Eutrophication is a process where the pool of nutrients in a lake increases as a result of an influx from outside the ecosystem. This increase in the pool of nutrients is then followed by changes in internal nutrient cycles (Ejsmont-Karabin 1983). Mineralization of phosphorus (P) by heterotrophs generally provides a sufficient amount of P to sustain primary production during periods of low P availability, but external pulses are required to induce algal blooms (Kamarainen et al. 2009). In eutrophic lakes, a smaller proportion of algal biomass is directly used by planktonic herbivores, while a greater proportion is indirectly consumed (after cell death) by bacterivores. This may accelerate the rate of nutrient regeneration (Ejsmont-Karabin 1983) and thus increase the pool of nutrients and the trophic state of lake waters in general. Experiments carried out by Bossard & Uehlinger (1993) have shown that the exclusion of crustaceans increases the residence time of total P by a reduced P loss through sedimentation. Thus, the presence of crustaceans should reduce the pool of phosphorus and, consequently, the trophic state of waters. This role of large cladocerans in the phytoplankton biomass control has been confirmed by Ejsmont-Karabin et al. (2004), although in some cases other zooplankton organisms may play the same role.
Fish can affect the processes of eutrophication as demonstrated by Stenson (1982). His manipulation of fish at the top of the ecosystem resulted in changes in nutrient cycles and the development of a new rotifer community. A significant structuring role of fish was also shown in 8-year studies on three eutrophic lakes (Jeppesen et al. 2000). Reduction in planktivores in the lakes resulted in an increase in cladoceran size and a decrease in chlorophyll a concentrations.
Zebra mussels
In experiments on the impact of Crustacea, bivalves (
The experiment was carried out from 31 July to 1 September 2012 and consisted of 12 treatments, each of which was replicated in triplicate mesocosms (36 mesocosms in total). The outdoor mesocosms were originally filled with 270 l of unfiltered water from the pelagic zone of eutrophic Lake Mikołajskie (498 ha; Masurian Lake District, northeastern Poland) and kept on the shore of that lake during the experiment. Mesocosms (plastic containers with internal dimensions of 0.94 m × 0.50 m, a height of 0.64 m and a capacity of 300 l) were devoid of sediments.
Three mesocosms were filled with unfiltered water that contained the natural abundance of zooplankton and served as the control (C). One-liter samples collected from each mesocosm were examined for zooplankton on the day the experiment started. According to the results of the observations, the control consisted of small cladocerans
The Crustacea (Cr) treatment was a mixture of crustaceans: 500 ind. of
We enriched the water in six treatments (18 mesocosms) with 1.728 mg l−1 N-NO3, 0.192 mg l−1 N-NH4 and 0.120 mg l−1 P-PO4, in order to obtain concentrations of nutrients typical of highly eutrophicated waters.
The fish treatment consisted in placing one individual of the ruffe (
One-liter samples were collected from each mesocosm on days 1, 12, 22 and 32 of the experiment to examine rotifers. The samples were fixed with Lugol’s solution, condensed on a plankton net with a mesh size of 30 μm, and again fixed in 2% formalin. Individual rotifer biomass was determined based on relationships between body length and body weight for each species (Ejsmont-Karabin 1998).
Rotifer trophic state indices (TSImean) were used to assess changes in the trophic state of the mesocosms based on: (1) the number of rotifers (N, ind. l−1): TSIN = 5.38 Ln(N) + 19.28; (2) total biomass of the rotifer community (B, mg w.wt. l−1): TSIB = 5.63 Ln(B) + 64.47; (3) percentage of bacterivores in the total number of rotifers (BAC, %): TSIBAC = 0.23 BAC+ 44.30; (4) ratio of the biomass of rotifers to their count (B:N, mg w.wt. ind.−1): TSIB:N = 3.85 (B:N)−0.318; (5) percentage of the form
The rotifer trophic state index (TSImean) was defined as a mean of the particular zooplankton indices. Although eutrophication is a continuous process, for practical reasons it has been assumed that mesocosms with a TSImean under 45 were mesotrophic, 45–55 were meso-eutrophic, 55–65 were eutrophic, and greater than 65 were hypertrophic (Ejsmont-Karabin 2012).
We used a generalized linear model (GLM) for statistical analysis, which was designed to assess the effect of one or more treatment factors on one or more dependent variables. Our analyses involved three factors, including treatment (A), the number of mesocosms (B), and time, i.e. date (C). We analyzed TSImean (averaged over all six TSI indices), TSIN based on the number of rotifers, TSIB based on rotifer biomass, TSIBAC based on the percentage of bacterivores in the total number of rotifers, TSIB/N based on the ratio of biomass to count. Two TSI indices (percentage of the
We constructed mixed GLMs to compare the treatments (A), interactions between treatment (A) and time (C), and the effects of mesocosm (B). The treatment and time (repeated measure) were specified as fixed factors, while the mesocosm was randomly nested within the treatments (B(A)). Data were loge transformed as necessary to help meet the assumptions of normality of residuals. When significant treatment effects were detected with ANOVA, Fisher’s LSD post hoc test (
Rotifers increased their abundance in 61% of the 36 mesocosms by the end of the experiment (Table 1). However, the addition of nutrients together with crustaceans and/or fish often resulted in a reduced number of rotifers, as rotifer density increased in only 25% of the treatments. The highest increase in rotifer density was observed in the control (2.5-fold), the Crustacea treatment (3.9-fold), the
Quantitative and qualitative features of rotifer communities used to calculate rotifer trophic state indices: N – the number of rotifers (ind. l−1), B– rotifer biomass (mg l−1), BAC – bacterivores in the total number of rotifers (%), TECTA – percentage of the tecta form in the
Treatment | No. | After 1 day of the experiment | After 32 days of the experiment | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
N | B | BAC | TECTA | B/N | IHT | N | B | BAC | TECTA | B/N | IHT | ||
Control | 1 | 714 | 0.160 | 5.3 | 50.0 | 0.236 | 96.4 | 1516 | 0.117 | 78.8 | 0.0 | 0.077 | 100.0 |
2 | 923 | 0.201 | 12.7 | 24.0 | 0.218 | 97.9 | 2498 | 0.187 | 89.4 | 7.2 | 0.075 | N/a | |
3 | 1346 | 0.363 | 15.3 | 15.8 | 0.269 | 95.5 | 3405 | 0.444 | 74.4 | 0.8 | 0.130 | 100.0 | |
C + Crustacea (Cr) | 1 | 700 | 0.185 | 5.1 | 15.4 | 0.264 | 89.0 | 2185 | 0.190 | 81.5 | 0.5 | 0.087 | 100.0 |
2 | 567 | 0.138 | 8.1 | 22.2 | 0.243 | 96.1 | 3993 | 0.424 | 83.4 | 3.9 | 0.106 | 100.0 | |
3 | 512 | 0.098 | 17.4 | 0.0 | 0.192 | 86.0 | 709 | 0.082 | 51.6 | N/a | 0.116 | 100.0 | |
C + Dreissena (Dp) | 1 | 380 | 0.088 | 1.3 | 0.0 | 0.290 | 87.5 | 520 | 0.076 | 51.7 | 0.0 | 0.147 | 100.0 |
2 | 78 | 0.017 | 1.3 | N/a | 0.217 | 50.0 | 818 | 0.119 | 43.6 | N/a | 0.145 | N/a | |
3 | 123 | 0.027 | 4.1 | 0.0 | 0.216 | 100.0 | 637 | 0.104 | 57.5 | N/a | 0.163 | N/a | |
C + Nutrients (N) | 1 | 217 | 0.040 | 2.3 | 100.0 | 0.184 | 100.0 | 1996 | 0.276 | 53.7 | N/a | 0.138 | N/a |
2 | 7338 | 1.652 | 5.2 | 33.7 | 0.225 | 92.2 | 2253 | 0.282 | 59.2 | 2.1 | 0.125 | 93.6 | |
3 | 3181 | 0.736 | 7.4 | 18.8 | 0.231 | 95.7 | 1065 | 0.135 | 80.2 | 2.2 | 0.127 | 98.6 | |
C + Fish (F) | 1 | 1147 | 0.270 | 7.1 | 8.0 | 0.236 | 95.2 | 1428 | 0.141 | 60.3 | 0.0 | 0.099 | 100.0 |
2 | 1616 | 0.358 | 14.0 | 39.1 | 0.222 | 95.9 | 2615 | 0.440 | 76.1 | 6.8 | 0.168 | 100.0 | |
3 | 1465 | 0.351 | 2.6 | 23.5 | 0.240 | 90.4 | 3044 | 0.285 | 66.0 | 0.0 | 0.094 | 100.0 | |
C + Crustacea + Dreissena (CrDp) | 1 | 408 | 0.090 | 2.2 | N/a | 0.220 | 90.5 | 186 | 0.045 | 50.0 | N/a | 0.241 | N/a |
2 | 136 | 0.030 | 0.7 | N/a | 0.224 | 33.3 | 135 | 0.021 | 28.1 | N/a | 0.151 | N/a | |
3 | 308 | 0.072 | 4.5 | 0.0 | 0.234 | 68.4 | 290 | 0.044 | 52.4 | N/a | 0.151 | N/a | |
C + Fish + Crustacea (FCr) | 1 | 726 | 0.189 | 0.8 | 0.0 | 0.260 | 85.6 | 1162 | 0.090 | 70.6 | 0.0 | 0.078 | 100.0 |
2 | 1907 | 0.479 | 7.0 | 41.9 | 0.251 | 92.0 | 3004 | 0.369 | 71.7 | 0.5 | 0.123 | 100.0 | |
3 | 1663 | 0.418 | 7.3 | 5.9 | 0.251 | 93.6 | 6988 | 0.469 | 85.3 | 3.5 | 0.067 | 100.0 | |
C + Nutrients + Crustacea (NCr) | 1 | 3190 | 0.682 | 6.5 | 26.9 | 0.214 | 96.4 | 4698 | 0.407 | 87.3 | 1.2 | 0.087 | 99.6 |
2 | 5304 | 1.072 | 5.5 | 19.8 | 0.202 | 93.6 | 2008 | 0.170 | 69.2 | 1.2 | 0.085 | 99.6 | |
3 | 4054 | 0.881 | 3.8 | 25.7 | 0.217 | 92.7 | 3442 | 0.465 | 48.8 | N/a | 0.135 | 100.0 | |
C + Nutrients + Dreissena (NDp) | 1 | 451 | 0.104 | 1.8 | N/a | 0.231 | 55.5 | 285 | 0.039 | 58.6 | N/a | 0.136 | 100.0 |
2 | 328 | 0.071 | 0.6 | N/a | 0.217 | 0.0 | 1886 | 0.316 | 65.9 | N/a | 0.168 | N/a | |
3 | 504 | 0.132 | 0.2 | 0.0 | 0.262 | 12.9 | 2132 | 0.311 | 63.9 | N/a | 0.146 | N/a | |
C + Nutrients + Fish (NF) | 1 | 3331 | 0.730 | 3.4 | 38.9 | 0.219 | 97.6 | 1153 | 0.112 | 79.9 | 0.5 | 0.097 | 99.6 |
2 | 2076 | 0.424 | 16.2 | 27.8 | 0.204 | 97.9 | 4719 | 0.573 | 47.8 | N/a | 0.121 | N/a | |
3 | 5327 | 1.285 | 1.3 | 35.4 | 0.241 | 84.8 | 772 | 0.062 | 35.6 | 0.0 | 0.081 | 99.2 | |
C + Nutrients + Dreissena + Crustacea (NDpCr) | 1 | 1003 | 0.217 | 0.0 | 0.0 | 0.217 | 0.0 | 844 | 0.133 | 73.2 | N/a | 0.158 | N/a |
2 | 584 | 0.132 | 0.9 | N/a | 0.227 | 54.5 | 1555 | 0.298 | 48.8 | N/a | 0.192 | N/a | |
3 | 251 | 0.065 | 0.0 | N/a | 0.258 | 14.3 | 647 | 0.144 | 49.6 | N/a | 0.223 | N/a | |
C + Nutrients + Fish + Crustacea (NFCr) | 1 | 1674 | 0.389 | 3.5 | 46.2 | 0.233 | 92.5 | 714 | 0.740 | 75.8 | 1.5 | 0.103 | 100.0 |
2 | 7374 | 1.619 | 6.5 | 40.5 | 0.221 | 94.5 | 2652 | 0.336 | 58.9 | 0.0 | 0.127 | 97.5 | |
3 | 3888 | 0.880 | 7.8 | 28.9 | 0.226 | 94.4 | 2990 | 0.342 | 60.6 | N/a | 0.114 | 100.0 |
Rotifer biomass in the control did not change throughout the experiment. It increased in four treatments and the mean increase was 1.9-fold (SD = 0.4). The highest increase in rotifer biomass was observed in the treatments with added
The
At the beginning of the experiment, rotifer communities were dominated by pelagic species, however, in the middle of the experiment they were significantly replaced by littoral species from the genera
R-squared statistics for mixed GLMs showed that the fitted models explained 89.9% of the variability in Loge[TSImean], 88.4% in Loge[TSIN], 86.3% in Loge[TSIB], 91.3% in Loge[TSIBAC], and 74.5% in Loge[TSIB/N], respectively. The Durbin-Watson (DWs) test indicated that there was no serial autocorrelation in the residuals for any of the mixed GLMs: Loge[TSImean] − DWs = 2.4,
Results of the effects of treatment, interaction of treatments × time and mesocosms on trophic state indices measured 4 times during the experiment. Mesocosms were treated as a random-nested factor in GLM.
Source | DF1/DF2 | R-Squared statistic (R2) of GLM, Durbin-Watson statistic (DWs; |
||
---|---|---|---|---|
Loge[TSIN] | ||||
A – Treatments | 11/72 | 17.33 | ||
B(A) – Mesocosms (Treatments) | 24/72 | 1.94 | ||
C– Time | 3/ 72 | 11.79 | ||
A × C– Treatments × Time | 33/72 | 2.98 | ||
Loge[TSIB] | ||||
A – Treatments | 11/72 | 17.24 | ||
B(A) – Mesocosms (Treatments) | 24/72 | 1.65 | ||
C– Time | 3/ 72 | 9.48 | ||
A × C– Treatments × Time | 33/72 | 2.96 | ||
Loge[TSIBAC] | ||||
A – Treatments | 11/68 | 2.08 | ||
B(A) – Mesocosms (Treatments) | 24/68 | 2.57 | ||
C– Time | 3/ 68 | 168.7 | ||
A × C– Treatments × Time | 33/68 | 1.28 | ||
Loge[TSIB/N] | ||||
A – Treatments | 11/72 | 1.98 | ||
B(A) – Mesocosms (Treatments) | 24/72 | 1.36 | 0.16 | |
C– Time | 3/ 72 | 33.90 | ||
A × C– Treatments × Time | 33/72 | 1.41 | 0.11 | |
Loge[TSImean] | ||||
A – Treatments | 11/72 | 16.04 | ||
B(A) – Mesocosms (Treatments) | 24/72 | 2.05 | ||
C – Time | 3/ 72 | 49.4 | ||
A × C– Treatments × Time | 33/72 | 2.37 |
The mean values of the trophic state index in all treatments were markedly higher at the end of the experiment than at its beginning (Fig. 1). However, during the first decade of the experiment with added
Changes in the mean values of the trophic state index in six experimental treatments without nutrients and six treatments with added nutrients
In most of our experiments, all treatment factors led to an increase in the rotifer trophic state indices. In all cases without the addition of nutrients, the rotifer trophic state indices indicated a high mesoeutrophic status at the beginning of the experiment and low eutrophic status at the end. In a few cases with the addition of nutrients, the trophic status was eutrophic. The increase resulted mostly from an increasing role of small detritophages in the rotifer communities. This observation is in accordance with Pejler’s (1983) suggestion that most species indicating eutrophic conditions feed on very small particles (i.e. bacteria), whereas species indicating oligotrophic conditions are usually filtrators consuming coarser particles.
The impact of fish on the trophic state is more complicated. Experiments conducted in mesocosms (Drenner et al. 1996) have shown that filter-feeding omnivorous fish interacted synergistically with the trophic state and usually increased the abundance of nanophytoplankton. Reinertsen & Langeland (1982) concluded that fish reduced the biomass of large cladocerans, resulting in an increase in the phytoplankton turnover. Our study seems to confirm the above conclusion, as the addition of nutrients to the mesocosms with fish and crustaceans did not change the trophic state. Experiments in enclosures (Hessen & Nilssen 1985) with added fertilizers, fish and competitors (Cladocera) provided evidence that the influence from potential competitors was less important than other factors.
A decrease in the trophic state may be expected in the experiments with
It is difficult to assess to what extent our results describe the conditions of the lake, i.e. changes in the trophic state of the lake due to the presence of crustaceans,
Our results clearly demonstrated that
In general, rotifer communities respond very quickly to changes in their environment, sometimes through complete reconstruction. Therefore, changes in the structure of their communities can be used to indicate changes in ambient conditions.