Eficiencia de absorcion de nutrientes de Gracilaria chilensis y Ulva lactuca en un sistema multitrofico integrado con el abalon rojo Haliotis rufescens.
The red abalone Haliotis rufescens (Swainson, 1822) is a non-native species of the Chilean coast which was introduced in 1977 for laboratory analysis (Godoy & Jerez, 1998). Since then, diverse investigations have been performed which have permitted the development of cultivating this species, thus giving rise to the rapid growth of commercial activities since the 90's. In the year 2006, Chile positioned itself as the fifth largest producer of abalones in the world with 304 ton. In 2009, 886 ton were produced (SERNAPESCA, 2009), demonstrating increased production and an industry that finds itself in expansion, with currently twenty-five companies related to the production of abalone in Chile (Flores-Aguilar et al., 2007). The majority of these installations are land-based cultures principally located in the northern region of the country and which take on seed production as well as the adult growth. Conversely, cultivation in the south is predominately sea-based, and, in some cases, provided with seeds produced in the north (Flores-Aguilar et al., 2007). In this way, there is a high expected potential for increasing abalone production in the future, based on cultivation site availability in the south of Chile as well as the expansion of the limits for sea-based cultivation in the north. This situation implies an increase of installations to support the rise in demand for seeds and supplies, bringing a greater pressure to the environment and possible conflicts, especially concerning wastewater which is currently discharged into the sea. This situation has been widely documented for different cultivated species of the world, where the rapid expansion of aquaculture has translated into a growing interest for scientists, industrialists, and governments alike in understanding and minimizing the impacts that these productive activities could have on the environment (Troell et al., 2006). Special concern is given to the eutrophication process, where an excessive quantity of N, P, and C[O.sub.2] and lowered levels of dissolved [O.sub.2], a product of intense animal cultivation in tanks, ponds, and coastal waters, has caused serious problems in coastal waters of the world (Fei, 2004; Yokoyama & Ishihi, 2010). Arising from this, the high effectiveness of using seaweeds for the treatment of wastewater produced by marine animal cultivation has been documented through the use of integrated cultures (Chopin et al., 2001; Fei, 2004; Bolton et al., 2009; Abreu et al., 2011). The Integrated Multi-Trophic Aquaculture (IMTA) model (Neori et al., 2004), couples species of distinct trophic or nutritional levels into the same system (FAO, 2009). For example, seaweeds, as primary producers, function as a biofilter by removing C[O.sub.2] and nutrient wastes, like dissolved nitrogen and phosphorus, from seawater and thus reduce nutrient discharge into the environment (Troell et al., 2003; Nobre et al., 2010). Additionally, the high nutrient uptake capacity of seaweed promotes its growth (Troell et al., 2006), generating potentially valuable biomass that can be used as a protein-enriched feed for other species or in human food, phycocolloids, cosmetics, and the medicine market, among other uses, thus increasing and diversifying the income of an IMTA system (Neori, 2008).
Until now, the principal consequence of abalone cultivation in Chile has been the harvesting of brown algae from natural marine beds for feed, causing an overexploitation of this resource (Vasquez, 2008). However, the successful development of Macrocystis farming (Westermeir et al., 2006; Macchiavello et al., 2010), currently allows abalone producers to count on fresh biomass. Nonetheless, other problems associated with abalone cultivation have not been noted, and the potential growth of farms and their concentration mainly in bay restricted areas, which possess multiple uses, makes necessary a sustainable plan for expansion in order to avoid environmental conflicts. In this same line, diverse studies have already address the environmental, social, and economical advantages of abalone-seaweed integrated cultivation (Troell et al., 2006; Robertson-Andersson et al., 2008; Bolton et al., 2009; Nobre et al., 2010). Thus, consolidation of abalone farming as an environmentally responsible aquaculture process is highly necessary, and implies an enormous opportunity for the industry to be recognized as one with positive environmental consequences, an especially important goal in Chile, where aquaculture is closely related with salmon farming and its negative environmental impacts of the last decade (Buschmann et al, 2009; FAO, 2009).
In this paper, we evaluated the temporal effectiveness of integrating a land-based culture of red abalone H. rufescens and two well-known algae of the Chilean coast, Ulva lactuca and Gracilaria chilensis, which have been studied in integrated systems, demonstrating high nutrient uptake efficiency and biomass production, and have been mentioned as the most suitable candidates for IMTAs (Neori et al., 2000; Abreu et al., 2009; Bolton et al., 2009). For our evaluation, the algae stocking density and water exchange rate were tested to establish the dissolved nutrient uptake efficiency of U. lactuca and G. chilensis, in addition to measuring the effects on growth rate and productivity of U. lactuca. It was expected that an adequate combination of these factors could maintain optimum efficiency for the integrated culture throughout the year and generate evidence to propose a base-line move from the traditional, monoculture of abalone in Chile, to a sustainable IMTA system.
MATERIALS AND METHODS
The experiments were performed at the Centro de Produccion de Semillas de Abalon of the Universidad Catolica del Norte, Coquimbo, Chile, located in the bahia La Herradura de Guayacan (30[degrees]S, 71[degrees]W). The center cultivates approximately 1200 adult organisms and 50000 seeds of red abalone H. rufescens (10 to 30 mm) with a total seawater flow of 100000 L [h.sup.-1]. The abalones are fed once per week with fresh seaweed, such as Macrocystis, Lessonia, and Ulva. Seawater is captured from the bay through filtered (5 mm) subsea tubes and is subsequently filtered to 50 [micro]m before being introduced into the culture.
Ulva lactuca and Gracilaria chilensis were collected from the bahia La Herradura de Guayacan and cultivated using water originating from the abalone culture, which was accumulated in a tank of 5000 L providing a constant flow of seawater to the cultivated algae. These cultures consisted of twenty-four white fiberglass tanks (twelve for each algae) with a volume of 250 L (100x50x50 cm) and a constant aeration, maintained in outdoor conditions. In these installations, we performed the experiments (Fig. 1). The abiotic conditions during the experiment 1 and 2 were temperature (15 [+ or -] 2[degrees]C), pH (7.9 [+ or -] 1), salinity (35 [+ or -] 1e%o), and photon flux density (794 [+ or -] 190 pmol photon [m.sup.-2] [s.sup.-1]). All these parameters were measured daily.
Experiment 1: Seaweed stocking density
For the experiment, four stocking densities of 1200, 1900, 2600, and 3200 g [m.sup.-2] for G. chilensis and U. lactuca were used. Three culture tanks, as described above (Fig. 1), were used for both G. chilensis and U. lactuca for each stocking density. In all treatments, the water exchange rate was maintained in a continuous seawater flow at 80 L [h.sup.-1]. The algae were cultivated for 60 days, and every 15 days, biomass was harvested to maintain the initial stocking density. Quantitative analysis was performed every 15 days for ammonium, nitrate, and phosphate. For that, three water samples (100 mL) were taken in the seawater inflow, abalone outflow and seaweed outflow (Fig. 1). The analyses were performed using the Strickland & Parson (1972) method, and the results were measured as [micro]mol [L.sup.-1] with a subsequent expression as nutrient uptake efficiency (%), using the following formula:
Nutrient uptake efficiency = 100 - (100 x [C.sub.So]/[C.sub.ao])
where: [C.sub.so] = seaweed outflow concentration, and Cao= abalone outflow concentration.
Experiment 2: Water Exchange Rate (WER)
Four WERs of 60, 80, 125 and 250 L [h.sup.-1] were used to test the nutrient uptake of G. chilensis and U. lactuca. For this experiment, the culture density was maintained at a constant of 1900 g [m.sup.-2]. The algae were cultivated for 60 days, and every 15 days, biomass was harvested to maintain the initial stocking density. The water sampling and analyses were performed and expressed following the same procedures as outlined in Experiment 1.
Experiment 3: Seasonal nutrient uptake efficiency, specific growth rate, and productivity of U. lactuca
Considering the results of the previous experiments, the seasonal experiment chose the species U. lactuca as a model, with a culture density of 1900 g [m.sup.-2] and a WER of 125 L [h.sup.-1]. This species was chosen for its lack of epiphytism in comparison with G. chilensis during experiments 1 and 2. From these same experiments, algae density and seawater flow were chosen based on the best uptake efficiency for N[H.sub.4], N[O.sub.3], and P[O.sub.4] during the cultivation of U. lactuca. Algae were cultivated for one year in twelve tanks of 250 L, as described in experiments 1 and 2. Temperature in culture tanks was registered daily. The algae were weighed monthly and the biomass surplus was withdrawn to maintain initial biomass. For each season, productivity (g [m.sup.-2] [d.sup.-1]) and specific growth rate (SGR) were calculated using the following formula:
SGR(%[d.sup.-1]) = Ln(Wf) - Ln(Wi)/T 100
where, Wf = final wet weight; Wi = initial wet weight; T = days
The homocedasticity and normality of all results were verified. A multivariate ANOVA analysis was conducted for each nutrient source (N[H.sub.4], N[O.sub.3], and P[O.sub.4]) of the experiments 1 and 2 to evaluate the effect of water exchange rate and stock density on uptake efficiency of G. chilensis and U. lactuca, respectively. For SGR and productivity, a one-way ANOVA analysis was performed in order to evaluate differences among seasons. A posterior Tukey's test was used when the treatments showed significant differences (P < 0.05).
During the development of the experiments, the abalone culture constantly supplied nutrients to the seawater. Table 1 reviews the active contribution of nutrients that the abalone culture provided (abalone outflow) and the effect of seaweed culture removing nutrients (seaweed outflow).
Experiment 1: Stocking density
The uptake efficiency of N[H.sub.4] was different between both macroalgae species (ANOVA, F = 28.973, P < 0.05) and stocking densities tested (ANOVA, F = 9.940, P < 0.05). Figure 2 shows that G. chilensis was able to uptake 100% of N[H.sub.4] for all stocking densities tested. However, in the case of U. lactuca, the N[H.sub.4] uptake efficiency was 100% only at the lowest densities (1200 and 1900 g [m.sup.-2]), while at 2600 and 3200 g [m.sup.-2] the N[H.sub.4] uptake efficiency decreased significantly (Tukey, P < 0.05), reaching 89 and 86%, respectively. For both species, N[O.sub.3] uptake efficiency was less than 100% for all stocking densities (Fig. 2). However, no statistical differences were found between the tested species (ANOVA, F = 0.301, P > 0.05) and stocking densities (ANOVA, F = 1.431, P > 0.05). For G. chilensis, values ranged from 65 to 88% at 1900 and 3600 g [m.sup.-2], respectively. U. lactuca showed low variation for N[O.sub.3] uptake efficiency, with the highest uptake efficiency registered at 1200 g [m.sup.-2] (83%) and the lowest at 3200 g [m.sup.-2] (65%). Statistical differences for P[O.sub.4] uptake efficiency were registered for different stocking densities (ANOVA, F = 3.757, P < 0.05). These were produced by the highest and lowest densities registered for U. lactuca (Tukey, P < 0 .05), with maximum P[O.sub.4] uptake efficiency at 1900 and 1200 g [m.sup.-2] (65 and 64%, respectively) and a minimum at 2600 and 3200 g [m.sup.-2] (13%). G. chilensis P[O.sub.4] uptake efficiency did not show significant differences (Tukey, P > 0.05) among stocking densities, and ranged from 38 to 24% at 2600 and 1200 g [m.sup.-2], respectively (Fig. 2).
Experiment 2: Water Exchange Rate (WER)
Figure 3 shows that uptake efficiency of N[H.sub.4], N[O.sub.3], and P[O.sub.4] was different among the WERs used (ANOVA, F = 114.077, P < 0.05) and among the species (ANOVA, F = 73.987, P < 0.05).
For G. chilensis, high N[H.sub.4] uptake efficiency was reached at both 80 and 125 L [h.sup.-1] when compared to uptake at 60 and 250 L [h.sup.-1] (Tukey, P < 0.05). The highest N[H.sub.4] efficiency uptake for this species was registered at 125 L [h.sup.-1] (96 [+ or -] 2%) and the lowest was at 60 L [h.sup.-1] (59 [+ or -] 3%). A similar situation was observed for the N[H.sub.4] uptake efficiency of U. lactuca, where the highest uptake, was registered at 80 L [h.sup.-1] and the lowest, at 250 L [h.sup.-1] (Tukey, P < 0 .05) (Fig. 3).
N[O.sub.3] uptake efficiency of G. chilensis showed differences between the lowest efficiencies at 125 and 250 L [h.sup.-1] (66 [+ or -] 4 and 67 [+ or -] 4%, respectively) and highest efficiency at 80 L [h.sup.-1] (85 [+ or -] 2%) (Tukey, P < 0.05). For U. lactuca, differences were obtained between the lowest N[O.sub.3] uptake efficiency at 250 L [h.sup.-1] (72 [+ or -] 3%) when compared to the efficiencies of 125 L [h.sup.-1] (82 [+ or -] 2%) and of 80 and 60 L [h.sup.-1] (89 [+ or -] 1%) (Tukey, P < 0.05).
P[O.sub.4] uptake efficiency of G. chilensis did not display significant differences at 60, 80, or 125 L [h.sup.-1] (36 [+ or -] 7%), however these treatments were significantly higher than the P[O.sub.4] uptake efficiency at 250 L [h.sup.-1] (16 [+ or -] 9%) (Tukey, P < 0.05). In the case of U. lactuca, P[O.sub.4] uptake efficiency decreased significantly from 60 L [h.sup.-1] (30 [+ or -] 8%) to 250 L [h.sup.-1] (14 [+ or -] 10%) (Tukey, P < 0.05).
At the end of Experiments 1 and 2, G. chilensis showed a high degree of epiphytism, principally detected through the abundant presence of brown filamentous algae.
Experiment 3: seasonal nutrient uptake of U. lactuca
The uptake efficiency of U. lactuca shows a clear seasonal variation for all nutrients studied (ANOVA, F = 778.348, P < 0.05), and increased from autumn and reached a peak in the spring before declining again in the summer (Fig. 4). For N[H.sub.4], N[O.sub.3], and P[O.sub.4] the highest uptake efficiencies were recorded in the spring with 100, 64 [+ or -] 1, and 47 [+ or -] 3%, respectively. The lowest uptake was recorded in the autumn for N[H.sub.4] (57 [+ or -] 2%) and P[O.sub.4] (26 [+ or -] 1%), while for N[O.sub.3] this was recorded in the summer (49 [+ or -] 1%).
Specific growth rate and productivity of U. lactuca
U. lactuca showed seasonal variation for SGR (ANOVA, F = 12.470, P < 0.05) and productivity (ANOVA, F = 17.276, P < 0.05), with a clear increase from autumn until summer and with ranges between 0.5 [+ or -] 0.2 to 2.6 [+ or -] 0.2 % [d.sup.-1] and 10 [+ or -] 6.1 to 73.6 [+ or -] 8.4 g [m.sup.-2] [d.sup.-1] for SGR and productivity, respectively (Fig. 5).
The temperatures registered in seaweed culture tanks were increasing from winter to summer (autumn 15 [+ or -] 1; winter 15 [+ or -] 2; spring 16 [+ or -] 1 and summer 20 [+ or -] 1[degrees]C).
The results show that both G. chilensis and U. lactuca were efficient in capturing the inorganic nutrients originating from the abalone culture in all of the experimental conditions tested, although there were differences depending on the stocking density and water exchange rate. However, the uptake efficiency of N[H.sub.4], N[O.sub.3], and P[O.sub.4] registered for both species was greater than the contribution of these nutrients given by the abalone culture, translating into a guaranteed total remediation of treated wastewater. Of the inorganic nutrient sources evaluated in this study, N[H.sub.4] was the most absorbed by U. lactuca and G. chilensis for both the stocking density and water exchange rate experiments. In this same line, the ability of algae to capture N[O.sub.3] and N[H.sub.4] has been well described, with various studies reporting the high affinity of both Gracilaria (Jones et al., 2001; Abreu et al., 2011) and Ulva (Harlin et al., 1978; Thomas & Harrison, 1987) in efficiently capturing N[H.sub.4].
The importance of seaweed stock density for the productivity and nutrient uptake efficiency in a biofiltration system has been widely documented (Neori et al., 1991; Chopin et al., 2001; Zhou et al., 2006). In Experiment 1, G. chilensis demonstrated a high uptake efficiency for the three sources of inorganic nutrients, which was clearly evidenced by the total removal of N[H.sub.4] in all stocking densities tested. These results confirm those reported for diverse species such as Gracilaria vermiculophylla (Abreu et al., 2011), Gracilaria bursa pastoris (Matos et al., 2006) and U. lactuca (Cohen & Neori, 1991), where stocking density has resulted in being inversely proportional to nutrient uptake. Furthermore, it has been reported that a high stocking density affects an adequate access to light, producing shading and limiting photosynthesis which ultimately diminished the productivity of the algae and thus the demand for nutrients (Matos et al., 2006). Given these results, it is possible to determine that the maximum density permitted to guarantee the greatest uptake of nutrients in U. lactuca is 1900 g [m.sup.-2], similar to the stocking density described by RobertsonAndersson et al. (2008) for this same species. This same stocking density could be recommended for G. chilensis, despite that uptake efficiency is maintained even at 2600 and 3200 g [m.sup.-2]. However, a lower density would permit a better operating control of the culture. This stocking density is lower than the 3000 g [m.sup.-2], reported by Abreu et al. (2011) for G. vermiculophyta and the 7000 g [m.sup.-2] recommended by Chow et al. (2001) when using G. chilensis for the treatment of wastewater originating from fish and oysters.
It is expected that the greatest uptake efficiency would be reached with the lowest water exchange rate (Chopin et al., 2001). This situation was clearly observed for U. lactuca where lower uptake efficiency was measured for all three nutrients at the high WER of 250 L [h.sup.-1], a situation which was repeated for G. chilensis with the uptake of P[O.sub.4]. However, a contrary situation was observed for G. chilensis where a lower uptake efficiency of N[H.sub.4] and N[O.sub.3] was observed at 60 L [h.sup.-1]. Despite that the cultures were maintained with constant aeration, these results could be associated with a deficiency of inorganic carbon (IC), which has already been mentioned as the first element that diminishes in a tank cultivation system (Craigie & Shacklock, 1995) and that directly affecting the capacity for photosynthesis. On the other hand, high epiphyte load detected on G. chilensis at the end of experiments too could explain the reduction of its uptake efficiency.
On the other hand, temperature has also been mentioned as a factor which limits uptake efficiency, especially when a low water exchange rate is maintained in systems exposed to varying local conditions, as were used in this study (Abreu et al., 2011). However, during this study, no temperature increase was detected that exceeded the tolerance limits of each species, but this factor should be given special consideration when performing cultivations in the north of Chile. For this, a water exchange rate of 125 L [h.sup.-1] is recommended for both species, which will effectively diminish nutrient concentration, cleaning a greater volume of wastewater while ensuring adequate conditions for algae cultivation.
At the end of Experiments 1 and 2, G. chilensis showed an important level of epiphytism, principally being affected by filamentous algae. Concerning this subject, several descriptions have been made mentioning epiphytism for Gracilaria, both for massive sea cultivations and in tanks (Oliveira et al., 2000), which is one of the principal problems for the commercial aquaculture of this species. Some authors have noted severe problems of epiphytes in algae used in biofiltration systems (Robertson-Andersson et al., 2008), affecting growth and, in some cases, producing a total loss of biomass. Instead, U. lactuca remained free of epiphytes and was thus chosen for the seasonal experiments.
During Experiment 3 it was possible to observe that uptake efficiency was clearly seasonal for the three nutrients evaluated, increasing in autumn and reaching a maximum efficiency in spring before diminishing in summer. This result allows a total removal of the N[H.sub.4] produced by the abalone culture in spring, while in autumn, winter and summer, only an uptake efficiency of 57 [+ or -] 2%, 79 [+ or -] 2% and 80 [+ or -] 2% respectively, is achieved. On the other hand, although the uptake efficiency for N[O.sub.3] and P[O.sub.4] was less than N[H.sub.4] in all seasons, it allowed a total removal of the nutrients produced by the abalone during the entire year. These results show high uptake efficiency in eliminating N[H.sub.4], N[O.sub.3], and P[O.sub.4] waste of the abalone H. rufescens cultivated on the coast of Chile. This is in agreement with various experiences in different latitudes which mentioned U. lactuca as one of the best candidates for use in a biofiltration system with abalones and other species (Cohen & Neori, 1991; Neori et al., 1996, 1998, 2000; Schuenhoff et al., 2002; Robertson-Andersson et al., 2008; Bolton et al., 2009; Da Silva et al., 2009).
Although the principal objective of this study was to determine the nutrient uptake efficiency of two algae from the Chilean coast, growth rate and seasonal productivity were also evaluated for U. lactuca, given the importance that the algae could have for the same abalone culture as a food source for adult specimens (Mai et al., 1994; Shpigel et al., 1996; Corazani & Illanes, 1998; Shpigel et al., 1999; Troell et al., 2006) or as a source of propagules for the settlement and feeding of abalone larvae and postlarvae (Munoz et al., 2012), as well as for other increasingly used purposes, such as a healthy food option for humans (Higashi-Okai et al., 1999; Yamori et al., 2001; Aceves et al., 2005).
The seasonal increase in growth rate and productivity of U. lactuca from autumn to summer has a close relationship with the seasonal uptake efficiency of N[H.sub.4], N[O.sub.3], and P[O.sub.4], as more nutrients are being captured during greater growth. This seasonal variation in biomass gain has been found among various species of algae used in integrated cultivation systems (Matos et al., 2006; Robertson-Andersson et al., 2008). As it has been reported several times, this situation appears to be predominately dependent on the seasonal variation of temperature and light (Neori et al., 1998), two recognized factors controlling the growth of algae (Bulboa & Macchiavello, 2001).
For the results registered in this study, we conclude that there is a sufficient basis for demonstrating the high possibility for changing the traditional, monoculture system of abalone in Chile to one of a sustainable IMTA system, including U. lactuca as a biofiltration unit to reach positive environmental externalities.
In this context, to reduce the N[H.sub.4], N[O.sub.3], and P[O.sub.4] output of an abalone production center with an approximate outflow of 100000 L [h.sup.-1], a total biomass of 760 kg of U. lactuca distributed in tanks at a stocking density of 1900 g [m.sup.-2] and with a water exchange rate of 125 L [h.sup.-1] would be needed. These installations would occupy an area of approximately 400 [m.sup.2].
Our results confirm that U. lactuca should be considered a serious candidate in the implementation of wastewater treatment plans from abalone cultures in Chile, as it presents important advantages such as high uptake efficiency, wide distribution and abundance, resistance to environmental variations, easy culture management, and scarce epiphytism.
Received: 27 February 2013; Accepted: 22 May 2014
We gratefully appreciate the efforts of the staff of AWABI of Universidad Catolica del Norte. We also thank Gonzalo Fredes and Sebastian Menares for providing figure 1 and Mario Edding for reviewing the earlier draft. The present study was supported by FONDEF (Grant D96/1102).
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Juan Macchiavello (1) & Cristian Bulboa (2)
(1) Departamento de Biologia Marina, Facultad de Ciencias del Mar, Universidad Catolica del Norte P.O. Box 117, Coquimbo, Chile
(2) Departamento de Ecologia y Biodiversidad, Facultad de Ecologia y Recursos Naturales Universidad Andres Bello, Avda. Republica 440, Santiago, Chile
Corresponding author: Cristian Bulboa (email@example.com)
Table 1. Nutrient concentration (N[H.sub.4], N[O.sub.3] and P[O.sub.4]) registered in seawater inflow, abalone outflow and seaweed outflow in each of the experiments. Data: Mean [+ or -] Standar deviation. Effluent Experiment Species Treatment Seawater inflow Abalone outflow 1200 g [m.sup.-2] Gracilaria 1900 g [m.sup.-2] Seaweed outflow chilensis 2600 g [m.sup.-2] 1 3200 g [m.sup.-2] 1200 g [m.sup.-2] Ulva lactuca 1900 g [m.sup.-2] Seaweed outflow 2600 g [m.sup.-2] 3200 g [m.sup.-2] Seawater inflow Abalone outflow 60 L [h.sup.-1] Gracilaria 80 L [h.sup.-1] Seaweed outflow 2 chilensis 125 L [h.sup.-1] 250 L [h.sup.-1] 60 L [h.sup.-1] Ulva lactuca 80 L [h.sup.-1] Seaweed outflow 125 L [h.sup.-1] 250 L [h.sup.-1] Seawater inflow Autumn Abalone outflow Seaweed outflow Seawater inflow Winter Abalone outflow 3 Ulva lactuca Seaweed outflow Seawater inflow Spring Abalone outflow Seaweed outflow Seawater inflow Summer Abalone outflow Seaweed outflow N[H.sub.4] N[O.sub.3] [micron]mol [micron]mol [L.sup.-1] [L.sup.-1] Experiment Species 0.176 [+ or -] 0.034 6.43 [+ or -] 1.19 0.889 [+ or -] 0.112 7.21 [+ or -] 0.47 0.000 2.91 [+ or -] 0.78 Gracilaria 0.000 3.45 [+ or -] 0.51 chilensis 0.000 2.96 [+ or -] 0.20 1 0.000 3.01 [+ or -] 0.18 0.000 2.01 [+ or -] 0.08 Ulva lactuca 0.000 1.95 [+ or -] 0.01 0.092 [+ or -] 0.013 2.96 [+ or -] 0.20 0.123 [+ or -] 0.074 1.89 [+ or -] 0.03 0.041[+ or -] 0.005 7.47 [+ or -] 0.31 1.045[+ or -] 0.002 8.00 [+ or -] 0.11 0.115 [+ or -] 0.002 2.14 [+ or -] 0.05 Gracilaria 0.120 [+ or -] 0.002 3.00 [+ or -] 0.20 2 chilensis 0.098 [+ or -] 0.012 3.54 [+ or -] 0.08 0.262 [+ or -] 0.013 4.83 [+ or -] 0.19 0.083 [+ or -] 0.014 1.53 [+ or -] 0.07 Ulva lactuca 0.030 [+ or -] 0.003 1.88 [+ or -] 0.13 0.071 [+ or -] 0.01 1.96 [+ or -] 0.06 0.141 [+ or -] 0.003 3.36 [+ or -] 0.09 0.10 [+ or -] 0.07 9.04 [+ or -] 0.95 1.20 [+ or -] 0.77 6.63 [+ or -] 0.97 0.54 [+ or -] 0.39 2.83 [+ or -] 0.45 0.01 [+ or -] 0.01 5.04 [+ or -] 0.93 0.47 [+ or -] 0.06 5.47 [+ or -] 2.19 3 Ulva lactuca 0.04 [+ or -] 0.01 1.57 [+ or -] 0.28 0.38 [+ or -] 0.31 4.67 [+ or -] 3.12 0.75 [+ or -] 0.53 5.17 [+ or -] 2.81 0.30 [+ or -] 0.16 1.95 [+ or -] 1.12 0.28 [+ or -] 0.09 6.71 [+ or -] 5.64 0.59 [+ or -] 0.12 3.75 [+ or -] 1.86 0.16 [+ or -] 0.05 2.03 [+ or -] 1.39 P[O.sub.4] [micron]mol [L.sup.-1] Experiment Species 1.16 [+ or -] 0.22 0.97 [+ or -] 0.26 0.70 [+ or -] 0.19 Gracilaria 0.75 [+ or -] 0.11 chilensis 0.65 [+ or -] 0.26 1 0.66 [+ or -] 0.20 0.53 [+ or -] 0.06 Ulva lactuca 0.42 [+ or -] 0.14 0.88 [+ or -] 0.16 0.79 [+ or -] 0.05 1.28 [+ or -] 0.01 1.95 [+ or -] 0.04 0.72 [+ or -] 0.02 Gracilaria 0.77 [+ or -] 0.01 2 chilensis 0.76 [+ or -] 0.01 1.00 [+ or -] 0.03 0.52 [+ or -] 0.01 Ulva lactuca 0.63 [+ or -] 0.02 0.80 [+ or -] 0.01 0.90 [+ or -] 0.02 0.78 [+ or -] 0.26 1.09 [+ or -] 0.05 0.76 [+ or -] 0.39 0.55 [+ or -] 0.14 0.93 [+ or -] 0.32 3 Ulva lactuca 0.64 [+ or -] 0.19 0.85 [+ or -] 0.25 1.20 [+ or -] 0.51 0.65 [+ or -] 0.20 0.75 [+ or -] 0.32 0.82 [+ or -] 0.33 0.63 [+ or -] 0.31
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|Title Annotation:||articulo en ingles|
|Author:||Macchiavello, Juan; Bulboa, Cristian|
|Publication:||Latin American Journal of Aquatic Research|
|Date:||Jul 1, 2014|
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