Aquaculture Research, 2016, 1–13
doi:10.1111/are.13163
The control of floating macrophytes by grass carp in net cages: experiments in two tropical hydroelectric reservoirs Fernando D Domingues1, Fernando L R M Starling2, Clarice C Nova3, Bruna R Loureiro4, Leonardo C e Souza1 & Christina W C Branco1 1
Departamento de Zoologia, Instituto de Bioci^encias, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro,
RJ, Brazil Companhia de Saneamento Ambiental do Distrito Federal – CAESB – Superintend^encia de Monitoramento e Controle de Recursos Hıdricos – PHI, SAIN- Area Especial – R1 – CAESB, Brasılia ,DF, Brazil 3 ~o em Ecologia, Instituto de Biologia, Universidade Federal do Rio Departamento de Ecologia, Programa de p os-graduacßa 2
de Janeiro, Rio de Janeiro, RJ, Brazil ~o Instituto de Pesca do Estado do Rio de Janeiro- FIPERJ, Niter oi, RJ, Brazil Fundacßa
4
Correspondence: C W C Branco, Departamento de Zoologia, Instituto de Bioci^encias, Universidade Federal do Estado do Rio de Janeiro, Av. Pasteur 458, Rio de Janeiro, RJ, Brazil, CEP:22290-240. E-mail:
[email protected]
Abstract The efficiency of grass carp (Ctenopharyngodon idella Val.) for biological control of floating aquatic macrophytes in net cages was assessed in two eutrophic tropical hydroelectric reservoirs through experiments using three macrophyte species (Eichhornia crassipes, Pistia stratiotes and Salvinia auriculata). A total of twenty experiments were performed in these reservoirs with a duration period between 21 and 30 days, during distinct seasons of the year. Sets of experiments were conducted using the three macrophyte species simultaneously in both reservoirs, and additional experiments were performed in one reservoir involving the separate use of each species. All macrophytes demonstrated significant growth in the absence of fish with total per day biomass increase rate ranging from 0.06 to 17.00%. The presence of grass carp significantly reduced macrophyte biomass in both reservoirs independent of fish size, stocking rate and available cage space. In all seasons, grass carp grazing pressure was higher for S. auriculata and lower for P. stratiotes. The results show that grass carp in net cages was able to use aquatic macrophytes as the only food source, controlling massive plant growth (especially S. auriculata and E. crassipes). Fish cages, already implemented in several reservoirs in Brazil,
© 2016 John Wiley & Sons Ltd
are easily manageable units at relatively low cost. Thus, biocontrol of macrophytes using caged grass carp is proposed as an effective low-budget ecotechnological tool to control consumable plants while avoiding the removal of desirable aquatic vegetation and the resultant impact on local fauna.
Keywords: biological control, Ctenopharyngodon idella, macrophytes, cage culture, Salvinia auriculata Introduction Aquatic macrophytes comprise a morphological and functionally diverse group of emergent, floating-leaved or totally submerged plants, which directly or indirectly influence water quality and the aquatic food web. Their direct influence is related to the fact that they are primary producers and source for organic detritus, capable of promoting change in physical and chemical conditions in the water column. The aquatic macrophytes allow the development of attached organisms (such as periphyton) and are grazed by a variety of invertebrates and vertebrates, also changing the structure of the ecosystem by increasing the complexity and spatial heterogeneity of habitats (Thomaz & Bini 2003; Esteves 2011). Indirect contributions of
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Control of floating macrophytes by grass carp F D Domingues et al.
macrophytes also play an important role in the metabolism of these environments through their influence on nutrient cycling processes and stock, providing physical basis for different niches, spawning sites, and refuges for small animals against predation (Scheffer 1998; Moss 2001). Aquatic macrophytes frequently proliferate when inputs of nutrients increase, mainly due to anthropogenic alterations, such as artificial eutrophication and changes in water flow. Massive proliferation can cause problems for navigation, fisheries, hydroelectricity generation and the recreational use of these ecosystems. Among free-floating aquatic plants, Eichhornia crassipes, Pistia stratiotes and Salvinia spp. have been associated with the most serious and particularly acute problems worldwide. Nevertheless, the occurrence of these plants in hydroelectric reservoirs is a fundamental problem and has gained special attention and importance in Brazil (Thomaz & Bini 1998). Three approaches can be used to remedy such infestations of aquatic plants: mechanical removal, chemical control and biological control. The first two forms of remediation are widely used worldwide, but their effectiveness is questionable. The mechanical removal of plants is a mitigating short-term technique and can be rather expensive as it may require frequent removal of the plants. On the other hand, the use of herbicides – chemical manipulation – while effective, has been considered unsuitable for regions where water is used for domestic supply and its indiscriminate use can cause resistance in plants (Vargas, Borem & Silva 2001; Pomp^eo 2008). Biological control, however, is characterized by the use of living organisms to control undesirable populations of other organisms (Howarth 1991). It is still an unexplored management technique in many tropical countries, and its effectivity varies greatly, depending on the organisms used. While making use of the biological control of plants, organisms from different groups can be used (Marlin, Hill, Ripley, Strauss & Byrne 2013). However, the main difficulty concerning this technique is the need for previous studies, to predict the potential impacts of controlling species in the environment. And, in the case of using an exotic species, the potential risk of an accidental introduction in the ecosystem must be evaluated. Nonetheless, if applied correctly, the biological control of macrophytes can be the most suitable technique as it can be considered environmentally friendly.
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Studies in different regions of the world have shown the great potential for the use of herbivorous fish for direct control of the overgrowth of aquatic macrophytes (e.g. Nandeesha, Keshavanath, Basavaraja, Varghese & Srikanth 1989; Van der Zweerde 1990; Petr 2000; Starling, Lazzaro, Cavalcanti & Moreira 2002; Gopalakrishnan, Rajkumar, Sun, Parida & Venmathi Maran 2011). One of the most widely used species is the grass carp, Ctenopharyngodon idella Val., an herbivorous species native to large river systems of eastern Asia; individual fish can consume large amounts of aquatic plants (Pıpalov a 2006) and have the capacity to tolerate temperatures from 0 to 33°C. According to FAO (2015) and FishBase (Froese & Pauly 2015) up to 2013, grass carp (C. idella) has been introduced in over 108 countries, primarily as a control agent of aquatic weeds. Today, it is one of the main freshwater fish farmed in southern Brazil (Garcia, Loebmann, Vieira & Bemvenuti 2004; Scherer, Augusti, Steffens, Boch, Hecktheuer, Lassari, Rad€ unz-Neto, Pomblum & Emanuelli 2005). Most studies with grass carp in Brazil have been related to fish farming (Costa, Rad€ uz-Neto, Lazzari, Losekann, Sutili, Brum, Veiverberg & Grzeczinski 2008), and research on its specific use for the biological control of aquatic weeds is still scarce in the country. However, some studies have already identified herbivory by grass carp as a promising ecotechnology to control submerged macrophytes in urban dams accompanied by long-term fisheries management (Viana & Starling 2003). One of the major impediments to the widespread use of grass carp to control aquatic plants has been the side effects that the release of specimens may cause in the environment – such as undesirable herbivory on native plants, which have an important ecological role in the aquatic ecosystem. The use of grass carp in cages is perhaps one means of overcoming the problem of uncontrolled herbivory on native plant species. Cage culture can be readily practiced in a wide range of open freshwater ecosystems, especially reservoirs. It uses simple technology for cage construction and operation, making it economically, socially and environmentally friendly. Currently, the Brazilian Government has been promoting aquaculture parks dedicated to the production of fish in net cages in the large public reservoirs of the country (Bueno, Ostrensky, Canzi, Matos & Roubach 2015). © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
Aquaculture Research, 2016, 1–13
Control of floating macrophytes by grass carp F D Domingues et al.
This study explores the hypothesis that the herbivory of grass carp on floating plants can be effective even under net cage conditions. The three species of floating macrophytes used in the experiments (E. crassipes Solms, P. stratiotes Linnaeus and Salvinia auriculata Aubl) have been causing several problems in Brazilian waters, resulting in acute water quality issues. Through a set of experimental trials, we try to illustrate, for the first time in the literature, whether the use of grass carp in cages is effective in the control of floating macrophyte biomass.
through these two reservoirs are used in the production of energy and domestic water supply for approximately 9 million people. In the surrounding area, there is a predominance of deforested areas, mainly used for animal ranching and farming. The reservoir is considered eutrophic (Gomes, Dias & Branco 2008), with a massive proliferation of aquatic plants, which are contained by artificial barriers and weekly removed by mechanical methods. Key characteristics of each reservoir are summarized in Table 1. Experimental methodology
Materials and methods Study area The efficiency of grass carp for the biological control of macrophytes was assessed in two hydroelectric reservoirs that have extensive areas of floating aquatic macrophytes under control by mechanical removal. One of the reservoirs is located in the central–western Brazil (Parano a Reservoir – 15°470 S, 47°490 W) and the other in the southeast region (Vig ario Reservoir – 22o390 S, o 0 43 52 W). As the Brazilian legislation (IBAMA 1998) limits the establishment of exotic species of fish in different water bodies, except when the species has been already detected in a watershed, the experiments were performed in reservoirs where the presence of grass carp had been previously detected (Lazzaro & Starling 2005; CEIVAP 2012). Parano a Reservoir was created in 1959 during the construction of Brasılia (D.C.) to mitigate the low air humidity during the months of April up to September, and to be a recreational area for the population. From its establishment, Parano a Reservoir has suffered a long period of artificial eutrophication, mainly due to the input of urban drainage and effluents from sewage treatment stations (STS), reaching critical levels during the 1980s and 1990s. After an intervention by the Environmental Sanitation Company of the Federal District (CAESB), the reservoir returned to an acceptable level of water quality. Thus, for the most part, the reservoir is considered mesotrophic (Angelini, Bini & Starling 2008). Vig ario Reservoir belongs to the Paraıba do Sul and Piraı river systems. It was built with the concept of dividing the waters between two watersheds in 1945, when two reservoirs were formed: Santana and Vigario. The waters that pass © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
Experiments were carried out in Parano a and Vigrio reservoirs with grass carp from fish farms and a three macrophytes species (E. crassipes, P. stratiotes and S. auriculata) collected from the sites of the experiments. All fish cages were kept with a 5.0mm mesh with an extra 0.7 mm net extension to the exterior to avoid predation by birds and fish escape. Two of the net cages were used to estimate the growth of macrophytes in the absence of fish (control cages), and the other two were used to estimate the growth of macrophytes subjected to herbivory by fish (treatment cages). The experiments were carried out during both wet (summer) and dry (winter) seasons. During both experiments, water temperature, electrical conductivity, pH and dissolved oxygen were measured next to the net cages. Average values of water temperature, dissolved oxygen, pH and electrical conductivity near the cages during the experimental periods in both reservoirs are shown in Table 2. Water temperature varied from 22 to 28°C, and values were slightly higher in Parano a Reservoir. Dissolved oxygen values ranged from 2.5 to 8.3 mg L1 and Table 1 Morphometric characteristics, nitrate and total phosphorous concentrations of the reservoirs Parano a and Vig ario (data from Starling et al. 2002 and Gomes et al. 2008) Reservoir
Paranoa
rio Viga
Surface area (km2) Average depth (m) Volume (hm3) Retention time (days) Nitrate* (mg L1) Total phosphorus* (mg L1)
38 14 498 295 0.67 (0.20) 0.045 (0.010)
3.33 9 27.6 2 0.93 (0.07) 0.087 (0.03)
*Annual average values standard deviations (SD).
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Control of floating macrophytes by grass carp F D Domingues et al.
lower values were found in Vigario Reservoir. pH values were close to neutrality (around 7.0) in both Parano a and Vigario, though values were not obtained for Vig ario’s phase I experiment. Electrical conductivity was higher in Parano a Reservoir, with an overall range from 53 to 120 lS cm1, considering both environments. In Parano a Reservoir, four net cages of 2.5 9 2.5 9 1.3 metres each (6.25 m² and 8.12 m³) were used. The cages were located in Riacho Fundo tributary near a sewage treatment station (STS), as this is the most eutrophic area of this ecosystem (Padovesi-Fonseca, Philomeno & Andreoni-Baptista 2009). Seven experiments were performed in this reservoir with an average duration of 21 days (three 7-day trials) from January (wet season/summer) to July (dry season/winter) of 2008. The three macrophytes species (3000 g of each) were added together, totalling 9000 g of plant in each one of the four cages. The initial fish biomass of approximately 3000 g (three adult fish, averaging 1065 g weight and 38.3 cm total length), corresponding to a fish stocking of about 370 g m3, was used in two of the four cages; the two cages with fish were considered as treatment cages. Macrophytes were removed at intervals of 7 days, washed, dried (48°C for 72 h) and weighed. After each weighing, macrophytes (9000 g) were replaced. At the end of each trial period, the fishes were weighed to determine any changes in biomass. By contrast, the experiments performed in Vigrio were conducted in four net cages with a 4.0 9 6.0 9 2.0 metres each (24.0 m² and 48.0 m³). Two sets of different experiments were conducted in this reservoir. The first experimental set, phase I, was designed to assess total macrophytes increase using a mixture of the three macrophytes, as was carried out in Parano a Reservoir. In each one of the four cages, 1200 g of fresh biomass of each
Aquaculture Research, 2016, 1–13
macrophyte (total of 3600 g) was added. Five to six young fish (average weight 200 g; average total length 22.0 cm), totalling 1000 g of initial fish biomass, was placed only in the two treatment cages. Experiments continued for 30 days, on average. Macrophytes were removed every 15 days, washed, dried (48°C for 72 h) and weighed. After each weighing, the amount of fresh macrophytes (3600 g) was again added to each cage. At the end of each experiment, the fishes of the two treatment cages were also weighed. Four experiments that lasted on average 30 days each were conducted from January (wet season/summer) to June (dry season/winter) of 2009. The second experimental trial in Vig ario Reservoir (Vig ario phase II) was conducted from July 2009 to May 2010 and consisted of three sets of experiments using only one species of macrophyte in the four cages at each time, totalling nine experiments. The objective was to determine the independent growth rate of each macrophyte species, eliminating or reducing the competition factor among them. A total of 3600 g of fresh macrophyte was placed in each one of the four cages and approximately 1000 g of fish biomass was used in each one of the two treatment cages. These experiments lasted an average of 30 days, consisting of two trials of 15 days. Every 15 days, macrophytes from all the four cages were withdrawn and their biomass replaced. Afterwards the macrophytes were thoroughly washed, dried (48°C for 72 h) and weighed. At the end of each experiment, with a single macrophyte species the fishes of the two treatment cages were also weighed. Macrophyte biomass estimates and herbivory rate measurements Based on the results obtained in control cages, a biomass increase rate (BIR, % per day) for each
Table 2 Average values and standard deviation of physical and chemical variables measured near the experimental cages in the two reservoirs Physical and chemical variables of water
Reservoir (January to July 2008) Paranoa rio Reservoir (Phase I) (January to June 2009) Viga rio Reservoir (Phase II) (July 2009 to May 2010) Viga
WT (°C)
DO (mg L1)
pH
EC (lS cm1)
25.3 2.3 23.7 1.7 24.7 1.9
6.6 1.7 5.3 1.2 3.7 1.2
7.2 0.7 – 6.9 0.7
109.3 11.0 71.6 14.0 65.4 11.7
WT, water temperature; DO, dissolved oxygen; EC, electrical conductivity.
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© 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
Aquaculture Research, 2016, 1–13
Control of floating macrophytes by grass carp F D Domingues et al.
macrophyte was estimated in accordance with the Malthusian growth model using MATLAB 10 software. The equivalence between fresh weight (biomass in grams) and dry weight (dry mass in grams) for each macrophyte species was estimated by linear regression (n = 12) using MATLAB 10 software. The duplication time in days (DT, days) was calculated for each macrophyte in control cages using the Malthusian growth model. In treatment cages, which aimed to estimate and compare the intensity of fish herbivory on each macrophytes species, the herbivory rate (HR, % per day) was based on the difference between the biomass increase rate (BIR, % per day) and an under-grazing biomass increase rate (UGBIR, % per day). The UGBIR index was estimated in cages where grass carp were present and is based on the results obtained in both control and grazing treatment cages, also estimated using the Malthusian growth model. Furthermore, the UGBIR was conceived through mathematical modelling and by considering intrinsic species growth rate, initial and final weights of macrophytes while being grazed by caged carp, and time. Statistical analysis An analysis of variance (ANOVA) was performed to verify the existence of significant differences between initial and final plants’ biomass in control and treatment cages. Checking was the same for replicates using paired t-tests performed in Statistica 7.0 software, for Windows 7 (Statsoft Inc., Tulsa, OK, USA). Results Natural growth rates of floating macrophytes The eutrophic conditions in Vig ario Reservoir (Gomes et al. 2008; CEIVAP, 2012) and in the experimental area in Parano a Reservoir (Starling et al. 2002; Padovesi-Fonseca et al. 2009) throughout the experimental period resulted in a remarkable growth of floating macrophytes in the absence of fish grazing pressure (control net cages). BIR (in % per day), DT (in days), UGBIR (in % per day) and HR (in % per day) are presented in Table 3. In Parano a Reservoir, final biomass values of all floating plants were significantly higher (assuming P < 0.0001) than initial biomass values in all seven experiments in control cages. BIR was highest for © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
Table 3 Results of the experiments in the Parano a and Vig ario reservoirs BIR (%)
DT (days)
Reservoir – wet season Paranoa Eichhornia crassipes 2.94 23.6 Pistia stratiotes 7.19 9.6 Salvinia auriculata 0.06 1229.2 Reservoir – dry season Paranoa E. crassipes 1.91 36.3 P. stratiotes 6.45 10.7 S. auriculata 6.26 11.1 rio Reservoir – Phase I – wet season Viga E. crassipes 5.06 13.7 P. stratiotes 6.61 10.5 S. auriculata 17.73 3.9 rio Reservoir – Phase I – dry season Viga E. crassipes 4.88 14.2 P. stratiotes 6.76 10.2 S. auriculata 9.04 7.7 rio Reservoir – Phase II Viga E. crassipes 5.25 13.2 P. stratiotes 5.22 13.3 S. auriculata 10.08 6.9
UGBIR (%)
HR (%)
10.07 5.66 33.86
13.01 12.85 33.92
16.98 0.93 35.43
18.89 5.52 41.69
3.96 2.27 6.65
9.02 8.88 24.38
6.38 1.20 12.10
11.26 7.97 21.14
6.27 0.28 4.96
11.53 4.94 15.04
BIR, biomass increase rate per day; DT, duplication rate of the macrophyte biomass in days; UGBIR, under-grazing biomass increase rate per day; HR, herbivory rate per day.
P. stratiotes in both wet and dry seasons (7.19 and 6.45% per day, respectively), followed by S. auriculata in dry season (6.26% per day) and E. crassipes in wet and dry seasons (2.94 and 1.91% per day, respectively). Similarly, in phase I of the experiment in Vig ario Reservoir, all floating macrophytes displayed significant biomass increase in both dry and wet seasons, with significantly higher BIR (P < 0.0001) for S. auriculata (17.73 and 9.04% per day, respectively) followed by P. stratiotes (P < 0.0001; 6.61 and 6.76% per day, respectively) and E. crassipes (P = 0.0002; 5.06 and 4.88% per day, respectively). When comparing BIR of each species in Vig ario Reservoir during phases I and II, it can be observed that P. stratiotes biomass increased slightly during phase I (polyculture) and that S. auriculata BIR during phase II was similar to that of the dry season of phase I, but lower than that of the rainy season. E. crassipes biomass increased slightly during phase II (monoculture). However, doubling rate for the three species was similar in both experimental phases with S. auriculata having the lowest time (3.9–7.7 days), P. stratiotes intermediate (10.2–13.3 days) and E. crassipes the highest (13.2–14.2 days).
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Control of floating macrophytes by grass carp F D Domingues et al.
Feeding rates and food preferences of grass carp Grass carp actively grazed on floating macrophytes throughout all seven experiments conducted in Paranoa Reservoir. Comparisons between control (without fish) and treatment cages showed that fish prevented the growth of S. auriculata, P. stratiotes and E. crassipes, resulting in significant suppression of aquatic plant biomass in cages stocked with grass carp (Fig. 1). In both dry and wet seasons, grass carp grazing pressure was higher for
Wet season E. crassipes
800
Dry weight (g)
Dry season
400 400 300 200 100 0 P. strationtes
Dry weight (g)
800
400
0 S. auriculata
800 600
Dry weight (g)
S. auriculata, with an herbivory rate above 30% of plant biomass daily. Herbivory rates were intermediate for E. crassipes and lower for P. stratiotes (Table 3). The same impact and food preference for grass carp on floating macrophytes were observed in the Vig ario Reservoir during phase I, with higher herbivory rates for S. auriculata followed by E. crassipes and P. stratiotes (Fig. 2). In this reservoir, slight differences were noted between dry and wet seasons in the control cages with S. auriculata. On comparing the feeding rates of grass carp in the two reservoirs, higher values were observed in Parano a Reservoir. During complementary trials in Vig ario Reservoir involving the offer of each aquatic macrophyte separately, there was a similar pattern of herbivory (Fig. 3). In fish cages, P. stratiotes biomass was significantly higher than those of E. crassipes (P < 0.001) and S. auriculata (P < 0.001), with no significant difference between the latter two. The grass carp herbivory pressure showed the same pattern in the other experiments within the study, with higher HR on S. auriculata, intermediate herbivory on E. crassipes and lower on P. stratiotes in both phases I and II. Conversion efficiency and fish growth
600
200
400 200 0
TC1
TC2
CC1
CC2
Figure 1 Biomass (grams of dry weight) produced in seven days of experimental trials in the Parano a Reservoir (wet and dry seasons). TC, treatment cages, macrophytes and fish; CC, control cages, only macrophytes. Bars represent mean, maximum and minimum and standard deviations.
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During all fish trials conducted in Parano a and Vig ario (phase I) Reservoirs, there was no significant fish growth over the trial period when fish fed exclusively and simultaneously on the three floating macrophytes (Fig. 4a). In fact, average fish biomass decreased slightly, although not statistically significantly (P > 0.05) during most experiments. On the other hand, during complementary trials in Vig ario Reservoir, where plants were offered separately (phase II), significant gains and losses in average biomass of grass carp were observed depending on the plant species provided and season of the year (Fig. 4b). During periods where only E. crassipes was offered, there was either significant fish biomass increase (June, November and December of 2009, P < 0.001) or loss (during April of 2010, P = 0.003). The same could be observed while the grass carp was being fed with S. auriculata where there was also both significant biomass decrease (January 2010, P = 0.03) and increase (February and March of 2010, P = 0.04). The carp cage populations supplied with © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
Control of floating macrophytes by grass carp F D Domingues et al.
Aquaculture Research, 2016, 1–13
2000
Wet season Dry season E. crassipes
2000
Dry weight (g)
Dry weight (g)
500 400 300 200
1000 500
0
0 TC1
P. strationtes
300
Dry weight (g)
1500
100
2000 250 200
CC2 TC2 CC1 Salvinia auriculata Eichornia crassipes Pistia stratiotes
Figure 3 Biomass (in grams of dry weight) produced in fifteen days of the experimental trials using only one species of macrophyte in the Vig ario Reservoir. TC, treatment cages, macrophytes and fish; CC, control cages, only macrophytes. Bars represent standard deviations.
150 100 50 0
Dry weight (g)
Vigário phase II
2500
S. auriculata
2000 1800 1600 1400 1200 1000 800 600 400 200 0
TC1
TC2
CC1
CC2
Figure 2 Biomass (grams of dry weight) produced in fifteen days of experimental trials in the Vig ario Reservoir (wet and seasons). TC, treatment cages, macrophytes and fish; CC, control cages, only macrophytes. Bars represent mean, maximum and minimum and standard deviations.
P. stratiotes produced no significant increase or decrease in biomass (from August to October of 2009). Discussion Natural growth of floating macrophytes Massive growth of floating macrophytes, which is a frequent environmental problem in eutrophic tropical water bodies, was very well documented during our net cage experiments in both Parano a and Vig ario reservoirs. Differences in growth rates between plant species were evident and highlight © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
the importance of fast-growing species, such as S. auriculata, as an aquatic weed, colonizing eutrophic waters. Indeed, the highest growth rates of all experiments were observed for S. auriculata in Vig ario Reservoir (10.08–17.73% day1), corresponding to a duplication time of 6.9– 3.9 days. The high growth rate of this species is well known and, together with its sensitivity to different agents of toxic pollutants, favours its use as bioindicator of pollution in aquatic ecosystems (Gardner & Al-Hamdani 1997; Valitutto, Sella, Silva-Filho, Pereira & Miekeley 2006; Wolff, Pereira, Castro, Louzada & Coelho 2012). Growth values for S. auriculata in this study are comparable to those found by Rubim and Camargo (2001) for S. auriculata molesta in Preto River (Brazil), where values between 11% and 20% per day for growth rate and 3.5–7.1 days for duplication time also in terms of dry weight were found. According to these authors, the highest growth rates in the literature occur when nutrient contents are elevated, which is the case in both reservoirs studied. Although similar growth rates for each species in control cages were found in phases I and II in Vig ario Reservoir, a shorter duplication time was observed for both S. auriculata and E. crassipes when grown in isolation. This is evidence of competition between plant species while they are growing together. Indeed, in contrast to what was
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Control of floating macrophytes by grass carp F D Domingues et al.
Biomass (g)
Paranoá
Vigário I
(a)
Biological control of floating aquatic weeds by grass carp
Biomass (C. idella)
1150 1050 950 850 750 650 550 450 350 250 150
Jul/08 Paranoá Jul/09 Vigário
Jan/08 Jan/09
Biomass (C. idella) - Vigário II
(b) 460
Ec
Ps
Ec
Sa
Ec
Biomass (g)
430 400 370 340 310 280 250
Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May │ 2009 2010
Figure 4 (a) Biomass changes of Ctenopharyngodon idella in grams from the beginning to the end of all the experiments in Parano a Reservoir (January to July of 2008) and in the experiments of phase I in Vig ario Reservoir (Vig ario I) (from January to June of 2009), all using the three macrophytes simultaneously; (b) biomass changes of C. idella in grams in phase II in Vig ario Reservoir (Vig ario II) (July of 2009 to May of 2010), using one macrophyte at each experiment. Ec = Eichhorina crassipes, Ps = Pistia stratiotes and Sa = Salvinia auriculata.
observed in the present study, Henry-Silva and Camargo (2005) in mesocosms experiments, designed to investigate the ecological interactions between E. crassipes and P. stratiotes, observed a greater competitive ability of E. crassipes regardless of the proportions of storage. However, it must be stressed that the occurrence of E. crassipes, S. auriculata and P. stratiotes in the same water body has been reported in several reservoirs in the Brazilian south and southeast regions (Thomaz, Bini, Souza, Kita & Camargo 1999; Tanaka, Cardoso, Martins, Marcondes & Mustaf a 2002; Valitutto et al. 2006). Such cooccurrence possibly demonstrates a frequently alternating dominance according to the seasons and location.
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The presence of grass carp significantly reduced biomass of floating macrophytes through grazing in both reservoirs, independent of fish size, stocking rate and available space in cages. Likewise, several studies have reported the effectiveness of grass carp in the control of submerged macrophytes in various aquatic systems (e.g. Khattab & El-Gharably 1989; Armellina, Bezic & Gajardo 1999) but no one has reported this action in cage cultures. In a study on the use of grass carp in aquaculture, Masser (2002) listed the common aquatic plants consumed by this species in order of preference. According to this list, there is a preference for succulent and low-fibre submerged plants. However, floating Salvinia was ranked tenth, Eichhornia ranked seventeenth and Pistia ranked eighteenth. Despite being ranked as an item consumed by grass carp, according to Gopalakrishnan et al. (2011), the use of this fish in the biocontrol of floating plants, such as E. crassipes, has received little attention, while being effective in preventing outbreaks. Thus, in agreement with the rank proposed by Masser (2002), the herbivory rate of grass carp on S. auriculata was higher in both reservoirs, indicating a greater control over this species. E. crassipes suffered a greater herbivory pressure while compared with P. stratiotes in the two reservoirs. Such results show selectivity by the fish in relation to the three macrophytes, regardless of level of stocking. Although the experiments in the two distinct reservoirs should not be compared, the difference related to age and fish stocks might help in the explanation of higher rates of herbivory on S. auriculata and E. crassipes observed in Parano a Reservoir when compared to Vig ario Reservoir. The consumption rates of the grass carp vary with fish size and are dependent on optimal temperatures (21–30°C) and dissolved oxygen concentrations (higher than 4 mg L1). According to Masser (2002) and Du, Liu, Tian, He, Cao and Liang (2006), juveniles (6–15 cm) consume 2– 10% of their body weight in vegetation each day and, as fish grow, the consumption rate increases. Fish weighing 1–1.2 kg, such as the adults used in the Parano a experiment, can consume more than their own body weight per day (Petr 2000; Masser 2002; Pıpalov a 2006). © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
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Control of floating macrophytes by grass carp F D Domingues et al.
In addition, some field observations during the experiments revealed differences between herbivory related to fish sizes in the two reservoirs: smaller fish in the Vig ario Reservoir experiments started consuming the roots of the macrophytes first, and then its leaves, which seemed to be easier, especially with regard to S. auriculata. The bulbous petioles of E. crassipes were not consumed by these smaller fish in Vig ario, unlike what was observed in Parano a. This difference was possibly related to the preference of young grass carp for soft and immature food, and a tendency to avoid the tougher leaves (Sutton 1977; Kilgen 1978). It is important to highlight that, during the present study, at high grass carp stocking densities, herbivory rates remained higher than the growth rates of macrophytes, yielding mostly controlled growth rates (UGGR negative), except in a few instances with P. stratiotes. The occurrence of such exceptions could be explained by a lower attractiveness of P. stratiotes for grass carp compared to the other two species of macrophytes. The amount of aquatic plants consumed by grass carp and its selectivity depend, besides grass carp age, on the fish stocking density and quality of food present. According to Pıpalov a (2006), in temperate regions, efficient biocontrol on average is obtained in the first year after stocking 150–250 kg ha1 of one-/two-year-old fish – with an individual weight of 250–400 g. For subtropical and tropical regions, the stocking density used has been variable: ranging from the lowest 90–120 kg ha1 (with individual fish weight of 20–40 g) in Egypt (Khattab & El-Gharably 1989) to highest values of 500 kg ha1 (with variated fish weight of fish) in Brazil (Viana & Starling 2003). Compared with this latter research, there was also a high stocking density in present study in both Parano a and Vig ario reservoirs, respectively, 4800 and 417 kg ha1, which facilitated effective biocontrol of the macrophytes as the plants were consumed prior to their growth increase, as verified in the control cages. A key question involving herbivory is the effectiveness of macrophytes use by fish and the conversion of plant into fish biomass. Only during the final trials in Vigario Reservoir (phase II) was there a significant increase in fish biomass. Possible explanations include (i) better conversion of plant into fish biomass by young fish than adult and (ii) better adaptation of fish to the consumption of preferred macrophytes when offered separately during last trials (phase II). © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
Hence, in a study on the nutritional value of E. crassipes, P. stratiotes and S. auriculata in aquaculture, Henry-Silva and Camargo (2002) found that the three species have nutritional value with potential use in ruminant feed. However, according to these authors, the isolated use of any of the species would probably not meet the protein requirements of adult fishes. Nonetheless, it is important to highlight that although macrophytes have shown higher nutritional values than some forage plants, their use in animal feeding requires further investigation. Such inquiry is necessary to quantify the acceptability and digestibility of macrophytes, especially of E. crassipes, which shows higher levels of magnesium, manganese and iron (Henry-Silva & Camargo 2006). The use of caged grass carp as an ecotechnological tool for the control of floating aquatic macrophytes in reservoirs The idea of inducing the consumption of floating macrophytes by grass carp, while confined in net cages, is an innovation that can be exploited as a management strategy to convert the excess of phosphorus (trapped as undesirable plant biomass into edible fish biomass). According to the recommendations of the Bangkok Declaration (FAO 2010), the increase in the use of aquatic plants as nutrient stocks in aquacultures must be enhanced throughout the world. Ctenopharyngodon idella has been introduced in over 108 countries for food, fish culture and aquatic vegetation management. This species is the third most produced aquatic organism worldwide, accounting for more than 5.2 million tons in 2013 (FAO 2015), and despite its introduction, via government action and local fisheries in many countries (Petr 2000; Innal & Erk’akan 2006), there are controversial factors associated with grass carp introduction. Among these, there are possible natural reproduction of fish, parasites dissemination, uncertainty of the effect over native fish populations, possibility that the removal of plants may eliminate endemic fish food and sites for spawning and refugee for other animals, difficulty of live capture, and increase in some unwanted plant species not consumed by grass carp (Allen & Wattendorf 1987; Pıpalov a 2006). Such grass carp introductions have been noted in a number of countries, where the species may
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have been restricted to particular basins, and have acclimatized without reproducing (Verreycken, Anseeuw, Van Thuyne, Quataert & Belpaire 2007), generally because of the absence of suitable conditions in which the pelagic eggs can be incubated (Copp, Bianco, Bogutskaya, Er€ os, Falka, Ferreira, Fox, Freyhof, Gozlan, Grabowska, Kov ac, Moreno-Amich, Naseka, Pen az, Povz, Przybylski, Robillard, Russell, Stakenas, Sumer, Vila-Gispert & Wiesner 2005). Grass carp also show limited spread from the various water bodies (pools to reservoirs) to which they have been introduced (Innal & Erk’akan 2006; Radhakrishnan, Kurup, Murphy & Xie 2012), but have been reported as spreading from overflowing farm ponds and lakes (Garcia et al. 2004). To mitigate such impacts, action is being taken to limit stocking triploid carp to non-aquaculture waters for biological control purpose only and within watersheds where grass carp are already present in the wild (Conover, Simmonds & Whalen 2007). In Brazil, over the past decade, there has been an increase in information on the use of grass carp in aquaculture (Costa et al. 2008; Veiverberg, R€ adunz Neto, Emanuelli, Ferreira, Mascke & Santos 2010). Thus, grass carp have already been recorded in the wild in Brazil in the East River basins, Upper Paran a River, in the Uruguay River (IBAMA 1998, 2005), and also documented in natural lakes such as in the Patos and Mirim lagoons (Garcia et al. 2004). Nevertheless, there are still few studies reporting the use of grass carp as a tool to control macrophytes. On the other hand, cage culture in inland waters has increased greatly in recent decades (Beveridge & Stewart 1997; Bueno et al. 2015) and has become one of the main examples of intensive fish culture in many countries, including Brazil (Conte, Sonoda, Shirota & Cyrino 2008; Carvalho, Silva, Ramos, Paes, Zanatta, Brand~ ao, Zica, Nobile, Acosta & David 2012). The use of net cages to raise tilapia and native fishes has now become very popular and it can be found in all major reservoirs throughout Brazil, mainly due to easy management and low cost. The results of the present study show that grass carp was able to use aquatic macrophytes as the only food source, controlling massive plant growth (especially S. auriculata and E. crassipes) in tropical reservoirs. Cages with fish, already operational in several reservoirs in Brazil for aquaculture, are easily managed units with relatively low costs.
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The cage culture of grass carp near massive proliferation of floating macrophyte in reservoirs can facilitate the plants’ transference from environment to cage. The key point from the suggestion above is that cage-based systems are cheap and easy to construct. Relative to the cost of removing aquatic macrophyte from reservoir, partial drying, transport and landfilling and its associated infrastructure (electricity, roads, land, etc.), transference to cage culture in the reservoir can be inexpensive. In most reservoirs, the aquatic plants are harvesting mechanically or even manually and for this purpose, floating barriers are frequently placed near areas of intense macrophyte proliferations. Maintaining caged grass carp in the vicinity of these floating macrophyte beds would enable to transfer part of the harvest plants into the cages to feed fish instead of landing and transporting them to landfills. This process of converting part of the undesirable plant biomass into edible fish flesh inside the aquatic ecosystem clearly avoids extra costs involved in trucking and disposing harvested macrophytes in landfills. The integration of floating macrophyte harvesting with fish production would be a very profitable strategy in many Brazilian reservoirs. In a system such as of the Santana reservoir, where the uncontrolled growth of aquatic plants is of 80 000 to 120 000 tons of plants per year (Valitutto et al., 2006), the costs with manual or mechanical harvesting of aquatic macrophytes and trucking of harvest plants to landfills or composite sites can reach up to millions of dollars per year (Antuniassi, Velini & Martins 2002; Pomp^eo 2008). The use of land for aquatic plant landfills and their maintenance also involve additional costs. Consequently, cages with grass carp can be suggested as an effective ecotechnological tool as already verified by Swar and Gurung (1988), capable of stocking young individuals that are protected against predation, and exerting a better control over the plants to be consumed, in this way preventing the removal of desirable submerged vegetation and the impact on local fauna. Finally, notwithstanding the potential for the biological control of floating macrophytes by grass carp herbivory when confined in net cages, the following additional information is still required to consolidate this promising environmental friendly aquaculture: (i) possible optimization of fish growth by adjusting the amount of food offered © 2016 John Wiley & Sons Ltd, Aquaculture Research, 1–13
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and available space inside cages aimed at producing edible fish from nuisance weed at low cost, (ii) evaluation of sanitary quality of grass carp fed exclusively on floating macrophytes from eutrophic ecosystems taking into account their land uses and pollution sources on the watershed and (iii) use of sterile triploid grass carp to prevent unwanted species introduction into ecosystems. Acknowledgments We thank the Light Energia S.A. and CAESB for providing funding and the use of facilities for this research. We thank Ana Carolina I. Dias, Daniel Farias, Izidro F. Sousa-Filho, J ulio S. Reis J unior, Rafael Couto, Yuri Katayama and Tatiane Freitas for field assistance. We would also like to thank an anonymous referee for the critical review of the manuscript. References Allen J.S.K. & Wattendorf R.J. (1987) Triploid grass carp: status and management implications. Fisheries 12, 20–24. Angelini R., Bini L.M. & Starling F. (2008) Efeito de difer~o do Lago ~es no processo de eutrofizacßa entes intervencßo Parano a (Brasılia - DF). Oecologia Brasiliensis 12, 564– 571. Antuniassi U.R., Velini E.D. & Martins D. (2002) Remocß~ao mec^ anica de plantas aqu aticas: an alise econ^ omica e operacional. Planta Daninha 20, 35–43. Armellina A.A.D., Bezic C.R. & Gajardo A. (1999) Submerged macrophyte control with herbivorous fish in irrigation channels of semiarid Argentina. Hydrobiologia 415, 265–269. Beveridge M.C.M. & Stewart J.A. (1997) Inland Fishery Enhancements. FAO technical Paper 374, FAO, Rome Italy. Bueno G.W., Ostrensky A., Canzi C., Matos F.T. & Roubach R. (2015) Implementation of aquaculture parks in Federal Government waters in Brazil. Reviews in Aquaculture, 7, 1–12. Carvalho E.D., Silva R.J.S., Ramos I.P., Paes J.V.K., Zanatta A.S., Brand~ao H., Zica E.O.P., Nobile A.B., Acosta A.A. & David G.S. (2012) Ecological features of large Neotropical reservoirs and its relation to health of cage reared fish. In: Health and Environment in Aquaculture (ed. by E.D. Carvalho, G.S. David & R.J. Silva), pp. 361–382. InTech, Rijeka. CEIVAP - Paraıba do Sul River Basin Agency (2012) Studies for identification, location and quantification of causes of the aquatic plants proliferation, especially weeds, along the Paraiba do Sul River, including
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