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Nutrient removal in a closed silvofishery system using three mangrove species (Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle)
Marine Pollution Bulletin 91 (2015) 243–248
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Nutrient removal in a closed silvofishery system using three mangrove species (Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle) R. De-León-Herrera a, F. Flores-Verdugo a, F. Flores-de-Santiago b,⇑, F. González-Farías b a b
Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Unidad Académica Mazatlán, Av. Joel Montes Camarena s/n, Mazatlán, Sinaloa 82040, Mexico Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, A.P. 70-305, Av. Universidad 3000, Ciudad Universitaria, Coyoacán D.F. 04510, Mexico
a r t i c l e
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Article history: Available online 12 December 2014 Keywords: Nutrient removal Dormitator latifrons Semi-arid region Mangrove
a b s t r a c t 3 The removal of ammonium (NH+4), nitrite (NO 2 ), nitrate (NO3 ), and phosphate (PO4 ) in a closed silvofishery system was examined using three mangrove species (i.e., Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle). Specifically, six closed tanks were installed for this experiment with a population of 60 Dormitator latifrons fishes per tank. We planted 40 seedlings in each of three experimental tanks separated by species, while the remaining tanks were used as control. During 15 weeks, nutrient concentrations among the three mangrove systems presented no significant differences (P > 0.05). However, nutrient removal variability was minimum during the last 2–5 weeks. Mangroves presented an average efficiency of 63% for the removal of NH+4 and NO 2 . Contrary, the average removal 3 potential of NO 3 and PO4 was 50%. Results from this study suggest that the three mangrove species 3 could be used in a closed silvofishery systems for the biological removal of NH+4, NO 2 , NO3 , and PO4 . Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Aquaculture has grown enormously over the past 30 years with an average annual rate of 8.8%. In 2008, 46% of the global human consumption of fish, crustaceans, and mollusks originated from aquaculture facilities (FAO, 2012). This expansion has mainly been driven by a considerable growth in productivity (Asche, 2008) and an increasing demand for aquatic resources (Jensen et al., 2014). In fact, mean annual global fish consumption climbed from 16 kg per capita in 2000 to 18.6 kg per capita in 2010 (FAO, 2012). By 2018, intensive aquaculture systems will provide half of the total demand of global fish for direct human consumption. Furthermore, aquaculture facilities are forecast to provide an additional 22 million tons of fish by the year 2022 (FAO, 2012). The increasing practices of aquaculture production have caused an escalating problem associated with eutrophication and hypereutrophication of adjacent bodies of waters (Bouwman et al., 2013; Herbeck et al., 2014). It has been noted that the principal factors in determining the extent of negative effects on the environment depends on the type of cultivated organisms, the location (i.e., ocean, coastal lagoons, reservoirs), the number of species, the ⇑ Corresponding author. Tel.: +52 (555) 623 0222x44636. E-mail addresses: (F. Flores-de-Santiago).
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http://dx.doi.org/10.1016/j.marpolbul.2014.11.040 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
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management practices (i.e., intensive, semi-intensive, extensive), and the quality and quantity of supplied food (Naylor et al., 2000; Fernandes et al., 2001; Islam and Tanaka, 2004; Islam, 2005; Schneider et al., 2005; Sarà, 2007; Bao et al., 2013; Buhmann and Papenbrock, 2013; Herbeck et al., 2014; Toufique and Belton, 2014). Aquaculture facilities contain various chemical compounds that can be very harmful for the organisms and the environment. This is commonly the result of a persistent accumulation of nutrients, especially in semi-closed or closed recirculating systems where little or no water is exchanged. The culture organisms convert about 10–35% of the nitrogen (N) and phosphorus (P) into biomass, while the rest is excluded as dissolved organic or inorganic nutrients into the aquaculture tank (Shimoda et al., 2007; Herbeck et al., 2014). As a consequence, aquaculture effluents contain a considerable amount of N and P compounds (Schneider et al., 2005; Buhmann and Papenbrock, 2013; Herbeck et al., 2014). Among these compounds, ammonium (NH+4) and nitrite (NO 2 ) are toxic for the cultured organisms, and nitrate (NO 3 ) is toxic only at higher concentrations (Camargo et al., 2005). If these compounds in the effluents leave the aquaculture facilities untreated, ammonium, nitrite, nitrate, and phosphate (PO3 4 ) can cause hyper-eutrophication of adjacent ecosystems (Herbeck et al., 2014). In fact, NO 3 and PO3 4 are assumed to be the limiting nutrients in freshwater and marine aquatic ecosystems (Sundareshwar et al., 2003). Therefore,
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high nutrient concentrations can cause massive algal blooms affecting the appearance and internal chemical cycles of local water ecosystems. The environmental problems caused by the excessive amount of nutrients in the aquaculture effluents, and the implementation of law enforcement restrictions, encouraged ecologists and engineers to develop several types of treatments for the optimal use of aquaculture effluents. Some of these techniques include reverse osmosis (Schoeman and Steyn, 2003), ion exchange (Kim and Benjamin, 2004), electrodialysis (Menkouchi Sahli et al., 2006), activated carbon process (Sison et al., 1995), chemical denitrification (Hu et al., 2002), and microbial treatment (Zaitsev et al., 2008). Although these techniques are effective at the removal of nutrients from contaminated water, the operational scale is small and the cost is expensive. Therefore, cost-efficient methods are currently not developed to deal with the intensive marine aquaculture industry (Páez-Osuna et al., 2003; Huang et al., 2012). As an alternative, natural and constructed wetlands have been suggested to filter aquaculture effluents due to their low operational cost (Lin et al., 2002, 2003). In the wetland treatment system, the aquatic macrophytes play a significant role in the removal of nutrients from water. The main transformation processes of N compounds in wetland soils include ammonification followed by nitrification and denitrification (Maltais-Landry et al., 2009; Buhmann and Papenbrock, 2013). With regards to P compounds, most of them (80–90%) occur in the form of organic phosphate in the wetland sediment. However, another part of the P is incorporated in plants, and just a small part is present in the form of orthophosphate in the soil (Buhmann and Papenbrock, 2013). Mangrove forests are among the most productive wetland ecosystems along the coastlines of tropical and sub-tropical regions (Bao et al., 2013). These ecosystems have been considered a tolerant group of plants for wastewater effluents due to their enormous demand for nutrients (Yang et al., 2008; Huang et al., 2012). In fact, they play important roles in removing and/or degrading pollutants, including nutrients (e.g., N and P), heavy metals, and pesticides from coastal lagoons and estuaries (Kristensen et al., 2008; Reef et al., 2010; Adame and Lovelock, 2011; Bayen, 2012), as well as controlling the aeration and microbial conditions in the soil (Zhang et al., 2010). Due to the aforementioned reasons, considerable attention has been directed towards the use of natural and constructed mangrove systems, as they provide an alternative low maintenance, low cost, and relative simple method for removal of nutrients (Ye et al., 2001; Páez-Osuna et al., 2003; Huang et al., 2012). The economic profit from aquaculture systems in mangrove environments depends on the support capacity of mangroves in removing nutrients (Rönnbäck, 1999). Therefore, mangroves have been used to remove N and P from wetlands and wastewater. For example, Wong et al. (1997) used two intertidal sampling locations of Kandelia candel and Aegiceras corniculatum trees in order to test the removal rate of organic carbon and total N. Results suggested that these two mangrove species have great potential for natural wastewater treatment. Tam and Wong (1995) applied soil column leaching experiments to assess the retention rate of nutrients and heavy metals in two types of mangrove soils receiving wastewater effluents. Results from this study demonstrated that mangroves were good traps of P and heavy metals, but were less efficient in retaining N from wastewater. Wu et al. (2008) studied the potential use of K. candel as a secondary treatment system for municipal wastewater. Results indicated that it is feasible to use the mangrove K. candel without tidal flushing, as a secondary treatment process for the removal of dissolved organic carbon, ammonia-N, and ortho-phosphates. Yang et al. (2008) performed a pilot-scale mangrove wetland including K. candel, A. corniculatum, and Sonneratia caseolaris for the removal of organic matter and nutrients.
Result from this work suggested that the treatment efficiency of S. caseolaris and A. corniculatum was higher compared to K. candel. Zhang et al. (2010) used a simulated wetland of Sonneratia apetala in order to assess the removal of nutrients and heavy metals using three concentration levels of wastewater. Results indicated that S. apetala had a great potential for the removal of nutrients and heavy metals in coastal areas. Moroyoqui-Rojo et al. (2012) studied the potential use of Laguncularia racemosa and Rhizophora mangle for the removal of inorganic nutrients within shrimp ponds. Results suggested that these two mangrove species presented similar nutrient removal rates and improve the water quality of shrimp aquaculture systems. It is important to mention that previous studies have mainly focused on the treatment efficiency of the mangrove K. candel in tropical latitudes, and no work has been done using the three mangrove species common to the semi-arid regions of the Americas (Avicennia germinans, L. racemosa, and R. mangle). The goal of this study was to investigate the removal of nutrients (i.e., NH+4, NO 2, 3 NO 3 , and PO4 ) by seedlings of A. germinans, L. racemosa, and R. mangle in a closed silvofishery system with a constant population of Dormitator latifrons fishes.
2. Materials and methods 2.1. Collection and monitoring of mangrove seedlings Propagules of A. germinans, L. racemosa, and R. mangle were collected along the Urias coastal lagoon, Pacific coast of Mexico located between 23°130 –23°110 N, and 106°230 –106°210 W. The mangrove forests of this semi-arid region typically bloom and produce their respective seeds and propagules during the summer months from June to September (Flores-de-Santiago et al., 2012). Once a sufficient number of propagules were collected, all threemangrove species were planted within individual polyurethane grids floating in a freshwater tank of 8000 l. During a period of 19 months, this hydroponic freshwater tank acted as a conditioning stage for the optimal development of the root system. After this conditioning phase, 40 randomly selected seedlings for each of the three species were separated into individual PVC pipes. Each PVC pipe contained sediment from the study area, had a length of 30 cm, diameter of 10 cm, and presented a constriction at the bottom allowing a 5 cm wide slit. This constriction is very important because it avoids sediment loss and, at the same time, allows mangrove roots to extend and grow outside of the pipe. The PVC pipes were then divided according to the mangrove species into three individual water tanks of 450 l each. These tanks, separated by mangrove species, presented a constructed wooden structure on the surface where all 40 PVC pipes with mangrove seedlings were supported. Salinity within each tank was increased 5 psu per week for a period of seven weeks until a constant concentration of 35 psu was reached and maintained through the experiment. Mangrove seedling height and root lengths were measured periodically using a flexible tape.
2.2. D. latifrons collection and growth A total of 550 juveniles of D. latifrons fishes were collected at the same location of the mangrove propagules. All fishes were transported to the research facility in plastic containers of 70 l. Total length and weight were measured for all fishes at the beginning and the end of the experiment using a standard biometry measuring tape and a digital balance (Ohaus GT 4800). The fishes were feed twice a day with a commercial product of 35% protein (Ángel-Pérez, 2012).
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2.3. Design and construction of the experimental silvofishery systems Six closed sub-surface recirculating water systems were installed for this investigation. Specifically, each system was designed with a vertical flow of water and, as mentioned before, presented a hydroponic mangrove arrangement suspended over the surface by a wooden structure. The first three tanks contained 40 mangrove seedlings each, separated by species, while the remaining three tanks acted as control, only with fishes and no mangrove seedlings. Moreover, each tank supported a constant population of 60 D. latifrons fishes with similar biometric characteristics. 2.4. Properties of water and nutrient analysis Dissolved oxygen, temperature, pH, and salinity were measured daily with a multi-parametric electronic instrument. Additionally, water samples were collected every seven days from all tanks. Water samples were filtered (Whatman GF/C, 45 lm) and chemical nutrient analysis was performed with spectrometric techniques. 3 Specifically, we measured NH+4, NO 2 , NO3 , and PO4 in triplicate following the techniques described by Strickland and Parson (1972). Nutrient removal quantification was based on the equation described by Paniagua-Michel and Garcia (2003):
RN ¼ ½ðC TÞ=C100
ð1Þ
where RN corresponds to the removal concentration in percentage. C is the nutrient concentration in the control tanks, and T is the nutrient concentration in the mangrove tanks. 2.5. Statistical analysis The growth rate of mangrove seedlings was assessed using linear regressions. Specifically, we used the coefficient of determination (R2) and analysis of variance F-test (ANOVA) as a first approach to examine the linear association between average growth and period of time. Additionally, in order to determine whether significant differences existed among the three mangrove species with regards to seedling height and root length, we applied a one-way ANOVA for the three species comparisons (n = 40 per species). The final growth of D. latifrons fishes was determined using exponential regressions between total length and weight from all fishes. Furthermore, the weight and total length between the control and mangrove tanks were examined using nonparametric Kruskal–Wallis statistical test. With regards to the nutrient concentrations, we applied the same non-parametric statistical test between the control and mangrove tanks per week. The chemical properties of water (i.e., dissolved oxygen, temperature, pH, salinity) between the control and mangrove tanks were examined using the same non-parametric Kruskal–Wallis statistical test. 3. Results
Fig. 1. Mangrove seedling height (a) and root length (b) from July 2012 through October 2012. Error bars are denoted for each species. Each graph depicts the linear equation, the coefficient of determination (R2), the number of data (n), and the Fobserved values (F). Asterisks indicate significant F-observed values at a = 0.05.
Fig. 2. Relation between total length and weight of Dormitator latifrons fishes in the control tanks (a) and in the mangrove seedlings tanks (b). Dashed lines represent the 95% confidence bands. Each graph depicts the exponential equation, the coefficient of determination (R2), the number of data (n), and the F-observed values (F). Asterisks indicate significant F-observed values at a = 0.05.
3.1. Growth of mangrove seedlings and D. latifrons fishes Fig. 1 depicts seedling height and root length from three dominant mangrove species of a semi-arid region of Mexico under full saltwater conditions (i.e., 35 psu). The growth rates using height and roots length presented significant differences (P < 0.05) among the three mangrove species since the second month. In fact, L. racemosa showed the highest growth rate of 6.94 cm/month, followed by A. germinans with 2.74 cm/month and R. mangle with 1.29 cm/ month. With regards to the mangrove radicular system, A. germinans presented the highest rate of 4.28 cm/month, followed by L. racemosa with 3.2 cm/month and R. mangle with 1.89 cm/month. Fig. 2 shows the exponential relation between weight and total
length of all D. latifrons fishes in the control tanks (Fig. 2a) and the mangroves system (Fig. 2b). Both graphs from Fig. 2 depict the pool sample of biometric results taken at the beginning and at the end of the experiment. It is important to mention that during the experiment, weight and length distribution of D. latifrons was not significant different between both treatments (P > 0.05). 3.2. Physical and chemical properties of water and nutrient removal percentages by treatment Table 1 shows the physical and chemical variables that were used to test whether these properties of water could change
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between the control and mangrove tanks. During the experiment, there were no significant differences (P > 0.05, n = 105 per variable) between the control and mangrove systems with regards to dissolved oxygen, temperature, pH, and salinity. Moreover, there were also no significant differences (P > 0.05, n = 15 per species) in nutrient concentrations among the three tanks containing the mangrove species. 3 Fig. 3 depicts the nutrient variability (NH+4, NO 2 , NO3 , and PO4 ) between the control and mangrove tanks as well as the nutrient removal percentages. All four inorganic nutrients presented a similar pattern between the two treatments until the addition of D. latifrons fishes on the third week. After this period, nutrient concentration in the control tanks increased compared with the mangrove systems. At the end of the experiment, all of the control tanks presented a higher concentration of nutrients compared with the mangrove tanks. Although nutrient concentration presented significant differences (P < 0.05, n = 15 per nutrient) between the control and mangrove tanks after the eight-week, the nutrient removal percentages showed minimum variability only during the last 2–5 weeks (Fig. 3). Mangroves showed a similar efficiency of 63 ± 2% and 63 ± 0.9% for the removal of NH+4 and NO 2 during the last five and two weeks respectively. Contrary, the average removal 3 potential of NO was slightly lower of 50 ± 7% and 3 and PO4 50 ± 5% during the last four and three weeks respectively.
4. Discussion In this study, we have analyzed the nutrient removal percent 3 age of NH+4, NO 2 , NO3 , and PO4 in a closed silvofishery system, by using three common mangrove species distributed in the semi-arid coast of Mexico. Due to the relatively recent worldwide aquaculture expansion, especially in tropical and sub-tropical latitudes, it is of utmost importance to understand to what degree mangroves could be used to decrease hyper-eutrophication conditions common to aquaculture ponds. It is important to mention that no work has been done previous to our investigation with regards to inorganic nutrient assimilation in silvofishery systems using A. germinans, L. racemosa, and R. mangle along semi-arid regions. The N cycle in mangroves is complex and depends on several environmental conditions. However, N transformation in mangroves occurs by five principal biological processes: ammonification, nitrification, denitrification, nitrogen fixation, and nitrogen assimilation. In our study, the growth of mangroves played a key role in the removal of inorganic forms of N. In fact, the N removal ability of mangroves increases according to the seedlings biomass (Tanner et al., 1995; Yang et al., 2008). Our results indicated that A. germinans, L. racemosa, and R. mangle presented a linear and positive growth in semi-arid regions by absorbing the available N and P from the metabolic residues of D. latifrons fishes and the excess of supplied food. It is well known that the growth rate of mangroves depends on the available nutrients (Saenger, 2002). Based on the statistical results from our study, it is evident that seedlings growth was different among the three mangrove species during our study. Specifically, L. racemosa showed the highest growth compared to A. Table 1 Averageand standard deviation of physical and chemical properties of water within the control and mangrove tanks. Variable
Control tanks
Mangrove tanks
O2 (mg/L) Temperature (°C) pH Salinity (psu)
4.98 ± 1.1 27.2 ± 1.3 7.7 ± 0.3 32 ± 2.6
4.93 ± 1.2 27.3 ± 1.6 7.7 ± 0.2 32 ± 3.1
Fig. 3. Time series of the average nutrient concentration (lM) and nutrient removal percentage (%) from the control and mangrove tanks. (a) NH+4; (b) NO 2 ; (c) NO3 ; and (d) PO3 4 . Black arrows represent the addition of Dormitator latifrons fishes. Error bars are denoted for each nutrient along the time series.
germinans and R. mangle. However, results from our study shows that there were no differences regarding nutrient assimilation rates among the three mangrove species. This result suggests that the three mangrove species have different metabolic adaptations to cue with the available nutrients. Moreover, it is important to mention that the variability of the physical and chemical properties of water were not a limiting factor in the nutrient removal rates and fish development during our experiment, as there were no differences between the control and mangrove tanks. Consequently, any of the three mangrove species could be used as a biological nutrient removal system in small aquaculture ponds along semi-arid regions. In general, the efficient assimilation of N depends on a series of chemical transformations. First, mineralization of organic N to NH+4 occurs followed by nitrification and denitrification. Nitrification is a process of bacterial oxidation where NH+4 is converted to NO 2 or NO 3 . In denitrification, NO3 is reduced to nitrous oxides and N2 where the NO 3 acts as the terminal acceptor during the oxidation of organic compounds (Bowmer, 1987). However, the nitrification and denitrification processes are not clear due to formation of N2O an intermediate product of both nitrification and denitrification (Tam et al., 2009). As mentioned before, NO 3 is removed by denitrification and mangrove uptake. It is obvious that the mangrove plants not only absorb NO 3 for their growth, they also enhance the efficiency of both nitrification and denitrification processes in a closed system (Wu et al., 2008). The assimilation of P in a mangrove system involves many pathways in a complex biogeochemical cycle. Although PO3 4 concentrations are lower compared to N-forms in aquaculture facilities, PO3 4 is considered a limiting nutrient in mangrove forests (Ye et al., 2001). Therefore, the
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principal mechanisms of reduction could include the uptake by the mangrove species (Greenway and Woolley, 1999). Many studies have demonstrated that mangroves could be used in constructed wetlands for nutrient removal treatments (e.g., Wong et al., 1997; Chu et al., 1998; Ye et al., 2001; Boonsong et al., 2003). However, little work has been done on the comparison of nutrient removal efficiencies of different mangrove species (Yang et al., 2008; Ye et al., 2001), especially in semi-arid regions. It is evident that our three mangrove species distributed in semiarid regions are quite different compared to the tropical Bruguiera gymnorrhiza, Rhizophora stylosa, A. corniculatum, and K. candel. The aforementioned tropical mangrove species removed more N and P (42–88%) compared to our mangroves (50–63%) (Wu et al., 2008; Yang et al., 2008; Huang et al., 2012). The most contrasting nutrients removal percentages were from Ye et al. (2001) where they reported N removal efficiencies of 92.7% and 98.0%, and P removal of 88% and 97.8% by K. candel and B. gymnorrhiza in pot-cultivation system under saltwater conditions. Consequently, the understanding of mangroves as importers or exporters of nutrients depends on the location and the environmental factors affecting the biological responses. 5. Conclusions Intensive aquaculture systems have grown enormously over the past decades, and yet, there are just a few studies that assess biological treatment of these effluents. This study aimed to examine the biological nutrient removal efficiency of semi-arid mangrove seedlings in closed silvofishery systems. The observed differences in nutrient concentrations between the mangrove and control tanks indicate a clear pattern that semi-arid mangroves are able to remove a considerable amount of inorganic nutrients. In particular, seedlings of A. germinans, L. racemosa, and R. mangle have potential to remove an average of 63% of NH+4 and NO 2 . Contrary, 3 the average removal efficiency of NO was 50% under 3 and PO4 the same treatments. Given the large geographic extent of impacted areas from aquaculture effluents, the incorporation of mangrove seedlings could be commonly used for close-aquaculture systems in the sub-tropics. For instance, many aquaculture facilities from semi-arid regions lack mechanisms of filtration. Thus, seedlings of A. germinans, L. racemosa, and R. mangle have potential to remove ammonium, nitrite, nitrate, and phosphate from such systems. Hence, the relative cheap cost of this mangrove filtration system makes it an ideal tool in countries where other traditional filtering techniques are economically prohibited. However, the variety of nutrient removal percentages with other commercial fisheries may require extensive studies to become fully evident. Acknowledgements The first author acknowledges financial support through a grant provided by the Consejo Nacional de Ciencia y Tecnología of México (Grant No. 255546). The funding for the field campaigns was provided by the Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM). The third author acknowledges financial support through a grant provided by the Dirección General Asuntos del Personal Académico (DGAPA-UNAM). References Adame, M.F., Lovelock, C.E., 2011. Carbon and nutrient exchange of mangrove forests with the coastal ocean. Hydrobiologia 663, 23–50. http://dx.doi.org/ 10.1007/s10750-010-0554-7.
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Nutrient removal in a closed silvofishery system using three mangrove species (Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle) R. De-León-Herrera a, F. Flores-Verdugo a, F. Flores-de-Santiago b,⇑, F. González-Farías b a b
Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Unidad Académica Mazatlán, Av. Joel Montes Camarena s/n, Mazatlán, Sinaloa 82040, Mexico Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, A.P. 70-305, Av. Universidad 3000, Ciudad Universitaria, Coyoacán D.F. 04510, Mexico
a r t i c l e
i n f o
Article history: Available online 12 December 2014 Keywords: Nutrient removal Dormitator latifrons Semi-arid region Mangrove
a b s t r a c t 3 The removal of ammonium (NH+4), nitrite (NO 2 ), nitrate (NO3 ), and phosphate (PO4 ) in a closed silvofishery system was examined using three mangrove species (i.e., Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle). Specifically, six closed tanks were installed for this experiment with a population of 60 Dormitator latifrons fishes per tank. We planted 40 seedlings in each of three experimental tanks separated by species, while the remaining tanks were used as control. During 15 weeks, nutrient concentrations among the three mangrove systems presented no significant differences (P > 0.05). However, nutrient removal variability was minimum during the last 2–5 weeks. Mangroves presented an average efficiency of 63% for the removal of NH+4 and NO 2 . Contrary, the average removal 3 potential of NO 3 and PO4 was 50%. Results from this study suggest that the three mangrove species 3 could be used in a closed silvofishery systems for the biological removal of NH+4, NO 2 , NO3 , and PO4 . Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Aquaculture has grown enormously over the past 30 years with an average annual rate of 8.8%. In 2008, 46% of the global human consumption of fish, crustaceans, and mollusks originated from aquaculture facilities (FAO, 2012). This expansion has mainly been driven by a considerable growth in productivity (Asche, 2008) and an increasing demand for aquatic resources (Jensen et al., 2014). In fact, mean annual global fish consumption climbed from 16 kg per capita in 2000 to 18.6 kg per capita in 2010 (FAO, 2012). By 2018, intensive aquaculture systems will provide half of the total demand of global fish for direct human consumption. Furthermore, aquaculture facilities are forecast to provide an additional 22 million tons of fish by the year 2022 (FAO, 2012). The increasing practices of aquaculture production have caused an escalating problem associated with eutrophication and hypereutrophication of adjacent bodies of waters (Bouwman et al., 2013; Herbeck et al., 2014). It has been noted that the principal factors in determining the extent of negative effects on the environment depends on the type of cultivated organisms, the location (i.e., ocean, coastal lagoons, reservoirs), the number of species, the ⇑ Corresponding author. Tel.: +52 (555) 623 0222x44636. E-mail addresses: (F. Flores-de-Santiago).
fl[email protected],
http://dx.doi.org/10.1016/j.marpolbul.2014.11.040 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
ffl[email protected]
management practices (i.e., intensive, semi-intensive, extensive), and the quality and quantity of supplied food (Naylor et al., 2000; Fernandes et al., 2001; Islam and Tanaka, 2004; Islam, 2005; Schneider et al., 2005; Sarà, 2007; Bao et al., 2013; Buhmann and Papenbrock, 2013; Herbeck et al., 2014; Toufique and Belton, 2014). Aquaculture facilities contain various chemical compounds that can be very harmful for the organisms and the environment. This is commonly the result of a persistent accumulation of nutrients, especially in semi-closed or closed recirculating systems where little or no water is exchanged. The culture organisms convert about 10–35% of the nitrogen (N) and phosphorus (P) into biomass, while the rest is excluded as dissolved organic or inorganic nutrients into the aquaculture tank (Shimoda et al., 2007; Herbeck et al., 2014). As a consequence, aquaculture effluents contain a considerable amount of N and P compounds (Schneider et al., 2005; Buhmann and Papenbrock, 2013; Herbeck et al., 2014). Among these compounds, ammonium (NH+4) and nitrite (NO 2 ) are toxic for the cultured organisms, and nitrate (NO 3 ) is toxic only at higher concentrations (Camargo et al., 2005). If these compounds in the effluents leave the aquaculture facilities untreated, ammonium, nitrite, nitrate, and phosphate (PO3 4 ) can cause hyper-eutrophication of adjacent ecosystems (Herbeck et al., 2014). In fact, NO 3 and PO3 4 are assumed to be the limiting nutrients in freshwater and marine aquatic ecosystems (Sundareshwar et al., 2003). Therefore,
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high nutrient concentrations can cause massive algal blooms affecting the appearance and internal chemical cycles of local water ecosystems. The environmental problems caused by the excessive amount of nutrients in the aquaculture effluents, and the implementation of law enforcement restrictions, encouraged ecologists and engineers to develop several types of treatments for the optimal use of aquaculture effluents. Some of these techniques include reverse osmosis (Schoeman and Steyn, 2003), ion exchange (Kim and Benjamin, 2004), electrodialysis (Menkouchi Sahli et al., 2006), activated carbon process (Sison et al., 1995), chemical denitrification (Hu et al., 2002), and microbial treatment (Zaitsev et al., 2008). Although these techniques are effective at the removal of nutrients from contaminated water, the operational scale is small and the cost is expensive. Therefore, cost-efficient methods are currently not developed to deal with the intensive marine aquaculture industry (Páez-Osuna et al., 2003; Huang et al., 2012). As an alternative, natural and constructed wetlands have been suggested to filter aquaculture effluents due to their low operational cost (Lin et al., 2002, 2003). In the wetland treatment system, the aquatic macrophytes play a significant role in the removal of nutrients from water. The main transformation processes of N compounds in wetland soils include ammonification followed by nitrification and denitrification (Maltais-Landry et al., 2009; Buhmann and Papenbrock, 2013). With regards to P compounds, most of them (80–90%) occur in the form of organic phosphate in the wetland sediment. However, another part of the P is incorporated in plants, and just a small part is present in the form of orthophosphate in the soil (Buhmann and Papenbrock, 2013). Mangrove forests are among the most productive wetland ecosystems along the coastlines of tropical and sub-tropical regions (Bao et al., 2013). These ecosystems have been considered a tolerant group of plants for wastewater effluents due to their enormous demand for nutrients (Yang et al., 2008; Huang et al., 2012). In fact, they play important roles in removing and/or degrading pollutants, including nutrients (e.g., N and P), heavy metals, and pesticides from coastal lagoons and estuaries (Kristensen et al., 2008; Reef et al., 2010; Adame and Lovelock, 2011; Bayen, 2012), as well as controlling the aeration and microbial conditions in the soil (Zhang et al., 2010). Due to the aforementioned reasons, considerable attention has been directed towards the use of natural and constructed mangrove systems, as they provide an alternative low maintenance, low cost, and relative simple method for removal of nutrients (Ye et al., 2001; Páez-Osuna et al., 2003; Huang et al., 2012). The economic profit from aquaculture systems in mangrove environments depends on the support capacity of mangroves in removing nutrients (Rönnbäck, 1999). Therefore, mangroves have been used to remove N and P from wetlands and wastewater. For example, Wong et al. (1997) used two intertidal sampling locations of Kandelia candel and Aegiceras corniculatum trees in order to test the removal rate of organic carbon and total N. Results suggested that these two mangrove species have great potential for natural wastewater treatment. Tam and Wong (1995) applied soil column leaching experiments to assess the retention rate of nutrients and heavy metals in two types of mangrove soils receiving wastewater effluents. Results from this study demonstrated that mangroves were good traps of P and heavy metals, but were less efficient in retaining N from wastewater. Wu et al. (2008) studied the potential use of K. candel as a secondary treatment system for municipal wastewater. Results indicated that it is feasible to use the mangrove K. candel without tidal flushing, as a secondary treatment process for the removal of dissolved organic carbon, ammonia-N, and ortho-phosphates. Yang et al. (2008) performed a pilot-scale mangrove wetland including K. candel, A. corniculatum, and Sonneratia caseolaris for the removal of organic matter and nutrients.
Result from this work suggested that the treatment efficiency of S. caseolaris and A. corniculatum was higher compared to K. candel. Zhang et al. (2010) used a simulated wetland of Sonneratia apetala in order to assess the removal of nutrients and heavy metals using three concentration levels of wastewater. Results indicated that S. apetala had a great potential for the removal of nutrients and heavy metals in coastal areas. Moroyoqui-Rojo et al. (2012) studied the potential use of Laguncularia racemosa and Rhizophora mangle for the removal of inorganic nutrients within shrimp ponds. Results suggested that these two mangrove species presented similar nutrient removal rates and improve the water quality of shrimp aquaculture systems. It is important to mention that previous studies have mainly focused on the treatment efficiency of the mangrove K. candel in tropical latitudes, and no work has been done using the three mangrove species common to the semi-arid regions of the Americas (Avicennia germinans, L. racemosa, and R. mangle). The goal of this study was to investigate the removal of nutrients (i.e., NH+4, NO 2, 3 NO 3 , and PO4 ) by seedlings of A. germinans, L. racemosa, and R. mangle in a closed silvofishery system with a constant population of Dormitator latifrons fishes.
2. Materials and methods 2.1. Collection and monitoring of mangrove seedlings Propagules of A. germinans, L. racemosa, and R. mangle were collected along the Urias coastal lagoon, Pacific coast of Mexico located between 23°130 –23°110 N, and 106°230 –106°210 W. The mangrove forests of this semi-arid region typically bloom and produce their respective seeds and propagules during the summer months from June to September (Flores-de-Santiago et al., 2012). Once a sufficient number of propagules were collected, all threemangrove species were planted within individual polyurethane grids floating in a freshwater tank of 8000 l. During a period of 19 months, this hydroponic freshwater tank acted as a conditioning stage for the optimal development of the root system. After this conditioning phase, 40 randomly selected seedlings for each of the three species were separated into individual PVC pipes. Each PVC pipe contained sediment from the study area, had a length of 30 cm, diameter of 10 cm, and presented a constriction at the bottom allowing a 5 cm wide slit. This constriction is very important because it avoids sediment loss and, at the same time, allows mangrove roots to extend and grow outside of the pipe. The PVC pipes were then divided according to the mangrove species into three individual water tanks of 450 l each. These tanks, separated by mangrove species, presented a constructed wooden structure on the surface where all 40 PVC pipes with mangrove seedlings were supported. Salinity within each tank was increased 5 psu per week for a period of seven weeks until a constant concentration of 35 psu was reached and maintained through the experiment. Mangrove seedling height and root lengths were measured periodically using a flexible tape.
2.2. D. latifrons collection and growth A total of 550 juveniles of D. latifrons fishes were collected at the same location of the mangrove propagules. All fishes were transported to the research facility in plastic containers of 70 l. Total length and weight were measured for all fishes at the beginning and the end of the experiment using a standard biometry measuring tape and a digital balance (Ohaus GT 4800). The fishes were feed twice a day with a commercial product of 35% protein (Ángel-Pérez, 2012).
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2.3. Design and construction of the experimental silvofishery systems Six closed sub-surface recirculating water systems were installed for this investigation. Specifically, each system was designed with a vertical flow of water and, as mentioned before, presented a hydroponic mangrove arrangement suspended over the surface by a wooden structure. The first three tanks contained 40 mangrove seedlings each, separated by species, while the remaining three tanks acted as control, only with fishes and no mangrove seedlings. Moreover, each tank supported a constant population of 60 D. latifrons fishes with similar biometric characteristics. 2.4. Properties of water and nutrient analysis Dissolved oxygen, temperature, pH, and salinity were measured daily with a multi-parametric electronic instrument. Additionally, water samples were collected every seven days from all tanks. Water samples were filtered (Whatman GF/C, 45 lm) and chemical nutrient analysis was performed with spectrometric techniques. 3 Specifically, we measured NH+4, NO 2 , NO3 , and PO4 in triplicate following the techniques described by Strickland and Parson (1972). Nutrient removal quantification was based on the equation described by Paniagua-Michel and Garcia (2003):
RN ¼ ½ðC TÞ=C100
ð1Þ
where RN corresponds to the removal concentration in percentage. C is the nutrient concentration in the control tanks, and T is the nutrient concentration in the mangrove tanks. 2.5. Statistical analysis The growth rate of mangrove seedlings was assessed using linear regressions. Specifically, we used the coefficient of determination (R2) and analysis of variance F-test (ANOVA) as a first approach to examine the linear association between average growth and period of time. Additionally, in order to determine whether significant differences existed among the three mangrove species with regards to seedling height and root length, we applied a one-way ANOVA for the three species comparisons (n = 40 per species). The final growth of D. latifrons fishes was determined using exponential regressions between total length and weight from all fishes. Furthermore, the weight and total length between the control and mangrove tanks were examined using nonparametric Kruskal–Wallis statistical test. With regards to the nutrient concentrations, we applied the same non-parametric statistical test between the control and mangrove tanks per week. The chemical properties of water (i.e., dissolved oxygen, temperature, pH, salinity) between the control and mangrove tanks were examined using the same non-parametric Kruskal–Wallis statistical test. 3. Results
Fig. 1. Mangrove seedling height (a) and root length (b) from July 2012 through October 2012. Error bars are denoted for each species. Each graph depicts the linear equation, the coefficient of determination (R2), the number of data (n), and the Fobserved values (F). Asterisks indicate significant F-observed values at a = 0.05.
Fig. 2. Relation between total length and weight of Dormitator latifrons fishes in the control tanks (a) and in the mangrove seedlings tanks (b). Dashed lines represent the 95% confidence bands. Each graph depicts the exponential equation, the coefficient of determination (R2), the number of data (n), and the F-observed values (F). Asterisks indicate significant F-observed values at a = 0.05.
3.1. Growth of mangrove seedlings and D. latifrons fishes Fig. 1 depicts seedling height and root length from three dominant mangrove species of a semi-arid region of Mexico under full saltwater conditions (i.e., 35 psu). The growth rates using height and roots length presented significant differences (P < 0.05) among the three mangrove species since the second month. In fact, L. racemosa showed the highest growth rate of 6.94 cm/month, followed by A. germinans with 2.74 cm/month and R. mangle with 1.29 cm/ month. With regards to the mangrove radicular system, A. germinans presented the highest rate of 4.28 cm/month, followed by L. racemosa with 3.2 cm/month and R. mangle with 1.89 cm/month. Fig. 2 shows the exponential relation between weight and total
length of all D. latifrons fishes in the control tanks (Fig. 2a) and the mangroves system (Fig. 2b). Both graphs from Fig. 2 depict the pool sample of biometric results taken at the beginning and at the end of the experiment. It is important to mention that during the experiment, weight and length distribution of D. latifrons was not significant different between both treatments (P > 0.05). 3.2. Physical and chemical properties of water and nutrient removal percentages by treatment Table 1 shows the physical and chemical variables that were used to test whether these properties of water could change
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between the control and mangrove tanks. During the experiment, there were no significant differences (P > 0.05, n = 105 per variable) between the control and mangrove systems with regards to dissolved oxygen, temperature, pH, and salinity. Moreover, there were also no significant differences (P > 0.05, n = 15 per species) in nutrient concentrations among the three tanks containing the mangrove species. 3 Fig. 3 depicts the nutrient variability (NH+4, NO 2 , NO3 , and PO4 ) between the control and mangrove tanks as well as the nutrient removal percentages. All four inorganic nutrients presented a similar pattern between the two treatments until the addition of D. latifrons fishes on the third week. After this period, nutrient concentration in the control tanks increased compared with the mangrove systems. At the end of the experiment, all of the control tanks presented a higher concentration of nutrients compared with the mangrove tanks. Although nutrient concentration presented significant differences (P < 0.05, n = 15 per nutrient) between the control and mangrove tanks after the eight-week, the nutrient removal percentages showed minimum variability only during the last 2–5 weeks (Fig. 3). Mangroves showed a similar efficiency of 63 ± 2% and 63 ± 0.9% for the removal of NH+4 and NO 2 during the last five and two weeks respectively. Contrary, the average removal 3 potential of NO was slightly lower of 50 ± 7% and 3 and PO4 50 ± 5% during the last four and three weeks respectively.
4. Discussion In this study, we have analyzed the nutrient removal percent 3 age of NH+4, NO 2 , NO3 , and PO4 in a closed silvofishery system, by using three common mangrove species distributed in the semi-arid coast of Mexico. Due to the relatively recent worldwide aquaculture expansion, especially in tropical and sub-tropical latitudes, it is of utmost importance to understand to what degree mangroves could be used to decrease hyper-eutrophication conditions common to aquaculture ponds. It is important to mention that no work has been done previous to our investigation with regards to inorganic nutrient assimilation in silvofishery systems using A. germinans, L. racemosa, and R. mangle along semi-arid regions. The N cycle in mangroves is complex and depends on several environmental conditions. However, N transformation in mangroves occurs by five principal biological processes: ammonification, nitrification, denitrification, nitrogen fixation, and nitrogen assimilation. In our study, the growth of mangroves played a key role in the removal of inorganic forms of N. In fact, the N removal ability of mangroves increases according to the seedlings biomass (Tanner et al., 1995; Yang et al., 2008). Our results indicated that A. germinans, L. racemosa, and R. mangle presented a linear and positive growth in semi-arid regions by absorbing the available N and P from the metabolic residues of D. latifrons fishes and the excess of supplied food. It is well known that the growth rate of mangroves depends on the available nutrients (Saenger, 2002). Based on the statistical results from our study, it is evident that seedlings growth was different among the three mangrove species during our study. Specifically, L. racemosa showed the highest growth compared to A. Table 1 Averageand standard deviation of physical and chemical properties of water within the control and mangrove tanks. Variable
Control tanks
Mangrove tanks
O2 (mg/L) Temperature (°C) pH Salinity (psu)
4.98 ± 1.1 27.2 ± 1.3 7.7 ± 0.3 32 ± 2.6
4.93 ± 1.2 27.3 ± 1.6 7.7 ± 0.2 32 ± 3.1
Fig. 3. Time series of the average nutrient concentration (lM) and nutrient removal percentage (%) from the control and mangrove tanks. (a) NH+4; (b) NO 2 ; (c) NO3 ; and (d) PO3 4 . Black arrows represent the addition of Dormitator latifrons fishes. Error bars are denoted for each nutrient along the time series.
germinans and R. mangle. However, results from our study shows that there were no differences regarding nutrient assimilation rates among the three mangrove species. This result suggests that the three mangrove species have different metabolic adaptations to cue with the available nutrients. Moreover, it is important to mention that the variability of the physical and chemical properties of water were not a limiting factor in the nutrient removal rates and fish development during our experiment, as there were no differences between the control and mangrove tanks. Consequently, any of the three mangrove species could be used as a biological nutrient removal system in small aquaculture ponds along semi-arid regions. In general, the efficient assimilation of N depends on a series of chemical transformations. First, mineralization of organic N to NH+4 occurs followed by nitrification and denitrification. Nitrification is a process of bacterial oxidation where NH+4 is converted to NO 2 or NO 3 . In denitrification, NO3 is reduced to nitrous oxides and N2 where the NO 3 acts as the terminal acceptor during the oxidation of organic compounds (Bowmer, 1987). However, the nitrification and denitrification processes are not clear due to formation of N2O an intermediate product of both nitrification and denitrification (Tam et al., 2009). As mentioned before, NO 3 is removed by denitrification and mangrove uptake. It is obvious that the mangrove plants not only absorb NO 3 for their growth, they also enhance the efficiency of both nitrification and denitrification processes in a closed system (Wu et al., 2008). The assimilation of P in a mangrove system involves many pathways in a complex biogeochemical cycle. Although PO3 4 concentrations are lower compared to N-forms in aquaculture facilities, PO3 4 is considered a limiting nutrient in mangrove forests (Ye et al., 2001). Therefore, the
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principal mechanisms of reduction could include the uptake by the mangrove species (Greenway and Woolley, 1999). Many studies have demonstrated that mangroves could be used in constructed wetlands for nutrient removal treatments (e.g., Wong et al., 1997; Chu et al., 1998; Ye et al., 2001; Boonsong et al., 2003). However, little work has been done on the comparison of nutrient removal efficiencies of different mangrove species (Yang et al., 2008; Ye et al., 2001), especially in semi-arid regions. It is evident that our three mangrove species distributed in semiarid regions are quite different compared to the tropical Bruguiera gymnorrhiza, Rhizophora stylosa, A. corniculatum, and K. candel. The aforementioned tropical mangrove species removed more N and P (42–88%) compared to our mangroves (50–63%) (Wu et al., 2008; Yang et al., 2008; Huang et al., 2012). The most contrasting nutrients removal percentages were from Ye et al. (2001) where they reported N removal efficiencies of 92.7% and 98.0%, and P removal of 88% and 97.8% by K. candel and B. gymnorrhiza in pot-cultivation system under saltwater conditions. Consequently, the understanding of mangroves as importers or exporters of nutrients depends on the location and the environmental factors affecting the biological responses. 5. Conclusions Intensive aquaculture systems have grown enormously over the past decades, and yet, there are just a few studies that assess biological treatment of these effluents. This study aimed to examine the biological nutrient removal efficiency of semi-arid mangrove seedlings in closed silvofishery systems. The observed differences in nutrient concentrations between the mangrove and control tanks indicate a clear pattern that semi-arid mangroves are able to remove a considerable amount of inorganic nutrients. In particular, seedlings of A. germinans, L. racemosa, and R. mangle have potential to remove an average of 63% of NH+4 and NO 2 . Contrary, 3 the average removal efficiency of NO was 50% under 3 and PO4 the same treatments. Given the large geographic extent of impacted areas from aquaculture effluents, the incorporation of mangrove seedlings could be commonly used for close-aquaculture systems in the sub-tropics. For instance, many aquaculture facilities from semi-arid regions lack mechanisms of filtration. Thus, seedlings of A. germinans, L. racemosa, and R. mangle have potential to remove ammonium, nitrite, nitrate, and phosphate from such systems. Hence, the relative cheap cost of this mangrove filtration system makes it an ideal tool in countries where other traditional filtering techniques are economically prohibited. However, the variety of nutrient removal percentages with other commercial fisheries may require extensive studies to become fully evident. Acknowledgements The first author acknowledges financial support through a grant provided by the Consejo Nacional de Ciencia y Tecnología of México (Grant No. 255546). The funding for the field campaigns was provided by the Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM). The third author acknowledges financial support through a grant provided by the Dirección General Asuntos del Personal Académico (DGAPA-UNAM). References Adame, M.F., Lovelock, C.E., 2011. Carbon and nutrient exchange of mangrove forests with the coastal ocean. Hydrobiologia 663, 23–50. http://dx.doi.org/ 10.1007/s10750-010-0554-7.
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