Issue
Knowl. Manag. Aquat. Ecosyst.
Number 420, 2019
Topical Issue on Fish Ecology
Article Number 28
Number of page(s) 7
DOI https://doi.org/10.1051/kmae/2019017
Published online 21 May 2019

© X. Qiu et al., Published by EDP Sciences 2019

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

The common carp, Cyprinus carpio, has been introduced into aquatic systems world-wide. Its broad environmental tolerances (Horoszewicz, 1973; Crivelli, 1981), high fecundity and long lifespan (Fischer et al., 2013) combine to make common carp a highly invasive species (Roberts et al., 1995). The wide distribution of common carp and the species' role as an ecosystem engineer makes common carp one of the more important species in freshwater systems (Parkos et al., 2003; Semenchenko et al., 2017) affecting water quality and submerged vegetation.

Common carp is benthivorous and forage by disturbing as much as the top 20 cm of lake sediment (Huser et al., 2016). This activity exerts substantial effects on ecosystem structure and function (Kaemingk et al., 2017), resuspending particulate matter and potentially releasing nutrients sequestered in the sediment into the water column. This resuspension of sediment by common carp is known to increase turbidity, although this is not always observed. Fletcher et al. (1985) found that the presence of carp did not increase water turbidity, whereas Chumchal et al. (2005) concluded turbidity increased along with chlorophyll a and total phosphorus (TP) levels in systems with common carp. Bajer and Sorensen (2015) implicated common carp reduced water clarity and damaged the macrophyte communities, but recorded no apparent effect on TP. Fischer et al. (2013) suggested that common carp reduced water clarity, increased nutrient concentrations and reduced macrophyte biomass. Additional nutrients excreted by the common carp (Roberts et al., 1995) have been shown to stimulate phytoplankton growth (Fischer et al., 2013).

Common carp can suppress submerged plants both indirectly by increasing light attenuation, and directly by uprooting plants during foraging and by consuming plants (King and Hunt, 1967; Crivelli, 1983). Analyses of common carp stomach contents have revealed plant tissues, seeds and detritus (Crivelli, 1981; Hinojosa-Garro and Zambrano, 2004). Bajer et al. (2009) demonstrated that common carp caused losses of vegetation over large areas for at least 4 years, damaging the ecological integrity of a shallow lake.

In addition, common carp can also affect the composition of submerged plant communities (Miller and Crowl, 2006) by feeding selectively on plants with higher food values. The experiment of Roberts et al. (1995) showed that common carp can exert a direct effect on Vallisneria sp. and Chara jibrosa, eliminating them from some systems, while no change was recorded in the abundances of Juncus ingens, Schoenoplectus validus or Myriophyllum papillasum. Miller and Crowl (2006) found that Ceratophyllum demersum and Scirpus validus were also significantly reduced by common carp, whereas Potamogeton pectinatus was unaffected. Common carp were also observed to consume more Chara aspera than other macrophytes, such as Typha latifolia, C. demersum and S. validus (Miller and Provenza, 2007).

Submerged plant communities play a central role in the ecological condition and sustainability of freshwater systems, and changes in the abundance and composition of such communities may have significant effects, not least on water quality. In shallow lakes, submerged plants play a key role in suppressing phytoplankton growth (Lemmens et al., 2018) and improving and maintaining water clarity. Any impact of common carp activities is thus likely to be ecologically significant. Although the literature on the effects of common carp on aquatic ecosystems is extensive, more work is still needed to understand effects on water quality, especially in systems dominated by submerged plants. In addition, less is known about how common carp influence macrophytes with different morphology, such as meadow formers (biomass equally distributed over depth, e.g. Vallisneria), and canopy formers (biomass distributed mostly at the top of the plant, e.g. Hydrilla).

Here we present results from a mesocosm experiment conducted to evaluate the effects of common carp on water quality of nutrients, total suspended solid (TSS) concentrations, light intensity, and submerged plant biomass. We hypothesized that common carp would have a negative impact on water quality by increasing nutrient levels in the water column, decreasing water clarity and on submerged plants with the impact more stronger for Vallisneria than for Hydrilla. The results of this study may inform lake managers interested in reducing or removing benthivorous fish to improve water quality of aquatic ecosystem.

2 Materials and methods

2.1 Experimental mesocosm set up

The mesocosm experiments were carried out in seven tanks (diameter = 1.2 m, height = 1.2 m) containing sediment, water, and plants. Sediment was obtained from Ming Lake, a eutrophic shallow water body in Guangzhou City. The sediment was air-dried, powered, and sieved through a stainless sieve (mesh size, 0.5 mm) to remove coarse debris (Zhang et al., 2016). The homogenized sediment was added as a 10 cm thick layer in each mesocosm (Zhang et al., 2016). We planted 30 individuals each of two species of submerged macrophytes evenly in the mesocosm: the meadow forming Vallisneria denseserrulata and the canopy forming Hydrilla verticillata. All plants originated from Huizhou West Lake in Huizhou, Guangdong Province and cultivated in Jinan University for several years. The V. denseserrulata and H. verticillata were washed with distilled water to remove periphyton and debris before planting. Before planting, 10 plants of each species were randomly selected and washed through a 1 mm mesh sieve and oven-dried at 80 °C to constant weight to determine the dry weight of the plants. Each V. denseserrulata plant was 30 cm in length with dry weights of 0.73 ± 0.19 g. For Hydrilla verticillata, we used apical shoots separated from their mother plants, each 30 cm in length with dry weights of 0.04 ± 0.01 g (Zhang and Liu, 2011). The biomass of V. denseserrulata and H. verticillata in each mesocosm at the beginning of the experiment were therefore 21.8 ± 5.8 g and 1.3 ± 0.2 g respectively.

The mesocosms were each filled to a depth of 1.0 m with rainwater (TN = 0.94 mg L−1, TP = 0.01 mg L−1) and allowed to equilibrate exposed to natural sunlight for seven weeks, after which nutrient concentrations of the water in the mesocoms were 0.63 ± 0.06 mg L−1 TN and 0.03 ± 0.01 mg L−1 TP.

Common carp bought from the market in Guangzhou City were habituated in 100 L tanks for two weeks before being introduced to the mesocosms. Two individuals (16.4 ± 1.5 cm in length and 63.8 ± 9.1 g in wet weight) were added to each of three mesocosms as common carp treatments. Another four mesocosms were maintained as no fish controls. The experiment ran for 12 weeks from June to September, 2017, during which time nitrogen (N) in the form of KNO3 and phosphorus (P) as NaH2PO4 were added to each mesocosm at a rate of 1.5 mg N L−1 wk−1 and 0.1 mg P L−1 wk−1, respectively, to mimic external nutrient loading (Zhang et al., 2014). Sampling took place biweekly, with nutrient addition taking place immediately after samples were taken (Zhang et al., 2016). The mesocosms were exposed to natural environmental conditions throughout the experiment.

At the end of the experiment, submerged plants were harvested from each tank, separated according to species and washed with distilled water to remove sediment, debris and attachments. Finally, the plants were oven-dried at 80°C to constant weight for about 24 h, and their dry biomasses recorded.

2.2 Sampling and analysis

Water samples (1 L) were collected from 30 cm below the surface in each mesocosm every two weeks for measurement of total nitrogen (TN), total phosphorus (TP), phytoplankton biomass as chlorophyll a (chl a), and total suspended solids (TSS). TN was determined by alkaline potassium persulfate UV spectrophotometry (APHA, 1998). TP was determined by ammonium molybdate UV spectrophotometry (APHA, 1998). Chl a was determined by acetone extraction UV spectrophotometry (Jespersen and Christolfersen, 1987). TSS was calculated by weighing filters dried at 108°C for 2 h. Light intensity was measured biweekly between 10 a.m. and noon, before water sampling, using an underwater irradiance meter (ZDS-10W) at 1.0 meter below the surface of the water.

2.3 Statistical analyses

Repeated measures analyses of variance (RM-ANOVAs) were conducted to analyze differences of treatment effect in these indexes and with time as repeated factor of time effect. Independent sample t-test was used to analyze differences in levels of TN and TP, chl a, TSS, light intensity on each sampling occasion and to test for difference in macrophyte biomasses between carp treatments and controls at the end of the experiment. All data were analyzed using SPSS 18.0. All results are presented as mean ± 1 SD.

3 Results

3.1 Nutrients

Concentrations of NO3N (RM-ANOVAs, treatment effect, F1, 10 = 64.0, p < 0.001), TN (F1, 10 = 42.8, p = 0.001) and TP (F1, 10 = 9.7, p = 0.026), but not NH4+-N (F1, 10 = 0.97, p = 0.370) (Fig. 1) were lower in common carp treatments than in the controls. Concentrations of TN and TP varied significantly over time (RM-ANOVAs, time effect, F5, 35 = 4.2, p = 0.006 and F5, 35 = 5.7, p = 0.001, respectively). NO3-N and TN were lower in the carp treatments than in the controls on each sampling occasion (t-test, p < 0.05), except on days 70 and 84 for TN. TP was lower in the carp treatment than in the controls on days 42 and 56 (t-test, p < 0.05).

thumbnail Fig. 1

Nitrogen and phosphorus in different treatments over time. Asterisks indicate significant differences between common carp treatments and the controls (p < 0.05). Bars indicate ±1 SD.

3.2 TSS and phytoplankton

Concentrations of TSS (Fig. 2) in the common carp treatment were higher than in the controls (RM-ANOVAs, treatment effect, F1, 10= 36.6, p = 0.002), while levels of chl a, representing phytoplankton abundance, were not (RM-ANOVAs, treatment effect, F1, 10= 2.9, p = 0.152), though this parameter was higher on day 28 (t-test, p < 0.05). Both TSS and chl a (Fig. 2) were seen to vary significantly over time (RM-ANOVAs, time effect, F5, 35 = 9.6, p < 0.001 and F5, 35 = 8.7, p < 0.001, respectively). TSS concentrations were higher in the common carp treatment than that in the controls on every sampling occasion except day 84 (t-test, p < 0.05).

thumbnail Fig. 2

TSS and chl a of phytoplankton in different treatments over time. Asterisks indicate significant differences between the common carp treatment and the controls (p < 0.05). Bars indicate ±1 SD.

3.3 Light intensity

The light intensity (Fig. 3) at 1.0 meter below the water surface of the common carp treatment was lower than in the controls (RM-ANOVAs, treatment effect, F1, 8 = 18.1, p = 0.008) and varied significantly over time (RM-ANOVAs, time effect, F4, 24 = 41.7, p = 0.024).

On each sampling occasion, light intensity was lower in the common carp treatment than in the controls (t-test, p < 0.05), except on day 84 (p > 0.05), indicating that the presence of fish increased light attenuation.

thumbnail Fig. 3

Light intensity in different treatments over time. Asterisks indicate significant differences between the common carp treatments and the controls (p < 0.05). Bars indicate ±1 SD.

3.4 Biomass of submerged plants

At the beginning of the experiment, biomass of H. verticillata was 1.25 ± 0.24 g/mesocosm (Fig. 4). At the end of the experiment, the biomasses did not differ between common carp treatments (77 ± 45 g/ mesocosm) and the controls (60 ± 22 g/mesocosm) (p > 0.05). Biomasses of V. denseserrulata on the other hand were lower in the common carp treatments than in the controls (t-test, p < 0.05) at the end of the experiment. Their biomasses decreased from 21.8 ± 5.8 g/ mesocosm at the beginning of the experiment to 1.7 ± 0.6 g/mesocosm at the end of the experiment in the controls, with an even greater loss in the common carp treatments.

thumbnail Fig. 4

Submerged plant biomass in different treatments. Asterisk indicates a significant difference between the common carp treatment and the controls (p < 0.05). Bars indicate ±1 SD.

4 Discussion

We found that the presence of common carp was associated with increased TSS concentration and light attenuation. Although we could find no significant relationship between fish presence and increased phytoplankton chl a, we did find that the presence of fish appears to reduce the biomass of V. denseserrulata. Contrary to our hypothesis, we found no evidence that common carp increase levels of TN and TP, but we did find an association between fish and declining water clarity.

Bioturbation by benthivorous fish can cause resuspension of sedimented materials (Cline et al., 1994) and increase levels of TSS in the water column (Lougheed et al., 1998; Parkos et al., 2003). This disturbance effect explains the reduced availability of light observed at the sediment surface in the common carp treatments.

Increased light attenuation may have a negative effect on submerged plant growth (Badiou and Goldsborough, 2015), especially for V. denseserrulata. This species produces a basal rosette of leaves, but does not form a canopy. The plant therefore depends more on light being available near the sediment for growth and survival. In this study, biomasses of V. denseserrulata in the common carp (total dry weight = 0.40 ± 0.69 g) were lower than in the controls (total dry weight = 1.70 ± 0.61 g). However, the degree to which this reduced biomass was caused directly by the grazing of fish or indirectly by light limitation linked to fish bioturbation cannot be determined from this study. Elsewhere, common carp have had a negative impact on submerged plants biomass (King and Hunt, 1967Badiou and Goldsborough, 2015).

The apparent lack of a significant effect of common carp on the biomass of H. verticillata is consistent with previous work showing that different plant species vary in their susceptibility to the effects of common carp (Zambrano and Hinojosa, 1999). Roberts et al. (1995) reported that common carp can directly consume Vallisneria, preferring it to H. verticillata. Also, H. verticillata has high rates of reproduction and growth (Shearer et al., 2007), which might compensate for any grazing losses. In addition, more biomass of H. verticillata is in a dense canopy distributed near the surface of water and thus less impacted by reduced light condition induced by carp activities. Therefore, the response of an aquatic ecosystem to common carp may be different depending on the dominant submerged plant species present. An aquatic ecosystem that is dominated by H. verticillata would be less sensitive to common carp than one dominated by V. denseserrulata.

Contrary to our hypotheses, concentrations of TN and TP were lower in mesocosms containing common carp than in the controls. However, most other studies have shown an increase in nutrients with common carp (Breukelaar et al., 1994; Chumchal et al., 2005). There are a couple of explanations for our results. There is a positive relationship between nutrient uptake by the leaves of macrophytes and water velocity, resulting from reduced thickness of the boundary layer around leaves in disturbed water (Westlake, 1967; Wheeler, 1980; Madsen and Søndergaard, 1983). The swimming of common carp may enhance nutrient uptake by leaves of submerged plants, thereby contributing to decreased nutrient concentrations in the water. In addition, phosphate and dissolved nitrogen in the water can also adsorb to the resuspended sediment particles caused by the fish bioturbation and with these dimentation of these particles carrying it to the bottom. Another explanation is associated with the high plant abundance in our experiments. While foraging activities by common carp can enhance the release of nutrients from sediment, the effect is likely to be mitigated when macrophytes are abundant due to their role in enhancing sedimentation (Qin and Threlkeld, 1990; Cline et al., 1994). Additionally, activities by carp may increase the water exchange between deeper layer and surface layer which may increase oxygen concentrations at the sediment-water interface and thus decreased the sediment P release by oxidizing the surficial sediments. Whether denitrification is a possible mechanism causing nitrogen loss in our experiments is unknown as we did not measure dissolved oxygen in the surficial sediment. Finally, common carp may also consume some particles suspended in water column, further helping to reduce nutrient levels (Boers et al., 1991; Roberts et al., 1995). Note that in this experiment we added nutrients to mimic external nutrient loading. The concentrations of TN and TP might have increased due to the bioturbation of the fish if no nutrients were added during the experiment simulating a system without external loading. However, a system without nutrient additions may not reflect a real lake.

The effect of common carp on phytoplankton is more variable. Previous studies have demonstrated that common carp have positive effects on the growth and biomass of phytoplankton (Breukelaar et al., 1994; Roberts et al., 1995). However, Fischer et al. (2013) was not able to observe any increase in chl a in treatments with common carp present and Lougheed et al. (1998) found no significant correlation between chl a concentration and common carp biomass. Likewise in this study, we found no significant difference in chl a between common carp treatment and controls, possibly because of the high abundance of macrophytes (density = 61.5 gm−2) limiting phytoplankton growth in both treatments.

In conclusion, in ecosystems dominated by submerged plants, common carp can negatively impact water clarity by increasing TSS concentration which increase light attenuation in the water column. However, contrary to our expectations, common carp presence reduced the concentrations of TN and TP and had no significant impact on phytoplankton biomass (chlorophyll a). The fish can also reduce the biomass of V. natans but not H. verticillata, which has important implications for plant management. By planting carp-resistant or carp-tolerant plants we can minimize their impact because decline of submerged plants can markedly alter many aspects of aquatic ecosystem. Our findings indicate that the removal of common carp would be a useful practice for managers to protect and maintain water clarity in well-vegetated aquatic ecosystems.

Acknowledgements

We thank the two anonymous reviewers for their constructive editorial comments. This research was supported by the National Natural Science Foundation of China (No. 41771100; 41811530056); the Natural Science Foundation (No. 1608085MD85) and the Key Projects of Education Department (No. KJ2017A161) of Anhui province, China; and with additional support from the Chinese-Belarusian Joint Project of Belarussian Republican Foundation for Fundamental Research (B18KI-007).

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Cite this article as: Qiu X, Mei X, Razlutskij V, Rudstam LG, Liu Z, Tong C, Zhang X. 2019. Effects of common carp (Cyprinus carpio) on water quality in aquatic ecosystems dominated by submerged plants: a mesocosm study. Knowl. Manag. Aquat. Ecosyst., 420, 28.

All Figures

thumbnail Fig. 1

Nitrogen and phosphorus in different treatments over time. Asterisks indicate significant differences between common carp treatments and the controls (p < 0.05). Bars indicate ±1 SD.

In the text
thumbnail Fig. 2

TSS and chl a of phytoplankton in different treatments over time. Asterisks indicate significant differences between the common carp treatment and the controls (p < 0.05). Bars indicate ±1 SD.

In the text
thumbnail Fig. 3

Light intensity in different treatments over time. Asterisks indicate significant differences between the common carp treatments and the controls (p < 0.05). Bars indicate ±1 SD.

In the text
thumbnail Fig. 4

Submerged plant biomass in different treatments. Asterisk indicates a significant difference between the common carp treatment and the controls (p < 0.05). Bars indicate ±1 SD.

In the text

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