Abstract
The oligotrophication of freshwater is the reduction of the nutrient concentration in the water column, which causes the depletion of organic matter and diminishes the biological production of the ecosystem. To elucidate the zooplankton response to nutrient depletion (oligotrophication), an experiment was performed in mesocosms simulating real scenarios. Phytoplankton and zooplankton inocula were collected in the Upper Paraná River Floodplain and subjected to combinated nutrient and transparency treatment. We evaluated whether resource limitation and increased transparency (both associated with oligotrophication) affect the size structure of planktonic crustaceans. The effects of predation were corroborated in the treatments with low nutrient concentrations. Thus, the oligotrophic scenario (high transparency and low nutrient concentration) indicated a decreased size structure of zooplankton, probably because of the predation pressure, supporting the predictions of the size-efficiency hypothesis (SEH). When resources were abundant (in treatments with high nutrient concentrations), the decrease in the size structure indicated that the enrichment of nutrients favoured small individuals. Our results showed that nutrient and transparency manipulation affected species richness, the abundance of individuals, and the zooplankton community size structure. Therefore, we suggest that oligotrophication affects predation and competition dynamics in zooplankton.
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Introduction
Eutrophication is the natural process of ageing in aquatic ecosystems that has been accelerated by human activities (Pinto-Coelho et al. 2005; Smith and Schindler 2009; Dias et al. 2012). However, some human activities can also lead to the oligotrophication of freshwater, promoting the depletion of organic matter. This phenomenon is characterised by the reduction of nutrient concentration in the water column and is reflected in the reduction of biogenic production at all trophic levels (Ney 1996; Stockner et al. 2000). Chains of dams are a common source of this effect because retain seston and nutrients diminishing the fertility of downstream environments (Ney 1996). While ecological research on eutrophic lakes has been extensively conducted since the 1960s, studies of ecosystem responses associated with nutrient load reduction in lacustrine environments are still incipient, and most are restricted to the effects on biomass and phytoplankton community structures (Anderson et al. 2005).
The reduction in algal biomass due to oligotrophication changes the trophic structure of food webs, modifying the size structure of intermediary communities in the trophic cascade (zooplankton), leading to reduced fish production (Stockner et al. 2000; Anderson et al. 2005). Consequently, oligotrophication also affects the transparency of aquatic environments. Increasing water transparency implies a greater vulnerability of zooplankton to predation because it improves the effectiveness of visually oriented predators, which potentiates the effect of the trophic cascade (Hansson et al. 2004; Bramm et al. 2009). Predation by fish is an important regulatory mechanism because of its influence on the size structure of the zooplankton community (Stemberger and Miller 2003; Jeppesen et al. 2004; Quintana et al., 2015). Furthermore, the zooplankton body-size structure reflects the influence of nutrient enrichment (Zhang et al. 2013; Tavşanoğlu et al. 2017) and competition for resources (Hall et al. 1976; Quintana et al. 2015). Thus, zooplankton body size is a fundamental functional characteristic of the dynamics of energy in the trophic web (Barnett et al. 2007; García-Comas et al. 2016).
Oligotrophication can also affect the competitive interactions between zooplankton species (Semenchenko et al. 2007) because it reduces the number of primary resources. As exploitative competition occurs among zooplankton species (Lampert and Sommer 2007), the decrease in resources increases competition. In addition, increased transparency due to oligotrophication can affect the competitive behaviour of the species, since top-down control can only be observed in some species (Semenchenko et al. 2007). The ecological implications of size-dependent predation for competitive interactions between herbivorous zooplankton were delineated and defined as the size-efficiency hypothesis (SEH; Brooks and Dodson 1965). According to this hypothesis, the efficiency of grazing is associated with size because larger zooplankton have a more effective collection apparatus and can filter larger algae, exerting extensive control over the phytoplankton biomass.
In the Upper Paraná River, the canals, rivers, lagoons, islands, and floodplains form a complex river–floodplain system that shelters a high diversity of species, whose regional biodiversity maintenance depends largely on the heterogeneity of habitats inherent to the system (Agostinho et al. 2004; Roberto et al. 2009). The ecological integrity of this ecosystem has been weakened by human interference, especially with respect to upstream reservoirs, which affected the flood pulse of the river (Agostinho et al. 2004). As dam operations interfere with the natural flooding regime downstream, ecological connectivity is reduced, and habitats change, destabilising the function and structure of aquatic communities (Leira and Cantonati 2008; Lansac-Tôha et al. 2009; Bovo-Scomparin et al. 2013). Consequently, long-term studies have revealed the impoverishment of water and increase in transparency in the Paraná River, mainly after the installation of the Porto Primavera Reservoir in 1998 (Roberto et al. 2009; Bonecker et al. 2013; Rodrigues et al. 2015). These changes were attributed to seston retention and sedimentation along the reservoir chain, leading to the depletion of phytoplankton (Bovo-Scomparin et al. 2013) and zooplankton (Bonecker et al. 2013).
The zooplankton size structure has been studied based on changes in community composition (Brooks and Dodson 1965; Moreira et al. 2016), mean body length/weight (Wang et al. 2007; Jeppesen et al. 2004), relative abundance of different size classes (Bonecker et al. 2011; Zhang et al. 2013), biomass–size spectra (Brucet et al. 2010; Tavşanoğlu et al. 2017), and size diversity (Quintana et al. 2015; Tavşanoğlu et al. 2017). To investigate the oligotrophication effects (an increase in transparency and reduced nutrients of waters) on the size structure of planktonic microcrustaceans (minimum, mean, and maximum body lengths; relative abundance of different size classes; and changes in the community), we used an experimental approach based on a real situation, and predicted the following: (1) when low nutrient levels and high transparency levels are combined in the same scenario, the transparency effect overcomes the effect of low nutrients, eliminating larger herbivores and liberating the niche for smaller ones, reducing the size structure; (2) low nutrient levels induce an increase in the size structure because, according to the SEH, larger individuals have competitive advantages and, when dominant, competitively suppress the smaller herbivores; and (3) high transparency levels diminish the community size structure because it increases the fish predation effect (Fig. 1).
Methods
The experimental units consisted of polyethylene mesocosms (1.0 m high and 1.4 m diameter) with a maximum capacity of 1000 L of water, which were supplied with water filtered from the Paraná River (characterised by oligotrophic conditions, Roberto et al. 2009) through a plankton net (40 µm mesh). They were placed in an experimental field of 10 × 15 m. Artificial macrophytes were placed in each treatment (in the same amount of cover in each enclosure) to produce zooplankton refuge and simulate the natural environment (we did not want to test macrophyte effect). To simulate the high diversity of plankton from the floodplain, plankton were previously collected from three different environments: a connected lake and a non-connected lake, both associated with the Paraná River, and in the river itself. For a better representation of the community, the zooplankton were sampled with plankton nets of different mesh sizes (40 and 68 μm). The zooplankton were conditioned for three days in mesocosms, similar to those used as experimental units for acclimation. The inocula of zooplankton were added homogeneously and randomly to each mesocosm for the different treatments. For each mesocosm, 30 individuals (abundance approximated to natural stocks in shallow lakes in the Upper Paraná River Floodplain) of the fish species Moenkhausia forestii Benine, Mariguela, & Oliveira, 2009 were also added; this species was chosen because it is common to the Upper Paraná River, omnivorous, and includes microcrustaceans in its diet (Quirino et al. 2015). Specimens of this species were captured with a 0.4-cm net trawl near aquatic macrophytes, acclimatised in mesocosms for one week prior to the experiment, and fed plankton. The acclimation period of zooplankton and fish was defined based on a pilot experiment.
Previous field data were obtained from a long-term ecological study (Roberto et al. 2009) and provided the reference levels of transparency and nutrients, which were considered the control scenario, i.e., the nutrient level before the building of several reservoirs. The transparency was manipulated by changing the inorganic turbidity. A 2 × 2 full-factorial experiment (Fig. 1), with two inorganic turbidity levels (T1 = 15 NTU, current level recorded in the river; T2 = 35 NTU, previous level recorded in the river) and two nutrient concentration levels (N1 = 100 μg L–1 of nitrate [NO3] and 5 μg L–1 of phosphate [PO4]–current level; N2 = 360 μg L–1 of nitrate and 18 μg L–1 of phosphate–previous level). The turbidity treatments were maintained by the addition of sterile clay and the use of submerged pumps (in all replicates) to avoid sedimentation and aerate the water of the mesocosms. No clay was added to the T1 treatment. Previously to experiment, we compared mesocosms with and without sterile clay: we found that sterile clay did not affect the nutrient concentration levels. The different concentrations of nutrients were maintained by the addition of nitrate and phosphate to avoid the depletion of nutrients over time in the form of NaNO3 and KHPO4.
The treatments were randomly replicated (three replicates) in four combinations, totalling 12 experimental units. High-transparency treatments (T1) potentiate the effect of predation (Bramm et al. 2009), while low transparency treatments (T2) weaken it; increased turbidity affects the efficiency of visual predators (decreases the prey–predator encounter rate). It was still assumed that nutrient-poor treatments (N1) potentiate the effect of resource competition (Quintana et al. 2015) and that enriched treatments (N2) reduce resource competition. Thus, the treatments were combined to represent different scenarios of the environmental conditions on the floodplain of the Upper Paraná River, which would produce different effects of predation and competition interactions on the assembly of planktonic microcrustaceans. The T1N1 treatment with high transparency and low nutrient levels represented the current oligotrophic situation of the Paraná River, potentiating the effects of predation by fish and competition for food. The T2N2 treatment simulated the natural conditions of the river, based on past data, with lower levels of transparency and high nutrients, simulating the weakening of effects of predation and competition; and the T1N2 and T2N1 treatments represented intermediate scenarios, with the maximisation of only one of the factors. It is noteworthy that the treatments were not set to evaluate whether there is predation on the community structure of zooplankton in the Upper Paraná River Floodplain, since previous studies have already identified this effect (Bonecker et al. 2011; Simões et al. 2012). Moreover, one previous experimental study showed that without fish in the mesocosm, the microcrustacean abundance reached 150 ind L–1 (de Melo et al. 2019), ~ 3.5 times higher than in the present study.
The physical and chemical variables (dissolved oxygen [mg L–1], water temperature [°C], pH, and turbidity [NTU]) were measured daily in each treatment using a multiparameter probe (HORIBA U-21). Water samples were obtained at the beginning and end of the experiment for the determination of the chlorophyll-a concentration (μg L–1; Golterman et al. 1978).
The experiment duration was 24-days. The zooplankton community was sampled at the beginning and end of the experiment, totalling 24 samples. For this, 10 L of water were filtered in each mesocosm with a 40-μm mesh plankton net. We conducted a previous pilot experiment and found that 10 L of filtered water were sufficient without the loss of information. The zooplankton samples were fixed with formaldehyde solution (4%) buffered with calcium carbonate.
The abundance of individuals (ind L–1) was obtained by means of sub-samples with a Hensen–Stempell pipette (2.5 mL), counting at least 10% of the sample concentrated in modified Sedgewick–Rafter chambers under an optical microscope (Bottrell et al. 1976). Samples that presented a small number of individuals were quantified completely.
The richness of species, abundance of individuals, size structure, mean body size, and relative abundance of size classes of planktonic microcrustaceans were analysed. A total of 30 adult individuals from each species were measured in each sample. Young cladocerans and juvenile copepods (nauplii and copepodids) were also measured (Bonecker et al. 2011). The measurements of cladocerans and copepods were performed under an optical microscope (Olympus CX41) with a 10 × objective and eyepiece micrometre. The body length was considered the largest body axis of individuals, except for the spines. For the determination of size classes, the taxa were grouped into four ranges, according to the average of all respective length measurements: (1) individuals sized up to 300 μm; (2) sized over 300 μm and up to 600 μm; (3) sized greater than 600 μm and up to 1000 μm; and (4) sized greater than 1000 μm (Bonecker et al. 2011).
The analysis of factorial variance was used to verify the effect of transparency and nutrient treatments on (1) the difference in species richness and abundance of individuals at the beginning of the experiment and (2) the average body length of individuals at the end of the experiment.
Relative abundances were grouped according to size class. Changes in the proportions at the beginning and end of the experiment were evaluated using the chi-square test for each treatment.
These analyses were conducted using R software (R Development Core Team 2015) and the BiodiversityR package (Kindt and Coe 2005).
Results
The water temperature was higher in the treatments with lower transparency, ranging from 25.33 to 32.20 °C, whereas in the treatments with high transparency, the temperature varied between 22.28 and 31.64 °C (Table 1). The concentrations of dissolved oxygen (DO) varied between 6.96 mg L–1 in T1N1 and 8.12 mg L–1 in T2N2, and the pH of the water tended to be alkaline, with a mean ranging between 8.46 and 9.10.
The chlorophyll-a concentration differed among nutrient treatments (factorial ANOVA, F1, 12 = 29.579, p < 0.001) and transparencies (factorial ANOVA, F1, 12 = 6.361, p = 0.036). The T1N2 treatment had the highest mean chlorophyll-a concentration (61.25 μg L–1) (Table 1), followed by T2N2 (48.42 μg L–1). In T1N1, the mean chlorophyll-a concentration was 30.87 μg L–1, while that of T2N1 was the lowest (13.35 μg L–1).
The microcrustacean assemblage showed a total of 21 species (species list in Supplementary Material), comprising seven cladocerans and 14 copepods. The variation in species richness (Δ: final richness – initial richness) showed a marginally significant interaction (factorial ANOVA, F1, 12 = 3.505, p = 0.091, Fig. 2a), indicating that the nutrient concentration (a proxy of the resource availability) had different effects on the species richness at different transparency levels. In T1N2, under high transparency (higher predation intensity), the high concentration of nutrients presented a smaller difference in species richness than did the treatments with low nutrient concentrations (lower competition intensity). In contrast, in T2N2, under the lowest transparency (lower predation intensity), the lowest difference in species richness occurred at lower nutrient concentrations (greater competition intensity).
The variation in abundance among treatments showed a marginally significant interaction (factorial ANOVA, F1, 12 = 4.917, p = 0.057), indicating that nutrient concentrations had different effects on the abundance of individuals with low and high transparencies. The mean zooplankton abundance variation (difference in the abundance of individuals between beginning and end of the experiment) was more conspicuous in T2N1 (Fig. 2b), indicating that the population decreases with less chance of predation and a greater chance of competition. The T2N2 treatment presented a variation of 3.57–9.04 ind L–1, indicating that under a lower probability of predation and competition, populations tend to grow.
The mean body length of the microcrustacean assemblage differed between treatments (Fig. 3a) (factorial ANOVA, F = 7142, p = 0.028), with an increase in mean body length in T2N1 (lower intensity of predation and higher intensity of competition). The T1N1 treatment (greater intensity of predation and competition) presented a reduction in size, with a mean decrease of 224.26 μm in the mean body length of the assemblage at the end of the experiment (Fig. 3b). In both T2N1 and T2N2, the mean size decreased by approximately 53 μm at the end of the experiment (Fig. 3b). In contrast, in T1N2 (higher intensity of predation and lower competition), the mean body length increased by 102.18 μm at the end of the experiment. The smallest and largest sizes recorded in each treatment varied during the experiment (Fig. 3c, d). In T2N1, both the smallest and largest size decreased at the end of the experiment, with the smallest size ranging from 460 to 225 μm and the largest size ranging from 2210 to 1430 μm. In the treatments with the highest intensity of predation (T1N2 and T1N1) the largest size decreased at the end of the experiment, with decreases from 2280 to 1410 μm in T1N2 and from 2100 to 1620 μm in T1N1.
The relative abundance of the size classes differed significantly between the beginning and end of the experiment in the treatments T1N2 (χ2 = 41.407, df = 3, p < 0.001), T2N1 (χ2 = 18.305, df = 3, p < 0.001), and T2N2 (χ2 = 9.010, df = 3, p = 0.029) (Fig. 4b–d). In T1N2 individuals, sizes larger than 1000 μm increased in importance (+ 20.93%), while the proportion of the size range between 600 and 1000 μm decreased (− 33.31%). For individuals up to 300 μm and between 300 and 600 μm in size, the percentage increased (+ 5.53% and + 6.86%, respectively). In the T2N1 treatment, the relative abundances of the bands of sizes up to 300 μm, greater than 1000 μm, and between 300 and 600 μm increased (+ 12.80%, + 5.48%, and + 0.47%, respectively), while that of sizes between 600 and 1000 μm decreased (− 18.74%). In T2N2, the percentage of individuals between 600 and 1000 μm decreased (− 12.68%), while that of individuals greater than 1000 μm, between 300 and 600 μm, and up to 300 μm increased (+ 5.25%, + 3.90%, and + 3.53%, respectively). Treatment T1N1 (Fig. 4a) presented a marginally significant difference between the proportions of size classes (χ2 = 6.621, df = 3, p = 0.085).
Discussion
Our results showed that nutrient and transparency manipulation affected the species richness, abundance of individuals, and the zooplankton community size structure. Since the simulated treatments implied different scenarios of ecological interactions (facilitating or mitigating predation and facilitating or attenuating competition for food resources) and represented real situations, it is possible to suggest that oligotrophication affects the interactions of competition and predation in aquatic ecosystems.
The negative effect of nutrient-poor treatments on the species richness and abundance, as well as the positive effect of nutrient enrichment on the species richness, community abundance (Fig. 2b), and largest individuals in T2N2 (Fig. 3d), corroborated our prediction that larger individuals have competitive advantages and, when dominant, competitively suppress smaller herbivores. This response could be related to competitive interactions, since the reduction of resource availability (in T1N1 and T2N1) limited the proliferation of individuals, probably because of the competition for exploitation (Gause 1934; Lampert and Sommer 2007; Sommer et al. 2012). In contrast, the increase in the concentration of resources in T1N2 and T2N2 (high values of chlorophyll-a) favoured the abundance of individuals because of the weakening of the effects of the exploitative competition. The relationship between increased abundance and nutrient enrichment in productive systems is common in observational and experimental studies (Pinto-Coelho et al. 2005; Simões et al. 2015; de Melo et al. 2019). The high abundance of individuals observed in T2N2 at the end of the experiment was related to the scenario of lower predation and greater availability of resources, showing that the diminished transparency in the treatment attenuated predation pressure (Jeppesen et al. 2004; Hambright 2008) and potentiated the effect of resource availability.
Alternatively, some studies have shown that zooplankton abundance may increase with the intensification of predation pressure by fish, attributing this pattern to the mitigation of competitive exclusion through the control of dominant populations via predation (Hobæk et al. 2002) and through the positive effect of predation on nutrient cycling (Attayde and Hansson 2001; Dias et al. 2012). This relationship is in accordance with the increased abundance observed in T1N2, which presented a higher rate of predator–prey encounters because of the high transparency. The increased abundance in this treatment is also justified because the high availability of food can compensate for predation pressure, replacing losses through the recruitment of new individuals, since the availability of resources is a preponderant factor in egg production and the ontogenesis process (Bramm et al. 2009; Sommer et al. 2012). This result shows an important effect regarding the balance of forces between predation and competition that organises the structure of the communities (Semenchenko et al. 2007).
Interactions between predation and competition affected zooplankton sizes, especially under T1N1 treatment, where oligotrophic conditions caused a decrease in mean body size. High transparency improves the visual range of fish (Bramm et al. 2009), whose predation is selective and based on prey size (Brooks and Dodson 1965; Hall et al. 1976). In ponds with a high fish abundance, selective predation leads to a smaller size structure because large adult prey are more effectively captured, especially in the sexual maturity stage. Consequently, the recruitment of new individuals of larger species is impaired (Drenner et al. 2009). The relationship between size-selective predation and the decrease in the zooplankton size spectrum/diversity (Hansson et al. 2004; Jeppesen et al. 2004; Pinto-Coelho et al. 2005; Hambright 2008) and the effect of nutrients on the trophic structure of the community (Jeppesen et al. 2000; Semenchenko et al. 2007) are well documented in the literature.
Treatments with low resource availability (T1N1 and T2N1) did not show evidence of competitive exclusion, which is in accordance with SEH; the mean size (Fig. 3b) and greatest length (Fig. 3d) decreased at the end of the experiment. In addition, the availability of resources observed in T1N2 favoured the larger individuals (Fig. 4b), who, even undergoing predation, contributed to the increased mean size at the end of the experiment. As described for the T2N2 treatment, the decrease in the mean size in the T2N1 treatment could be a result of the decrease in the competitive efficiency of the larger herbivores due to the low transparency (Fig. 3b) or feeding interference of the suspended clay during the filtration and respiration processes (Rellstab and Spaak 2007). In this scenario, food scarcity must have constrained populations of large herbivores, sufficiently regulating them to avoid the competitive suppression of smaller crustaceans throughout the experiment. As it promotes the control of competition interactions, resource limitations favour size variability in the community (Hall et al. 1976; Quintana et al. 2015).
Because of the predation pressure and high availability of resources in the T1N2 treatment, it was expected that exploitative competition would decrease, and consequently, the size structure would shift to smaller individuals. Experimental studies have shown that zooplankton exposure to light enables individuals to overcome the predation effect due to higher resource availability compared to that in turbid environments, because light regimes quantitatively and qualitatively affect phytoplankton (Bramm et al. 2009). The improvement in food quality and availability promotes the recruitment of new individuals (Drenner et al. 2009). Therefore, the intense reproduction of large crustaceans allows them to explore and change their resource base to a wider variety, enhancing the competitive effect on smaller crustaceans (Vanni 1986; Straile and Geller 1998).
Our results showed that the variation in nutrient load may modify the effect of transparency on the crustacean assembly size structure. The effect of this interaction between the factors was evident when we compared the results of the T1N1 and T1N2 treatments: the predation pressure under greater transparency decreased the mean body size of the community (T1N1). However, when the nutrient concentration was high (T1N2), the availability of resources compensated for the loss of large individuals by selective predation and increased size structure. A larger zooplankton structure is also associated with high grazing pressure (Bonecker et al. 2011; Iglesias et al. 2011). However, when high predation pressure leads to a decrease in zooplankton biomass, grazing pressure also decreases, even if the size structure increases simultaneously (Wang et al. 2007). This explains the high concentration of chlorophyll-a in the T1N2 treatment, whose inverse relationship between mean body size and total zooplankton abundance can be attributed to the ability of some key species to avoid predation (Wang et al. 2007). The weakening of exploitative competition among larger individuals reduces the intensity of resource depletion, allowing intermediate-size populations to increase (Zhang et al. 2013). This suggests that predation by fish may have a negative effect on abundance but a positive effect on the size structure of zooplankton. By affecting large herbivores, predation attenuates the impact of certain size ranges on competitive relationships, releasing resources to the neighbouring size classes. Therefore, the success of the size classes adjacent to the group most affected by predation pressure accounts for the increase in the zooplankton size structure in the T1N2 treatment.
The first prediction (interaction between low nutrient levels and high transparency levels reduce the size structure) was partially confirmed because, in oligotrophic scenarios, the effects of predation and competition on size are not inverse, but are summed to favour smaller individuals, which decreases the size distribution of planktonic crustaceans; the SEH did not fully apply to oligotrophic conditions. The second prediction (low nutrient levels induce an increase in the size structure) was supported by the aggregate data of community structure and increase in mean body length in the T2N1 treatment. When resources were abundant (i.e., in the T2N2 treatment), the decrease in the size structure indicated that the enrichment of nutrients favoured smaller individuals. However, under higher pressure predation (T1N1), the decrease in the size structure at low nutrient levels counter-acted the competitive exclusion effect of the SEH. In the third prediction (high transparency levels diminish the community size structure), the effects of predation were corroborated in the treatments with low nutrient concentrations; under these conditions, the level of transparency regulated the size structure, and the increase in predation pressure decreased the size structure.
Thus, this study showed that oligotrophication affects the structure and size of the zooplankton community because of increased predation pressure and resource shortages. In real scenarios, when a chain of dams promotes the oligotrophication of downstream systems, it changes ecological interactions along the food chain, which will drive the decrease in the supply to secondary production and, consequently, fish stocks.
References
Agostinho A, Thomaz S, Gomes L (2004) Threats for biodiversity in the floodplain of the Upper Paraná River: effects of hydrological regulation by dams. Int J Ecohydrol Hydrobiol 4:255–268
Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726. https://doi.org/10.1007/BF02804901
Anderson JN, Jeppesen E, Sondergaard M (2005) Ecological effects of reduced nutrient loading (oligotrophication) on lakes: an introduction. Freshw Biol 50:1589–1593. https://doi.org/10.1111/j.1365-2427.2005.01433.x
Attayde JL, Hansson LA (2001) The relative importance of fish predation and excretion effects on planktonic communities. Limnol Oceanogr 46:1001–1012
Barnett AJ, Finlay K, Beisner BE (2007) Functional diversity of crustacean zooplankton communities: towards a trait-based classification. Freshw Biol 52:796–813. https://doi.org/10.1111/j.1365-2427.2007.01733.x
Bonecker C, Azevedo F, Simões N (2011) Zooplankton body-size structure and biomass in tropical floodplain lakes: relationship with planktivorous fishes. Acta Limnol Bras 23:217–228
Bonecker CC, Simões NR, Minte-Vera CV et al (2013) Temporal changes in zooplankton species diversity in response to environmental changes in an alluvial valley. Limnol Ecol Manag Inl Waters 43:114–121. https://doi.org/10.1016/j.limno.2012.07.007
Bottrell HH, Duncan GZ et al (1976) A review of some problems in zooplankton production studies. Nor J Zool 24:419–456
Bovo-Scomparin V, Train S, Rodrigues L (2013) Influence of reservoirs on phytoplankton dispersion and functional traits: a case study in the Upper Paraná River, Brazil. Hydrobiologia 702:115–127
Bramm ME, Lassen MK, Liboriussen L et al (2009) The role of light for fish-zooplankton-phytoplankton interactions during winter in shallow lakes - a climate change perspective. Freshw Biol 54:1093–1109. https://doi.org/10.1111/j.1365-2427.2008.02156.x
Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150(80):28–35
Brucet S, Boix D, Quintana XD et al (2010) Factors influencing zooplankton size structure at contrasting temperatures in coastal shallow lakes: implications for effects of climate change. Limnol Oceanogr 55:1697–1711. https://doi.org/10.4319/lo.2010.55.4.1697
Dias JD, Simões NR, Bonecker CC (2012) Zooplankton community resilience and aquatic environmental stability on aquaculture practices: a study using net cages. Braz J Biol 72:1–11
Drenner SM, Dodson SI, Drenner RW, Pinder JE III (2009) Crustacean zooplankton community structure in temporary and permanent grassland ponds. Hydrobiologia 632:225–233. https://doi.org/10.1007/s10750-009-9843-4
García-Comas C, Sastri AR, Ye L et al (2016) Prey size diversity hinders biomass trophic transfer and predator size diversity promotes it in Planktonic Communities. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2015.2129
Gause GF (1934) Experimental analysis of Vito Volterra’s mathematical theory of the struggle for existence. Science 79(80):16–17. https://doi.org/10.1126/science.79.2036.16-a
Golterman HL, Clymno RS, Ohnstad MAM (1978) Methods for physical and chemical analysis for fresh waters: IBP handbook no. 8. Blackwell Scientific Publications, Oxford
Hall DJ, Threlkeld ST, Burns CW, Crowley PH (1976) The size-efficiency hypothesis and the size structure of Zooplankton communities. Annu Rev Ecol Syst 7:177–208. https://doi.org/10.1146/annurev.es.07.110176.001141
Hambright KD (2008) Long-term zooplankton body size and species changes in a subtropical lake: implications for lake management. Arch für Hydrobiol 173:1–13. https://doi.org/10.1127/1863-9135/2008/0173-0001
Hansson LA, Gyllström M, Ståhl-Delbanco A, Svensson M (2004) Responses to fish predation and nutrients by plankton at different levels of taxonomic resolution. Freshw Biol 49:1538–1550. https://doi.org/10.1111/j.1365-2427.2004.01291.x
Hobæk A, Manca M, Andersen T (2002) Factors influencing species richness in lacustrine zooplankton. Acta Oecologica 23:155–163
Iglesias C, Mazzeo N, Meerhoff M et al (2011) High predation is of key importance for dominance of small-bodied zooplankton in warm shallow lakes: evidence from lakes, fish exclosures and surface sediments. Hydrobiologia 667:133–147. https://doi.org/10.1007/s10750-011-0645-0
Jeppesen E, Jensen JP, Sondergaard M et al (2000) Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshw Biol 45:201–218. https://doi.org/10.1046/j.1365-2427.2000.00675.x
Jeppesen E, Jensen JP, Bramm ME et al (2004) Impact of fish predation on cladoceran body weight distribution and zooplankton grazing in lakes during winter. Freshw Biol 49:432–447
Kindt R, Coe R (2005) Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. In: World Agroforestry Centre (ICRAF), Nairobi
Lampert W, Sommer U (2007) Limnoecology: the ecology of lakes and streams. Oxford University Press, Oxford
Lansac-Tôha FA, Bonecker CC, Velho LFM et al (2009) Biodiversity of zooplankton communities in the Upper Paraná River floodplain: interannual variation from long-term studies. Brazilian J Biol 69:539–549
Leira M, Cantonati M (2008) Effects of water-level fluctuations on lakes: an annotated bibliography. Hydrobiologia 2008:171–184
Moreira RA, Rocha O, dos Santos RM et al (2016) Composition, body-size structure and biomass of zooplankton in a high-elevation temporary pond (Minas Gerais, Brazil). Oecologia Aust 20:81–93. https://doi.org/10.4257/oeco.2016.2002.06
Ney JJ (1996) Oligotrophication and its discontents: effects of reduced nutrient loading on reservoir fisheries. Am Fish Soc Sim 16:285–295
Pinto-coelho R, Pinel-alloul B, Havens KE (2005) Crustacean zooplankton in lakes and reservoirs of temperate and tropical regions: variation with trophic status. Can J Fish Aquat Sci 361:348–361. https://doi.org/10.1139/F04-178
Quintana XD, Arim M, Badosa A et al (2015) Predation and competition effects on the size diversity of aquatic communities. Aquat Sci 77:45–57. https://doi.org/10.1007/s00027-014-0368-1
Quirino BA, Carniatto N, Gaiotto JV, Fugi R (2015) Seasonal variation in the use of food resources by small fishes inhabiting the littoral zone in a Neotropical floodplain lake. Aquat Ecol 49:431–440. https://doi.org/10.1007/s10452-015-9535-2
Rellstab C, Spaak P (2007) Starving with a full gut? Effect of suspended particles on the fitness of Daphnia hyalina. Hydrobiologia 2007:131–139
Roberto M, Santana N, Thomaz S (2009) Limnology in the Upper Paraná River floodplain: large-scale spatial and temporal patterns, and the influence of reservoirs. Braz J Biol 69:717–725
Rodrigues LC, Simões NR, Bovo-Scomparin VM et al (2015) Phytoplankton alpha diversity as an indicator of environmental changes in a neotropical floodplain. Ecol Indic 48:334–341. https://doi.org/10.1016/j.ecolind.2014.08.009
Semenchenko VP, Razlutskij VI, Feniova IY, Aibulatov DN (2007) Biotic relations affecting species structure in zooplankton communities. Hydrobiologia 579:219–231. https://doi.org/10.1007/s10750-006-0411-x
Simões NR, Lansac-Tôha FA, Velho LFM, Bonecker C (2012) Intra and inter-annual structure of zooplankton communities in floodplain lakes: a long-term ecological research study. Rev Biol Trop 60:1819–1836
Simões NR, Nunes AH, Dias JD et al (2015) Impact of reservoirs on zooplankton diversity and implications for the conservation of natural aquatic environments. Hydrobiologia 758:3–17. https://doi.org/10.1007/s10750-015-2260-y
Smith VH, Schindler DW (2009) Eutrophication science: where do we go from here? Trends Ecol. Evol 24:201–207
Smith VH, Tilman GD, Nekola JC (1998) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Poll 1998:179–196
Sommer U, Adrian R, De Senerpont DL et al (2012) Beyond the Plankton Ecology Group (PEG) model: mechanisms driving plankton succession. Annu Rev Ecol Evol Syst 43:429–448. https://doi.org/10.1146/annurev-ecolsys-110411-160251
Stemberger RS, Miller EK (2003) Cladoceran body length and Secchi disk transparency in northeastern U.S. lakes. Can J Fish Aquat Sci 60:1477–1486. https://doi.org/10.1139/f03-124
Stockner JG, Rydin E, Hyenstrand P (2000) Cultural oligotrophication: causes and consequences for fisheries resources. Fisheries 25:7–14. https://doi.org/10.1577/1548-8446(2000)025%3c0007:CO%3e2.0.CO;2
Straile D, Geller W (1998) Crustacean zooplankton in Lake Constance from 1920 to 1995: response to eutrophication and re-oligotrophication. Arch für Hydrobiol Spec Issues Adv Limnol 53:255–274
Tavşanoğlu ÜN, Šorf M, Stefanidis K et al (2017) Effects of nutrient and water level changes on the composition and size structure of zooplankton communities in shallow lakes under different climatic conditions: a pan-European mesocosm experiment. Aquat Ecol 51:257–273. https://doi.org/10.1007/s10452-017-9615-6
Team RC (2015) R: a language and environment for statistical computing
de Melo TX, Dias JD, Simões NR, Bonecker CC (2019) Effects of nutrient enrichment on primary and secondary productivity in a subtropical floodplain system: an experimental approach. Hydrobiologia 827(1):171–181
Vanni MJ (1986) Competition in zooplankton communities: suppression of small species by Daphnia pulex. Limnol Oceanogr 31:1039–1056. https://doi.org/10.4319/lo.1986.31.5.1039
Wang S, Ping X, Wu S, Haijun W (2007) Crustacean zooplankton size structure in aquaculture lakes: is larger size structure always associated with higher grazing pressure? Hydrobiologia 575:203–209. https://doi.org/10.1007/s10750-006-0394-7
Zhang J, Xie P, Tao M et al (2013) The impact of fish predation and cyanobacteria on zooplankton size structure in 96 subtropical lakes. PLoS ONE 8:e76378. https://doi.org/10.1371/journal.pone.0076378
Acknowledgements
We would like to thank Universidade Federal do Pará and Universidade Estadual de Maringá by logistic support. J.E.M. Braz was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). We thank the two anonymous reviewers who substantially contributed to the improvement of the manuscript, and C. Joko by zooplankton illustrations. In this project, J.D. Dias and C.C. Bonecker were supported by Conselho Nacional de Desenvolvimento a Pesquisa (CNPq) from Brazil.
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Braz, J.E.M., Dias, J.D., Bonecker, C.C. et al. Oligotrophication affects the size structure and potential ecological interactions of planktonic microcrustaceans. Aquat Sci 82, 59 (2020). https://doi.org/10.1007/s00027-020-00733-z
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DOI: https://doi.org/10.1007/s00027-020-00733-z