Microb Ecol (1989) I8:261-273
MICROBIAL ECOLOGY 9 Springer-Verlag N e w York Inc. 1989
The Relative Importance of Different Ciliate Taxa in the Pelagic Food Web of Lake Constance Helga Miiller Limnological Institute, University of Konstanz, P.O. Box 5560, D-7750 Konstanz, Federal Republic of Germany
Abstract. Abundance, biovolume, and species composition of pelagic ciliates in Lake Constance were recorded over two annual cycles (1987/88). Production was estimated from mean annual biovolumes and size-specific growth rates obtained from the literature. Cell concentrations and biovolumes ranged from 0.1 to 120 cells m1-1 and from 3 to 1,200 m m 3 m -3, respectively. Mean annual values were, respectively, 6.8 cells ml-' and 94 m m 3 m -3 in 1987, and 12.0 cells ml -~ and 130 m m 3 m -3 in 1988. In both years, prostome nanociliates (< 20/~m) dominated numerically, while strobiliids in the size range 20-35 um contributed most significantly to ciliate production. Ciliate community production, according to a crude calculation, yielded approximately 10-15 g C m -z year-'.
Introduction
The ecological significance ofciliates in the food web of pelagic systems is well documented. Within the last decade, ciliate abundance, biomass, and species composition in marine and fresh waters have been investigated at various locations, as reviewed by Porter et al. [32], Fenchel [13], and Beaver and Crisman [4]. Ciliate communities in lakes are mixed assemblages of species that differ greatly in size; cell volumes of pelagic ciliates range over 3 orders of magnitude. Generally, small species dominate numerically, while large forms, though low in numbers, contribute significantly to total ciliate biomass. Therefore, if the relative importance of different ciliate taxa is judged by cell concentrations, ecological relevance of small species may be overestimated. Large forms, in contrast, will be overrepresented if the comparison is based on biomass data. Production estimates are a more adequate tool for evaluating the contribution of different taxonomic groups to the transfer of matter in food webs. Whereas ciliate production over short time intervals has been measured in situ [6, 42, 50], a different approach is needed to estimate production over larger periods of time. Maximum growth rates of ciliates under optimal food conditions are a function of cell volume and temperature [11, 15]. Therefore, production of ciliate taxa or size classes has been calculated from biomass field data and from size-specific growth rates measured in laboratory cultures [16, 26, 27]. Under
262
H. Miiller
suboptimal conditions, the growth rates of ciliates also depend on the quality a n d q u a n t i t y o f f o o d [2, 2 3 , 34, 4 4 , 4 5 , 4 9 , 51]. F o o d l i m i t a t i o n , t h e r e f o r e , must also be considered in estimates of ciliate production in natural waters. In this study, the importance of different ciliate taxa in Lake Constance relative to each other was evaluated on the basis of abundance and biomass field data. Potential production of the different taxa was roughly estimated from mean annual biovolumes and size-specific growth rates derived from literature data. The data presented here also allow estimation of the order of magnitude of ciliate community production in Lake Constance.
Methods Samples were taken weekly (biweekly during the cold season) at the site of maximum depth (147 m) of "0berlinger See," the northwestern part of Lake Constance, from February 1987 through December 1988. A 2 m long 4 liter capacity water sampler was used to collect an entire water column from the upper 20 m, by ten hauls. Ciliates were counted with the Uterm6hl technique in samples fixed with Lugol's solution (final concentration: 0.4 g K.I liter -1, 0.2 g J liter 1) integrated over the depth intervals 0-4 m, 4-8 m, and 8-20 m in 1987, and from 0-8 m and 8-20 m in 1988. Bottoms of 50 ml settling chambers were scanned at 160-fold magnification. Up to 30 different forms were grouped into five size classes (100 ~m), and were recorded separately. The smallest ciliates observed were less than 10 ~tm in diameter. Additional subsamples were fixed with HgC12 (final concentration: 0.6 mg m1-1) at each sampling occasion in 1987 and monthly in 1988. From this material, protargol-stained permanent slides were prepared with a technique [28] slightly modified from those of Tuffrau [48] and Foissner [18] and personal communication. These preparations served for taxonomic identification of the forms distinguished in the Uterm6hl counts. Examination of these slides at 400- and 1,000-fold magnification also revealed that there was no significant group of ciliates smaller than 10 gm which might have been overlooked in the routine counts. With respect to ciliate taxonomy, the scheme of Corliss [7] was followed. Identifications were based on the publications of Kahl [25], Dragesco [10], Bick [5], Foissner and Wilbert [17], Curds [8], and Curds et at. [9]. Ciliates were usually identified to genus (in three cases, to species). Genera identified by protargol staining, that could not be distinguished in the Lugol-fixed material, were placed in the same counting group. Genera that covered a large size range were separately recorded in different size classes (Table 1). The protargol preparations were also used to estimate mean cell volumes separately for each counting group. The linear dimensions of the ciliates were measured by a microscope with imageanalysis system (KONTRON, MOP-Videoplan) and the respective cell volumes were calculated by approximation to prolate spheroids. Generally, biovolume estimates were based on measurement of 50-150 cells selected randomly from material prepared in different seasons. Seasonal variability in cell size of a counting group was not significantly greater than the variation in size observed in the same group within a single sample. The only exception was a population of Histiobalantium present from February to May 1987, which was of considerably larger cell size compared to the rest of the investigation period, and was treated as a separate group (Table 1). Cell shape of most ciliates was well preserved by the protargol technique. For one species, Epistylis rotans, cell volumes of 60 protargol-stained cells were compared to cell volumes estimated from photographs of 60 live cells. A 10% difference observed between the mean cell volume of fixed and live ceils was not statistically significant. Therefore, no correction factor was used to compensate for shrinkage due to fixation. The protargol technique is not suited for preparation of large Heterotrichida that will rupture during this procedure; the cell volumes of this group were estimated from live and Lugolfixed material. The biovolume was converted to carbon according to Fenchel and Finlay [14] using a conversion factor of 0.071 g C (ml cell volume) -1. Generation times (G) and intrinsic growth rates (rm) at 8.5"C were calculated from mean cell volumes (V) according to Finlay [15]: log G = 0.3317-1og V + 0.3615; rm = In 2.(G) -t. Using rm
263
Relative Importance of Ciliates Table 1,
Relevant ciliate genera in Lake Constance, size classes and cell volumes (V) Size class
Prostomatida Pseudobalanion pL Urotricha furcata
V (jttm0
G (8.5"C) (hours)
r~ (8.5"C) (d -l)
(r) (d-')
0.75
1 1
1,300 1,700
24.8 27.1
0.67 0.61
2 3 5
7,200 37,000 820,000
43.7 75.3 210.4
0.38 0.22 0.08
3 4 4
34,000 68,000 176,000
73.2 92.1 126.3
0.23 0.18 0.13
Pcritrichida Vorticella on Anabaena on diatoms on diatoms Epistylis rotans
2 2 3 4
16,000 10,000 37,000 24,000
57.0 48.8 75.3 65.2
0.29 0.34 0.22 0.25
Heterotrichida Stentor/Condylostoma
5
1,300,000
245.2
0.07
1 2 3 4 4 4
2,700 6,500 32,000 77,000 119,000 24,000
31.6 42.3 71.7 96.0 110.9 65.2
0.52 0.39 0.23 0.17 0.15 0.25
Haptorida Askenasia
Paradileptus Scuticociliatida Histiobalantium Feb-May 1987
Oligotrichida Halteria/Strobilidium Strobilidiurn sp. Strombidium .
Strobilidium Codonella/ Tintinnidium
[
f
j
0.35
Size classes 1-5 refer to largest cell diameters of 100 ~m, respectively. Generation times (G) and intrinsic growth rates (r=) at 8.5"C were calculated according to the method of Finlay [15]. Highest observed net growth rates (r) of Prostomatida (
MICROBIAL ECOLOGY 9 Springer-Verlag N e w York Inc. 1989
The Relative Importance of Different Ciliate Taxa in the Pelagic Food Web of Lake Constance Helga Miiller Limnological Institute, University of Konstanz, P.O. Box 5560, D-7750 Konstanz, Federal Republic of Germany
Abstract. Abundance, biovolume, and species composition of pelagic ciliates in Lake Constance were recorded over two annual cycles (1987/88). Production was estimated from mean annual biovolumes and size-specific growth rates obtained from the literature. Cell concentrations and biovolumes ranged from 0.1 to 120 cells m1-1 and from 3 to 1,200 m m 3 m -3, respectively. Mean annual values were, respectively, 6.8 cells ml-' and 94 m m 3 m -3 in 1987, and 12.0 cells ml -~ and 130 m m 3 m -3 in 1988. In both years, prostome nanociliates (< 20/~m) dominated numerically, while strobiliids in the size range 20-35 um contributed most significantly to ciliate production. Ciliate community production, according to a crude calculation, yielded approximately 10-15 g C m -z year-'.
Introduction
The ecological significance ofciliates in the food web of pelagic systems is well documented. Within the last decade, ciliate abundance, biomass, and species composition in marine and fresh waters have been investigated at various locations, as reviewed by Porter et al. [32], Fenchel [13], and Beaver and Crisman [4]. Ciliate communities in lakes are mixed assemblages of species that differ greatly in size; cell volumes of pelagic ciliates range over 3 orders of magnitude. Generally, small species dominate numerically, while large forms, though low in numbers, contribute significantly to total ciliate biomass. Therefore, if the relative importance of different ciliate taxa is judged by cell concentrations, ecological relevance of small species may be overestimated. Large forms, in contrast, will be overrepresented if the comparison is based on biomass data. Production estimates are a more adequate tool for evaluating the contribution of different taxonomic groups to the transfer of matter in food webs. Whereas ciliate production over short time intervals has been measured in situ [6, 42, 50], a different approach is needed to estimate production over larger periods of time. Maximum growth rates of ciliates under optimal food conditions are a function of cell volume and temperature [11, 15]. Therefore, production of ciliate taxa or size classes has been calculated from biomass field data and from size-specific growth rates measured in laboratory cultures [16, 26, 27]. Under
262
H. Miiller
suboptimal conditions, the growth rates of ciliates also depend on the quality a n d q u a n t i t y o f f o o d [2, 2 3 , 34, 4 4 , 4 5 , 4 9 , 51]. F o o d l i m i t a t i o n , t h e r e f o r e , must also be considered in estimates of ciliate production in natural waters. In this study, the importance of different ciliate taxa in Lake Constance relative to each other was evaluated on the basis of abundance and biomass field data. Potential production of the different taxa was roughly estimated from mean annual biovolumes and size-specific growth rates derived from literature data. The data presented here also allow estimation of the order of magnitude of ciliate community production in Lake Constance.
Methods Samples were taken weekly (biweekly during the cold season) at the site of maximum depth (147 m) of "0berlinger See," the northwestern part of Lake Constance, from February 1987 through December 1988. A 2 m long 4 liter capacity water sampler was used to collect an entire water column from the upper 20 m, by ten hauls. Ciliates were counted with the Uterm6hl technique in samples fixed with Lugol's solution (final concentration: 0.4 g K.I liter -1, 0.2 g J liter 1) integrated over the depth intervals 0-4 m, 4-8 m, and 8-20 m in 1987, and from 0-8 m and 8-20 m in 1988. Bottoms of 50 ml settling chambers were scanned at 160-fold magnification. Up to 30 different forms were grouped into five size classes (100 ~m), and were recorded separately. The smallest ciliates observed were less than 10 ~tm in diameter. Additional subsamples were fixed with HgC12 (final concentration: 0.6 mg m1-1) at each sampling occasion in 1987 and monthly in 1988. From this material, protargol-stained permanent slides were prepared with a technique [28] slightly modified from those of Tuffrau [48] and Foissner [18] and personal communication. These preparations served for taxonomic identification of the forms distinguished in the Uterm6hl counts. Examination of these slides at 400- and 1,000-fold magnification also revealed that there was no significant group of ciliates smaller than 10 gm which might have been overlooked in the routine counts. With respect to ciliate taxonomy, the scheme of Corliss [7] was followed. Identifications were based on the publications of Kahl [25], Dragesco [10], Bick [5], Foissner and Wilbert [17], Curds [8], and Curds et at. [9]. Ciliates were usually identified to genus (in three cases, to species). Genera identified by protargol staining, that could not be distinguished in the Lugol-fixed material, were placed in the same counting group. Genera that covered a large size range were separately recorded in different size classes (Table 1). The protargol preparations were also used to estimate mean cell volumes separately for each counting group. The linear dimensions of the ciliates were measured by a microscope with imageanalysis system (KONTRON, MOP-Videoplan) and the respective cell volumes were calculated by approximation to prolate spheroids. Generally, biovolume estimates were based on measurement of 50-150 cells selected randomly from material prepared in different seasons. Seasonal variability in cell size of a counting group was not significantly greater than the variation in size observed in the same group within a single sample. The only exception was a population of Histiobalantium present from February to May 1987, which was of considerably larger cell size compared to the rest of the investigation period, and was treated as a separate group (Table 1). Cell shape of most ciliates was well preserved by the protargol technique. For one species, Epistylis rotans, cell volumes of 60 protargol-stained cells were compared to cell volumes estimated from photographs of 60 live cells. A 10% difference observed between the mean cell volume of fixed and live ceils was not statistically significant. Therefore, no correction factor was used to compensate for shrinkage due to fixation. The protargol technique is not suited for preparation of large Heterotrichida that will rupture during this procedure; the cell volumes of this group were estimated from live and Lugolfixed material. The biovolume was converted to carbon according to Fenchel and Finlay [14] using a conversion factor of 0.071 g C (ml cell volume) -1. Generation times (G) and intrinsic growth rates (rm) at 8.5"C were calculated from mean cell volumes (V) according to Finlay [15]: log G = 0.3317-1og V + 0.3615; rm = In 2.(G) -t. Using rm
263
Relative Importance of Ciliates Table 1,
Relevant ciliate genera in Lake Constance, size classes and cell volumes (V) Size class
Prostomatida Pseudobalanion pL Urotricha furcata
V (jttm0
G (8.5"C) (hours)
r~ (8.5"C) (d -l)
(r) (d-')
0.75
1 1
1,300 1,700
24.8 27.1
0.67 0.61
2 3 5
7,200 37,000 820,000
43.7 75.3 210.4
0.38 0.22 0.08
3 4 4
34,000 68,000 176,000
73.2 92.1 126.3
0.23 0.18 0.13
Pcritrichida Vorticella on Anabaena on diatoms on diatoms Epistylis rotans
2 2 3 4
16,000 10,000 37,000 24,000
57.0 48.8 75.3 65.2
0.29 0.34 0.22 0.25
Heterotrichida Stentor/Condylostoma
5
1,300,000
245.2
0.07
1 2 3 4 4 4
2,700 6,500 32,000 77,000 119,000 24,000
31.6 42.3 71.7 96.0 110.9 65.2
0.52 0.39 0.23 0.17 0.15 0.25
Haptorida Askenasia
Paradileptus Scuticociliatida Histiobalantium Feb-May 1987
Oligotrichida Halteria/Strobilidium Strobilidiurn sp. Strombidium .
Strobilidium Codonella/ Tintinnidium
[
f
j
0.35
Size classes 1-5 refer to largest cell diameters of 100 ~m, respectively. Generation times (G) and intrinsic growth rates (r=) at 8.5"C were calculated according to the method of Finlay [15]. Highest observed net growth rates (r) of Prostomatida (
