S H A L L O W L A K E S
Shallow lake restoration and water quality management
by the combined effects of polyaluminium chloride addition
and benthivorous fish removal: a field mesocosm experiment
Fabiana Arau´jo .Vanessa Becker.Jose´ Luiz Attayde
Received: 31 March 2015 / Revised: 17 November 2015 / Accepted: 29 November 2015 / Published online: 10 December 2015 Ó Springer International Publishing Switzerland 2015
Abstract Polyaluminium chloride (PAC) has been used in lake restoration and water quality management as a flocculent to remove algal biomass and organic matter from the water column and increase water transparency. However, benthivorous fish may sus-pend the sedimented flocs and reduce the efficiency of PAC in improving water quality. Therefore, we hypothesized that PAC is more efficient in reducing algal biomass, suspended solids and total phosphorus concentrations in the water, and increasing water transparency, when benthivorous fish is removed. To test this hypothesis, we performed a field experiment
combining the presence and absence of PAC (2 mg Al l-1) with the presence and absence of benthivorous fish (350 g m-2). Contrary to our hypothesis, no significant interactions were found between the effects of PAC addition and benthivorous fish removal on the measured variables. Both techniques significantly decreased chlorophyll a and phosphorus concentrations and increased water transparency, but their effects were independent of each other. The above results suggest that either of the treatments may improve water quality, but this goal would be better achieved by the combina-tion of both techniques than by the applicacombina-tion of one or other technique in isolation.
Keywords Coagulation Flocculation
Biomanipulation Prochilodus Tropical semi-arid
Introduction
Cultural eutrophication of freshwater and coastal marine ecosystems is a global environmental problem caused by an increase in the nutrient supply to these ecosystems leading to highly undesirable changes in surface water quality. The most important and com-monly cited water quality variables of concern are the accumulation of algal biomass and reduction of water transparency, which are readily perceived by the public (Smith,1998; Smith et al.,1999). Reducing the external load of nutrients is the first and most important method used to control eutrophication and
Guest editors: M. Bekliog˘lu, M. Meerhoff, T. A. Davidson, K. A. Ger, K. E. Havens & B. Moss / Shallow Lakes in a Fast Changing World
F. Arau´jo (&) V. Becker J. L. Attayde
Programa de Po´s-Graduac¸a˜o em Ecologia, Centro de Biocieˆncias, Universidade Federal do Rio Grande do Norte, Natal, Brazil
e-mail: fabianabio@gmail.com; fabianabio@gmail.com.br V. Becker
Laborato´rio de Recursos Hı´dricos e Saneamento Ambiental (LARHISA), Centro de Tecnologia, Universidade Federal do Rio Grande do Norte, Natal, Brazil
J. L. Attayde
Departamento de Ecologia, Centro de Biocieˆncias, Universidade Federal do Rio Grande do Norte, Natal, Brazil
to restore eutrophic lakes and reservoirs. However, the internal loading of nutrients can delay the recovery of shallow lakes after reduction of the external loading (Marsden,1989; Jeppesen et al.,1991; Van der Molen & Boers, 1994; Søndergaard et al., 2000, 2003). Therefore, additional measures are often needed to improve the water quality of shallow lakes (Cooke et al.,2005; Hilt et al.,2006).
Water quality improvement can be achieved through coagulation and flocculation. Coagulation is a process commonly used in drinking water treatment to remove dissolved natural organic matter (NOM) and colloidal inorganic and organic particles (Edz-wald,1993) by aluminium (Al), calcium or iron salts (Cooke et al., 2005). The coagulation by Al salts occurs by interaction of Al hydrolysis species with NOM and destabilization of suspended particles, adsorption of NOM onto particulate aggregates and its subsequent removal by sedimentation of flocks formed (Jiang & Graham,1998; Pernitsky & Edzwald,
2006). As a result, the flocculation by aluminium salts removes organic (including algal biomass) and inor-ganic matter, and total phosphorus (TP) present in suspended particles resulting in the improvement of water transparency after flocks settling (Jiang & Graham, 1998; Hullebusch et al., 2002; Reitzel et al., 2003; Auvray et al., 2006). Many successful cases of Al application as restoration measure have been reported (Cooke et al., 2005). Polyaluminium chloride (PAC) has been used as an alternative for alum because it has a higher efficiency of turbidity reduction based on the same equivalent alum dose, a wider working pH range and a lower coagulant cost to achieve the same efficiency (Jiang & Graham,1998). Another technique used to improve lake water quality is the removal of planktivorous and/or ben-thivorous fishes (Meijer et al., 1994, 1999; Perrow et al., 1997; Hansson et al., 1998; Drenner & Hambright, 1999; Mehner et al., 2002; Jeppesen et al., 2007, 2012). The ultimate goal of such biomanipulation is the reduction of algal biomass and the increase of water transparency. The removal of planktivorous fish increases the abundance of large zooplankton, which in turn can suppress phytoplank-ton biomass (Carpenter et al., 1985; Meijer et al.,
1994), but within a limited range of P loads (Jeppesen et al.,1990,1991). On the other hand, the removal of benthivorous fish reduce the bioturbation of lake sediment and the translocation of nutrients from the
sediment to the water column decreasing algal biomass and primary production (Andersson et al.,
1978; Meijer et al., 1990; Breukelaar et al., 1994; Cline et al., 1994; Lougheed et al.,1998; Schaus & Vanni,2000; Volta et al.,2013).
Although the efficiency of biomanipulation and Al application in improving water quality are well documented, studies on the effects of both techniques combined are so far limited (Jeppesen et al., 2012). Bioturbation by benthivorous fish may suspend the sedimented flocks of organic matter and reduce the efficiency of the flocculent PAC in improving water quality. Therefore, we hypothesized that the applica-tion of PAC is more efficient in reducing algal biomass, suspended solids and TP concentrations in the water, and increasing water transparency, when benthivorous fish is removed. To test this hypothesis, we performed a field experiment combining the presence and absence of the flocculent PAC (2 mg Al l-1) with the presence and absence of benthivorous fish (Prochilodus brevis). We expected to find a synergistic interaction between the effects of PAC addition and benthivorous fish removal on the mea-sured variables. In other words, we expected that the effects of both techniques combined are stronger than the sum of their effects in isolation.
Materials and methods
Study area and experimental design
The experiment was performed in an eutrophic shallow man-made lake located at the Serido´ Ecolog-ical Station, Serra Negra do Norte, Rio Grande do Norte, Brazil (6°34049, 300S; 37°1502000W). The lake
was meso-eutrophic during the study period (October– November/2013) with chlorophyll a and TP concen-trations ranging between 13–72 and 41–227 lg l-1 (minimum–maximum values), respectively.
The experiment was carried out in 20 mesocosms of 6 m3 (4 m29 1.5 m), placed side by side in the littoral zone of the reservoir. The mesocosms were open to the atmosphere at the top and to the sediment at the bottom but were isolated from the adjacent lake water by a film of transparent plastic. The experiment consisted of a 2 9 2 factorial design where four treatments with five replicates were randomly allo-cated to the 20 mesocosms. The treatments were in the
presence of fish with (?Al ? Fish) or without Al addition (-Al ? Fish) and the absence of fish with (?Al - Fish) or without Al addition (-Al - Fish).
The benthivorous fish used in the experiment, Prochilodus brevis, is native from the Brazilian semi-arid region and is the most abundant fish species in the studied lake, accounting for 86% of the total fish biomass caught in the lake before the start of the experiment. Four fishes (352.6 ± 65.7 g each) were added to each mesocosm of the fish treatments just after the first water sampling within the mesocosms to measure the initial conditions of the experimental units (T0). The stocking density of 3,500 kg ha-1or 350 g m-2used in our experiment is within the range of natural densities (0–6,000 kg ha-1) found in lakes of semi-arid region during the dry season (Angeler et al.,2002).
Polyaluminium chloride (PAC; PANFLOC TE1018—Pan-Americana S/A) was diluted with lake water and it was applied at the water surface in the mesocosms. PAC was added 1 day after the fish was stocked in the mesocosms and water sampling (T1) occurred 1 day after PAC addition. The chosen dose (2 mg Al l-1) was the lower dose able to remove more than 80% of total P and turbidity of lake water after 30 min of sedimentation in a jar test with the lake water carried out before the start of the experiment. Sampling and samples analysis
Water samples were collected at 13 days intervals for 8 weeks after PAC addition. A total of five samples after fish and PAC manipulation (T1–T5) and one sample before (T0) were taken from each mesocosm. Sampling was performed always between 06 h 00 and 10 h 00 a.m. Water transparency was measured with a Secchi disc and water samples were collected with a PVC tube (1.5 m length, 5 cm diameter) at different points of each mesocosms and integrated in a 30 l bucket. Subsamples were taken for turbidity, sus-pended solids, chlorophyll a and phosphorus analyses. Turbidity was measured with a turbidimeter AP2000 and TP concentration was measured with a spec-trophotometer by the acid ascorbic method after persulphate digestion (Murphy & Riley,1962; Valder-rama, 1981). Samples were filtered on 1.2 lm glass fibre filters (VWR 696) for the determination chloro-phyll-a concentration after ethanol extraction (Jes-persen & Christoffersen,1987) and for determination
of suspended solids concentration by gravimetric method (APHA,1998). The organic suspended solids (OSS) were determined by the difference between total suspended solids (TSS) and inorganic suspended solids (ISS) after burning the organic matter in the glass fibre filters at 550°C. The filtered water was used to measure the soluble reactive phosphorus (SRP) concentration by the ascorbic acid method (Murphy & Riley, 1962). Water samples were also collected outside the mesocosms in two different points of the lake for the analysis of the same variables in the natural environment. The fishes were recaught from each mesocosm with a casting net and weighed at the end of the experiment.
Statistical analysis
A two-way repeated measures ANOVA was per-formed to test the isolated and combined effects of benthivorous fish removal (Fish) and PAC addition (PAC), water transparency and turbidity, OSS and ISS, soluble reactive and TP and chlorophyll-a concentra-tions. The data were log transformed to meet the assumptions of ANOVA. A post hoc power analysis was performed to assess the chance of the two-way ANOVA in detecting significant interaction between the two factors (G*Power; Faul et al.,2007). We used Cohen’s definition of small (0.1), medium (0.25) and large (0.4) effects (Cohen, 1988). Fish growth was expressed as the ratio between the final and initial fish weight in each mesocosm of the fish treatments. To test for treatment effects on fish growth, we used a t test for independent samples. The significance level defined was a = 0.05.
Results
We found no significant effects of PAC addition, benthivorous fish removal or their interaction on the measured variables at the start of the experiment, indicating that treatments had similar initial conditions (Table 1). The concentration of TSS and OSS decreased shortly after the beginning of the experi-ment in all treatexperi-ments and remained low in treatexperi-ments without fish but tended to increase in the treatments with fish (Fig. 1a, c). Water turbidity decreased over time in all treatments until day 26 but increased on day 39 except in the treatment with PAC and no fish
(Fig.1d). The Secchi depth remained low in the lake and in the two treatments with fish during the experiment but increased in the treatments without fish especially in the one with PAC (Fig.1e). On the other hand, chlorophyll a concentrations increased in the fish treatments during the experiment but tended to decline in the absence of fish, especially with PAC addition (Fig.1f). Total phosphorus concentration decreased over time in all treatments and in the lake until day 26, but on day 39, it increased in the lake and the mesocosms, especially in the ones with fish (Fig.1g). SRP concentration increased during the experiment in the lake and in all the treatments except the one with PAC addition and fish removal (Fig. 1h). The two-way repeated measures ANOVA results showed that PAC addition and benthivorous fish removal had significant effects on the measured variables but most of these effects were time depen-dent (Table 2). Both PAC addition and fish removal significantly improved water quality decreasing water turbidity, suspended solids, chlorophyll a and phos-phorus concentrations, and increasing Secchi depth (Fig.2; Table2). However, there was no significant interaction between the effects of PAC addition and benthivorous fish removal (Fig.2; Table2). Results of the post hoc power analysis showed that the power of the significance test of the interaction term of the two-way ANOVA model was high for TSS, OSS, Secchi depth and chlorophyll-a concentration (effect size [0.4) but low for ISS, turbidity, TP and SRP (effect
size B0.1). No significant difference in fish growth was observed during the experiment between the two fish treatments (Fig. 3, t test = -1.038, P = 0.33).
Discussion
The hypothesis tested with our experiment is that the application of the flocculent PAC and the removal of benthivorous fish interact synergistically to improve the water quality of shallow lakes. We predicted that PAC addition would improve water quality only in the absence of benthivorous fish. This is because benthiv-orous fish can resuspend the sedimented algae and organic matter that is removed from the water column by PAC application. Moreover, they can also translo-cate phosphorus from the sediment to the water column contributing to the internal P loading and stimulating phytoplankton growth (Vanni,2002). Contrary to our prediction, no significant interaction was found between the effects of PAC addition and benthivorous fish removal on the measured variables. The lack of interaction between their effects on chlorophyll a con-centration and water transparency was clearly not a result of a lack of power of the statistical test. Therefore, we are confident that both techniques significantly decreased algal biomass and increased water transparency independently of each other.
The above results suggest that either of the techniques may improve water quality, but this goal
Table 1 Average values (± 1 SD) of total suspended solids (TSS), organic suspended solids (OSS), inorganic suspended solids (ISS), turbidity, Secchi depth, chlorophyll-a (Chl-a),
total phosphorus (TP) and soluble reactive phosphorus (SRP) concentrations in the four treatments and in the lake just before the start of the experiment (T0)
TSS OSS ISS Turbidity Secchi depth Chl-a TP SRP Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD -PAC ? Fish 53.4 19.2 15.1 2.4 38.3 16.8 69.8 26.8 0.25 0.06 31.3 7.3 121.7 28.8 15.4 3.4 ?PAC ? Fish 59.4 23.0 16.7 3.3 42.8 19.8 71.9 25.2 0.26 0.04 30.2 6.5 126.0 24.3 13.7 3.1 -PAC - Fish 51.6 11.0 14.9 1.5 36.7 9.7 62.7 18.6 0.26 0.05 21.0 12.2 116.0 16.8 12.3 2.6 ?PAC - Fish 68.9 45.8 17.2 8.1 51.6 37.8 89.0 62.6 0.23 0.08 30.5 9.3 135.0 54.0 16.0 5.1 Lake 37.1 30.1 14.5 7.8 22.6 22.3 32.7 17.7 0.35 0.07 27.7 0.5 89.5 38.9 13.1 2.0 F P F P F P F P F P F P F P F P Fish 0.10 0.75 0.00 0.97 0.15 0.71 0.08 0.78 0.27 0.61 0.54 0.47 0.03 0.86 0.336 0.57 PAC 0.44 0.52 0.39 0.54 0.43 0.52 0.32 0.58 0.03 0.17 0.17 0.69 0.23 0.64 0.58 0.46 Fish ? PAC 0.00 0.95 0.05 0.834 0.01 0.91 0.10 0.75 0.58 0.46 0.55 0.47 0.01 0.92 3.34 0.09 Results of the two-way ANOVA (F-ratios; P values) to test for the effects of fish, PAC and their interaction (Fish 9 PAC) just before the experiment started (T0)
would be better achieved by the combination of both techniques than by the application of one or other technique in isolation. The application of the
flocculent PAC in the absence of benthivorous fish showed the best improvement in water quality, decreasing TSS from 68.9 to 13.9 mg l-1 and water
Fig. 1 Average values (±1 SD) of total, organic and inorganic suspended solids (SS), turbidity, Secchi depth, chlorophyll-a, total phosphorus and soluble reactive phosphorus (SRP) concentrations in the four treatments and in the lake during the experiment
turbidity from 89 to 8.5 NTU and increasing water transparency from 0.23 to 0.70 m on average from the start to the end of the experiment. In addition, this was the only treatment in which we observed reductions in chlorophyll-a concentration (from 30.5 to 15.3 lg l-1, on average) from the start to the end of the experiment.
As far as we know, combining these techniques to improve water quality of shallow lakes is not a common practice, and we found only one study that have combined them in Kollelev Lake, Denmark (Jeppesen et al.,2012). In this lake, PAC application resulted in a reduction of TP concentrations, but no changes were observed in water transparency, con-trary to our experiment where PAC application increased Secchi depth. One year after the biomanip-ulation of cyprinid removal and perch stocking, an immediate and strong improvement in water clarity in aluminium treated basins coincided with a gradual reduction in TP concentrations (Jeppesen et al.,2012). In agreement with the experience in Kollelev Lake, our mesocosm experiment shows that the combination of PAC application and biomanipulation is a good way to improve water quality of shallow lakes.
In the coagulation–flocculation process, TP is removed by adsorption and interaction with floccu-lated particles (Ratnaweera et al., 1992) which decrease ISS and turbidity from water after floc settling. A number of laboratory experimental studies have shown the good performance of PAC in both
turbidity and phosphorus removal (Reitzel et al.,2003; Gao et al.,2005; Chen & Luan,2010; Julio et al.,2010; Yang et al.,2010). The application of PAC in whole lake experiments has shown its efficacy in removing phosphorus from the water column (Reitzel et al.,
2005; Lopata & Gawron´ska, 2008; Egemose et al.,
2011; Jancˇula & Marsˇa´lek, 2012) and turbidity in shallow lakes (Hullebusch et al.,2002), in agreement with our results. As a consequence, the improvement in water transparency is observed mainly due to particle sinking due to coagulation–flocculation. Also, the flocks formed in coagulation–flocculation process can trap particles as algal and cyanobacteria cells and sink, removing algal biomass from the water column (Jancˇula & Marsˇa´lek,2011). In our study, PAC had a marginally significant effect (P = 0.08) in decreasing chl-a concentration in water column. This can be explained by two factors. First, the flocks formed by algae cells have low density making them difficult to settle (Edzwald, 1993; Henderson et al., 2008b). In addition, algae characteristics such as lipid accumu-lation, mucilage production and ionic regulation can affect coagulation (Henderson et al.,2008a,2010) and sedimentation (Reynolds, 2006), which can increase the coagulant demand in algae-rich waters (Takaara et al.,2007).
The neotropical benthivorous fish curimata˜ (Prochilodus brevis) significantly increased water turbidity, phosphorus and chlorophyll-a concentra-tions and decreased water transparency. This has been
Table 2 Results of the two-way repeated measures ANOVA (F-ratios and P values) to test for the effects of fish, PAC, time and their interaction on total suspended solids (TSS), organic
suspended solids (OSS), inorganic suspended solids (ISS), turbidity, Secchi depth, chlorophyll-a (Chl-a), total phosphorus (TP) and soluble reactive phosphorus (SRP) concentrations TSS OSS ISS Turbidity Secchi Chl-a TP SRP
F P F P F P F P F P F P F P F P Fish 10.65 0.01 3.15 0.12 15.99 0.00 15.26 0.00 17.00 0.00 13.16 0.00 17.36 0.00 5.36 0.04 PAC 0.59 0.46 0.18 0.68 13.69 0.01 15.35 0.00 8.82 0.01 3.69 0.08 8.45 0.01 6.19 0.03 Fish 9 PAC 0.56 0.47 1.20 0.31 0.06 0.81 0.0004 0.98 0.72 0.41 0.62 0.45 0.02 0.89 0.05 0.82 Time 20.64 0.00 8.01 0.00 9.79 0.00 27.72 0.00 12.37 0.00 2.15 0.07 49.23 0.00 26.62 0.00 Time 9 Fish 5.49 0.00 0.61 0.69 3.10 0.02 6.59 0.00 10.99 0.00 5.42 0.00 3.75 0.00 2.16 0.07 Time 9 PAC 1.56 0.19 0.67 0.65 1.73 0.15 4.05 0.00 2.95 0.02 2.24 0.06 4.33 0.00 5.41 0.00 TIME 9 Fish 9 PAC 0.80 0.55 0.85 0.52 1.48 0.22 1.06 0.39 1.28 0.28 0.84 0.53 0.26 0.93 3.37 0.01
Fig. 2 Mean (dots) and standard deviation (bars) of total, organic and inorganic suspended solids, turbidity, Secchi depth, chlorophyll-a, total phosphorus and soluble reactive phosphorus (SRP) concentrations in four treatments
previously reported for other benthivorous fish species such as bream (Abramis brama), common carp (Cyprinus carpio) and gizzard shad (Dorosoma cepe-dianum), which are common in temperate eutrophic shallow lakes (Andersson et al.,1978; Meijer et al.,
1990; Breukelaar et al.,1994; Lougheed et al.,1998; Schaus & Vanni, 2000; Godwin et al., 2011; Volta et al.,2013). It has been suggested that a reduction of 70–85% of benthivorous fish biomass (Meijer et al.,
1990; Hosper & Meijer, 1993; Perrow et al., 1997; Hansson et al., 1998) and the maintenance of their population depressed (Godwin et al.,2011) is neces-sary for a long-term improvement of lake water quality by biomanipulation. In our study, we compared two contrasting levels of benthivorous fish (presence/ absence) because these were the most relevant levels to test our hypothesis. Because we were not able to reject the null hypothesis of no interaction manipulat-ing these two contrastmanipulat-ing levels of fish, we are much more confident to conclude that benthivorous fish does not change the effects of PAC additions. However, no biomanipulation consist of removing all fish from a lake and one should not over interpret the results of the fish effects in our experiment. Finally, fish growth was positive but similar in both fish treatments, suggesting that it is not affected by PAC addition at least in the short term.
In summary, our results allow us to reach three conclusions: (i) a low dose of PAC may clear the water (through precipitation of seston) regardless of fish
manipulation; (ii) total fish removal may clear the water (through reduction of resuspension) regardless of flocculation and (iii) there seems to be no interac-tive effect of PAC addition and fish removal on the measured variables. Therefore, either of the tech-niques may improve water quality, but this goal would be better achieved by the combination of both techniques than by the application of one or other technique in isolation.
Acknowledgements We thank Maria Marcolina L. Cardoso, Pablo Rubim, Mariana R. A. Costa, Ba´rbara Bezerra, Caroline G. B. de Moura, Leonardo Teixeira e Alexander Ferreira for field and laboratory assistance. We would like to thank Kemal A. Ger for helping us in the English language review. We also thank two anonymous reviewers for their comments and suggestions to improve the manuscript. Funding was given by Conselho Nacional de Desenvolvimento cientı´fico e Tecnolo´gico (CNPq) through the Project 562676/2010-4. Fabiana Arau´jo was supported by a fellowship from Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior (CAPES).
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