Ciliate populations in temporary freshwater ponds: seasonal dynamics and influential factors

Abstract

SUMMARY 1. The ciliate populations of two temporary ponds in southern Ontario were studied throughout their aquatic phases in 2001. Pond I (∼1 ha) held water for 98 days, whereas Pond II (∼0.25 ha) held water for 34 days. Populations were assessed both within the ponds themselves and within a series of enclosures in which invertebrate predator pressure was manipulated.

2. In the natural pond water, total ciliate abundance in Pond II rose rapidly from day 1 increasing two orders of magnitude by day 7. In contrast, total abundance in Pond I began at the same level as in Pond II but increased much more slowly, reached a plateau of around 500 individuals L⁻¹, and increased again late in the hydroperiod.

3. Despite being only 500 m apart, the two ponds were fairly dissimilar in terms of their species richness and species composition. Pond I contained 50 species compared with 70 species for Pond II, with only 24 species shared. Additional species occurred within the enclosures raising the total species richness to 145 species; 88 from Pond I, 104 from Pond II, with 47 species (30%) in common. Pond II contained more mid‐sized ciliates (50–200 μm), whereas Pond I was dominated by smaller ciliates, especially in mid‐May and early June. In Pond I, cumulative species richness throughout the hydroperiod was highest in the predator addition enclosures (65 ± 4 species), followed by the partial‐predator exclusion enclosures (50 ± 4). Lowest species richness was found in the control enclosures (39 ± 2) and in the pondwater controls (39 ± 0). Differences between the ciliates in the natural pond water and the enclosures appeared to be related to a greater concentration of phytoplankton within the enclosures (perhaps resulting from extensive growth of duckweed, Lemna, outside), and higher densities of zooplankters in the pond.

4. The physicochemical environment influenced species richness, total abundance and the number of rare species (27 in Pond II versus 13 in Pond I). Variation in ciliate abundance in Pond I could be explained by the number of days after filling (39%) and enclosure treatment (23%). These two parameters also explained 72% of the variation in species richness in Pond I (46 and 26%, respectively). Sixty‐five per cent of the variation in abundance in Pond II could be explained by the measured parameters: number of days after filling 27%, pH 19%, and nitrate levels 12%. Fifty‐two per cent of the variation in species richness was explained by the environmental parameters, of which pH was the most influential. Species succession was a strong feature of both ponds and its relationship to environmental variables and the presence of other organisms is discussed.

5. Addition of invertebrate predators resulted in higher abundance and higher species richness for a limited time period in one of the ponds – suggesting that differences in foodweb dynamics may influence ciliate community composition.

Introduction

Ciliates and other protoctists are believed to play a significant metabolic role in freshwater systems (Wetzel, 1983; Beaver & Crisman, 1989). In marine environments, ciliates have been recognised as an important link between bacteria and pelagic zooplankters in a ‘microbial loop’ (e.g. Sleigh, 1989; Pierce & Turner, 1992), and, in Lake Michigan, experimental studies have shown that a large fraction of picoplankton carbon is directly transferred to higher trophic levels via a picoplankton‐protoctist‐zooplankton coupling (Carrick et al., 1991). Ciliates are believed not only to route energy through their consumption of primary producers and subsequent ingestion by predaceous and detritivorous metazoans (Sleigh, 1989; Wickham, 1995), but also as photosynthesizers via phytoflagellate symbionts (Sorokin, 1999). High rates of growth and reproduction make ciliates major organic matter transformers.

Despite such pivotal roles, the basic biology and population dynamics of ciliates in fresh waters are not well known for a variety of methodological and taxonomical reasons summarised by Finlay et al. (1988). Such information as does exist has come primarily from large lentic bodies, such as lakes (Goulder, 1974; Petersen, 1990; James, Burns & Forsyth, 1995) and reservoirs (Salvado & Gracia, 1991), with some studies also having been carried out in running waters (Taylor, 1981; Madoni, 1983; Baldock & Sleigh, 1988). A few studies have considered the seasonal development of ciliates in ponds (Grolière & Njine, 1973; Kusano, Kusano & Watanabe, 1987; Guhl, Finlay & Schink, 1994; Finlay & Esteban, 1998), but almost no data are available from temporary freshwater ponds – in which metazoans demonstrate interesting traits related to the transient nature of the habitat (Williams, 2001).

The purpose of this study was twofold: first, to describe the ciliate taxa, their population dynamics, and seasonal succession over the differing aquatic phases of two temporary ponds in southern Ontario, Canada; secondly, to attempt to relate these finding to environmental factors that may have influenced them, the latter including a predator field‐manipulation experiment.

Methods

The two ponds are located in Vandorf, Ontario (44°00′N, 79°23′W), and were sampled throughout their aquatic phases in 2001. Both ponds were filled by snowmelt water in early spring. Pond I was initially approximately 1 ha in area with a maximum depth of 27 cm, and held water from 4 April until 17 July (98 days). Pond II was smaller (∼0.25 ha) but deeper (maximum 66 cm) and held water from 7 April until 17 May (34 days). Both are eutrophic and fishless in nature, and they are separated by a distance of only 500 m. Mixed deciduous woodland and hay fields surround both ponds, although Pond II is somewhat more open in exposure.

Routine sampling

A weekly sampling programme was set up by comprising analyses for ciliates, water chemistry (using a Hydrolab H₂O multiprobe: Hydrolab Corporation, Austin, TX, U.S.A.; and portable Hach Kit spectrophotometer DR2000: Hach Company, Loveland, CO, U.S.A.), and chlorophyll a (acetone extraction method; American Public Health Association, 1995). Ciliate samples were taken by submerging a closed 35 cm³ container adjacent to the substrate, removing the lid and sealing it once full. Two such replicates were taken at each sampling site and these were pooled in the field. Because of the time required to identify the large number of species present, only samples from Pond I were examined alive, those from Pond II were preserved with mercury chloride. After thorough mixing, 10 cm³ were withdrawn from each of the 280 cm³ samples, and placed in an Utermöhl chamber (Phyco Tech Inc., MI, USA); fresh and preserved samples were treated identically. After settling, the ciliates were examined under an inverted microscope. Species in low abundance were concentrated using vacuum filtering (1.2 μm) under low pressure. Identifications were always made on live specimens, using the following keys: 1930, 1931, 1932, 1935); Bick (1972); Corliss (1979); 1982, 1983); Foissner et al. (1991); Foissner, Berger & Kohmann (1992, 1994); Foissner et al. (1995).

The manipulations

As part of a larger study on invertebrate community dynamics, a predator manipulation experiment was set up in the two ponds. Six, water‐tight, galvanised sheet‐metal enclosures, each measuring 2.3 m in diameter and 0.7 m in height, were installed in each pond prior to snowmelt. They were randomly located within relatively homogeneous areas of depth, substrate and exposure, and were forced into the bed to a depth of approximately 10 cm, effectively corralling sections of pond. Within each pond, two of the enclosures were covered with a fine (1 mm), white mesh that excluded the entry of aerially colonising insect predators (primarily Coleoptera and Odonata) – although they may subsequently have contained predators that hatched from dormant eggs laid on the pond bottom in the previous year. Another two enclosures served as ‘predator addition’ manipulations to which were added, weekly, specimens of the seasonally predominant predators present in the ponds. This amounted to a total of 30 beetle larvae (Rhantus sp., Agabus sp., Acilius sp.) added to each enclosure in Pond I (on days 28, 35 and 42) and 20 in the Pond II enclosures (on days 27 and 34). A total of 120 dragonfly nymphs (Sympetrum obtrusum, S. internum, S. costiferum) was also added to each of the two enclosures in Pond I (on days 49, 56, 63, 70, 77 and 84). No odonates were added to Pond II as it had dried up by this time. The last two enclosures in each pond served as controls in an attempt to determine any enclosure effects. Thus alongside the samples taken from the ponds themselves, termed ‘outside enclosures’, samples of water, chlorophyll a and ciliates were also taken from each of the three treatments.

Physicochemical environment

The depth of Pond I initially increased during the first week after snowmelt, then gradually decreased at around day 42 (Fig. 1). Thereafter, depth increased because of rainfall and then declined to 0 on day 98. The pattern in Pond II was one of uniform decline from day 1 to day 42 (Fig. 2). In both ponds, outside the enclosures, water temperatures, turbidity, nitrate, ammonia (higher in Pond I) and total phosphorus (more variable in Pond I) steadily increased until they reached a maximum prior to dry up (1, 2). Conductivity inversely followed water depth. The pH tended to become lower over the aquatic phase in Pond I (range: 5.5–6.4) but increased in Pond II (range: 6.8–7.3). Dissolved oxygen dropped by a similar amount in both ponds, but the start and end concentrations were lower in Pond I. Chlorophyll a peaked only once in Pond II (day 6), but three times in Pond I (days 21, 49 and prior to dry up).

Figure 1.

Seasonal variation in physicochemical parameters in Pond I. Mean values are shown for the pond water (‘Outside enclosures’), the control enclosures, and the two predator manipulation enclosures. Error bars for chlorophyll indicate ±1SE (n = 2).

Figure 2.

Seasonal variation in physicochemical parameters in Pond II. Mean values are shown for the pond water (outside enclosures), the control enclosures, and the two predator manipulation enclosures. Error bars for chlorophyll indicate ±1SE (n = 2).

In Pond II, within the enclosures, all measured parameters showed patterns that were very similar to those seen in the pond itself, with the exception of ammonia which was higher (P < 0.05, from a Fisher's LSD test applied after a repeated measures anova) in the control enclosures (Fig. 2). This was the case also for Pond I in terms of depth, temperature and ammonia, although pH, conductivity and dissolved oxygen were occasionally higher in the enclosures (P < 0.01 from a repeated measures anova; Fig. 1). Although initially very similar to the concentrations in the pond, Pond I enclosures showed marked decreases in nitrate, total phosphorus and turbidity prior to dry up (P < 0.05 from a repeated measures anova). Chlorophyll a levels in the Pond I enclosures were very similar to those in the outside water until around day 28, the beginning of the predator addition treatment. Thereafter, the enclosure controls and both predator‐manipulation treatments (especially the predator addition) rose significantly above background levels (P < 0.01; Fig. 1). Chlorophyll a levels in Pond II were similar amongst all treatments and controls (P = 0.78; Fig. 2). Chlorophyll a levels were generally higher in Pond I, with maxima occurring at the beginning of the hydroperiod in Pond II but much later (May to June) in Pond I. Maxima prior to dry up in both ponds were likely a concentration effect because of rapidly decreasing pond volumes.

Population dynamics

Outside the enclosures, total ciliate abundance rose rapidly from day 1 in Pond II such that there was two orders of magnitude increase by day 7 (Fig. 3a). This higher level was maintained throughout the aquatic phase of the pond. In contrast, total abundance in Pond I began at the same level as in Pond II but increased much more slowly, reached around 230–340 individuals L⁻¹ for much of the pond's life, but increased again late in the aquatic phase (probably a concentration effect of decreasing water volume).

Figure 3.

(a) Seasonal development of total ciliate abundance in ponds I and II (mean ± 1SE; n = 2). (b) Seasonal development of three size groups in the ciliate communities of the two ponds (data averaged from two replicates). (c) Relative abundance of the dominant ciliate feeding strategies (data from two replicates). Feeding groups are: a, algivores; b, bacteriovores; h, predators on heterotrophic flagellates; p, predators on other protoctists, including ciliates; o, omnivores; other, unknown prey.

Despite being only 500 m apart, the two ponds were fairly dissimilar in terms of their species richness and species composition. Pond I contained 50 species compared with 70 species for Pond II, with only 24 species shared. Further, similarity in species between the replicate samples taken within each pond were modest (56% in Pond I; 43% in Pond II), and only around half of the 24 species occurring in both ponds were found in all four replicates combined. Such high spatial heterogeneity belied the visually homogeneous appearance of the habitat (in terms of depth, substrate, water chemistry, light regime, macrophyte composition) within each pond. Most of the ciliates present belonged to the Kinetofragminophora (Pond I: 19 species; Pond II: 29 species) and Polyhymenophora (19 and 22 species, respectively), with slightly fewer Oligohymenophora (12 and 19 species, respectively). Species are given in Appendix1, Appendix2.

On day 1, Pond I was dominated by a single small (<50 μm) species, Urotricha farcta (Fig. 3b). Thereafter, the predominant species were as listed in Appendix 1 (where high abundance species, 800–8480 individuals L⁻¹, are marked with ‘*’ in the prey column).

In Pond II, larger sized ciliates predominated on the first day (Fig. 3b): Stentor polymorphus, Spirostomum minus, Loxodes magnus and Paramecium caudatum (Appendix 2). Throughout the remainder of the hydroperiod, no single species predominated, except briefly, between days 20 and 27 in one replicate, in which the medium‐sized Epistylis chrysemydis comprised between 26 and 49% of the ciliate community. The larger ciliates gradually diminished as Pond II dried, whereas they were more persistent in Pond I. Medium‐sized ciliates were rare early on in both ponds, but became a major component in Pond II, in Pond I their relative numbers fluctuated.

In both ponds, the majority of ciliate species could be categorised as bacterial and/or algal feeders (Fig. 3c; based on Foissner & Berger, 1996). Pond I was dominated initially by species that fed on algae, bacteria and heterotrophic flagellates (the generalist ‘abh’ category), followed for the rest of the hydroperiod by species belonging to more distinct feeding categories (e.g. bacteria, omnivores, algae/bacteria). Facultative algivores and bacterivores were better represented in Pond II, where there was no initial dominance of generalist feeders. The relative abundance of algivores in Pond II followed the seasonal trend in phytoplankton (as measured by Chlorophyll a; Fig. 2). Predators (i.e. ciliates that fed on other protoctists/ciliates) were not common in either pond.

Within the enclosures, in both ponds, total ciliate abundance began with low values, similar to those seen in the ponds themselves (Fig. 4a). In Pond I, abundances rose in the enclosure controls and the partial predator exclusion treatments to exceed those of the pond by around day 28. By days 63–70 they exceeded the pond populations considerably. Abundances in the predator addition enclosures began to exceed those in the pond by the end of the first week (prior to the actual addition of the invertebrates on day 28) and greatly exceeded the pond controls to the end of the hydroperiod (10 000 ciliates L⁻¹ versus ∼1000 ciliates L⁻¹, respectively) when they had returned to the same level as the enclosure controls and the partial predator exclusion treatments. In contrast, development of ciliate numbers in the Pond II enclosures closely followed densities outside (Fig. 4a). There was initially (within 6 days) a very rapid increase from 4000 to 27 000 ciliates L⁻¹, a level which was sustained until the end of the hydroperiod. Densities in Pond I peaked at >100 000 ciliates L⁻¹ (in partial predator exclusion, day 70) primarily comprising small species such as U. farcta, U. furcata, U. nigricans, H. grandinella, and P. cirrifera. Maximum density recorded in Pond II was 41 400 ciliates L⁻¹ (outside enclosures).

Figure 4.

(a) Seasonal development of ciliate abundance in the four treatment enclosures in ponds I and II (mean ± 1SE; n = 2). Arrows on day 1 represent beginning of partial‐predator exclusion manipulation. Arrows on days 27 and 28 represent beginning of predator addition manipulation. (b) Seasonal development of species richness (cumulative from the two replicates) inside and outside enclosures.

Additional species occurred within the enclosures: Kinetofragminophora, 15 and 10 species (ponds I and II, respectively); Polyhymenophora, 14 and 18 species and Oligohymenophora nine and six species. This raised the total species richness to 145 species; 88 from Pond I, 104 from Pond II, with 47 species (30%) in common (Appendix1, Appendix2). Over the 34‐day hydroperiod of Pond II, roughly twice the number of ciliate species were supported than during the first 34 days of Pond I (Fig. 4b). However, species richness in Pond I rose to near Pond II levels towards the end of its own hydroperiod (around day 98). Cumulative species richness throughout the hydroperiod was highest in the predator addition enclosures (65 ± 4 species), followed by the partial predator exclusion enclosures (50 ± 4). Lowest species richness was found in the control enclosures (39 ± 2) and in the pond controls (39 ± 0). As these two controls were similar, the differences seen in the others were likely the result of predator manipulation rather than because of enclosure effects. Interestingly, there was some increase in both the predator addition enclosures before the predators were added. After addition, these increases became larger. The results obtained in Pond II were less convincing: predator addition (54 ± 3), partial predator exclusion (50 ± 7), enclosure controls (44 ± 4) and pond controls (50 ± 3).

For each pond, seasonal ciliate abundance (log‐transformed) and species richness from all treatments and outside the enclosures were combined into a larger data set for analysis of the possible influence of environmental factors. Stepwise linear regression indicated that 69% of ciliate abundance in Pond I could be explained by the measured environmental parameters, with number of days after filling and treatment being the most influential (explaining 39 and 23% of the variation in ciliate abundance, respectively; P < 0.001). These two parameters also explained 72% of the variation in species richness in Pond I (46 and 26%, respectively; P < 0.001). Sixty‐five per cent of the variation in abundance in Pond II could be explained by the measured parameters, with number of days after filling accounting for 27% (P < 0.001), pH 19% (P < 0.001) and nitrate levels 12% (P < 0.001); water depth was excluded from the analysis as it was highly correlated with days after filling (r = 0.99). Fifty‐two per cent of the variation in species richness was explained by the environmental parameters, of which pH was the most influential (40%; P < 0.001).

Pond I was dominated by small ciliates (<50 μm) on two occasions, mid‐May and the first half of June (indicated as size group ‘1’ in Appendix 1); at times, some attained densities as high as 10 000–60 000 individuals L⁻¹. Medium‐sized (50–200 μm; size group ‘2’) species were less abundant (1300–3000 individuals L⁻¹). Large (>200 μm; size group ‘3’) species were less common but by virtue of their size contributed significantly to overall community biomass. Compared with Pond I, Pond II had a considerably higher frequency of mid‐sized ciliates (50–200 μm) (Fig. 5a,b; Appendix 2, where high abundance is indicated by ‘*’). In both ponds, large ciliates were abundant early and late in the hydroperiods. Based on a comparison of the first 34 days of each pond, the populations in Pond II appeared to be more stable than in Pond I (see Appendix1, Appendix2).

Figure 5.

Relative seasonal development of most abundant ciliate species in (a) Pond I (all samples combined) and (b) Pond II (all samples combined).

Persistent species (i.e. those present during the entire aquatic phase) comprised about 10% of the ciliate communities in both ponds. Sporadic species were especially notable in Pond II where almost 20% of species appeared only once and >40% appeared no more than twice (see Appendix1, Appendix2, where they are marked with ‘s’).

Feeding groups

The proportions of the major ciliate feeding categories (based on those established by Foissner & Berger, 1996) did not differ markedly among the treatments and the controls, and were thus combined for each pond (Fig. 6). Algivores and bacteriovores were the most common in both ponds: the former ranging between 37 and 88% in Pond I and between 47 and 56% in Pond II; and the latter ranging between 29 and 67% in Pond I and between 22 and 70% in Pond II. There were more algivorous species in Pond II (48%) than in Pond I (40%), although their abundance was greater in Pond I. In Pond II, bacteriovore relative abundance increased as the pond dried‐up; in Pond I there was a similar but more variable trend. Facultative algae feeders were most numerous in Pond II early in the season (e.g. 38% of the relative abundance on day 7 was because of U. gallina alone) but thereafter decreased rapidly. Pond I contained only one, although very abundant, facultative algivore, Pelagohalteria cirrifera.

Figure 6.

Seasonal development of the dominant ciliate feeding groups in ponds I and II (all samples combined). Second y‐axis show the percentage of predators.

Omnivorous ciliates (known to feed on autotrophs, other protoctists and even on small metazoans; Foissner & Berger, 1996) were moderately important parts (21%) of the communities of both ponds early in the season but thereafter declined in Pond I (Fig. 6; also marked with ‘o’ in the prey column of Appendix1, Appendix2).

Although 13–14% of all species in the two ponds were predators, feeding chiefly on other ciliates, their abundance never exceeded 5% (Pond I) and 8% (Pond II) of the total ciliate community (Fig. 6; predator peaks occurred at around the same time (days 13–21) in both ponds.

Discussion

Compared with ciliate abundance in permanent ponds, maximum ciliate densities in the two Vandorf ponds were anywhere from 10 to 150% lower (Goulder, 1971b; Grolière & Njine, 1973; Hatano & Watanabe, 1981; Kusano et al., 1987; Berninger, Wickham & Finlay, 1993; Guhl et al., 1994). Further, ciliate abundance in permanent waters often shows a bimodal seasonal pattern, with maximum ciliate abundance in spring and autumn co‐occurring with thermal mixing (e.g. Goulder, 1971a; Müller et al., 1991). Ciliate abundance increased as the habitat was drying up in both ponds, possibly as a result of warmer water and other ‘favourable’ physical conditions in late summer (Wang, 1928). The Vandorf ponds are devoid of any nutrient bursts corresponding to thermal mixing, relying instead on progressive nutrient release from the breakdown of dead aquatic vegetation and riparian leaf litter input from the previous year. Hatano & Watanabe (1981) found that high abundance of bacterivorous protoctists in the leaf litter of a small pond was closely related to litter decomposition in late autumn and spring. Densities of algae were low throughout the season in our ponds, and it is likely that much of the communities in both ponds relied on bacteria for food. Indeed, facultative bacterial feeders were frequently more abundant than facultative algivores. Bacterial counts showed this food source to be three times higher in Pond II, possibly explaining the much higher abundance of ciliates there; although ciliate richness was similar in both ponds.

Variance in total ciliate abundance in the Vandorf ponds could best be explained (39 and 27%, respectively, for ponds I and II, from stepwise linear regression) by the number of days after filling. Overall, dissolved oxygen concentration did not emerge as an influential factor, but on a species level it might be, and some species did disappear when dissolved oxygen levels went below 2 mg L⁻¹ (see Appendix1, Appendix2). There are also indications that light availability restricted the distribution of photosynthetic species (e.g. S. viride and E. alatus), as these occurred only early in the hydroperiod of Pond I, when light penetration was greatest (before Lemna covered the surface and turbidity increased). Overall ciliate abundance is also likely to have been influenced by several biotic factors such as competition and predation, both from other ciliates and zooplankton/meiobenthos (Gilbert, 1989; Gilbert & Jack, 1993).

Compared with other studies, the species richness in ponds I and II was high (88 and 104, respectively), although many species were rare. In Pond I, for example, six of the 88 species made up >50% of the total ciliate abundance. Rare species are often considered to be a ‘passive’ compartment of total richness (Finlay, Maberly & Cooper, 1997; Finlay & Esteban, 1998), yet maintaining an ecological function especially in transient ecological niches. Although the upper end of the range of ciliate richness from permanent ponds is comparable (109 species), the lower end is considerably less so (36 species) (Grolière & Njine, 1973; Dillon & Bierle, 1980; Hatano & Watanabe, 1981; Kusano et al., 1987; Madoni, 1991; Guhl et al., 1994). Of course, species richness is also dependent on the amount of sampling effort (see Wang, 1928) and taxonomic expertise, and on methods of retrieving ‘seedbank’ species – for example, Fenchel, Esteban & Finlay (1997) increased their species list from 20 to 137 by applying various enrichment techniques.

It is curious that the species richness in Pond I was lower (by 15%) than that in Pond II given that the former held water for almost three times as long. Further, the habitat present in Pond II appeared less varied. For example, Pond II is situated in a hayfield with essentially only one type of vegetation (Phalaris sp.), whereas Pond I supports a wide variety of typical wetland plants. In theory, a more heterogeneous habitat should provide a wider range of microhabitats thereby increasing species richness. Species richness in Pond I increased with time in a fashion similar to that noted in permanent freshwater bodies (Müller et al., 1991), but this was not so for Pond II. One cautionary note is that differences between the two ponds may have been affected to some extent by identifications made on live and preserved samples (ponds I and II, respectively). Counting of live samples may underestimate very small ciliates, whereas using a fixative may distort others (see review by Pierce & Turner, 1992).

Some of the Vandorf ponds' genera were in common with those found in European permanent ponds, for example: Paramecium (Grolière & Njine, 1973); Spirostomum, Epistylis and Halteria (Madoni, 1991); Halteria, Euplotes and Prorodon (Finlay & Esteban, 1998); and in Japanese ponds: Halteria, Frontonia and Spirostomum (Hatano & Watanabe, 1981). Loxodes, abundant in Pond II, has been recorded as being an important ciliate in pond sediments (Goulder, 1971b; Finlay & Esteban, 1998). This global distribution of ciliates corresponds well with the notion that microorganisms are ubiquitous because of their small size and high abundance which generate high levels of random dispersal (Finlay, 2002).

Interestingly, Pond II did not show any clear domination of a few single taxa as was the case in Pond I. In Pond I, dominant ciliate taxa alternated or were replaced almost on a weekly basis. Replacement of dominant taxa every 1–4 weeks has been recorded from permanent ponds (Bick, 1973; Kusano et al., 1987). It is known that the abundance of single ciliate species often fluctuates widely in response to availability of a suitable food resource and competition, or predation (Finlay & Esteban, 1998), with seasonal events such as detritus formation by litter feeders in spring, leaf fall in autumn and selective predation, resulting in species replacement (Kusano et al., 1987). Pond II was spatially more homogeneous than Pond I, but temporally more heterogeneous in that each week there was a substantial decrease (∼10 cm) in depth. The latter, perhaps combined with other changes (such as large changes in conductivity), may have created an unstable environment that reduced competition among its species, allowing survival of a greater diversity.

In dynamic habitats, such as temporary ponds, abiotic factors are constantly changing and are reflected in biotic changes such as species composition, species richness and abundance. A seasonal succession of ciliates was evident in both ponds I and II. Such successions have been previously recorded in the ciliates of permanent fresh waters (Beaver & Crisman, 1989; Carrick & Fahnenstiel, 1990; Müller et al., 1991), and are generally considered to be driven by thermal regimes and food resources (Beaver & Crisman, 1989). Other studies, of both freshwater and marine ciliates, have added the following factors: light and oxygen regime, water chemistry, presence of metabolites, and the abundance of predators such as copepods, ostracods and rotifers (Fenchel, 1987; Sleigh, 1989; Pierce & Turner, 1992). Ciliates typically have very short generation times (1–2 days) combined with high reproductive capacities, species substitution therefore can occur rapidly. As habitat conditions change, species appear and disappear in association with a large, local diversity of temporarily rare and encysted species. From this ‘pool’, new species are able to very quickly fill vacant niches (Finlay & Esteban, 1998).

In the Vandorf ponds, species could be categorised into groups according to their time of appearance and length of residence. A number of species appeared early (pioneering or early successional species), of which some disappeared quickly (sporadic residents) whereas others persisted for the entire hydroperiod (regular residents; e.g. Spirostomum ambiguum, and species of Urotricha and Uronema). Some species did not appear until the mid‐aquatic phase (mid‐successional species; e.g. Brachonella spiralis and Obertrumia aurea), and some not until the end of the hydroperiod (late successional species; e.g. Stokesia vernalis, Vorticella aquadulcis and Dileptus bivacuolatus). Further, some species were spatially well‐distributed, whereas others were rare (e.g. found in less than two replicates). It should be noted, however, that these patterns were based on only one full year of intensive sampling. The literature indicates that both consistency (especially in Epistylis and Strobilidium) and inconsistency in occurrence pattern can be expected over several years in permanent waters (Müller et al., 1991).

In our experimental enclosures, in both ponds, total ciliate abundance tended to follow the pattern seen outside enclosures for the first 28 days. Thereafter, in Pond I, ciliate abundance inside the enclosures exceeded that of the pondwater control – primarily because of small ciliates, such as Urotricha, Cyclidium and Uronema, growing rapidly.

Two possibilities may explain the difference in ciliate abundances between the enclosures and the pond water. First, there was more phytoplankton inside the enclosures, as indicated by the chlorophyll a concentrations, and many of the ciliate species recorded were algivores. Although chlorophyll a did not emerge as a significant factor in the stepwise linear regression, Pond I peak in relative abundance of algivorous species corresponded with high chlorophyll a levels between days 42 and 49. Previous studies (see review by Beaver & Crisman, 1989) have found ciliate abundance and biomass to be strongly related to chlorophyll a, and algivorous ciliates in the benthos have been shown to peak in summer when the production rate of benthic algae was high (Stanley, 1972; Fenchel, 1975). In Pond I, the water surface outside the enclosures became densely covered by duckweed (Lemna) from the middle of the hydroperiod onwards, thus reducing the light available to photosynthetic organisms. Accordingly, the pond water had lower chlorophyll a concentrations and thus less food for algivorous ciliates. Madoni (1991) has also shown that a dense cover of Lemna reduces this trophic group. We are uncertain why Lemna, although present, did not thrive in the enclosures. Pond II did not support duckweed, and there the treatments and controls were alike, both in terms of ciliate abundance and chlorophyll a concentrations and the proportion of algal‐feeding species was higher (44%).

Secondly, the enclosures may have restricted the distribution of organisms including potential predators of ciliates, such as suspension feeders and some carnivorous copepods and other crustaceans (Stoecker & Capuzzo, 1990; Jack & Gilbert, 1997). Wiackowski, Brett & Goldman (1994) and Jack & Gilbert (1997) have suggested that seasonal succession in the crustacean zooplankton community may be a strong determinant of ciliate community dynamics and composition, and have shown that the relative frequency of small ciliates increases, alongside a decrease in larger ciliates, as zooplankton increases. There was a higher abundance of zooplankton (especially ostracods, cladocerans, cyclopoid and harpacticoid copepods, and large rotifers) outside the enclosures in both ponds I and II (A. K. Magnusson & D. D. Williams, unpublished data). Overall reduction in zooplankton within the enclosures may well have resulted in the higher abundance of ciliates compared with the ponds themselves.

Despite being in close proximity, the ciliate communities of the two Vandorf ponds were quite different. Both supported a high diversity of species, including many rare species that presumably can exploit the rapidly changing environment that these ponds represent. Length of the hydroperiod was clearly a significant factor in community structure and development, and there was evidence to suggest that dissolved oxygen concentration, amount of light, the availability of phytoplankton as food and the presence of zooplankton as predators, were also influential. Species succession was strongly evident throughout the hydroperiod, as were shifts in cell size. Establishment of the enclosures significantly increased ciliate species richness, probably by broadening the range of niches available.

Acknowledgments

We gratefully acknowledge funding for this project from the Natural Sciences and Engineering Research Council of Canada, and thank Catherine Febria and Dr Dani Boix for help in the field. We are also very grateful to Dr and Mrs Peter van Nostrand for permission to work on their property.

Table Appendix1.

Seasonal development of ciliates in Pond I (total from all enclosures), with notes on ciliate size (1 = 10–50 μm; 2 = 50–200 μm; 3 > 200 μm), habitat preference (p indicates planktonic, all other ciliates are benthic), high abundance species ( *), sporadic species (s), feeding preference [a = algae, b = bacteria, c = cyanobacteria, d = diatoms, h = heterotrophic flagellates, O = omnivorous, P = predator (mostly ciliates and some small metazoans), Hi = histophagous], light requirement (L indicates that light is required by this species), low oxygen demands (O), and presence in treatments (+1, +2 predator addition; −1, −2 partial predator exclusion; c1, c2 enclosure controls; o1, o2 outside enclosures). Species in bold were present in both ponds. Days in bold indicates low levels of dissolved oxygen in the pond water.

Ciliate species	Days after flooding															Size	Prey	Light/ Oxygen	Treatment
	1	7	14	21	28	35	42	49	56	63	70	77	84	91	98				+1	+2	−1	−2	c1	c2	o1	o2
Stentor polymorphus (Mueller 1773) Ehrenberg (1830)	80	120	60	80												3	O	O	+	+	–	–			o	o
Stentor multiformis (Mueller 1786) Ehrenberg (1838)		10		20												3 s	ab	O								o
Chilodonella cucullulus Mueller (1786)			40		20											2 s					–
Strombidium viride Stein (1867)	100	80	40	20		40	530									2p	abd	L	+	+			c		o	o
Loxodes rostrum (Mueller 1773), Ehrenberg (1830)				20	140		40									2	O	O						c
Stentor coeruleus (Pallas 1766) Ehrenberg (1831)		10		80	40	140	20	20								3	O	O				–	c		o	o
Euplotes alatus Kahl (1932)			40		20	140	40	60	20							2		L	+	+
Lacrymaria olor (Mueller 1786) Bory de Saint‐Vincent (1824)			20	40		120	20			40						3	P		+	+
Litonotus fusidens (Kahl 1926) Foissner et al. (1995)1 , [link]			20		60		40	20			40					2	P		+					c
Nassula ornata Ehrenberg (1833)								100	40	20	20					3	c		+	+					o
Stylonychia mytilus Foissner et al. (1991)1 , [link]			140	220	360	480	420	100	160	120	80	60				3*	O		+	+	–	–		c	o	o
Loxodes striatus (Engelmann 1862), Penard (1917)			80	100	40	20	40	40				20				3	acd	O	+	+	–	–				o
Stylonychia pustulata (Mueller 1786) Ehrenberg (1835)			20			20	240			40		20				2	O		+				c
Brachonella spiralis (Smith 1897) Jankowski (1964)					40			80		10		40				2	ah		+	+						o
Obertrumia aurea (Ehrenberg 1833) Foissner (1987)								140			20	40				3	c		+	+
Askenasia volvox (Eichwald 1852) Kahl (1930)										60	660	100	60			1p	ad		+	+	–	–
Stentor igneus Ehrenberg (1838)										40			20			3 s	abd	O					c
Phascolodon vorticella Stein (1859)		20		180	320	10	20				20		60			2p	ad			+		–	c		o
Gastrostyla steinii Engelmann (1862)		10										20	40	40		2	O		+	+
Spathidium spathula (Mueller 1786), Woodruff & Spenser (1922)		10											40	50		2	P			+						o
Metopus galeatus Kahl (1927)							40		20			40		20		2	abh			+				c	o
Acineta grandis Kent (1881)												40		80		3 s	P									o
Stokesia vernalis Wenrich (1929)												20		20		2 ps	abd								o
Amphileptus pleurosigma (Stokes 1884) Foissner (1984)														60	190	3	P			+			c
Monilicaryon monilatus (Stokes 1886) Jankowski (1967)														40	100	3	O									o
Astylozoon faurei Kahl (1935)														120	420	1p	b				–	–				o
Paraurostyla viridis (Stein 1859) Borror (1972)														10	200	2	b									o
Paraurostyla weissei (Stein 1859) Borror (1972)														500	300	3	O					–		c
Glaucoma scintillans Ehrenberg (1830)														240	300	2	b			+	–
Vorticella infusionum Foissner et al. (1992)1 , [link]														100	300	2	b				–
Vorticella marginata Stiller (1931)														200	400	2	b				–
Ctedoctema acanthocryptum Stokes (1884)													100		200	1	b				–
Aspidiska cicada (Mueller 1786) Claparede & Lachmann (1858)													40		200	1	b		+	+
Placus luciae Kahl (1930)													20	100	550	2	O			+						o
Disematostoma buetschlii Lauterborn (1894)													40	20	200	2p	ab	L	+	+
Holophrya spirogyrophaga Leipe (1989)													20	40	300	3										o
Colpidium kleini Foissner (1969)												40			1600	2 s	b								o
Opisthonecta henneguyi Faure‐Fremiet (1906)												180	240	920	540	2	bh			+	–	–	c	c
Spirostomum minus Roux (1901)											60			260	500	3	b	O	+		–	–			o	o
Strobilidium caudatum (Fromentel 1876) Foissner (1987)											20		40	40	520	2	abd	L	+		–
Oxytricha similis Engelmann (1862)											20	40	120	680	140	2	b			+	–	–	c	c	o
Prorodon cinereus Penard (1922)									60	80			20	330	90	3	P			+	–	–		c		o
Urotricha globosa Schewiakoff (1892)								100							50	1 ps	ab								o
Vorticella aquadulcis Foissner et al. (1992)1 , [link]								20			20				100	1	ab									o
Trachelophyllum vestitum Stokes (1884)								20					70	200	800	3*			+	+	–	–				o
Campanella umbellaria (Linnaeus 1758) Goldfuss (1820)								60				20	40	80	20	2	b		+		–					o
Prorodon margaritifer Claparede & Lachmann (1858)								60			40	10	60	200	1450	3*	P		+	+	–	–	c	c	o	o
Metopus es (Mueller 1776) Lauterborn (1916)							80			20		100	840	2420	3000	2*	ah		+	+	–		c
Uroleptus caudatus Claparede & Lachmann (1858)							1340	120		50		220	1540		500	2*	ah		+	+	–	–	c
Holosticha kessleri Wrzesniowski (1877)							60	240	240	40	180	160	160		1800	2*	bd		+	+		–	c	c	o	o
Vorticella microstoma Foissner et al. (1992)1 , [link]						240	120	20	240	20				160	80	2	ab									o
Holophrya teres (Ehrenberg 1833) Foissner et al. (1994)1 , [link]						120	400	40				40			550	2	O		+	+				c
Dileptus bivacuolatus Da Cunha (1915)						40							50	60	250	2			+		–		c
Pleurotricha grandis Stein (1859)						240			40		20		180	2700	340	3*	ab		+	+	–	–	c	c	o	o
Oxytricha chlorelligera Kahl (1932)						1050	400	20	140		60		340	100	1500	2	bdh		+	+	–		c
Holophrya gracilis Penard (1922)						40	720	40	100	40	180	620	80	360	5000	2*			+	+	–	–	c	c
Pelatractus lacrymariaeformis Kahl (1930)						600	560	40	860	80	140	440	80	310	1860	2*				+	–	–	c	c	o	o
Aspidiska lynceus (Mueller 1773) Ehrenberg (1830)					60	80									50	1	b		+	+
Vorticella campanula Ehrenberg (1831)					1020	530	780	20	240	60	240	20			100	2	ab		+	+	–	–	c	c	o	o
Urotricha venatrix Kahl (1935)					80	140	200		100	40	20	80			50	2			+	+
Holosticha pullaster (Mueller 1773) Foissner et al. (1991)1 , [link]					140		240	60	40	100	20	200	240	1170	260	2	abd		+	+	–	–	c	c	o
Prorodon niveus Ehrenberg (1833)				120	80	50				20			160	20	60	3	P			+		–	c	c	o	o
Phialina pupula Mueller (1786)				20					280	400	260	80	100	320	300	2	P		+	+	–	–		c		o
Frontonia acuminata (Ehrenberg 1833) Buetschli (1889)			20		60	160	400	40	40	20				200	200	2	O	L/O	+	+	–		c			o
Opisthotricha elongata Smith (1897)			20	120	1600	500	800	20	20			100		680	150	3*			+	+	–
Spirostomum teres Claparede & Lachmann (1858)			20				840				20		40	160	400	3p*	abd	O	+	+	–	–	c		o	o
Euplotes patella (Mueller 1773) Ehrenberg (1831)			20			370	920	200	260	80	160	60	140	80	100	2	O	L	+	+	–	–	c	c	o	o
Philasterides armatus Kahl (1931)			40		20	400	200	140	20	320	60	160	360		1900	2*	Hi		+	+	–	–	c	c	o
Holophrya discolor Ehrenberg (1833)			80		80	200	280	20	640	40	40	40		180	50	2	O		+	+	–	–	c		o	o
Pelagohalteria cirrifera (Kahl 1932) Foissner et al. (1988) 1			10	60			30600	36090	420	12080	43640	39580	4260	10680	27440	1p*	a		+	+	–	–	c	c	o	o
Euplotes muscicola Kahl (1932)			40	20	60		80	40	40	60	160	120	40	320	150	2		L	+	+	–		c	c	o	o
Urotricha agilis (Stokes 1886) Kahl (1930)			20	60	40	80	4220	1260	210	200	690	460	100	460	5460	1*	bh		+	+	–	–	c	c	o
Cyclidium glaucoma Mueller (1773)			100	260	1280	4640	6920	4140	500	4280	16460	30480	560	1860	12400	1*	b		+	+	–	–	c	c	o	o
Phialina coronata Claparede & Lachmann (1858)		20	20											100	200	3	P							c		o
Sterkiella histriomuskorum Foissner et al. (1991)1 , [link]		80	120	140	520	150	180	60	40			80			200	2	O		+	+	–	–		c	o
Frontonia atra (Ehrenberg 1833) Buetschli (1889)		20		20	120	540	300	40	40		60	220	20	20	100	3	d	L/O	+	+	–	–		c	o	o
Chilodonella uncinata (Ehrenberg 1838) Strand (1928)		40		100	80	40	60	100	280	660	1130	1760	1560	1420	1080	1*	b		+	+	–	–	c		o	o
Spirostomum ambiguum (Mueller 1786) Ehrenberg (1835)	10	50	20		140		300		20		20			260	950	3*	abh	O	+	+	–	–	c		o	o
Paramecium aurelia Foissner et al. (1994)1 , [link]	50	40	100		30						40	120	520	1600	1840	2*	b		+	+	–	–	c	c	o
Urostyla grandis Ehrenberg (1830)	135				80				120		120	100	200	1000	2490	3*	O		+	+	–	–	c	c	o	o
Nassula picta Greeff (1888)	20						240	380	240	140	140	100	100	180	170	2	c (O)		+	+	–	–	c	c	o
Paramecium caudatum Ehrenberg (1833)	210	130	100	80		80			80	140	160	920	920	8480	6600	3*	ab		+	+	–	–	c	c	o	o
Frontonia leucas Ehrenberg (1838)	10	10		20	40	430	880	20	40		100	100	220	910	1200	3*	O	L/O	+	+	–	–	c	c	o	o
Halteria grandinella (Mueller 1773) Dujardin (1841)	35	220	60	80	590	1020	20500	30240	900	14200	91220	39480	4240	23300	45700	1*	ab		+	+	–	–	c	c	o	o
Urotricha farcta Claparede & Lachmann (1859)	400	890	400	560	2300	3880	7380	6600	1520	20560	52500	26260	1780	1360	34400	1*	abh		+	+	–	–	c	c	o	o
Urotricha furcata Schewiakoff (1892)	20	20	80	500	1500	4220	8100	6380	1920	22460	52400	26260	2000	1650	36700	1p*	ab		+	+	–	–	c	c	o	o
Uronema nigricans (Mueller 1786) Florentin (1901)	315	70	540	540	1420	3600	4820	5080	460	4280	14340	30580	520	1770	11900	1*	bh		+	+	–	–	c	c	o	o
Urotricha pelagica Kahl (1935)	75	10	60	120	120	880	2040	200	1000	220	10480	4280	600	620	2140	1p*	ab		+	+	–	–	c	c	o	o

¹ Foissner, Blatterer, Berger & Kohmann (1991); Foissner, Berger, Blatterer & Kohmann (1995); Foissner, Berger & Kohmann (1992, 1994); Foissner, Skogstad & Pratt (1988).

Table Appendix2.

Seasonal development of ciliates in Pond II. (see legend to Appendix 1 for explanations)

Ciliate species	Days after flooding						Size	Prey	Light/ Oxygen	Treatment
	1	6	13	20	27	34				+1	+2	−1	−2	c1	c2	o1	o2
Astylozoon fallax Engelmann (1862)		200					2 ps	b									o
Euplotes patella (Mueller 1773) Ehrenberg (1831)		100					2	O	L								o
Stentor coeruleus (Pallas 1776) Ehrenberg (1831)		100					3	O	O			–
Strongylidium lanceolatum Kowalewski (1883)		200					2 s							c
Plagiopyla nasuta Stein (1860)		400	200				2	abh				–				o
Pseudochilodonopsis fluviatilis Foissner (1988)		4800	850				2*	d			+	–	–			o	o
Trachelophyllum vestitum Stokes (1884)		800	250				3				+	–	–				o
Cohnilembus verminus Mueller (1786)		400	400				2				+						o
Paracolpidium truncatum (Stokes 1885) Ganner & Foissner (1989)		300	200				2	b					–
Litonotus varsaviensis Wrzesniowski (1870)			100				2	P				–
Lembadion lucens (Maskell 1887) Kahl (1931)			400				2 s	O			+	–
Aspidiska lynceus (Mueller 1773) Ehrenberg (1830)			100				1	b									o
Tintinnidium pusillum Entz (1909)			400				2 s	abd			+				c
Stichotricha secunda Perty (1849)			100				2	abd					–
Bursaridium pseudobursaria (Faure‐Fremiet 1924) Kahl (1927)		300		400			2p	a							c		o
Codonella cratera (Leidy 1877) Imhof (1885)		400		200			2p	d a?								o
Pseudocohnilembus pusillum (Quennerstedt 1869) Foisner & Wilbert (1981)		1500	200	100			1	b		+		–		c
Dysteria navicula Kahl (1928)			100	500			1										o
Obertrumia aurea (Ehrenberg 1833) Foissner (1987)			1700	400			3	c			+	–	–	c	c	o
Urotricha ovata Kahl (1926)			2000	400			1	a			+			c	c
Disematostoma buetschlii Lauterborn (1894)			700	200			2p	ab	L	+				c		o
Condylostoma vorticella Ehrenberg (1833)			600	900			2					–	–	c			o
Metopus campanula Kahl (1932)			500	100			2	abh		+	+	–				o
Paradileptus elephantinus (Scev. 1897) Kahl (1931)				400			3 ps	O									o
Phialina coronata Claparede & Lachmann (1858)				600			3 s	P			+						o
Strongylidium californicum Kahl (1932)				200			3 s					–
Brachonella spiralis (Smith 1897) Jankowski (1964)				1200			2 s	ah									o
Stylonychia pustulata (Mueller 1786) Ehrenberg (1835)	190	3500	2700	2000	200		2*	O		+		–	–	c	c	o	o
Didinium nasutum (Mueller 1773) Stein (1859)	20	1500	1150	1800	1200		2*	P		+		–	–	c	c	o	o
Paramecium caudatum Ehrenberg (1833)	40	100		500	1100		3	ab			+	–		c	c	o	o
Stentor polymorphus (Mueller 1773) Ehrenberg (1830)	20		900	3000	1400		3*	O	O	+	+	–	–			o	o
Holosticha algivora Kahl (1932)		2700	500	200	200		2	ah						c	c		o
Strombidium viride Stein (1867)		100	550	500	100		2p	abd	L	+	+	–		c
Holophrya teres (Ehrenberg 1833) Foissner et al. (1994) 1		400	200	800	200		3	O				–	–		c	o	o
Loxodes striatus (Engelmann 1862) Penard (1917)		100	300	200	300		3	acd					–
Histriculus vorax (Stokes 1891) Corliss (1960)		300	200		100		2	b								o
Vorticella campanula Ehrenberg (1831)		700		700	1700		2	ab				–		c	c
Spathidium spathula (Mueller 1786) Woodruff & Spenser (1922)		700		1000	100		2	P				–	–		c	o
Lacrymaria olor (Mueller 1786) Bory de Saint‐Vincent (1824)		300			100		3	P							c
Paramecium aurelia Foissner, Berger & Kohmann (1992)			700	900	500		2	b		+	+	–	–		c	o	o
Climacostomum virens (Ehrenberg 1838) Stein (1859)			100	200	300		3						–				o
Enchelys pupa Mueller‐Ehrenberg‐Schewiakoff (1893)			1200	700	100		2			+	+	–		c	c
Colpidium colpoda (Losana 1829) Stein (1860)			100	600	1100		2	abh		+	+					o
Spathidium breve Kahl (1930)			600	700	200		2	P			+		–				o
Condylostoma arenarium Spiegel (1926)				300	200		3					–	–
Pseudoblepharisma tenue Kahl (1926)				200	200		2	b								o
Tintinnidium fluviatile (Stein 1863) Kent (1881)				300	300		2p	ad		+		–
Lembadion bullinum (Mueller 1786) Perty (1849)					200		2	O									o
Opercularia cylindrata Wrzesniowski (1870)					3500		2 s										o
Opisthotricha elongata Smith (1897)					300		3 s									o
Trachelophyllum sigmoides Kahl (1926)						300	3										o
Metopus es (Mueller 1776) Lauterborn (1916)						100	2	abh								o
Spirostomum loxodes Stokes (1885)						500	3	ab	O		+			c
Chilodontopsis depressa (Perty 1852) Blochmann (1895)					300	600	2	abd								o
Cinetochilum margaritaceum (Ehrenberg 1831) Perty (1849)					1300	1400	1	ab		+	+				c	o
Marituya pelagica Gajewskaja (1928)					100	200	2p	acd (O)								o
Frontonia leucas Ehrenberg (1838)			300		2100	100	3*	O	L/O	+	+	−		c			o
Dysteria ovalis Gourret & R. (1886)			100			400	2								c	o
Loxophyllum meleagris (Mueller 1773) Dujardin (1841)			2000			200	3	P							c
Phialina vermicularis Mueller‐Ehrenberg (1831)			200			200	2	P				–
Dileptus bivacuolatus Da Cunha (1915)			200	300		400	2								c		o
Bursaria truncatella Mueller (1773)			2100	1300		100	3*	O		+				c	c		o
Pseudochilodonopsis piscatoris (Blochmann 1895) Foissner (1979)			600	700		3100	2	ad		+	+	–	–	c	c	o
Epistylis chrysemydis Bishop & Jahn (1941)			400	12200	15300	1800	2*	ab		+	+		–	c	c	o	o
Chilodonella uncinata (Ehrenberg 1838) Strand (1928)			2100	11200	3700	200	1*	b		+	+	–	–	c		o	o
Stokesia vernalis Wenrich (1929)			1000	600	1400	100	2p	abd		+	+	–	–		c		o
Vorticella aquadulcis Foissner et al. (1992)			200	5100	1800	1700	1*	ab		+	+	–	–		c		o
Metopus pulcher Kahl (1927)		400				2300	2	abh									o
Podophrya soliformis (Lauterborn 1908) Kahl (1931)		100			100	100	2				+						o
Oxytricha fallax Stein (1859)		100		500		1000	2	O				–
Uroleprus dispar Stokes (1886)		1200		400	500	400	2					–			c	o
Paraurostyla viridis (Stein 1859) Borror (1972)		300	400		200	100	2	b						c
Stylonychia vorax Stokes (1885)		300	500			200	2	O		+						o
Actinobolina vorax (Wenrich 1929) Kahl (1930)		600	200	300		200	2	P				–
Loxodes rostrum (Mueller 1773) Ehrenberg (1830)		200	500	1200		300	2	O	O	+		–	–	c	c	o
Trachelophyllum apiculatum (Perty 1852) Claparede & Lachmann (1859)		1400	350	200		100	2	O		+	+	–		c	c	o	o
Tachysoma pellionellum (Mueller 1773) Borror (1972)		4300	2800	600		1100	2*	abcd		+	+			c		o	o
Euplotes taylori Garnjobst (1928)		6400	100	200		500	2*		L			–		c			o
Phascolodon vorticella Stein (1859)		300	200	200	400	200	2p	ad		+					c	o	o
Phialina pupula Mueller (1786)		200	1200	1400	200	900	2	P		+	+	–	–	c		o	o
Oxytricha similis Engelmann (1862)		1200	1000	1100	100	5000	2	b									o
Prorodon niveus Ehrenberg (1833)		100	50	1100	1200	700	3*	P		+	+	–			c		o
Frontonia acuminata (Ehrenberg 1833) Buetschli (1889)		400	4800	9000	6400	4900	2*	O	L/O	+	+	–	–	c	c	o	o
Cyclidium glaucoma Mueller (1773)		2700	3500	3800	2100	2200	1*	b		+	+	–	–	c	c	o	o
Pelagohalteria cirrifera (Kahl, 1932) Foissner et al. (1988) 1		5400	1400	400	350	1100	1p*	a		+		–	–	c		o	o
Holophrya discolor Ehrenberg (1833)		1400	2750	2500	900	1300	2*	O		+	+	–	–		c	o	o
Holophrya gracilis Penard (1922)		4800	900	1400	1200	700	2*			+	+	–	–		c	o	o
Pleuronema coronatum Kent (1881)		1000	1700	3100	2600	700	2*	O		+	+	–	–	c	c	o	o
Carchesium pectinatum (Zacharias 1897) Kahl (1935)		500	2000	3700	6200	5300	2p*	b?		+	+	–			c	o	o
Monodinium balbiani Fabre‐Domergue (1888)		800	1600	2800	2200	1000	2*	P		+	+	–	–	c	c	o	o
Vorticella microstoma Foissner et al. (1992)		1100	1600	2800	1600	3100	2*	ab		+	+		–	c	c	o	o
Vorticella natans Faure‐Fremiet (1924)		500	100	400	2100	100	2p*	ab			+				c		o
Euplotes muscicola Kahl (1932)		500	600	900	200	500	2		L	+	+			c	c	o
Halteria grandinella (Mueller 1773) Dujardin (1841)		12400	1400	1500	1400	2300	1*	ab		+	+	–	–	c	c	o	o
Askenasia volvox (Eichwald 1852) Kahl (1930)		1100	400	300	200	100	1p	ad					–		c	o	o
Spirostomum teres Claparede & Lachmann (1858)	10		300			100	3p	abd	O				–	c
Uroleptus gallina (Mueller 1786) Foissner et al. (1991)1 , [link]	440	1800	1250			200	2*	a			+	–	–	c	c	o
Spirostomum ambiguum (Mueller 1786) Ehrenberg (1835)	60	3300	500	300		4900	3*	abh	O	+	+	–	–	c	c		o
Urotricha pelagica Kahl (1935)	40	10600	5800	5700	3000	6500	1p*	ab		+	+	–	–	c	c	o	o
Urotricha farcta Claparede & Lachmann (1859)	20	7000	10100	10500	6100	4900	1*	abh		+	+	–	–	c	c	o	o
Urotricha furcata Schewiakoff (1892)	40	7500	9700	10500	6300	5500	1p*	ab		+	+	–	–	c	c	o	o
Uronema nigricans (Mueller 1786) Florentin (1901)	190	3100	3100	3300	2000	2100	1*	bh		+	+	–	–	c	c	o	o
Spirostomum minus Roux (1901)	50	3700	550	400	100	2600	3*	b	O	+	+	–	–	c	c	o	o
Loxodes magnus Stokes (1887)	40	100	300	200	600	300	3	O	O	+	+	–	–			o	o

¹ See footnote of Appendix 1 for explanation.