Journal of Applied Phycology 11: 473–477, 1999. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.
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A preliminary comparison of the mariculture potential of Porphyra purpurea and Porphyra umbilicalis George P. Kraemer1,∗ & Charles Yarish2 1 Division
of Natural Sciences, Purchase College, State University of New York, Purchase, NY 10577, USA of Ecology and Evolutionary Biology, University of Connecticut at Stamford, Stamford, CT 06901,
2 Department
USA (∗ Author for correspondence; e-mail:
[email protected]) Received 26 September 1999; revised 27 October 1999; accepted 28 October 1999
Key words: aquaculture, light, photosynthesis, Porphyra
Abstract Due to their rapid growth and nutrient assimilation, Porphyra spp. are good candidates for bioremediation and polyculture. The production potential of two strains of P. purpurea and P. umbilicalis from north-east USA was evaluated by measuring rates of photosynthesis (as O2 evolution) of material grown at 20 ◦ C. Photosynthetic rates of P. umbilicalis were 80% higher than P. purpurea over the temperature range 5–20 ◦ C, at both sub-saturating and saturating irradiances (37 and 289 µmol photon m−2 s−1 ). Porphyra umbilicalis was more efficient at low irradiances (higher α) and had a higher Pmax (23.0 vs 15.6 µmol O2 g−1 DW min−1 ) than P. purpurea, suggesting that P. umbilicalis is a better choice for mass culture, where self-shading may be severe.
Introduction An emerging problem of coastal mariculture activities is the significant loading of inorganic nutrients into local waters (Beveridge, 1987). Nutrient enrichment from fish farming is equivalent to that of municipal sewage (Ackefors & Enell, 1994). Many coastal areas already suffer from eutrophication-driven blooms of phytoplankton and weedy macroalgae, creating aesthetic problems, the development of severe hypoxia in bottom waters, and the death or departure of ecologically and economically important biota. The reduction of nutrient leaching from fish food and trapping faecal matter can reduce nutrient loading from mariculture operations (Phillips et al., 1993). Another promising approach is to integrate the culture of finfish or shellfish with macroalgae; i.e. polyculture (e.g. Neori et al., 1996; Cohen & Neori, 1998). Since macroalgae concentrate nutrients by a factor as high as 105 (Chopin et al., 1990), growing and harvesting macroalgae in conjunction with fish production can remove excess nutrients from the mariculture effluent.
Kautsky et al. (1996) integrated the agarophyte Gracilaria into salmon mariculture in Chile and reduced the release of nitrogen (N) and phosphorus (P) by 56% and 94%, respectively. Preliminary pilot scale farms integrating seaweed and finfish (nori/salmonid) mariculture in the Gulf of Maine have already produced positive results (Chopin & Yarish, 1998, 1999). The red alga Porphyra (nori) is the most valuable maricultured seaweed, with an annual value of over $US 1.8 billion (Jensen, 1993). Porphyra spp. are fast growing, requiring less than 40 days from seeding to first harvest in net culture, and may be repeatedly harvested every 9–15 days (Merrill, 1989). The high productivity, coupled with nutrient accumulation (63170% higher than natural levels in other macroalgae; Chopin & Yarish, 1998, 1999) makes Porphyra an excellent choice for eutrophication abatement via polyculture, while also providing a valuable product upon harvest (Mumford & Miura 1988; Cuomo et al., 1993). The most efficient bioremediator and nori producer will combine high rates of production with rapid nutrient assimilation, both of which are light-dependent
474 processes. Light energy is required for active transport (uptake) of nutrients and the photosynthetic production of carbon skeletons for final assimilation into organic form (Turpin, 1991). The effects of light on these processes cascade through to influences on growth rate. Porphyra spp. inhabit intertidal to shallow, subtidal environments (Yarish et al., 1999), and as a consequence, different species are likely to differ in their photosynthesis-irradiance characteristics (Huppertz et al., 1990). An important consequence is that some Porphyra spp. may photosynthesize at higher rates under saturating light, or may out-perform conspecifics at sub-saturating irradiances. In fact, productivity at sub-saturating irradiances may be a better predictor of success than rates under saturating irradiances since self-shading in tank culture systems increases with increasing culture density (Craigie & Shacklock, 1985; Craigie, 1999). Therefore, the control of production by light is a particularly important consideration in the selection of a marine macrophyte for bioremediation and biomass production. The relationship between photosynthetic rate (P) and irradiance (I) is a useful tool for evaluating primary production. Short-term P-I measurements enable rapid estimates of production by many samples and, therefore, the measurement of photosynthetic rate can be used in the primary selection of potential Porphyra strains for bioremediation. Growth measurements are also important, but are not as useful for preliminary evaluations since they require relatively long periods, and cannot account for tissue losses due to reproduction, senescence, and herbivory. To choose among the candidates (there are at least seven species of Porphyra from New York to New Brunswick, Canada), evaluation of the photosynthetic potential of local Porphyra species has begun. Presented here are preliminary results that (a) compare production by two species of Porphyra (P. umbilicalis and P. purpurea), and (b) examine the relationship between photosynthetic production by Porphyra umbilicalis and growth and measurement temperature.
Materials and methods The strains of Porphyra purpurea and P. umbilicalis used here are currently in culture (both foliose gametophytic and conchocoelis phases) at the Marine Biotechnology Laboratory of the University of Connecticut at Stamford. P. purpurea (strain NY-4) was originally collected from boulders at a mid-tidal, exposed
location on South Manursing Island, near Rye (NY) during July (1997). It is present from late June through early October (Yarish et al., 1999). P. umbilicalis (strain ME-40) was collected from a high-energy site on Matthews Island (ME) during September (1996), where it occurs year-round. Gametophytes were grown from conchospores in von Stosch’s seawater enrichment (Ott, 1965) at defined temperatures (P. umbilicalis at 10 ◦ and 20 ◦ C; P. purpurea at 20 ◦ C) and at approximately 50 µmol photon m−2 s−1 under a 12:12 L:D cycle. Blade samples (2.0–2.5 cm2 , 4.5–6.0 mg DW) were removed with a razor blade and maintained at the growth temperature until use (within 90 min). Samples were placed in 12-mL incubation chambers (Hansatech) filled with filtered (0.22 µm), autoclaved seawater (30 p.s.u.). Samples were incubated at temperatures ranging from 5 to 20 ◦ C. The chamber temperature was maintained (± 0.5 ◦ C) by a recirculating water bath. Prior to measurement of photosynthetic rate, the oxygen concentration in the chamber was reduced to 20–25% of saturation by bubbling with N2 and 1– 2 mg NaHCO3 was added to ensure that the rate of photosynthesis was not limited by inorganic carbon. The rate of oxygen production was monitored for 8– 12 min at sub-saturating and saturating irradiances (37 and 289 µmol photon m−2 s−1 , respectively). Rates were standardized to dry weight (DW). For the comparison of P. purpurea and P. umbilicalis grown at 20 ◦ C, an average of six replicates per treatment was recorded. Data were analyzed via ANOVA following natural log transformation. When ANOVA indicated treatment effects, Scheffé’s post hoc test was used to distinguish between the means. An average of seven replicates was recorded for the growth temperature – measurement temperature combinations employing P. umbilicalis.
Results The two Porphyra species, grown at 20 ◦ C, varied in their photosynthesis-irradiance (P-I) characteristics (Figure 1). When P-I data were fitted to the Webb model (Webb et al., 1974), the estimated Pmax and α values for P. purpurea were 15.6 µmol O2 g−1 DW min−1 and 0.191 of µmol O2 g−1 DW min−1 (µmol photon m−2 s−1 )−1 , respectively. The same parameters were estimated as 23.0 µmol O2 g−1 DW min−1 and 1.04 µmol O2 g−1 DW min−1 (µmol photon m−2 s−1 )−1 , respectively, for P. umbilicalis. These
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Figure 1. Photosynthesis-irradiance relationship for Porphyra purpurea and P. umbilicalis grown at 20 ◦ C and 50 µmol photon m−2 s−1 . The data were fitted to the equation of Webb et al. (1974). Pmax and α for Porphyra purpurea were estimated at 15.6 µmol O2 g−1 DW min−1 and 0.191 µmol O2 g−1 DW min−1 (µmol photon m−2 s−1 )−1 , respectively. Pmax and α for Porphyra umbilicalis were estimated at 23.0 µmol O2 g−1 DW min−1 and 1.04 µmol O2 g−1 DW min−1 (µmol photon m−2 s−1 )−1 , respectively. The insets present the full P-I curve, up to irradiances of 2650 µmol photon m−2 s−1 .
translate into saturating irradiances (Ik values) of 82 and 22 µmol photon m−2 s−1 for P. purpurea and P. umbilicalis, respectively. When grown at 20 ◦ C, P. umbilicalis had higher levels of production than P. purpurea at all measurement temperatures, and at both saturating and subsaturating irradiances (Figure 2). At 10, 15, and 20 ◦ C, P. umbilicalis photosynthesized at rates that averaged 53% higher than P. purpurea. Production by P. umbilicalis measured at 5 ◦ C was more than double the production by P. purpurea at both irradiances. The overall difference in the photosynthetic rates of the two species was significant (P. umbilicalis > P. purpurea; F = 19.6, p < 0.0001). The temperature at which the blades were incubated also had a significant effect on measured rate (F = 10.7, p < 0.0001). Average photosynthetic rates for P. purpurea ranked 5 ◦ C < 10 ◦ C = 15 ◦ C < 20 ◦ C. While temperature also significantly affected photosynthetic rates of P. umbilicalis, the results were more complicated; 5 ◦ C =
Figure 2. Rate of photosynthesis (O2 production) by Porphyra purpurea and P. umbilicalis as a function of measurement temperature. Both species were grown at 20 ◦ C, and c. 50 µmol photon m−2 s−1 . A) Incubation irradiance = 37 µmol photon m−2 s−1 . B) Incubation irradiance = 289 µmol photon m−2 s−1 . Error bars are standard deviation.
10 ◦ C, 10 ◦ C = 15 ◦ C, 5 ◦ C < 15 ◦ C, (5 ◦ C, 10 ◦ C, 15 ◦ C) < 20 ◦ C. The photosynthetic response to measurement temperature differed between the two species (Figure 2). The increase in the photosynthetic rate of P. purpurea with increasing temperature at 37 µmol photon m−2 s−1 appeared linear. At 289 µmol photon m−2 s−1 , the apparent Q10 for the 5–15 ◦ C range was 4.2. Rates peaked at 15 ◦ C and declined at 20 ◦ C, though the latter data were variable. Porphyra umbilicalis exhibited the more expected pattern with Q10 values for 37 and 289 µmol photon m−2 s−1 of 2.1 and 2.0, respectively. Rates of photosynthesis by P. umbilicalis increased exponentially as a function of measurement temperature at both saturating and sub-saturating irradiances and at both growth temperatures (Figure 3). The measured rates of material grown at 10 ◦ C and measured at 10 ◦ C appeared anomalously low. The ratios of the rate of light-replete to light-limited production (photosynthetic rate289/photosynthetic rate37 ) did not differ significantly as a function of growth or measurement temperature. On average, rates of production
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Figure 3. Rate of photosynthesis (O2 production) by Porphyra purpurea and Porphyra umbilicalis as a function of growth and measurement temperatures. Filled circles represent measurements made at 37 µmol photon m−2 s−1 . Open circles represent measurements at 289 µmol photon m−2 s−1 .
by P. umbilicalis were 47% higher at saturating than sub-saturating irradiance.
Discussion The primary objective of this study was to evaluate the rate of production as a function of irradiance by two Porphyra species, both candidates for integration with fin- or shellfish mariculture as a means of reducing the release of inorganic nutrients, and at the same time producing a salable product. When grown at 20 ◦ C, the ME-40 strain of P. umbilicalis was markedly more productive at all irradiances than strain NY-4 of P. purpurea. Further experimentation is needed to determine whether the relationship extends to growth at winter (i.e., 5–10 ◦ C) temperatures. Interestingly, both P. umbilicalis and P. purpurea exhibited much higher rates of production (16–23 µmol O2 g−1 DW min−1 ) than that reported for P. yezoensis (6–15 µmol O2 g−1 DW min−1 ), the commercially cultured Asian species (Chaoyuan et al., 1984; Zhang et al., 1997). The better photosynthetic performance exhibited by P. umbilicalis was surprising. Porphyra umbilicalis is present all year-round along the coast of Maine, where sea surface temperatures generally range between 0–15 ◦ C (Neefus, pers. comm.), whereas P. purpurea was collected from an area in Long Island Sound (NY) where water temperatures range between 2–23 ◦ C (Yarish et al., 1994). The a priori expectation was that P. purpurea would have been more tolerant of higher temperatures than P. umbilicalis. Both the laboratory measurements (here
and Yarish et al., 1998) and the seasonal occurrence of P. purpurea (June–October) suggest a lower tolerance of higher temperatures than that of P. umbilicalis. Photosynthetic rates of P. purpurea did not increase when the measurement temperature was increased from 15 ◦ C to 20 ◦ C. Additionally, optimum temperatures for the vegetative growth of the conchocoelis phase of P. purpurea, (grown under 10–40 µmol photon m−2 s−1 ) ranged between 10–15 ◦ C (Yarish et al., 1998, Chopin et al., in press), with an upper (lethal) temperature between 20–25 ◦ C. Photosynthesis by P. umbilicalis was also more efficient than P. purpurea at low light levels, as seen from the α values obtained from the composite P-I curves. This was surprising, because P. umbilicalis possesses a thicker thallus (> 80 µm) than P. purpurea (35–50 µm; Yarish, unpubl. data) and Enríquez et al. (1995) have shown a strong, negative relationship between thallus thickness and both Pmax and α . Other local species (e.g. P. linearis and P. leucosticta) are thinner (25–50 µm) and, therefore, represent potentially more productive species. Not only did P. umbilicalis exhibit a higher capacity for light harvesting at low irradiances (reflected in a higher α), but carbon fixation capacity (Pmax ) was also higher. A positive correlation between (α) and Pmax has been observed for many macrophytes (e.g. Enríquez et al., 1995). Over all temperatures (both growth and measurement), P. umbilicalis exhibited rates of photosynthesis at sub-saturating irradiance that were relatively high (ca. 70%) compared with those at saturating irradiance. This efficiency at subsaturating irradiances is attractive in a mariculture candidate. The Ik value obtained for P. umbilicalis was one-sixth that reported by Enríquez et al. (1995) for an unidentified Mediterranean Porphyra species, while Pmax values were similar. The results presented here show significant differences in the photosynthetic capacity of two species of Porphyra, potential candidates for polyculture with fin- or shellfish mariculture. Compared with P. purpurea, P. umbilicalis exhibited more efficient use of low light and higher maximum rates of photosynthesis under light saturation. The next step in the evaluation of these and other species of Porphyra is the measurement of the rates of nutrient uptake and the maximum tissue nutrient concentration, necessary to determine the optimum harvest schedule. Coupled with measurements of production, these estimates will enable the correct choice of Porphyra species for polyculture applications.
477 Acknowledgements This work was supported by the Connecticut Sea Grant College Program under a grant from NOAA Office of Sea Grant, USA Department of Commerce (C. Yarish), and the National Sea Grant College Program (C. Yarish), the State of Connecticut Critical Technologies Program, and a NY State UUP Professional Development Grant (G. Kraemer).
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