Does turbidity induced by Carassius carassius limit phytoplankton growth? A mesocosm study
It is well established that benthivorous fish in shallow lakes can create turbid conditions that influence phytoplankton growth both positively, as a result of elevated nutrient concentration in the water column, and negatively, due to increased attenuation of light. The net effect depends upon the degree of turbidity induced by the benthivores. Stocked Carassius carassius dominate the benthivorous fish fauna in many nutrient-rich Chinese subtropical and tropical shallow lakes, but the role of the species as a potential limiting factor in phytoplankton growth is ambiguous. Clarification of this relationship will help determine the management strategy and cost of restoring eutrophic lakes in China and elsewhere. Our outdoor mesocosm experiment simulating the effect of high density of crucian carp on phytoplankton growth and community structure in eutrophic shallow lakes suggests that stocking with this species causes resuspension of sediment, thereby increasing light attenuation and elevating nutrient concentrations. However, the effect of light attenuation was insufficient to offset the impact of nutrient enhancement on phytoplankton growth, and significant increases in both phytoplankton biomass and chlorophyll a concentrations were recorded. Crucian carp stocking favored the dominance of diatoms and led to lower percentages (but not biomass) of buoyant cyanobacteria. The dominance of diatoms may be attributed to a competitive advantage of algal cells with high sedimentation velocity in an environment subjected to frequent crucian carp-induced resuspension and entrainment of benthic algae caused by the fish foraging activities. Our study demonstrates that turbidity induced by stocked crucian carp does not limit phytoplankton growth in eutrophic waters. Thus, removal of this species (and presumably other similar taxa) from subtropical or tropical shallow lakes, or suspension of aquaculture, is unlikely to boost phytoplankton growth, despite the resulting improvements in light availability.
KeywordsCrucian carp Nutrients Resuspension Suspended solids Phytoplankton community Shallow lakes China
In most shallow lakes, benthivorous fish such as common carp (Cyprinus carpio) are important factors determining water clarity (Weber and Brown 2009; Bernes et al. 2013; Villizzi et al. 2015). Benthivorous fish select food by sucking in sediment and ejecting all but the retained food particles back into the water column. The process often causes sediment resuspension, resulting in non-algal turbidity (hereafter referred to as “turbidity”) in the water column (Richardson et al. 1995).
While the role of benthivorous fish in creating turbid conditions in shallow lakes is well established, the net effect of sediment resuspension on standing crops of phytoplankton can be both positive and negative (Weber and Brown 2009). Many studies have shown that stocking common carp or bream (Abramis brama) enhances phytoplankton growth in shallow lakes and ponds as indicated by measurements of biomass or chlorophyll a concentration (Havens 1991; Breukelaar et al. 1994). Likely, mechanisms include increased nutrient levels mediated by benthic foraging activity and subsequent excretion (Lamarra 1975; Havens 1991), algal entrainment following resuspension of benthic material in the water column (Roozen et al. 2007), and predation of phytoplankton grazers such as crustacean zooplankton (Weber and Brown 2015). However, several studies have also reported that light attenuation resulting from benthic feeding may serve to limit phytoplankton growth despite the abovementioned positive factors. For instance, a 60-day mesocosm experiment using common carp and fishless controls conducted by Wahl et al. (2011) found that mesocosms with carp (277–430 kg ha−1) developed high turbidity but low chlorophyll a concentrations compared with controls. Badiou and Goldsborough (2015) examined the effects of interactions between common carp and nutrient addition on phytoplankton biomass in mesocosms in Delta Marsh, Manitoba, Canada. They found that under nutrient-enriched conditions, high densities of carp (1320–1720 kg ha−1) suppressed phytoplankton growth, which was not the case in the fish-free controls and the low carp biomass treatments (600–720 kg ha−1). It can therefore be concluded that benthivorous fish can inhibit phytoplankton growth in shallow lakes if the turbidity caused by benthic feeding is high.
Crucian carp (Carassius carassius), a common benthivore belonging to the Cyprinidae family, is widely distributed in Eastern Asia. In shallow lakes in subtropical and tropical China, it benefits from the warm climate and intensive aquaculture (FAO 2004–2015) and is often the dominant benthivore (Gao et al. 2014). Like common carp, crucian carp causes sediment resuspension via benthic foraging, thereby increasing lake turbidity. Thus, a central question for lake managers seeking to reverse anthropogenic eutrophication is whether turbidity linked to high densities of crucian carp limits or stimulates phytoplankton growth in nutrient-rich waters. Perceptions of the role of crucian carp may influence the strategy and cost of managing and restoring many eutrophic shallow lakes in China and elsewhere. However, because the net effect of benthivorous fish on phytoplankton growth depends upon the degree of fish-induced turbidity, insight obtained from studies of common carp may not necessarily hold true for crucian carp due to the morphological and behavioral differences between the two species. Adult crucian carp are typically smaller than similar-aged common carp and have a terminal mouth not well suited for digging into the sediment (Wu 1964). Field observations have shown that suspended solid concentrations in two other Chinese lakes, West Lake and Lake Wuli, where crucian carp are abundant, rarely reach 50 mg L−1 (Chen et al. 2013; Z. Liu and J. Yu, unpublished data). These values are lower than those recorded by Wahl et al. (2011) and Badiou and Goldsborough (2015) (total suspended solid (TSS) > 100 mg L−1), suggesting that foraging crucian carp generate lower concentrations of suspended solids than common carp, even at high densities, and that the resulting light attenuation may therefore not be sufficient to limit phytoplankton growth.
We conducted a mesocosm experiment to explore the effects of crucian carp on phytoplankton growth in eutrophic shallow lakes. Our aim was to determine whether the turbidity induced by high densities of stocked fish limits phytoplankton growth or not. We hypothesized (1) that crucian carp would suspend the sediments and thereby increase both nutrient concentrations and light attenuation and (2) that the net effect of crucian carp on phytoplankton biomass would be positive due to the relatively low expected turbidity compared to true benthivores such as common carp.
Materials and methods
The outdoor mesocosm experiment was conducted from 3 to 19 October 2013 at the Taihu Lake Laboratory Ecosystem Research Station, located in Meiliang Bay, on the northern edge of Lake Taihu. Six cylindrical, high-density polyethylene tanks (74 cm height × 94 cm upper diameter × 81 cm bottom diameter) located in a square concrete pond (4 m side × 0.5 m water depth) were filled with a 10-cm layer of lake sediment and 300 L water collected from the Meiliang Bay. The sediments had previously been sieved (mesh size 1.7 mm) to remove large invertebrates and mixed to ensure uniformity. The water was screened using a 64-μm mesh filter to remove crustacean zooplankton and inorganic particles.
Crucian carp with an average length of 11 ± 0.5 cm and a biomass of 18 ± 1 g was obtained from a local aquaculture pond and acclimatized in lake water for 5 days before the experiment began. The fish were added randomly to three mesocosms (one fish per tank), approximating a natural density of 360 kg ha−1, which is high but comparable to the density recorded in turbid shallow lakes such as the West Lake in tropical China (Gao et al. 2014) and in many aquaculture ponds. The remaining three mesocosms without crucian carp functioned as controls. To prevent fish from jumping out of the mesocosms, the top of each tank (including the control tanks) was covered by a thin gauze.
During the experiment, nutrients (5 μg P L−1 day−1 and 130 μg N L−1 day−1) were added to each mesocosm (both treatments) on a daily basis to simulate external loading. Phosphorus and nitrogen were introduced separately as aqueous solutions of potassium dihydrogen phosphate (KH2PO4) and potassium nitrate (KNO3), the dominant inorganic nutrient forms in Lake Taihu (Xu et al. 2010).
Sampling and analytical methods
On the mornings of days 0 (October 3), 4, 8, 12, and 16 of the experiment, light intensity in each mesocosm was measured at four depths (0, 10, 20, and 30 cm) using a digital lux meter (ZDS-10W, Shanghai, China). Ratios of light intensity at each depth (10, 20, and 30 cm) relative to the water surface (0 cm) were used to calculate changes in light attenuation over time and between treatments. Thereafter, a small (1 L) depth-integrated water sample was collected from each mesocosm using a tube sampler (8 cm diameter, 64 cm length) and analyzed in the laboratory for suspended solid (SS), nutrients, and chlorophyll a (chl-a).
TSS was determined from 100 to 200 mL water samples filtered through pre-combusted (450 °C for 2 h) and pre-weighed GF/C filters, which were then dried to a constant weight at 60 °C for 48 h. After determining TSS, the filters were combusted in a muffle furnace at 550 °C for 2 h, cooled in a desiccator, and finally weighed to determine the level of inorganic suspended solid (ISS). The proportion of TSS comprising inorganic particles (ISS percentage) was used to reflect changes in turbidity due to resuspension. Total nitrogen (TN), total phosphorus (TP), total dissolved nitrogen (TDN), and total dissolved phosphorus (TDP) concentrations were measured according to Chinese standard methods (Jin and Tu 1990). Chl-a concentrations were measured spectrophotometrically from the matter retained on a GF/C filter and extracted in a 90% (v/v) acetone/water solution for 24 h. No correction for pheophytin interference was performed (SEPA 2002).
At the start and end of the experiment, a 1 L depth-integrated sample from each mesocosm was treated with 10 mL Lugol’s iodine solution and sedimented for 48 h. The supernatant was removed, and the residue was collected and examined under ×100–×400 magnification for enumeration of phytoplankton. Phytoplankton was identified to its genus level following Hu (2006) and using, as far as possible, recent taxonomic revisions (Guiry and Guiry 2014). The biomass of common phytoplankton taxa was calculated based on cell size measurements of at least 30 cells of each taxon and using formulae for geometric shapes approximating cell forms (Zhang and Huang 1991). For less common taxa, biomass calculations were based on fewer measurements; otherwise, at least 1000 cells of each taxon were counted per sample. Phytoplankton biovolume was multiplied by 0.29 to obtain an approximation of dry weight (Reynolds 1984).
Differences in zooplankton communities (rotifers, cladocerans, and copepods) between treatments were also recorded at the end of this experiment. Rotifers were counted directly from phytoplankton samples at ×100 magnification (at least 100 individuals of the most abundant taxa). Microcrustaceans were collected by filtering depth-integrated water samples (10 L) through a 64-μm net and subsequently preserved in 4% formaldehyde. Crustacean zooplankton were counted at ×40 magnification. Species identifications were made according to Wang (1961), Chiang and Du (1979), and Shen and Du (1979). Zooplankton biomass (dry weight) was estimated using equations from Huang (1999). We measured up to 40 individuals of each taxon, whenever possible.
Nutrient data, light intensity, suspended solids, and chl-a concentrations were compared between the mesocosms with and without crucian carp, using a permutational univariate analysis of variance (PERMANOVA+, PRIMER v. 7). PERMANOVA is the equivalent of an ANOVA performed on similarity values generated from non-metric multi-dimensional scaling performed on ranked Bray-Curtis similarities and uses permutations to test the significance of differences between groups (Anderson et al. 2008). Differences between mesocosms with and without crucian carp were tested using Monte Carlo P values (P < 0.05), which provided an approximation of significance based on asymptotic theory and should be used in preference to the permutational P values when the number of unique permutations is 999. At the beginning of experiment, phytoplankton communities were compared using Student’s t test (P < 0.05) to check the homogeneity among tanks. The final zooplankton and phytoplankton biomass and percentages of each taxon were also compared using Student’s t test performed with the statistical package SPSS, version 16.0 (IBM Corporation, Somers, NY, USA). Prior to analysis, the phytoplankton and zooplankton data were log10 transformed to meet the requirements of normal distribution and homogeneity of variance.
Student’s t test revealed that the biomass of copepods (dominated by nauplii) and cladocerans (only small-sized Bosmina, Chydorus, and Spapholeberis) did not differ significantly between mesocosms at the end of the experiment (t test, P > 0.05; Fig. 5c), whereas the biomass of rotifers (dominated by Brachionus and Keratella) was higher in the controls (0.232 mg L−1 on average) than in the carp treatments (0.094 mg L−1 on average) (t test, P < 0.001; Fig. 5c) (see supplementary file for zooplankton community). Consequently, the zooplankton-to-phytoplankton biomass ratio (Zoop/Phyt), although low in all treatments, was significantly higher in the controls than in the carp mesocosms (t test, P = 0.034; Fig. 5d).
As expected, increased light attenuation and elevated nutrient concentrations were observed in the mesocosms with crucian carp (Figs. 2 and 3), and we attribute this to resuspension of sediment particles resulting from benthic foraging activity (Fig. 1). Stocking with crucian carp also led to elevated phytoplankton biomass and chlorophyll a concentrations (Figs. 4 and 5a), demonstrating that the turbidity induced by crucian carp resuspension of sediment was not sufficient to hamper the growth of phytoplankton. Our results differ from those of Wahl et al. (2011) and Badiou and Goldsborough (2015) who found a light limitation of phytoplankton growth in mesocosms stocked with high densities of common carp at similar turbidity levels. The chl-a concentrations in the fish-free mesocosms in their experiments were >100 μg L−1, i.e., much higher than those recorded in our mesocosms (<25 μg L−1 in the mesocosms without crucian carp). Self-shading resulting from high densities of phytoplankton probably rendered light a main factor limiting phytoplankton growth in their mesocosms. Therefore, in their case, a further increase in light attenuation resulting from the addition of common carp impacted on phytoplankton growth negatively.
In our study, reduced top-down control resulting from the lower density of rotifers may to some extent have boosted phytoplankton growth in the mesocosms stocked with crucian carp (Fig. 5c). However, the low zooplankton-to-phytoplankton biomass ratio in all treatments, perhaps due to the pre-filtered (64 μm) water and the short experimental duration (16 days), indicates an overall low grazing pressure (Jeppesen et al. 2011). The conditions are, however, similar to that in subtropical or tropical shallow lakes, where large-bodied zooplankton are generally very scarce because of the high abundance of small-sized fish (Liu et al. 2014). A more likely explanation of higher phytoplankton biomass in our crucian carp tanks is a fish-induced enhancement of nutrient availability (Fig. 2a, c) when nutrients from fertile sediments are transported to overlying water by the foraging actions. The higher ISS percentage and TN and TP concentrations recorded in the mesocosms holding crucian carp support this suggestion (Figs. 1b and 2a, c). Similar observations are available for common carp (Breukelaar et al. 1994; Richardson et al. 1995). In addition to sediment resuspension, fish excretion may also have contributed to the increased nutrient concentrations in the water (Lamarra 1975). Dissolved nutrient levels in the mesocosms, however, did not change significantly following the introduction of crucian carp (Fig. 2b, d), possibly reflecting a rapid nutrient uptake by phytoplankton. Similarly, He et al. (2015) found a significant increase in total nutrient levels but only a minor increase in dissolved forms in mesocosms exhibiting sediment resuspension compared with static mesocosms. In our study, turbidity was much greater in the fish mesocosms (ISS > 100 mg L−1) than in the reference lakes, Lake Taihu and Lake Wuli, probably due to the small volume of the mesocosms. However, the increased light attenuation caused by fish-induced sediment resuspension was more than compensated by enhanced nutrient availability, leading to a net increase in phytoplankton biomass.
Benthivorous fish can affect not only biomass of phytoplankton but also community composition (Havens et al. 1991; Roozen et al. 2007; Jeppesen et al. 2012). Benthic fish-induced resuspension may favor phytoplankton species with relatively large cells and high sedimentation velocity, such as diatoms. In contrast, small-sized, mobile, or buoyant algal species may dominate in more static waters (Kruk et al. 2010; Kang et al. 2013; He et al. 2015). In our study, crucian carp significantly enhanced the contribution and biomass of diatoms and reduced the contribution but not the biomass of cyanobacteria (Fig. 5b) relative to the controls, which might be attributed to increased competitiveness of certain large algal cells and entrainment of benthic algae caused by crucian carp foraging activities. Our results support the field observations by Roozen et al. (2007) that the fraction of non-motile algae is positively related to the concentration of inorganic solids resuspended by benthivorous fish. In addition, previous studies have reported that adult crucian carp graze preferentially on cyanobacteria, for instance Microcystis spp. in eutrophic lakes (Liu et al. 2007). However, due to a lack of gut content data, we cannot determine the importance of consumption for the observed changes in the phytoplankton communities.
The results of our study are of significance to the management of Chinese shallow lakes. China is the world’s largest producer of crucian carp, contributing more than 90% of total global production (FAO 2004–2015). Besides fish ponds, crucian carp are also commonly cultivated in natural waterbodies such as lakes and reservoirs (Z. Liu and J. Yu, unpublished data). So far, evidence of the effects of crucian carp stocking on lake eutrophication is scarce. Lake managers occupied with restoration efforts have been uncertain about whether the reduced turbidity that follows removal of crucian carp will inhibit or stimulate phytoplankton growth. Our study suggests that at identical levels of external nutrient input, high densities of crucian carp will increase the biomass of phytoplankton. Thus, in addition to removal of true benthivorous fish such as common carp, removal of crucian carp or cessation of carp culture, in general, may be a valuable step in reducing eutrophication.
The authors wish to express their gratitude to Xiaolong Zhu, Xiaoxia Chen, and Ruijie Shen for the support in the field and in the laboratory. This study was supported by the National Science Foundation of China (31500379 and 41571086); by the MARS (Managing Aquatic ecosystems and water Resources under multiple Stress) project funded under the Seventh EU Framework Programme, Theme 6 (Environment Including Climate Change), Contract No. 603378 (http://www.mars-project.eu); and by the CLEAR (a Villum Kann Rasmussen Centre of Excellence project).
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