Breakage of cyanobacterial filaments by small- and large-sized Daphnia: are there any temperature-dependent differences?
Filamentous cyanobacteria disturb food collection in Daphnia by mechanical interference with the filtering apparatus by the long trichomes. The intensity of this interference depends on the water temperature and the Daphnia body size. However, Daphnia are capable of breaking down the filaments, therefore improving the palatability of the cyanobacteria. The main objective of this study was to test whether the shortening of cyanobacterial filaments and the ensuing clearance rate of Daphnia would increase at higher temperatures to a greater degree in small-bodied Daphnia species than in large-bodied one. Laboratory feeding experiments were conducted in order to measure variation in the length of Cylindrospermopsis raciborskii trichomes and to calculate clearance rate. The filament length and the cyanobacteria clearance rate by Daphnia were calculated following their exposure to grazing by large-bodied D.pulicaria and small-bodied D. longispina in 20, 24, and 28°C. Rising temperature did not affect the intensity of breakage of C. raciborskii trichomes by D. pulicaria and caused decrease in clearance rate of this species, whereas for D. longispina, the temperature increase enhanced both filament breakage and clearance rate. We suggest that these temperature-related changes may affect relative competitive performance of Daphnia species in the presence of cyanobacteria.
KeywordsDaphnia Cyanobacteria Filament length Zooplankton Body size Temperature
Cyanobacteria are known to be an inadequate source of food for Daphnia for a variety of reasons, including low nutritional value and a lack of essential compounds (especially polyunsaturated fatty acids and sterols). They are also difficult for Daphnia to consume due to their size and shape (Porter & Orcutt, 1980; Lampert, 1987; von Elert & Wolffrom, 2001). Moreover, some cyanobacterial species or strains produce toxins (Leflaive & Ten-Hage, 2007). Cyanobacterial filaments and colonies can interfere with the food collection of daphnids by clogging their filtering apparatus, thus limiting Daphnia feeding efficiency. When cyanobacterial filaments are abundant, daphnids increase the frequency of rejection movements by their postabdominal claws (Gliwicz & Siedlar, 1980; Kirk & Gilbert, 1992). As a result, the presence of cyanobacterial filaments leads to higher rates of respiration as well as reduced rates of feeding and assimilation and may also cause egg abortion (Porter & McDonough, 1984; Hawkins & Lampert, 1989; DeBernardi & Giussani, 1990; Gilbert & Durand, 1990; Bednarska & Slusarczyk, 2013). Nevertheless, Daphnia, like other zooplankton taxa such as copepods and rotifers, are able to break down cyanobacterial filaments into small particles, thereby improving their palatability (Dawidowicz, 1990; Bouvy et al., 2001; Gulati et al., 2001). It has been shown that short non-toxic cyanobacterial filaments cause lower reduction in the growth rate and fecundity of Daphnia in comparison with longer ones (Bednarska et al., 2014). Cyanobacterial filaments could, therefore, serve as a supplementary food for zooplankton herbivores, especially under food-limiting conditions (DeBernardi & Giussani, 1990; Gilbert & Durand, 1990).
Both water temperature and cladoceran body size may affect the interference with cyanobacterial filaments. At higher temperatures, decreased water viscosity increases the flow through the filter screens, which in turn leads to more intensive mechanical interference by cyanobacteria filaments with Daphnia filtering combs (Abrusán, 2004). Small-bodied cladocerans are known to be more resistant to such interference than large-sized species, because they have a relatively narrow gap in their carapace, which prevents filaments from entering the filtration chamber (Gliwicz & Siedlar, 1980; Porter & McDonough, 1984; Panosso & Lürling, 2010). It has also been suggested that the food-gathering process is qualitatively different between Daphnia species which differ in body size, due to variation in the hydrodynamics of water flow through the filtering apparatus. Due to the lower values of the Reynolds number, the filtering combs of small-bodied species act more as paddles than sieves, which reduces clogging of the filters (Abrusán, 2004).
Additionally, in tropical and subtropical waters, high temperatures and selective grazing on other algae by some zooplankton taxa, e.g., copepods, promote cyanobacterial blooms (Hong et al., 2013), which results in small grazers (small-bodied cladocerans, copepods and rotifers) predominating in zooplankton communities; large cladocerans rarely occur there (Gillooly & Dodson, 2000). Furthermore, in temperate lakes during the summer, when there is a relatively high abundance of cyanobacteria, small-bodied species dominate large-bodied ones, a phenomenon known as “midsummer decline” (Sommer et al., 1986; Müller-Navarra et al., 2000; Wagner et al., 2004).
We suggest that temperature-driven variations in cyanobacterial filament breakage and clearance rate may affect the competitive abilities of Daphnia species which differ in body size. An evaluation of the shortening of cyanobacterial filaments and the clearance rate was made by measuring the filament lengths of a non-toxic strain of Cylindrospermopsis raciborskii, which were exposed to grazing by two Daphnia species differing in body size, under various thermal conditions. The objective of the study was to test the hypothesis that shortening of cyanobacterial filaments, and the clearance rate would increase with rising temperature, due to increase the flow through the filter screens, for small-bodied Daphnia, but stay on the same level (or increase less) for large-bodied species that are more vulnerable to interference by cyanobacteria filaments.
Materials and methods
Origin and body size (mm) of 4-day-old experimental Daphnia clones
Body size (mm)
Lake Roś, Poland
Lake Roś, Poland
Lake Roś, Poland
Unknown Lake, Czech Republic
Lake Brome, Canada
Lake Brome, Canada
We used an analysis of variance (ANOVA) test followed by the Tukey-HSD test for multiple comparisons to investigate the effects of temperature and species on the differences in clearance rate and mean length of the filaments. The factor ‘clone’ was nested within the species. Prior to the analysis, data for filament length and clearance rate were log-transformed. We used the Kolmogorov–Smirnov two-sample test to check if the mean filament lengths of the samples had a divergent distribution. The mean filament lengths used in the analyses were divided into size class intervals of 30 μm. Both analyses were performed using Statistix 9.0 software.
Mean length (μm) of cyanobacterial filaments Cylindrospermopsis raciborskii in three thermal regimes: 20, 24, and 28°C
Results of the Kolmogorov–Smirnov two-sample test comparing distribution of cyanobacterial filaments (Cylindrospermopsis raciborskii) length in treatment with large-bodied D. pulicaria and small-bodied D. longispina to the control treatment without any animals in three thermal regimes: 20, 24, and 28°C
D. longispina vs control
D. pulicaria vs control
D. longispina vs control
D. pulicaria vs control
D. longispina vs Control
D. pulicaria vs Control
Shortening of the cyanobacteria filaments varied significantly among the clones within both of the Daphnia species (species * clone interaction; ANOVA, F = 3.80, P = 0.0097). Variation in the mean length of the cyanobacterial filaments, however, was observed only among the D. longispina clones (only clone Dl6 differed significantly from clone Dl4; clone DlE did not differed significantly from both of them), whereas D. pulicaria clones did not differ significantly.
Both studied Daphnia species investigated in the study broke up filaments of the cyanobacterium C. raciborskii, but with different intensities dependent on temperature. At 20°C, the effect of small-bodied D. longispina on mean cyanobacteria filament length was negligible, while D. pulicaria shortened the filaments significantly. Breakage of the cyanobacterial filaments remained unchanged for the large-bodied D. pulicaria across the range of temperatures tested, whereas for the small-bodied D. longispina, it increased. Similarly, as the temperature increased, the clearance rate for D. pulicaria decreased, whereas for D. longispina, the clearance rate increased. Consequently, the difference between the two species tended to decrease with exposure to increasing water temperature. At 28°C, the reduction in cyanobacterial filament length was nearly identical for both Daphnia species, but the clearance rate for cyanobacteria was still 2.5 times higher for D. pulicaria. We have observed only little variation among clones of both Daphnia species. Although D. pulicaria clones come from two genetically divergent clades (Colbourne et al., 1998), we have not found statistically significant differences in shortening of cyanobacteria filaments as well as clearance rate.
The observed decreases in the mean lengths of cyanobacterial filaments could have contributed to the increase in ingestion rate of filaments by Daphnia, which generally prefer smaller-sized food particles within the range of 2–50 μm (Geller & Müller, 1981; Sommer, 1988). A propensity to consume cyanobacterial filaments has been previously reported for a number of Daphnia species (Dawidowicz, 1990; Gilbert & Durand, 1990; Kurmayer, 2001; Reichwaldt & Abrusán, 2007). As demonstrated experimentally, another large-bodied Daphnia species, D. magna, was able to control the population growth of filamentous cyanobacteria (at a temperature of 20°C) as long as the density of the cyanobacteria remained low (Dawidowicz et al., 1988). Breakage of cyanobacterial trichomes was suggested as an important mechanism allowing Daphnia to maintain such population control (Dawidowicz, 1990). If we can generalize about our observations of D. pulicaria, one could expect a relative decrease in the efficiency of filamentous cyanobacteria breakage by large-bodied daphnids at elevated temperatures. In addition, it has been found that cyanobacterial filaments of Aphanizomenon gracile decrease in length in the presence of Daphnia infochemicals (Cerbin et al., 2013). Considering that cyanobacteria population growth increases with rising temperatures, and that some of the morphological characteristics of cyanobacterial trichomes change with increasing temperature (e.g., trichomes were shorter and wider; Soares et al., 2013), these changes would not be followed by an increase in filament processing and utilization by large-bodied Daphnia. The lack of positive effect of temperature on filament shortening and the decreasing cyanobacteria clearance rate by D. pulicaria could be explained by the susceptibility of this large-bodied species to mechanical interference.
On the other hand, filament breakage increased in the smaller D. longispina with increasing temperature, along with an increase in clearance rate for the cyanobacteria. Such an adaptation may allow D. longispina to graze on filaments more efficiently as the water warms up. Consequently, the relative performance of the small-bodied Daphnia species may increase, which would mitigate, but not reverse, the competitive superiority of the larger D. pulicaria. It has been suggested that the mere presence of cyanobacteria cannot reverse the competitive advantage of the larger-bodied species over the smaller-bodied ones (Kurmayer, 2001), even at higher temperatures (Sikora & Dawidowicz, 2014). Yet it is probable that the superior utilization of cyanobacterial filaments by small-bodied zooplankton compared to their larger-bodied congeners (Gulati et al., 2001) contributes, along with other factors, not tested in the experiment: e.g., toxicity of cyanobacteria (Jiang et al., 2014a, b) or fish predation (Havens et al., 2015), to the dominance of small-bodied species in tropical and subtropical lakes and in temperate lakes during the “midsummer decline.” Such investigation of the interactions between Daphnia and cyanobacteria should be factored into the prediction of the potential effects of climate change on temperate lakes.
The results of our study show that small-sized Daphnia increase the intensity of filament’ breakage and the clearance rate for cyanobacteria with rising water temperature more than in the large-bodied species. Better utilization of cyanobacterial filaments with increasing temperature by small-bodied zooplankton could be, together with other factors, responsible for the observed dominance of small-bodied cladoceran species in warm-water lakes, where cyanobacteria are frequently the major food source for filter-feeding zooplankton.
We are grateful to Paweł Koperski for his great help and for the valuable comments he made on the manuscript, and also to Tomasz Karasek and Jacek Radzikowski for their assistance in the laboratory. We would like to thank Adam Petrusek, as well as two anonymous referees for the comments and suggestions on earlier versions of the manuscript. Financial support by grant N N305 134440 was from the Polish Ministry of Science and Higher Education to Piotr Dawidowicz.
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