Water temperature was measured using maximum-minimum thermometers at the upstream and downstream ends of the farm. Air temperature and wind velocity were recorded hourly at the Kaneohe Marine Corps Air Station, which operated a weather station nearby on Kaneohe Bay. The daily maximum and minimum temperatures were averaged to obtain weekly values. Wind direction and velocity were averaged by week and expressed as the north wind vector in knots per hour (velocity xcos 0, where 8 is the angle of the average wind velocity with respect to north). Transformation of the data produced a positive number for wind velocity when the normal trade winds were blowing and a negative number when the winds reversed and blew from the south. Light energy was measured in Honolulu, about 20 miles away, by the National Weather Service, Pacific Region, and was averaged by week. Salinity was measured with a hand-held refractometer (A/O Special Scale Model) accurate to 2 ppt. The pH was measured with a portable Beckman pH meter by placing the electrode in water in the upstream and downstream pens; the meter was accurate to 0.2 pH units. The total biomass production of the farm was estimated for the year by adding up the amount of seaweed harvested from the pens. The farm was partially harvested twice during the study and completely harvested (and dismantled) at the completion of the study. Statistical analyses were conducted using programs in MSTAT (Michigan State University, Lansing, MI). Differences between means were compared using Student’s t-test. Correlation coefficients were calculated using Pearson’s r. RESULTS
Appearance and growth rates of seaweeds Usually there was a striking difference in appearance of upstream and downstream thalli of all three species. Upstream thalli were large and darkly pigmented compared to downstream thalli, which were straw colored. Downstream thalli were also more fragmented than upstream thalli (a consequence of ice-ice, the necrosis of narrow bands of tissue which causes the thalli to break apart). The first three rows of pens contained healthy-appearing thalli whereas the last two (downstream) rows contained unhealthy-appearing thalli. When healthy-appearing thalli were placed in downstream pens, they lost their dark pigmentation by the following week. Table 1 gives means and standard deviations of growth rates averaged over the study. Downstream growth rates averaged only half the upstream rates and the differences were significant for all three species (P < 0.01). Upstream thalli of tambalang grew 45% faster than the other two species (PC 0.01). Seasonal fluctuations in growth rates were small compared to the week-toweek variations. However, tambalang grew approximately 15% faster in sum-
249
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
TABLE 1 Seaweed growth rates (% per day) and standard deviations (s.d.) for three species of algae obtained in Kaneohe Bay, Hawaii, during 55 consecutive weeks Species
Condition
Growth rate
s.d.
Tambalang Elkhorn Spinosum Tambalang Elkhorn Spinosum
Upstream Upstream Upstream Downstream Downstream Downstream
5.06 3.51 3.52 2.07** 1.43** 2.29**
1.34 1.05 1.36 1.05 0.71 1.21
**Significant
differences
between upstream
and downstream
growth rates at PC 0.01.
TABLE 2 Seasonal growth rates (% per day) and standard deviations (in parentheses) of seaweeds in Kaneohe Bay, Hawaii. Summer, 22 June to 21 September; fall, 22 September to 21 December; winter, 22 December to 21 March; and spring, 22 March to 21 June Species
Tambalang Tambalang Elkhorn Elkhorn Spinosum Spinosum *Significant
Condition
Growth rate
Upstream Downstream Upstream Downstream Upstream Downstream differences
Summer
Fall
Winter
Spring
6.23 (0.95) 1.94(1.23) 3.33 (0.98) l.OO(O.71) 4.05(1.33) 2.70(1.18)
4.41*(0.93) 2.43(0.92) 2.98(0.&j) 1.47(0.83) 3.52(1.17) 2.22(1.49)
4.15*(1.35) 2.27 (0.95) 3.76( 1.23) 1.75(0.65) 3.36( 1.57) 2.23(1.26)
5.25(1.24) 1.92(0.99) 3.95(1.16) 1.61(0.77) 3.05(1.24) 2.00(0.86)
between summer and the fall and winter values at P < 0.05.
TABLE 3 Correlation coefficients between growth rates of seaweeds grown at the upstream or downstream rows of the experimental seaweed farm in Kaneohe Bay, Hawaii, over 55 consecutive weeks Tambalang UP Tambalang Tambalang Elkhorn Elkhorn Spinosum *Significant
UP Down
Elkhorn Down
Up
Down
Up
Down
0.004
0.520** -
0.700* 0.182
0.461** 0.372** -
0.456** 0.300* 0.409**
UP Down UP at P < 0.05; **significant
Spinosum
at P< 0.01.
250
E.P. GLENN AND MS. DOTY
mer than in winter and fall (PcO.05) (Table 2). There was a moderate correlation among growth rates over the study (Table 3 ). A total of 3600 kg wet weight of seaweed was harvested from the farm, equivalent to an annual production of 130 tonnes/ha. The dry weight of the thalli averaged approximately 16% of the wet weight; hence the production was equivalent to 20.8 tonnes/ha per year of dry matter. The standing density of seaweeds in the pens at the terminal harvest was 7.5 kg/m*. The individual species were not separated when the pens were harvested, but elkhorn and spinosum thalli were noted to be much less abundant in the harvested material than tambalang thalli. Environmental parameters Table 4 gives means and standard deviations of upstream and downstream water quality factors, as well as maximum and minimum air temperatures, light energy, and the velocity of the northerly component of the wind. There were only two significant differences between upstream and downstream measurements: oxygen levels and degree of water motion. The oxygen level was 1 ppm higher in the downstream pens (PC 0.05), presumably due to the photosynthesizing mass of seaweeds in the intervening pens. Water motion was 20% lower downstream than upstream (PC 0.01 ), presumably due to the obstruction of the current by the mass of seaweeds in the pens. Water temperature closely paralleled air temperature. The max/min thermometers left in the water were occasionally lost, resulting in an incomplete data set. Hence, only the air temperatures were used in further statistical analyses. Oxygen content was the only water-quality factor that showed an obvious seasonal trend, being lowest in winter. Ammonia, nitrate and phosphate concentrations tended to have stable base levels punctuated by irregularly occurring very high levels. The pH and salinity were relatively constant over the study, within the range of accuracy of the instrument used for measurement; pH was 8.0 to 8.2 and salinity was 32 to 34 ppt upstream and downstream. The weekly mean maximum/minimum air temperature ranged from a low of 21 oC to a high of 27 QC with little seasonal fluctuation. Light energy showed a seasonal trend, with the winter minimum being half that of the summer maximum. The strength of the trade winds varied from week to week, but the north vector was strongly negative during only 6 weeks. The most prolonged period of southerly winds was during January and February. Correlations between growth rates and environmental factors A correlation matrix was calculated relating upstream and downstream growth rates of the three seaweeds to the environmental factors (Table 5). Eight of the correlation coefficients were statistically significant (P < 0.05 ) . However, the coefficients of determination (r’) were all low. No single envi-
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
251
TABLE 4 Environmental and water-quality factors measured at the upstream and downstream ends of the Kaneohe Bay, Hawaii, seaweed farm. Data could not be collected for some of the variables in some weeks, making the number of observations less than 55 for some variables Mean Nitrate (,ng-atm/l) Upstream Downstream Ammonia (pg-atm/l) Upstream Downstream Phosphate (pg-atm/l) Upstream Downstream Water motion (DIF)a Upstream Downstream Oxygen (mg/l) Upstream Downstream Air temperature ( ‘C ) Maximum Minimum Water temperature ( ‘C 1 Upstream max. Upstream min. Downstream max. Downstream min. Light energy (g Cal/cm* per day ) North wind velocity (knots/h) “DIF = diffusion increase factor. *-**Significant differences between **p
s.d.
Number
1.44 1.10
1.11 0.97
51 51
1.98 2.01
2.17 2.21
44 44
0.66 0.62
0.29 0.27
51 51
44.9 37.6* 7.22 8.25*
13.0 10.8
53 53
1.99 2.15
53 53
27.6 20.8
1.10 1.60
55 55
27.7 22.6 28.0 23.1 371 1.83
1.54 1.21 1.31 1.40 18 2.17
46 46 46 46 55 45
upstream
and downstream
measurements
at *PC 0.05 or
ronmental factor explained more than 20% of the variation in any seaweed growth rate. Upstream tambalang growth rate was positively correlated with light level and phosphate level, whereas upstream elkhorn growth rate was negatively correlated with maximum and minimum air temperature. Downstream tambalang growth rate was negatively correlated with ammonia and phosphate and positively correlated with water motion, whereas downstream elkhorn growth rate was negatively correlated with phosphate. None of the correlation coefficients for upstream or downstream spinosum was statistically significant. Stepwise multiple linear regression analyses did not significantly improve the correlation between growth rate and environmental variables for any species. None of the resulting equations could account for more than 25%
E.P. GLENN AND MS. DOTY
252 TABLE 5
Correlation coefficients between upstream and downstream growth rates and environmental rameters measured over 55 consecutive weeks in Kaneohe Bay, Hawaii
pa-
Growth rate Elkhorn
Tambalang
Light energy Max. air temp. Min. air temp. Water motion North wind Nitrate Ammonia Phosphate Dissolved oxygen *Significant
Spinosum
UP
Down
UP
Down
Up
Down
0.341** -0.193 0.208 - 0.047 0.283 - 0.043 - 0.038 0.476** -0.159
- 0.294 0.068 -0.031 0.318* 0.086 0.086 - 0.425** - 0.343 - 0.039
0.206 - 0.448** -0.317* 0.152 0.275 -0.132 0.029 0.111 0.040
-0.178 -0.181 - 0.264 0.123 - 0.082 0.048 -0.146 - 0.350* 0.253
- 0.055 0.002 0.084 - 0.026 0.130 0.216 -0.187 - 0.009 - 0.209
- 0.032 -0.114 0.177 -0.061 0.027 0.026 -0.277 0.030 0.071
at P < 0.05; **significant
at P < 0.01.
of the variation in growth rate regardless of which combination of independent variables was tried (data not shown). Growth rates and environmental factors during a period of prolonged wind reversal The differences in appearance of upstream and downstream thalli tended to reverse when the normal northeasterly trade winds failed and wind blew from the south. Normally the wind reversals last for only a few days, but one lasted for a month and was studied in detail with respect to algal growth rate and environmental factors. Data obtained during this period (weeks 32 to 34) were compared to data over the entire study (Table 6). The upstream growth rates of all three seaweeds were much lower than normal during the wind reversal and were depressed for several weeks after the trade winds returned. Downstream growth rates did not change significantly during the period of wind reversal, although by the end of the period the downstream tagged thalli had increased in pigmentation and looked healthier. North wind velocity during this period became negative but of the same magnitude as during the rest of the study. The flow of water through the pens reversed as a result of the wind reversal, but none of the water quality factors changed significantly. Downstream oxygen level remained higher than upstream level except for week 34, when the upstream measurement was 11.8 ppm and the downstream measurement was 8.8 ppm. Water motion was within
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
253
TABLE 6 Seaweed growth rates and environmental factors (standard deviations in parentheses) upstream and downstream in Kaneohe Bay, Hawaii, during the major period of wind reversal (5 January to 2 February 1977)
Growth rates (%/day) Tambalang Elkhorn Spinosum Water motion (DIF) Nitrate-N (pg-atm/l) Ammonia-N (pg-atm/l) Phosphate-P (p-atm/l) North wind (knots/h) PH Salinity (ppt) Oxygen (mg/l) **Values significantly
different
Upstream
Downstream
2.78 2.38 2.08 40.7 0.80 2.13 0.51 - 1.88 8.0 32 7.79
1.51 1.41 1.39 36.1 0.48 2.05 0.47 - 1.88 8.0 32 8.95
(0.44)** (0.54)** (1.25)** (17.4) (0.26) (1.42) (0.06) (2.38)** (0.2) (2) (2.28)
(0.62) (0.30) (0.78) (15.7) (0.11) (1.40) (0.10) (2.38) (0.2) (2) (0.72)
from mean values over the total study period at P-c0.01.
the normal range upstream and downstream throughout the period of southerly winds. DISCUSSION
Kaneohe Bay appears to be a fertile site for eucheumatoid cultivation. A growth rate of 3.5% per day is considered good in commercial cultivation (Parker, 1974; Braud and Perez, 1979; Liu and Ping, 1984; Adnan and Porse, 1987; Luxton et al., 1987). Upstream tambalang exceeded this target figure by 45% and upstream elkhorn and spinosum matched the target figure. The total biomass output from the farm exceeded that of commercial farms in The Philippines, which have been estimated to produce from 4.5 tonnes/ha dry weight (Miura, 1980) to 13 tonnes/ha (Parker, 1974; Doty, 1986). Much higher productivities have been extrapolated based on growth rate data not only for eucheumatoids (Doty, 1973; Parker, 1974) but Gracilmia and other red seaweeds (LaPointe and Ryther, 1978; DeBusk and Ryther, 1984; Hanisak, 1987) but yields as high as the present ones have rarely been achieved on farms or in large-scale culture (Hanisak, 1987). It is not known how many modules of the size tested here could be placed on a hectare of reef-flat and farmed productively, given the growth inhibition observed within the 25 pens at the downstream end of the farm. The production of these seaweeds is seasonal in many regions, but growth rates in Kaneohe Bay were high throughout the year, except when the trade
254
E.P. GLENN
AND
MS.
DOW
winds failed. There were approximately 45 days of lowered production due to wind reversal during the 55 weeks of this study. The results suggest a range of environmental values over which good eucheumatoid growth can be expected (although even better growth cannot be excluded outside this range of values). Ammonia and/or nitrate levels in the range of 1-2 p-atm/l were sufficient as nitrogen sources; 0.5-1.0 fi-atm/l of phosphate was sufficient as a phosphorus source. Even lower nutrient levels can support Eucheuma growth; Dawes et al. (1976) found a positive growth response to nitrogen but not phosphorus for what is now called E. isiforme var. denudatum at levels one tenth those measured in Kaneohe Bay. Diurnal minimum and maximum temperatures averaging 21°C and 28”C, respectively, supported high growth rates of these three species, and there was no evidence of growth limitation due to temperature at any time of year. Mairh et al. (1986) found that elkhorn did not grow at temperatures below 20°C in Japanese coastal waters, whereas we previously reported (Glenn and Doty, 1981) the photosynthetic temperature response of all three species increased up to 32 ‘C, then sharply declined. The correlation between light levels and growth of tambalang and its greater growth rate in summer and spring than in winter and fall suggest that light may become limiting for this species. Tambalang thalli tied to a line extending over the reef into deep water grew fastest just below the surface, and growth rate declined with depth and decreasing light intensity (Russell, 1983) as did photosynthetic capacity (Glenn and Doty, 1981). Water motion per se was not correlated with growth rate nor was the velocity of the wind, so long as it blew from the north or northeast. However, the direction of the wind appeared to be the most important factor in the growth of the seaweeds. Downstream growth rate was severely depressed compared to upstream during normal wind conditions, and when the winds reversed, upstream growth rate decreased rapidly to a low level. Presumably the wind affected the algae by reversing the direction of water flow through the pens. However, one of the measured water quality factors changed significantly during the wind reversal. The cause of the downstream growth inhibition was not discovered. There was no strong evidence for a nitrogen or phosphorus limitation. Dense seaweed cultures may become limited by the diffusion rate of carbon dioxide into the water (DeBusk and Ryther, 1984) but in this study pH, which is an indicator of carbon dioxide level, did not change appreciably and the oxygen content rose by only 1 ppm, on average, in the passage of water through the farm. Hence it is unlikely that carbon limitation was the cause of the downstream growth inhibition. It has been noticed by others that seaweeds grown in dense cultures exhibit autoinhibition of growth, due to the release of toxic or inhibitory substances into the water (Hanisak, 1987).
GROWTH OF THREE SEAWEED SPECIES IN HAWAII
255
ACKNOWLEDGEMENTS
This work was partially supported by the Sea Grant College Program, No. NA 85AA-D-CG082 and the Aquaculture Development Program Hawaii State Department of Land and Natural Resources.
Grant of the
REFERENCES Adnan, H. and Porse, H., 1987. Culture of Eucheuma cottonii and Eucheuma spinosum in Indonesia. Hydrobiologia, 151/152: 355-358. Braud, J.P. and Perez, R., 1979. Farming on pilot scale of Eucheuma spinosum (Florideophyceae) in Djibouti waters. Proc. 9th Int. Seaweed Symp., pp. 533-539. Dawes, C.J., LaClaire, J.W. and Moon, R.E., 1976. Culture studies on Eucheuma nudum J. Agardh, a carrageenan producing red alga from Florida. Aquaculture, 7: l-10. DeBusk, T.A. and Ryther, J.H., 1984. Effects of seawater exchange, pH and carbon supply on the growth of Gracilaria tikuahiae in large scale cultures. Bot. Mar., 27: 357-362. Doty. M.S., 1971. Measurement of water movement in reference to benthic algal growth. Bot. Mar., 14: 32-35. Doty, M.S., 1973. Eucheuma Farming for Carrageenans. Sea Grant Advisory Report, UNIHISEAGRANT-AR-73-02,21 pp. Doty, M.S., 1977. Eucheuma - current marine agronomy. In: R.W. Krauss (Editor), The Marine Plant Biomass of the Pacific Northwest Coast. Oregon State University Press, Corvallis, OR, pp. 203-214. Doty, M.S., 1986. The production and uses of Eucheuma. FAO Fish. Tech. Pap. No. 281, pp. 123161. Doty, M.S., 1988. Prodromus ad Systematica Eucheumatoideorum: a tribe of commercial seaweeds related to Eucheuma (Solieroaceae, Gigartinales). In: LA. Abbott (Editor), Taxonomy of Economic Seaweeds. California Sea Grant No. T-CSGCP-018, pp. 159-208. Glenn, E.P. and Doty, M.S., 1981. Photosynthesis and respiration of the tropical red seaweeds, Eucheuma striatum (Tambalang and Elkhorn varieties) and E. denticulatum: Aquat. Bot., 10: 353-364. Hanisak, M.D., 1987. Cultivation of Gracilaria and other macroalgae in Florida for energy production. In: K.T. Bird and P.H. Benson (Editors), Seaweed Cultivation for Renewable Resources. Elsevier, Amsterdam, pp. 191-218. LaPointe, B.E. and Ryther, J.H., 1978. Some aspects of the growth and yield of Gracilaria tikuahiae in culture. Aquaculture, 15: 185-193. Liu, S. and Ping, Z., 1984. The commercial cultivation of Eucheuma in China. Proc. 11th Int. Seaweed Symp., pp. 243-245. Luxton, D.M., Robertson, M. and Kindley, M.J., 1987. Farming of Eucheuma in the South Pacific islands of Fiji. Hydrobiologia, 151/152: 359-362. Mairh, O.P., Soe-Htun, U. and Ohno, M., 1986. Culture of Eucheuma striatum (Rhodophyta, Solieriaceae) in subtropical waters of Shikoku, Japan. Bot. Mar., 29: 185-191. Miura, A., 1980. Seaweed cultivation: present practices and potentials. In: E.M. Borgese (Editor ), Ocean Yearbook 2. University of Chicago Press, Chicago, IL, pp. 57-68. Parker, H.S., 1974. The culture of the red algal genus Eucheuma in The Philippines. Aquaculture, 3: 425-439. Russell, D.J., 1983. Ecology of the imported red seaweed Eucheuma striatum Schmitz on Coconut Island, Oahu, Hawaii. Pacific Sci., 37: 87-107. Strickland, .J.D.H. and Parsons, T.R., 1972. A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada, Ottawa, Ont., Bull. No. 167,309 pp.