Food spectrum of Branchinecta orientalis—are anostracans omnivorous top consumers of plankton in temporary waters?

Food spectrum of Branchinecta orientalis—are anostracans omnivorous top consumers of plankton... Abstract Anostracans are key elements of temporary ponds, due to the high abundance and importance as food for waterbirds. Except for a few large species, they are generally considered to be herbivorous filter feeders. However, this assumption is not supported by empirical data. In fact, there is a lack of quantitative experimental studies on their trophic role in the food webs of temporary waters. Here, we briefly revise the available data about the feeding spectrum of anostracans. Moreover, we present experimental data on the feeding behaviour of a key species of soda pans, Branchinecta orientalis. We show that B. orientalis is able to ingest a wide range of prey items, ranging from pico-sized algae, to motile prey such as copepods, with no significant differences in the ingested biomass from the different food types. We do not find evidence for sex and size-specific differences in the ingestion rates in adult animals. Our results clearly show that B. orientalis is an omnivorous planktivore. Based on our data and existing studies, we suggest refuting the general theorem that most anostracans are herbivorous filter feeders. More empirical data from the field are needed to fully appreciate the trophic role of these key consumers of temporary waters. INTRODUCTION Temporary ponds comprise very diverse ecosystems regarding size, shape, hydroperiod and water chemistry (Williams, 2006). They are widespread throughout the world, but are especially prevalent in arid and semi-arid climatic regions (Brendonck, 1996). Although the number of studies increased in the last decade, temporary ponds and their communities are still largely understudied compared to larger and more permanent water bodies (Céréghino et al., 2008; Céréghino et al., 2014; Marrone et al., 2017). Our knowledge about their food webs is particularly limited (Boix et al., 2016). Anostracans are a group of branchiopod crustaceans present almost exclusively in fishless temporary waters. In temporary ponds, anostracans (as well as the other large branchiopod crustaceans) are key elements, reaching high densities (Horváth et al., 2013a) and possibly having a strong impact on zooplankton communities through competition (Jocque et al., 2010). Moreover, anostracans are important food for waterbirds along their migration routes (Malone, 1965; Silveira, 1998; Boros et al., 2006; Sanchez et al., 2007; Horváth et al., 2013a) and during breeding seasons (Krapu, 1974). The general biology and feeding ecology of anostracans are not well understood (Marrone et al., 2017). Our knowledge on the diet of anostracans is mostly derived from anecdotal observations or correlative studies. There is a particular lack of quantitative data from controlled experiments. At present, anostracans are generally considered to be non-selective filter feeders (Brendonck, 1993). Filter-feeding organisms such as zooplankters have an important role in ecosystem functioning, since they are a key link from phytoplankton and bacteria to vertebrates (Persson et al., 2007) and drive trophic cascades (Carpenter et al., 1985). The majority of anostracans are predominantly considered herbivorous, feeding on algae in addition to organic and inorganic detritus which they filter from the water column or by mixing and scraping the bottom sediment. However, recent evidence suggests that they occasionally ingest nematodes and small zooplankters such as rotifers (see Table I). Only a few larger species were well documented to be predominantly predators, feeding on larger crustaceans such as copepods and other anostracans (White et al., 1969; Rogers et al., 2006; Rogers and Timms, 2017). Table I: Literature review about the diet composition and suggested feeding mode of anostracan species Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) Table I: Literature review about the diet composition and suggested feeding mode of anostracan species Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) According to two studies performed with large anostracan species (Branchinecta gigas and B. ferox), anostracan nauplii feed on small organic particles and algae (Daborn, 1975; Fryer, 1983). As they grow, their diet presumably broadens towards larger particles. For small anostracan species (<4 cm in length), there is only scattered information on the diet of adults. These data were collected with diverse field and laboratory methods and in many cases without any standardized experimental test (Table I). According to the very few existing examples, ingestion rates are increasing with the size of adults within a given species (Daborn, 1975; Dumont and Ali, 2004). In large predatorial anostracan species (e.g. Branchinecta ferox and B. raptor), the morphology of thoracopods implies that they gradually lose the ability of filter feeding with growth, probably once they reach 4–5 cm in length (Fryer, 1983; Rogers et al., 2006). Moreover, these large anostracan species are considered of being able to actively capture motile animal prey (White et al., 1969; Fryer, 1983; Rogers et al., 2006). Taken together, with the exception of large predatory taxa, we currently lack a good understanding about the diet of anostracans in their environment, which would be needed to assess their trophic role in the food web of temporary waters. Based on the existing data, size and feeding characteristics seem to lack a general pattern between different sexes of the same anostracan species. While differences in size were observed for some species (e.g. larger females in B. gigas; Daborn, 1975; larger males in Streptocephalus proboscideus; Brendonck, 1989), both sexes reach approximately the same size in others (Belk and Rogers, 2002; Miličić et al., 2013; Horváth and Vad, 2015). Among the few studies that tested for sex-related differences in ingestion rates, Bernice (1971) found no differences in Streptocephalis dichotomus, while in some other Streptocephalus species, females ingested more food than males (Dierckens et al., 1995; Ali et al., 1996), probably due to the high energetic demand of egg production (Ali et al., 1996). The genus Branchinecta occurs on all continents except Australia (Obregón-Barboza et al., 2002). It includes diverse species regarding body size and life history. Most species are smaller sized (up to 3 cm in length) and generally believed to be filter feeders and scrapers (Daborn, 1977; Paggi, 1996). This genus also contains the largest (predatory) anostracan species, such as B. gigas and B. raptor, that can grow up to 10 cm in body length (Daborn, 1975; Rogers et al., 2006). The target species of our study, Branchinecta orientalis, inhabits mineral-rich temporary waters and is distributed between 55° and 30° N in Europe and Asia (Mura and Takami, 2000). In Central European populations, adult B. orientalis usually range from 1.5 to 3 cm (pers. obs.), but can grow up to 4.1 cm (Petkovski, 1991). This makes them comparable to other Branchinecta species that are generally considered filter feeders, while predatory Branchinecta have a larger adult size range of 5–10 cm. Branchinecta orientalis is the most abundant anostracan species in Central European saline temporary waters, soda pans (Horváth et al., 2013b). Soda pan communities lack fish and macrovegetation (except in some cases around the shoreline). Picoplanktonic algae are the key primary producers in these naturally hypertrophic systems (Vörös et al., 2005, 2008; Somogyi et al., 2009). Both phyto- and zooplankton communities can reach very high densities during the wet phase (Horváth et al., 2014). Branchinecta orientalis reaches densities up to 13 ind L−1, which makes it an important food source for waterbirds (Horváth et al., 2013a). In spite of its ecological importance and high biomass, we are at present unaware about the diet of B. orientalis and its potential effects on the food web of soda pans. We experimentally test here the adult diet of the anostracan species B. orientalis (of comparable body size to many anostracan species considered as filter feeders). By using this species as model organism for anostracan feeding, our aims are to (1) examine their diet and compare the ingestion rates on different food types, ranging from pico-sized algae to large crustacean zooplankton; and (2) to determine whether ingestion rates depend on sex or body size. METHODS Cultivation of B. orientalis and plankton for feeding experiments All eggs and animals used in the experiments were collected in the Seewinkel region of Austria. To hatch animals, sediment containing resting eggs was collected from the soda pan Oberer Stinkersee (47.813722 N, 16.792889 E) and stored dry at 4°C in the dark for several months. After sieving and centrifuging the sediment by using the sugar flotation method (Onbe, 1978; Marcus, 1990), we incubated the eggs for hatching in a climate chamber, with a light regime 16:8 L:D and temperature of 18°C. Once animals started to hatch, we picked them out manually and transferred to larger plastic containers (25–35 adult animals in 21 L volume) filled with artificial soda water (NaHCO3 solved in distilled water, with conductivity of 1 mS cm−1) and constantly aerated. They were fed daily with a mix of algal food (Cryptomonas sp., Scenedesmus sp., Chlamydomonas sp.), which was at a later stage combined with zooplankton (rotifer Brachionus asplanchnoidis, cladoceran Moina brachiata, copepod Arctodiaptomus spinosus). Algal cultures were raised on WC medium, which was refreshed regularly (to keep them in exponential growth phase). Zooplankton was kept in 3 L volume jars in a medium of the same chemical composition as the anostracan medium, and fed regularly with a mix of algal food (Cryptomonas sp. and Chlamydomonas sp.). All phyto- and zooplankton cultures were kept under the same light regime and temperature conditions as anostracans. For testing the size dependency of ingestion rates, live anostracans were collected from Mittlerer Stinkersee (47.807044 N, 16.788180 E). These animals were used as a larger size class in our experiment, because the anostracans raised in the lab did not reach the maximum body size of the individuals from the field. They were kept and maintained in the same manner as the population hatched in the climate chamber, and used in feeding experiments only several days after collection from the field. Experimental design and data analyses Experiments were carried out with adult individuals. Animals were considered adult once mating was observed (around 4-week-old in case of animals hatched in the lab). At the onset of an experiment, body length of 10 individuals from all groups involved was measured (males, females, small and big animals). Body length was measured from the tip of the head to the end of cercopods (by means of photographs taken of live animals placed in a narrow transparent tube above grid lined paper). In our experiments, we incubated two female B. orientalis per replicate (except when we tested for sex differences, where we used two females vs. two males). For medium, we used 70 mL of artificial soda water at a conductivity of 1 mS cm−1 (same as in the cultures). The number of replicates in algal feeding tests (three) was usually lower than in the predatory tests (four to five), as we noticed an overall low variation between replicates in case of algal food. Controls (without B. orientalis) for all food types were run in parallel. To avoid algal sedimentation, medium was gently mixed in the algal feeding tests (both controls and vials with B. orientalis) with regular intervals (30 min) and immediately before sampling phytoplankton for quantification. To quantify filter feeding on phytoplankton, we offered two algae with different sizes as food in separate experiments (in concentrations equal to 2.5 mg L−1 dry weight, 5× higher than the concentration considered as saturating food abundance for Daphnia magna; Porter et al., 1982). A coccoid green algae Mychonastes sp. (Sphaeropleales; diameter 2–3 μm) was used as picoplankton (mean concentration 384 400 cells mL−1), and the green flagellate Chlamydomonas sp. (Chlamydomonadales) represented a larger unicellular food (7–18 μm length; mean concentration 33 600 cells mL−1). In the predatory feeding test, two zooplankters representative for soda pan communities were used (Horváth et al., 2014; Tóth et al., 2014): a copepod (Arctodiaptomus spinosus, 20 per vial, 3.8 mg L−1 dry weight) and a rotifer (Brachionus asplanchnoidis, 450 per vial, 3.2 mg L−1 dry weight). The length of adult A. spinosus is 0.65–1.16 mm (Bottrell et al., 1976), while it is between 0.185 and 0.510 mm for B. asplanchnoidis (Michaloudi et al., 2017). They were collected from soda pans in the Seewinkel region, and cultivated in the lab during the experiments. We offered a comparable biomass to B. orientalis in all tested food types (2.5–3.8 mg dry weight biomass L−1). Experiments were run for 40 min for B. asplanchnoidis, 1 hour for A. spinosus, 2 hours for Chlamydomonas sp. and 4 hours for Mychonastes sp. The length of experiments was decided for each food type based on ingestion rates observed in pre-experimental trials, where we counted the remaining algal cells or zooplankton individuals at multiple time points, until the effect of anostracan feeding became evident. For comparing differences between sex and size groups, experiments were set the same way as already described, with only a few minor differences in density and variety of food types tested. We used Chlamydomonas sp. (concentration 2.5 mg L−1 dry weight) as food in the filter feeding and B. asplanchnoidis (100 per vial) in the predatory feeding test to compare ingestion rates between males and females. To compare different adult size groups, we used Mychonastes sp. (concentration 2.5 mg L−1 dry weight) and Chlamydomonas sp. (concentration 7.5 mg L−1 dry weight) in filter feeding and A. spinosus (20 per vial, 3.8 mg L−1 dry weight) in predatory feeding tests. In an additional test, we offered two species of cladocerans to B. orientalis, M. brachiata (40 per vial) and D. magna (20 per vial, separately tested on two different age classes). These cladocerans are frequent members of zooplankton communities in soda pans and, therefore, it is relevant to check if they also represent a prey of B. orientalis. Besides, adults of D. magna are the largest representatives of crustacean zooplankton in these habitats and offering them as food allows for conclusions on the dietary size-spectrum of B. orientalis. Here, we only recorded whether these species were consumed by B. orientalis, without comparing ingestion rates with other food types. Body length of a cladoceran M. brachiata is around 1 mm, while D. magna ranges between 1 and 2 mm as juvenile and 2–5 mm as adult (pers. obs.). Per replicate, we offered cladocerans to two female anostracans for 20 min in 70 mL volume of medium (prepared the same way as explained above). Calculation of biomass and ingestion rates Biovolume of the algal food was approximated by measuring cellular dimensions and approximating them to simple geometrical bodies (sphere for Mychonastes sp. and depressed ellipsoid for Chlamydomonas sp.). Furthermore, we calculated the dry weight biomass per cell using the approximation that carbon biomass (~14% of biovolume) comprises 40% of total dry weight (Bowie et al., 1985). In zooplankton, B. asplanchnoidis and A. spinosus biomass per individual were calculated from the average weight of dried individuals (0.5 μg per individual for B. asplanchnoidis and 13.5 μg per individual for A. spinosus). Biomass ingestion rate per anostracan in the experiments was calculated based on the equations from Marin et al. (1986), with assumption that food concentration at the beginning of the experiment was below saturating concentration: M=gC0VmN with M being the ingested biomass per animal and time (in μg h−1); g is the grazing coefficient; C0 is the prey concentration (phytoplankton: cells/mL; zooplankton: individuals/mL) offered at the beginning of the experiment; V is the volume of medium (in mL); m is the average biomass (in μg) per phytoplankton cell or zooplankton individual; N is the number of anostracans per vial. The grazing coefficient (g) was calculated for all food types according to the following formula: g=k−ln(Ct)−ln(C0)t where C0 is the cell concentration of phytoplankton or concentration of zooplankton per unit volume offered as food at the beginning of experiment; Ct is the cell concentration of phytoplankton or concentration of zooplankton offered as food at the end of experiment, k is the growth rate based on the change of algal concentration in controls (applicable for phytoplankton); t is the duration of the experiment (expressed in hours). Statistical analyses One-way ANOVA was used to test for differences in biomass ingestion rates of the two algal and zooplankton groups in B. orientalis (normality and homogeneity of variances were met according to Shapiro–Wilk and Levene’s tests). Tukey’s post hoc test was applied to identify significant differences among different food types. In parallel with testing the differences in ingestion rates between males and females, we also tested for size difference in relation to sex. We first tested if the data on B. orientalis body length and ingestion rates for different food items follow a normal distribution with Shapiro–Wilk tests (separately for males and females). Length data were not normally distributed, so we applied Kruskal–Wallis rank sum test to test for differences in length between males and females. Afterwards, we checked whether there were any sex-related differences in ingestion rates. In the experiments with B. asplanchnoidis, we excluded one replicate in both the male and female treatments, where all rotifers were eaten before the end of the experiment. As data were normally distributed (ingestion rates on Chlamydomonas sp. and B. asplanchnoidis) and the assumption of homogeneity of variances was not violated (based on F test), we applied Student’s t-test to test for significant differences. The same procedure was applied to test length and feeding differences between two size classes of adult animals (mean ± SD: small: 1.44 ± 0.13 cm; big: 2.46 ± 0.22 cm). We checked for normality and homogeneity of variances before performing each test. The length differences between the two size classes were checked with Student’s t-test. Then, ingestion rates for feeding on Mychonastes sp., Chlamydomonas sp. and A. spinosus were compared between the two size classes. We used Kruskal–Wallis rank sum test for Mychonastes sp. and A. spinosus and Student’s t-test for Chlamydomonas sp. All data were analysed in R (R Core Team, 2014). RESULTS Anostracan diet width and ingestion rates Anostracans ingested all food types (small and large algae, rotifers and copepods) (Fig. 1a). Biomass ingestion rates on the picoalgae Mychonastes sp. (mean ± SD: 10.38 ± 7.26 μg h−1 or 20.8 ± 14.5 × 105 cells per hour), the larger algae Chlamydomonas sp. (30.55 ± 14.35 μg h−1; or 49.8 ± 23.4 × 104 cells per hour), the rotifer B. asplanchnoidis (123.37 ± 55.77 μg h−1; or 246.73 ± 111.55 individuals per hour) and the copepod A. spinosus (101.50 ± 123.68 μg h−1; or 7.54 ± 9.18 individuals per hour) were not significantly different from each other (ANOVA: F(3,11) = 1.62, P = 0.24; Fig. 1b). However, once an outlier from the A. spinosus treatment was removed (ingestion rate was above 300 μg h−1, while all others were ≤200 μg h−1; see Fig. 1b) we found significant difference between food types (ANOVA: F(3,10) = 5.3, P = 0.02), where ingestion rates on B. asplanchnoidis were significantly higher than those observed on Mychonastes sp. (Tukey’s post hoc test: P = 0.02). Fig. 1. View largeDownload slide (a) Colouration of B. orientalis intestine after feeding them first with sole algal (Chlamydomonas sp.) and then zooplankton (Arctodiaptomus spinosus) food. (b) Biomass ingestion rates on different food types. ANOVA showed no significant difference (n.s.) between the four groups (F(3,11) = 1.62, P = 0.24). When an outlier for the A. spinosus feeding test result was removed (ingestion rate above 300 μg h−1), ANOVA showed significant variance between the groups (F(3,10) = 5.30, P = 0.02), with significant difference between Mychonastes sp. and B. asplanchnoidis (Tukey’s post hoc test: P = 0.02). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Fig. 1. View largeDownload slide (a) Colouration of B. orientalis intestine after feeding them first with sole algal (Chlamydomonas sp.) and then zooplankton (Arctodiaptomus spinosus) food. (b) Biomass ingestion rates on different food types. ANOVA showed no significant difference (n.s.) between the four groups (F(3,11) = 1.62, P = 0.24). When an outlier for the A. spinosus feeding test result was removed (ingestion rate above 300 μg h−1), ANOVA showed significant variance between the groups (F(3,10) = 5.30, P = 0.02), with significant difference between Mychonastes sp. and B. asplanchnoidis (Tukey’s post hoc test: P = 0.02). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. The two cladocerans M. brachiata and juvenile Daphnia magna were both efficiently ingested by B. orientalis (they were all removed within 20 min). However, fairy shrimps were not feeding on adult D. magna (~5 days and older, which meant >1.5 mm in body length), which represented the only food type that was not ingested. Sex differences There was no significant difference in body length between males and females (mean ± SD: 1.41 ± 0.13 cm for males and 1.44 ± 0.13 cm for females; Kruskal–Wallis rank sum test: χ2 = 0.40, P = 0.525). Differences in food ingestion rates were also not significant, neither in case of filter feeding on Chlamydomonas sp. (males: 12.95 ± 8.70 μg h−1, females: 15.88 ± 8.50 μg h−1; t-test: t = 0.54, P = 0.60) nor in predatory feeding on B. asplanchnoidis (males: 95.20 ± 54.33 μg h−1, females: 92.32 ± 38.44 μg h−1; t-test: t = −0.20, P = 0.85) (Fig. 2). Fig. 2. View largeDownload slide Comparison of biomass ingestion rates between males and females on (a) algal food Chlamydomonas sp. (t-test, t = 0.54, P = 0.60); and (b) zooplankton Brachionus asplanchnoidis (t-test, t = −0.20, P = 0.85). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Fig. 2. View largeDownload slide Comparison of biomass ingestion rates between males and females on (a) algal food Chlamydomonas sp. (t-test, t = 0.54, P = 0.60); and (b) zooplankton Brachionus asplanchnoidis (t-test, t = −0.20, P = 0.85). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Size differences Adults raised in the lab from eggs were significantly smaller (mean ± SD: 1.44 ± 0.13 cm) than the adult animals collected on the field (mean ± SD: 2.46 ± 0.22 cm; t-test: t = 12.839, P < 0.001). However, we did not observe any significant difference in biomass ingestion rates, neither for filter feeding on Mychonastes sp. (small: 10.38 ± 7.26 μg h−1, big: 21.12 ± 8.22 μg h−1; Kruskal–Wallis rank sum test: χ2 = 2.33, P = 0.13) and Chlamydomonas sp. (small: 63.63 ± 11.38 μg h−1, big: 126.47 ± 61.84 μg h−1; t-test: t = 1.73, P = 0.22), nor for predatorial feeding on A. spinosus (small: 101.50 ± 123.68 μg h−1, big: 57.25 ± 49.64 μg h−1; Kruskal–Wallis rank sum test: χ2 = 0.06, P = 0.80) (Fig. 3). Fig. 3. View largeDownload slide Comparison of biomass ingestion rates in two size groups of adult animals on (a) picoplanktonic algae Mychonastes sp. (Kruskal–Wallis rank sum test: χ2 = 2.33, P = 0.13); (b) algae Chlamydomonas sp. (t-test: t = 1.73, P = 0.22); and (c) zooplankton Arctodiaptomus spinosus (Kruskal–Wallis rank sum test: χ2 = 0.06, P = 0.80). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Fig. 3. View largeDownload slide Comparison of biomass ingestion rates in two size groups of adult animals on (a) picoplanktonic algae Mychonastes sp. (Kruskal–Wallis rank sum test: χ2 = 2.33, P = 0.13); (b) algae Chlamydomonas sp. (t-test: t = 1.73, P = 0.22); and (c) zooplankton Arctodiaptomus spinosus (Kruskal–Wallis rank sum test: χ2 = 0.06, P = 0.80). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. DISCUSSION In our feeding experiments, B. orientalis was capable of capturing and ingesting a high variety of food types, differing both in size and in trophic level (phyto- and zooplankton). The results thus clearly show that B. orientalis is an omnivorous predator. Adult D. magna was the only food item B. orientalis was not able to ingest. As B. orientalis effectively preyed on juvenile D. magna, this indicates an upper prey size limit. It appears that anostracans in our experiments consumed slightly more zooplankton than phytoplankton biomass when offered in comparable amounts (Fig. 1B). It was more expressed in the rotifer B. asplanchnoidis, probably due to limited motility of this species, which makes it an easy prey for anostracans compared to the motile copepod. However, the estimated feeding rates on algae should be seen as conservative estimates, as food concentrations were below saturating levels (see Supplement 1). Although Petkovski (1991) noted that females were generally larger than males in B. orientalis, we did not find significant sex-specific size differences. Moreover, we did not find significant differences in the ingestion rates between males and females, in spite of the fact that females were producing eggs at the time of the experiment. Daborn (1975) noted for B. gigas that assimilation rates in males were lower than in females, while motion of extremities (and consequently filtration rates) were slightly higher than in females suggesting that this way males ingest more food and compensate for lower assimilation efficiency. Bernice (1971) found no difference in ingestion rates between males and females of Streptocephalus dichotomus, species of comparable size to B. orientalis. Males probably spend more energy in swimming by searching for females, while females use energy mostly for egg production, which would explain similar food consumption (Daborn, 1975). Food ingestion rates between the two studied size classes of adult anostracans showed no significant difference in any of the tested food types. It suggests that once adult and capable of predation, the filtering ability of B. orientalis does not change considerably with growth. It is possible that in long-term experiments, the effect of body size on feeding rates would be easier to observe, due to higher metabolic demands (Daborn, 1975). In our experiments, we tested ingestion rates in short-term experiments (2–4 hours). From this, we could conclude that there is no change in the ability of filter feeding with growth. Size-dependent decrease in ingestion rates on phytoplankton was not observed in our experiments, not even with Mychonastes sp. as smaller sized algal food. On the contrary, ingestion rates for both algae types were slightly higher in animals of larger body size. Considering that there was no significant difference between feeding on algae (true filter feeding) and on copepods (motile animals, which could be regarded as some form of an active predation mode of feeding), our results show that B. orientalis is capable of employing two alternative feeding modes in its adult life stage with similar efficiency. In rock pools, the anostracan Branchipodopsis were observed to feed both by filtering water and scraping benthic particles. This flexible feeding behaviour is probably an adaptation to low-nutrient content (Brendonck et al., 2000). In general, being omnivorous and having a broad diet spectrum might be an advantage in temporary habitats with short inundation phase. The omnivorous diet of B. orientalis is probably a good example of adaptation to the short inundation phase of anostracan habitats and the fact that they need to grow and reach maturity very fast (Beladjal et al., 2003; Sanchez and Angeler, 2007). In many cases, filter feeding is not in conflict with the ingestion of small-sized zooplankton such as rotifers and small cladocerans together with phytoplankton (Table I). However, in some studies, deductions on anostracan diet were based on indirect evidence, e.g. on trunk limb morphology in Branchinecta gaini (Paggi, 1996) or mouth orientation in S. dichotomus (Bernice, 1971). Diverse crustacean remains were found in the gut content of both species, but it was assumed that anostracans ingested them only when the prey was already dead. Branchinecta gaini individuals reached 2 cm in body length (Paggi, 1996), while S. dichotomus reached up to 2.7 cm (Bernice, 1971), which is comparable with our experimental B. orientalis animals, as well as with most anostracan species (ranging between 1 and 3 cm in length; Sanchez et al., 2007). For studying diet composition, gut content studies have some limitations, because food groups have different resistance to gut digestion (Mertens et al., 1990). Moreover, gut content cannot provide information on whether the prey was actively captured alive or was picked up as part of detritus, which results in different interpretations of the trophic role of anostracans. On the other hand, our experimental tests with single species offered as food only prove that B. orientalis was able to ingest diverse members of phyto- and zooplankton and that it actively predates on zooplankton. These experiments do not inform about possible preferences for a certain food types in the field. In numerous zooplankton taxa, it was shown that omnivorous feeding enhances growth and reproduction (Kleppel et al., 1998; Breteler et al., 1999). Anostracans fed with a mixed diet (algae + zooplankton) grew faster coupled with higher fecundity than animals fed on pure algal diet (Dumont and Ali, 2004). Hence, it is possible that the omnivorous feeding described here overall enhances food quality for anostracans. Therefore, we need both more in situ studies and empirical tests, resulting in a critical re-evaluation of the existing knowledge about anostracans. The community structuring role of anostracans in temporary ponds is still little studied (Sanchez and Angeler, 2007). We found that the diet of B. orientalis is very diverse, comprising of most phyto- and zooplankton community members, making this species a top consumer of soda pans. During spring, anostracans and copepods both reach very high densities in soda pans, with a maximum dry-weight biomass of 23 mg L−1 of for Arctodiaptomus spp. and 7 mg L−1 for anostracans (Horváth et al., 2013a). Calculating with the mean consumption rate in our experiment (2.4 mg of Arctodiaptomus per day) and the maximum density of B. orientalis from the field (13 ind L−1), this implies strong top-down effect of B. orientalis on zooplankton. Anostracans occur only in spring, while Arctodiaptomus stays until the pans dry out. It is possible that the short life span of B. orientalis enables coexistence of the two groups even due to interactions through competition and predation. Competition and predation effects can be difficult to discriminate. Negative correlations between B. orientalis and some cladoceran species were recorded previously (Sanchez et al., 2007). It is in agreement with the implications of our findings, while it does not clarify the direct effects of B. orientalis on the zooplankton community. A predator–prey interaction between anostracans and copepods beside competition was suggested earlier, but not tested experimentally (Pociecha and Dumont, 2008). Waterkeyn et al. (2011) found that anostracans have a strong negative effect on the population size of diverse zooplankton groups, probably due to both types of interactions. Our study complements these results, by showing that anostracans can act as intraguild predators of a diverse array of zooplankton taxa (rotifers, cladocerans and copepods). CONCLUSIONS Contrary to assumption, anostracans seem to be omnivorous predators, capable of ingesting a wide range of food particles ranging from picoplankton to medium-sized zooplankton. Studies are needed to verify if the results shown for B. orientalis can be regarded a common trait in other (small-sized) anostracan species. Our results imply a more complex trophic role of anostracans than previously assumed, suggesting to further study possible food selection and related trade-offs of omnivorous feeding such as food quality and quantity at different trophic levels in the habitats of anostracans. Finally, more empirical data from the field are needed, to fully appreciate the trophic role of these key consumers of temporary waters. 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( 2006 ) Introduction to temporary waters. In Williams , D. D. (ed.) , The Biology of Temporary Waters . Oxford University Press , Oxford , pp. 1 – 4 . Author notes Corresponding editor: Karl Havens © The Author(s) 2018. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Plankton Research Oxford University Press

Food spectrum of Branchinecta orientalis—are anostracans omnivorous top consumers of plankton in temporary waters?

Journal of Plankton Research , Volume Advance Article (4) – May 30, 2018

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Abstract

Abstract Anostracans are key elements of temporary ponds, due to the high abundance and importance as food for waterbirds. Except for a few large species, they are generally considered to be herbivorous filter feeders. However, this assumption is not supported by empirical data. In fact, there is a lack of quantitative experimental studies on their trophic role in the food webs of temporary waters. Here, we briefly revise the available data about the feeding spectrum of anostracans. Moreover, we present experimental data on the feeding behaviour of a key species of soda pans, Branchinecta orientalis. We show that B. orientalis is able to ingest a wide range of prey items, ranging from pico-sized algae, to motile prey such as copepods, with no significant differences in the ingested biomass from the different food types. We do not find evidence for sex and size-specific differences in the ingestion rates in adult animals. Our results clearly show that B. orientalis is an omnivorous planktivore. Based on our data and existing studies, we suggest refuting the general theorem that most anostracans are herbivorous filter feeders. More empirical data from the field are needed to fully appreciate the trophic role of these key consumers of temporary waters. INTRODUCTION Temporary ponds comprise very diverse ecosystems regarding size, shape, hydroperiod and water chemistry (Williams, 2006). They are widespread throughout the world, but are especially prevalent in arid and semi-arid climatic regions (Brendonck, 1996). Although the number of studies increased in the last decade, temporary ponds and their communities are still largely understudied compared to larger and more permanent water bodies (Céréghino et al., 2008; Céréghino et al., 2014; Marrone et al., 2017). Our knowledge about their food webs is particularly limited (Boix et al., 2016). Anostracans are a group of branchiopod crustaceans present almost exclusively in fishless temporary waters. In temporary ponds, anostracans (as well as the other large branchiopod crustaceans) are key elements, reaching high densities (Horváth et al., 2013a) and possibly having a strong impact on zooplankton communities through competition (Jocque et al., 2010). Moreover, anostracans are important food for waterbirds along their migration routes (Malone, 1965; Silveira, 1998; Boros et al., 2006; Sanchez et al., 2007; Horváth et al., 2013a) and during breeding seasons (Krapu, 1974). The general biology and feeding ecology of anostracans are not well understood (Marrone et al., 2017). Our knowledge on the diet of anostracans is mostly derived from anecdotal observations or correlative studies. There is a particular lack of quantitative data from controlled experiments. At present, anostracans are generally considered to be non-selective filter feeders (Brendonck, 1993). Filter-feeding organisms such as zooplankters have an important role in ecosystem functioning, since they are a key link from phytoplankton and bacteria to vertebrates (Persson et al., 2007) and drive trophic cascades (Carpenter et al., 1985). The majority of anostracans are predominantly considered herbivorous, feeding on algae in addition to organic and inorganic detritus which they filter from the water column or by mixing and scraping the bottom sediment. However, recent evidence suggests that they occasionally ingest nematodes and small zooplankters such as rotifers (see Table I). Only a few larger species were well documented to be predominantly predators, feeding on larger crustaceans such as copepods and other anostracans (White et al., 1969; Rogers et al., 2006; Rogers and Timms, 2017). Table I: Literature review about the diet composition and suggested feeding mode of anostracan species Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) Table I: Literature review about the diet composition and suggested feeding mode of anostracan species Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) Species Size (cm) Feeding mode Diet Method Reference Branchinecta ferox ~4.5 Filtration, predation Dominantly calanoids, also Daphnia, algae, detritus Feeding experiment, lab observation Fryer (1983) Branchinecta gaini 0.2–2 Mostly scraping Algae, bryophyte, protozoa, rotifers, copepod remains, anostracans, chironomids Intestinal content Paggi (1996) Branchinecta gigas 5–10 Predation Dominantly copepods and anostracans Lab observation, intestinal content Fryer (1966), White et al. (1969) and Daborn (1975) Branchinecta mackini 1.6–2.6 Filtration Bacteria, organic particles Unspecified literature source Daborn (1977) 2.1 Scraping Bottom particles Lab observation Fryer (1966) Branchinecta raptor ~5.5 Predation Dominantly anostracans, also chironomid midges, mosquito larvae, cladocerans, copepods, and ostracods Lab observation Rogers et al. (2006) Branchinella occidentalis 2.2–5 Predation Micrometazoans, algae, diatoms, detritus, chironomid midge larvae, anostracans Lab observation, intestinal content Rogers and Timms (2017) Branchinella spinosa 1.3–4 Filtration, predation Algae, cladocerans, copepods, anostracan eggs Intestinal content Alonso (1985) Chirocephalus diaphanus ~1 Filtration, predation Algae, rotifers, small cladocerans Intestinal content, feeding experiment Sarma and Nandini (2002) Eubranchipus holmani 0.7–1 Filtration Desmids, silt particles, Protococcus-like algae Feeding experiment Modlin (1982) Eubranchipus vernalis 1.3–1.8 Bottom scraping Benthic diatoms, filamentous algae, desmids, platyhelminth eggs, shells of Arcella Material on the oral groove, in the gut and faeces Modlin (1982) Streptocephalus dichotomus 0.7–2.7 Filtration Dominantly algae, also ciliates, rotifers, nematods, nauplii, remains of copepods and anostracans Intestinal content Bernice (1971) Streptocephalus proboscideus 0.9–2.2 Filtration, predation Algae, fungi, ciliates, rotifers, cladocerans, nauplii of copepods and anostracans Feeding experiment Mertens et al. (1990), Brendonck (1993) and Dumont and Ali (2004) According to two studies performed with large anostracan species (Branchinecta gigas and B. ferox), anostracan nauplii feed on small organic particles and algae (Daborn, 1975; Fryer, 1983). As they grow, their diet presumably broadens towards larger particles. For small anostracan species (<4 cm in length), there is only scattered information on the diet of adults. These data were collected with diverse field and laboratory methods and in many cases without any standardized experimental test (Table I). According to the very few existing examples, ingestion rates are increasing with the size of adults within a given species (Daborn, 1975; Dumont and Ali, 2004). In large predatorial anostracan species (e.g. Branchinecta ferox and B. raptor), the morphology of thoracopods implies that they gradually lose the ability of filter feeding with growth, probably once they reach 4–5 cm in length (Fryer, 1983; Rogers et al., 2006). Moreover, these large anostracan species are considered of being able to actively capture motile animal prey (White et al., 1969; Fryer, 1983; Rogers et al., 2006). Taken together, with the exception of large predatory taxa, we currently lack a good understanding about the diet of anostracans in their environment, which would be needed to assess their trophic role in the food web of temporary waters. Based on the existing data, size and feeding characteristics seem to lack a general pattern between different sexes of the same anostracan species. While differences in size were observed for some species (e.g. larger females in B. gigas; Daborn, 1975; larger males in Streptocephalus proboscideus; Brendonck, 1989), both sexes reach approximately the same size in others (Belk and Rogers, 2002; Miličić et al., 2013; Horváth and Vad, 2015). Among the few studies that tested for sex-related differences in ingestion rates, Bernice (1971) found no differences in Streptocephalis dichotomus, while in some other Streptocephalus species, females ingested more food than males (Dierckens et al., 1995; Ali et al., 1996), probably due to the high energetic demand of egg production (Ali et al., 1996). The genus Branchinecta occurs on all continents except Australia (Obregón-Barboza et al., 2002). It includes diverse species regarding body size and life history. Most species are smaller sized (up to 3 cm in length) and generally believed to be filter feeders and scrapers (Daborn, 1977; Paggi, 1996). This genus also contains the largest (predatory) anostracan species, such as B. gigas and B. raptor, that can grow up to 10 cm in body length (Daborn, 1975; Rogers et al., 2006). The target species of our study, Branchinecta orientalis, inhabits mineral-rich temporary waters and is distributed between 55° and 30° N in Europe and Asia (Mura and Takami, 2000). In Central European populations, adult B. orientalis usually range from 1.5 to 3 cm (pers. obs.), but can grow up to 4.1 cm (Petkovski, 1991). This makes them comparable to other Branchinecta species that are generally considered filter feeders, while predatory Branchinecta have a larger adult size range of 5–10 cm. Branchinecta orientalis is the most abundant anostracan species in Central European saline temporary waters, soda pans (Horváth et al., 2013b). Soda pan communities lack fish and macrovegetation (except in some cases around the shoreline). Picoplanktonic algae are the key primary producers in these naturally hypertrophic systems (Vörös et al., 2005, 2008; Somogyi et al., 2009). Both phyto- and zooplankton communities can reach very high densities during the wet phase (Horváth et al., 2014). Branchinecta orientalis reaches densities up to 13 ind L−1, which makes it an important food source for waterbirds (Horváth et al., 2013a). In spite of its ecological importance and high biomass, we are at present unaware about the diet of B. orientalis and its potential effects on the food web of soda pans. We experimentally test here the adult diet of the anostracan species B. orientalis (of comparable body size to many anostracan species considered as filter feeders). By using this species as model organism for anostracan feeding, our aims are to (1) examine their diet and compare the ingestion rates on different food types, ranging from pico-sized algae to large crustacean zooplankton; and (2) to determine whether ingestion rates depend on sex or body size. METHODS Cultivation of B. orientalis and plankton for feeding experiments All eggs and animals used in the experiments were collected in the Seewinkel region of Austria. To hatch animals, sediment containing resting eggs was collected from the soda pan Oberer Stinkersee (47.813722 N, 16.792889 E) and stored dry at 4°C in the dark for several months. After sieving and centrifuging the sediment by using the sugar flotation method (Onbe, 1978; Marcus, 1990), we incubated the eggs for hatching in a climate chamber, with a light regime 16:8 L:D and temperature of 18°C. Once animals started to hatch, we picked them out manually and transferred to larger plastic containers (25–35 adult animals in 21 L volume) filled with artificial soda water (NaHCO3 solved in distilled water, with conductivity of 1 mS cm−1) and constantly aerated. They were fed daily with a mix of algal food (Cryptomonas sp., Scenedesmus sp., Chlamydomonas sp.), which was at a later stage combined with zooplankton (rotifer Brachionus asplanchnoidis, cladoceran Moina brachiata, copepod Arctodiaptomus spinosus). Algal cultures were raised on WC medium, which was refreshed regularly (to keep them in exponential growth phase). Zooplankton was kept in 3 L volume jars in a medium of the same chemical composition as the anostracan medium, and fed regularly with a mix of algal food (Cryptomonas sp. and Chlamydomonas sp.). All phyto- and zooplankton cultures were kept under the same light regime and temperature conditions as anostracans. For testing the size dependency of ingestion rates, live anostracans were collected from Mittlerer Stinkersee (47.807044 N, 16.788180 E). These animals were used as a larger size class in our experiment, because the anostracans raised in the lab did not reach the maximum body size of the individuals from the field. They were kept and maintained in the same manner as the population hatched in the climate chamber, and used in feeding experiments only several days after collection from the field. Experimental design and data analyses Experiments were carried out with adult individuals. Animals were considered adult once mating was observed (around 4-week-old in case of animals hatched in the lab). At the onset of an experiment, body length of 10 individuals from all groups involved was measured (males, females, small and big animals). Body length was measured from the tip of the head to the end of cercopods (by means of photographs taken of live animals placed in a narrow transparent tube above grid lined paper). In our experiments, we incubated two female B. orientalis per replicate (except when we tested for sex differences, where we used two females vs. two males). For medium, we used 70 mL of artificial soda water at a conductivity of 1 mS cm−1 (same as in the cultures). The number of replicates in algal feeding tests (three) was usually lower than in the predatory tests (four to five), as we noticed an overall low variation between replicates in case of algal food. Controls (without B. orientalis) for all food types were run in parallel. To avoid algal sedimentation, medium was gently mixed in the algal feeding tests (both controls and vials with B. orientalis) with regular intervals (30 min) and immediately before sampling phytoplankton for quantification. To quantify filter feeding on phytoplankton, we offered two algae with different sizes as food in separate experiments (in concentrations equal to 2.5 mg L−1 dry weight, 5× higher than the concentration considered as saturating food abundance for Daphnia magna; Porter et al., 1982). A coccoid green algae Mychonastes sp. (Sphaeropleales; diameter 2–3 μm) was used as picoplankton (mean concentration 384 400 cells mL−1), and the green flagellate Chlamydomonas sp. (Chlamydomonadales) represented a larger unicellular food (7–18 μm length; mean concentration 33 600 cells mL−1). In the predatory feeding test, two zooplankters representative for soda pan communities were used (Horváth et al., 2014; Tóth et al., 2014): a copepod (Arctodiaptomus spinosus, 20 per vial, 3.8 mg L−1 dry weight) and a rotifer (Brachionus asplanchnoidis, 450 per vial, 3.2 mg L−1 dry weight). The length of adult A. spinosus is 0.65–1.16 mm (Bottrell et al., 1976), while it is between 0.185 and 0.510 mm for B. asplanchnoidis (Michaloudi et al., 2017). They were collected from soda pans in the Seewinkel region, and cultivated in the lab during the experiments. We offered a comparable biomass to B. orientalis in all tested food types (2.5–3.8 mg dry weight biomass L−1). Experiments were run for 40 min for B. asplanchnoidis, 1 hour for A. spinosus, 2 hours for Chlamydomonas sp. and 4 hours for Mychonastes sp. The length of experiments was decided for each food type based on ingestion rates observed in pre-experimental trials, where we counted the remaining algal cells or zooplankton individuals at multiple time points, until the effect of anostracan feeding became evident. For comparing differences between sex and size groups, experiments were set the same way as already described, with only a few minor differences in density and variety of food types tested. We used Chlamydomonas sp. (concentration 2.5 mg L−1 dry weight) as food in the filter feeding and B. asplanchnoidis (100 per vial) in the predatory feeding test to compare ingestion rates between males and females. To compare different adult size groups, we used Mychonastes sp. (concentration 2.5 mg L−1 dry weight) and Chlamydomonas sp. (concentration 7.5 mg L−1 dry weight) in filter feeding and A. spinosus (20 per vial, 3.8 mg L−1 dry weight) in predatory feeding tests. In an additional test, we offered two species of cladocerans to B. orientalis, M. brachiata (40 per vial) and D. magna (20 per vial, separately tested on two different age classes). These cladocerans are frequent members of zooplankton communities in soda pans and, therefore, it is relevant to check if they also represent a prey of B. orientalis. Besides, adults of D. magna are the largest representatives of crustacean zooplankton in these habitats and offering them as food allows for conclusions on the dietary size-spectrum of B. orientalis. Here, we only recorded whether these species were consumed by B. orientalis, without comparing ingestion rates with other food types. Body length of a cladoceran M. brachiata is around 1 mm, while D. magna ranges between 1 and 2 mm as juvenile and 2–5 mm as adult (pers. obs.). Per replicate, we offered cladocerans to two female anostracans for 20 min in 70 mL volume of medium (prepared the same way as explained above). Calculation of biomass and ingestion rates Biovolume of the algal food was approximated by measuring cellular dimensions and approximating them to simple geometrical bodies (sphere for Mychonastes sp. and depressed ellipsoid for Chlamydomonas sp.). Furthermore, we calculated the dry weight biomass per cell using the approximation that carbon biomass (~14% of biovolume) comprises 40% of total dry weight (Bowie et al., 1985). In zooplankton, B. asplanchnoidis and A. spinosus biomass per individual were calculated from the average weight of dried individuals (0.5 μg per individual for B. asplanchnoidis and 13.5 μg per individual for A. spinosus). Biomass ingestion rate per anostracan in the experiments was calculated based on the equations from Marin et al. (1986), with assumption that food concentration at the beginning of the experiment was below saturating concentration: M=gC0VmN with M being the ingested biomass per animal and time (in μg h−1); g is the grazing coefficient; C0 is the prey concentration (phytoplankton: cells/mL; zooplankton: individuals/mL) offered at the beginning of the experiment; V is the volume of medium (in mL); m is the average biomass (in μg) per phytoplankton cell or zooplankton individual; N is the number of anostracans per vial. The grazing coefficient (g) was calculated for all food types according to the following formula: g=k−ln(Ct)−ln(C0)t where C0 is the cell concentration of phytoplankton or concentration of zooplankton per unit volume offered as food at the beginning of experiment; Ct is the cell concentration of phytoplankton or concentration of zooplankton offered as food at the end of experiment, k is the growth rate based on the change of algal concentration in controls (applicable for phytoplankton); t is the duration of the experiment (expressed in hours). Statistical analyses One-way ANOVA was used to test for differences in biomass ingestion rates of the two algal and zooplankton groups in B. orientalis (normality and homogeneity of variances were met according to Shapiro–Wilk and Levene’s tests). Tukey’s post hoc test was applied to identify significant differences among different food types. In parallel with testing the differences in ingestion rates between males and females, we also tested for size difference in relation to sex. We first tested if the data on B. orientalis body length and ingestion rates for different food items follow a normal distribution with Shapiro–Wilk tests (separately for males and females). Length data were not normally distributed, so we applied Kruskal–Wallis rank sum test to test for differences in length between males and females. Afterwards, we checked whether there were any sex-related differences in ingestion rates. In the experiments with B. asplanchnoidis, we excluded one replicate in both the male and female treatments, where all rotifers were eaten before the end of the experiment. As data were normally distributed (ingestion rates on Chlamydomonas sp. and B. asplanchnoidis) and the assumption of homogeneity of variances was not violated (based on F test), we applied Student’s t-test to test for significant differences. The same procedure was applied to test length and feeding differences between two size classes of adult animals (mean ± SD: small: 1.44 ± 0.13 cm; big: 2.46 ± 0.22 cm). We checked for normality and homogeneity of variances before performing each test. The length differences between the two size classes were checked with Student’s t-test. Then, ingestion rates for feeding on Mychonastes sp., Chlamydomonas sp. and A. spinosus were compared between the two size classes. We used Kruskal–Wallis rank sum test for Mychonastes sp. and A. spinosus and Student’s t-test for Chlamydomonas sp. All data were analysed in R (R Core Team, 2014). RESULTS Anostracan diet width and ingestion rates Anostracans ingested all food types (small and large algae, rotifers and copepods) (Fig. 1a). Biomass ingestion rates on the picoalgae Mychonastes sp. (mean ± SD: 10.38 ± 7.26 μg h−1 or 20.8 ± 14.5 × 105 cells per hour), the larger algae Chlamydomonas sp. (30.55 ± 14.35 μg h−1; or 49.8 ± 23.4 × 104 cells per hour), the rotifer B. asplanchnoidis (123.37 ± 55.77 μg h−1; or 246.73 ± 111.55 individuals per hour) and the copepod A. spinosus (101.50 ± 123.68 μg h−1; or 7.54 ± 9.18 individuals per hour) were not significantly different from each other (ANOVA: F(3,11) = 1.62, P = 0.24; Fig. 1b). However, once an outlier from the A. spinosus treatment was removed (ingestion rate was above 300 μg h−1, while all others were ≤200 μg h−1; see Fig. 1b) we found significant difference between food types (ANOVA: F(3,10) = 5.3, P = 0.02), where ingestion rates on B. asplanchnoidis were significantly higher than those observed on Mychonastes sp. (Tukey’s post hoc test: P = 0.02). Fig. 1. View largeDownload slide (a) Colouration of B. orientalis intestine after feeding them first with sole algal (Chlamydomonas sp.) and then zooplankton (Arctodiaptomus spinosus) food. (b) Biomass ingestion rates on different food types. ANOVA showed no significant difference (n.s.) between the four groups (F(3,11) = 1.62, P = 0.24). When an outlier for the A. spinosus feeding test result was removed (ingestion rate above 300 μg h−1), ANOVA showed significant variance between the groups (F(3,10) = 5.30, P = 0.02), with significant difference between Mychonastes sp. and B. asplanchnoidis (Tukey’s post hoc test: P = 0.02). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Fig. 1. View largeDownload slide (a) Colouration of B. orientalis intestine after feeding them first with sole algal (Chlamydomonas sp.) and then zooplankton (Arctodiaptomus spinosus) food. (b) Biomass ingestion rates on different food types. ANOVA showed no significant difference (n.s.) between the four groups (F(3,11) = 1.62, P = 0.24). When an outlier for the A. spinosus feeding test result was removed (ingestion rate above 300 μg h−1), ANOVA showed significant variance between the groups (F(3,10) = 5.30, P = 0.02), with significant difference between Mychonastes sp. and B. asplanchnoidis (Tukey’s post hoc test: P = 0.02). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. The two cladocerans M. brachiata and juvenile Daphnia magna were both efficiently ingested by B. orientalis (they were all removed within 20 min). However, fairy shrimps were not feeding on adult D. magna (~5 days and older, which meant >1.5 mm in body length), which represented the only food type that was not ingested. Sex differences There was no significant difference in body length between males and females (mean ± SD: 1.41 ± 0.13 cm for males and 1.44 ± 0.13 cm for females; Kruskal–Wallis rank sum test: χ2 = 0.40, P = 0.525). Differences in food ingestion rates were also not significant, neither in case of filter feeding on Chlamydomonas sp. (males: 12.95 ± 8.70 μg h−1, females: 15.88 ± 8.50 μg h−1; t-test: t = 0.54, P = 0.60) nor in predatory feeding on B. asplanchnoidis (males: 95.20 ± 54.33 μg h−1, females: 92.32 ± 38.44 μg h−1; t-test: t = −0.20, P = 0.85) (Fig. 2). Fig. 2. View largeDownload slide Comparison of biomass ingestion rates between males and females on (a) algal food Chlamydomonas sp. (t-test, t = 0.54, P = 0.60); and (b) zooplankton Brachionus asplanchnoidis (t-test, t = −0.20, P = 0.85). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Fig. 2. View largeDownload slide Comparison of biomass ingestion rates between males and females on (a) algal food Chlamydomonas sp. (t-test, t = 0.54, P = 0.60); and (b) zooplankton Brachionus asplanchnoidis (t-test, t = −0.20, P = 0.85). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Size differences Adults raised in the lab from eggs were significantly smaller (mean ± SD: 1.44 ± 0.13 cm) than the adult animals collected on the field (mean ± SD: 2.46 ± 0.22 cm; t-test: t = 12.839, P < 0.001). However, we did not observe any significant difference in biomass ingestion rates, neither for filter feeding on Mychonastes sp. (small: 10.38 ± 7.26 μg h−1, big: 21.12 ± 8.22 μg h−1; Kruskal–Wallis rank sum test: χ2 = 2.33, P = 0.13) and Chlamydomonas sp. (small: 63.63 ± 11.38 μg h−1, big: 126.47 ± 61.84 μg h−1; t-test: t = 1.73, P = 0.22), nor for predatorial feeding on A. spinosus (small: 101.50 ± 123.68 μg h−1, big: 57.25 ± 49.64 μg h−1; Kruskal–Wallis rank sum test: χ2 = 0.06, P = 0.80) (Fig. 3). Fig. 3. View largeDownload slide Comparison of biomass ingestion rates in two size groups of adult animals on (a) picoplanktonic algae Mychonastes sp. (Kruskal–Wallis rank sum test: χ2 = 2.33, P = 0.13); (b) algae Chlamydomonas sp. (t-test: t = 1.73, P = 0.22); and (c) zooplankton Arctodiaptomus spinosus (Kruskal–Wallis rank sum test: χ2 = 0.06, P = 0.80). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. Fig. 3. View largeDownload slide Comparison of biomass ingestion rates in two size groups of adult animals on (a) picoplanktonic algae Mychonastes sp. (Kruskal–Wallis rank sum test: χ2 = 2.33, P = 0.13); (b) algae Chlamydomonas sp. (t-test: t = 1.73, P = 0.22); and (c) zooplankton Arctodiaptomus spinosus (Kruskal–Wallis rank sum test: χ2 = 0.06, P = 0.80). Box gives the interquartile range and whiskers give the approximate 95% confidence intervals. DISCUSSION In our feeding experiments, B. orientalis was capable of capturing and ingesting a high variety of food types, differing both in size and in trophic level (phyto- and zooplankton). The results thus clearly show that B. orientalis is an omnivorous predator. Adult D. magna was the only food item B. orientalis was not able to ingest. As B. orientalis effectively preyed on juvenile D. magna, this indicates an upper prey size limit. It appears that anostracans in our experiments consumed slightly more zooplankton than phytoplankton biomass when offered in comparable amounts (Fig. 1B). It was more expressed in the rotifer B. asplanchnoidis, probably due to limited motility of this species, which makes it an easy prey for anostracans compared to the motile copepod. However, the estimated feeding rates on algae should be seen as conservative estimates, as food concentrations were below saturating levels (see Supplement 1). Although Petkovski (1991) noted that females were generally larger than males in B. orientalis, we did not find significant sex-specific size differences. Moreover, we did not find significant differences in the ingestion rates between males and females, in spite of the fact that females were producing eggs at the time of the experiment. Daborn (1975) noted for B. gigas that assimilation rates in males were lower than in females, while motion of extremities (and consequently filtration rates) were slightly higher than in females suggesting that this way males ingest more food and compensate for lower assimilation efficiency. Bernice (1971) found no difference in ingestion rates between males and females of Streptocephalus dichotomus, species of comparable size to B. orientalis. Males probably spend more energy in swimming by searching for females, while females use energy mostly for egg production, which would explain similar food consumption (Daborn, 1975). Food ingestion rates between the two studied size classes of adult anostracans showed no significant difference in any of the tested food types. It suggests that once adult and capable of predation, the filtering ability of B. orientalis does not change considerably with growth. It is possible that in long-term experiments, the effect of body size on feeding rates would be easier to observe, due to higher metabolic demands (Daborn, 1975). In our experiments, we tested ingestion rates in short-term experiments (2–4 hours). From this, we could conclude that there is no change in the ability of filter feeding with growth. Size-dependent decrease in ingestion rates on phytoplankton was not observed in our experiments, not even with Mychonastes sp. as smaller sized algal food. On the contrary, ingestion rates for both algae types were slightly higher in animals of larger body size. Considering that there was no significant difference between feeding on algae (true filter feeding) and on copepods (motile animals, which could be regarded as some form of an active predation mode of feeding), our results show that B. orientalis is capable of employing two alternative feeding modes in its adult life stage with similar efficiency. In rock pools, the anostracan Branchipodopsis were observed to feed both by filtering water and scraping benthic particles. This flexible feeding behaviour is probably an adaptation to low-nutrient content (Brendonck et al., 2000). In general, being omnivorous and having a broad diet spectrum might be an advantage in temporary habitats with short inundation phase. The omnivorous diet of B. orientalis is probably a good example of adaptation to the short inundation phase of anostracan habitats and the fact that they need to grow and reach maturity very fast (Beladjal et al., 2003; Sanchez and Angeler, 2007). In many cases, filter feeding is not in conflict with the ingestion of small-sized zooplankton such as rotifers and small cladocerans together with phytoplankton (Table I). However, in some studies, deductions on anostracan diet were based on indirect evidence, e.g. on trunk limb morphology in Branchinecta gaini (Paggi, 1996) or mouth orientation in S. dichotomus (Bernice, 1971). Diverse crustacean remains were found in the gut content of both species, but it was assumed that anostracans ingested them only when the prey was already dead. Branchinecta gaini individuals reached 2 cm in body length (Paggi, 1996), while S. dichotomus reached up to 2.7 cm (Bernice, 1971), which is comparable with our experimental B. orientalis animals, as well as with most anostracan species (ranging between 1 and 3 cm in length; Sanchez et al., 2007). For studying diet composition, gut content studies have some limitations, because food groups have different resistance to gut digestion (Mertens et al., 1990). Moreover, gut content cannot provide information on whether the prey was actively captured alive or was picked up as part of detritus, which results in different interpretations of the trophic role of anostracans. On the other hand, our experimental tests with single species offered as food only prove that B. orientalis was able to ingest diverse members of phyto- and zooplankton and that it actively predates on zooplankton. These experiments do not inform about possible preferences for a certain food types in the field. In numerous zooplankton taxa, it was shown that omnivorous feeding enhances growth and reproduction (Kleppel et al., 1998; Breteler et al., 1999). Anostracans fed with a mixed diet (algae + zooplankton) grew faster coupled with higher fecundity than animals fed on pure algal diet (Dumont and Ali, 2004). Hence, it is possible that the omnivorous feeding described here overall enhances food quality for anostracans. Therefore, we need both more in situ studies and empirical tests, resulting in a critical re-evaluation of the existing knowledge about anostracans. The community structuring role of anostracans in temporary ponds is still little studied (Sanchez and Angeler, 2007). We found that the diet of B. orientalis is very diverse, comprising of most phyto- and zooplankton community members, making this species a top consumer of soda pans. During spring, anostracans and copepods both reach very high densities in soda pans, with a maximum dry-weight biomass of 23 mg L−1 of for Arctodiaptomus spp. and 7 mg L−1 for anostracans (Horváth et al., 2013a). Calculating with the mean consumption rate in our experiment (2.4 mg of Arctodiaptomus per day) and the maximum density of B. orientalis from the field (13 ind L−1), this implies strong top-down effect of B. orientalis on zooplankton. Anostracans occur only in spring, while Arctodiaptomus stays until the pans dry out. It is possible that the short life span of B. orientalis enables coexistence of the two groups even due to interactions through competition and predation. Competition and predation effects can be difficult to discriminate. Negative correlations between B. orientalis and some cladoceran species were recorded previously (Sanchez et al., 2007). It is in agreement with the implications of our findings, while it does not clarify the direct effects of B. orientalis on the zooplankton community. A predator–prey interaction between anostracans and copepods beside competition was suggested earlier, but not tested experimentally (Pociecha and Dumont, 2008). Waterkeyn et al. (2011) found that anostracans have a strong negative effect on the population size of diverse zooplankton groups, probably due to both types of interactions. Our study complements these results, by showing that anostracans can act as intraguild predators of a diverse array of zooplankton taxa (rotifers, cladocerans and copepods). CONCLUSIONS Contrary to assumption, anostracans seem to be omnivorous predators, capable of ingesting a wide range of food particles ranging from picoplankton to medium-sized zooplankton. Studies are needed to verify if the results shown for B. orientalis can be regarded a common trait in other (small-sized) anostracan species. Our results imply a more complex trophic role of anostracans than previously assumed, suggesting to further study possible food selection and related trade-offs of omnivorous feeding such as food quality and quantity at different trophic levels in the habitats of anostracans. Finally, more empirical data from the field are needed, to fully appreciate the trophic role of these key consumers of temporary waters. 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Journal of Plankton ResearchOxford University Press

Published: May 30, 2018

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