Mierob Ecol (1987) 14:55-66
Seasonal Succession of a Microphagotroph Community in a Small Pond During Litter Decomposition H. Kusano, T. Kusano, and Y. Watanabe Departmentof Biology,TokyoMetropolitanUniversity,Fukazawa2-1-1, Sctagaya-ku,Tokyo 158 Japan Abstract. Temporal dynamics of a lentic microphagotroph community were studied during leaf litter decomposition from December to May. Small plastic vessels containing leaf litter were placed on a pond bottom. They were sampled periodically to collect microphagotrophs. Three abiotic factors and abundance of two food items were also measured to analyze the autogenic and allogenic phenomena during a microphagotroph succession. Three behavior types were recognized in dominant taxa: a free-swimming type, a vagile (creeps on substratum, sometimes swims) type, and a voluntarily fixed type. Dominant taxa changed from the free-swimming to the vagile type up to mid-March, and the reverse change occurred from midApril. Principal component analysis (PCA) indicated four factors affecting the dynamics of the community: water temperature as a seasonal factor, detritus Volume on the litter surface as a habitat factor, and densities of bacteria and small flagellates as food factors. Taxa replacement appeared to occur through two mechanisms. (1) Dominance of small holotrichs, a free-swimming type, was brought about by a high bacterial density caused by seasonal events, i.e., leaf fall in December and detritus formation by litter feeders in mid-April. This is an allogenic aspect of community dynamics. (2) The free-swimming type was replaced by the vagile one during the period with high taxa diversity. This replacement occurred through intertaxa competition for scarce food and/or selective predation by larger microphagotrophs. It is an autogenic process within the community.
Introduction
Microphagotrophs, such as protozoans and rotifers, have been implicated as important in nUtrient regeneration [9] and in food chains [ 14]. They commonly show periodic changes in lentic environments, called "seasonal succession.'" Seasonal succession ofmicrophagotrophs involves both autogenic and allogenie aspects; the former occurs through the interspecific interactions in a community, while the latter depends on seasonal weather factors such as a shift in water temperature. The pattern of seasonal change in microphagotrophs is generally determined by some conditions characteristic of a given aquatic environment, e.g., seasonal fluctuation of water temperature or source of organic matter. A
56
H. Kusano et al.
m i c r o p h a g o t r o p h c c o m m u n i t y d e p e n d s on bacteria a n d microalgae as a f o o d resource. In habitats where h e t e r o t r o p h i c o r g a n i s m s d e p e n d on a l l o c h t h o n o u s organic matter, it is expected that the frequency a n d a m o u n t o f supplied organic m a t t e r strongly control the d o m i n a n c e o f m i c r o p h a g o t r o p h s . T h e r e p l a c e m e n t o f d o m i n a n t p r o t o z o a after an input o f organic m a t t e r has been studied u n d e r l a b o r a t o r y conditions with different a m o u n t s o f v a r i o u s nutrients [1, 2]. T h e p o p u l a t i o n growth o f each species was f o u n d to be regulated b y bacterial density, d e c o m p o s i t i o n product, a n d interspecific relations. In the course o f such a process o f organic m a t t e r d e c o m p o s i t i o n , relatively small ciliates d o m i n a t e d just after high bacterial density. As bacterial density decreased, the n u m b e r o f p r o t o z o a n species increased a n d small ciliates were replaced by o t h e r larger species [ 1]. As m o r e organic m a t t e r was a d d e d a n d as w a t e r t e m p e r a t u r e was increased, sapropelic species, tolerant to a n a e r o b i c conditions, a p p e a r e d after the occurrence o f high bacterial density [12]. W i t h a low bacterial density, c o m p e t i t i v e d o m i n a n c e o f m i c r o p h a g o t r o p h s c a n n o t be d e t e r m i n e d b y their growth rates b u t b y the food level threshold necessary for growth [ 16] a n d the ability to endure s t a r v a t i o n [8]. W h e n organic m a t t e r supplied as a single e v e n t brings a b o u t the r e p l a c e m e n t o f d o m i n a n t m i c r o p h a g o t r o p h species, it is an autogenic process and independent o f seasonal factors. Since the seasonal change in w e a t h e r is so slow c o m p a r e d with the generation t i m e o f m i c r o p h a g o t r o p h s , it is difficult to distinguish w h e t h e r the c o m m u n i t y d y n a m i c s results f r o m the interspecific interaction or the w e a t h e r factors prevailing in the field. T h e p u r p o s e o f the present study was to analyze the relation between autogenic a n d allogenic factors in the r e p l a c e m e n t o f d o m i n a n t m i c r o p h a g o t r o p h s . T h e field survey was c o n d u c t e d in a lentic litter layer, a c o m m o n habitat for m i c r o p h a g o t r o p h s . It has been s h o w n that they play a role in the f o o d link between bacteria a n d larger p h a g o t r o p h s [ 10]. In the present study, two m e t h o d s were applied. O n e was the artificial p l a c e m e n t o f l e a f litter to control tree species f r o m which litter was d e r i v e d a n d degree o f d e c o m p o s i t i o n . T h e o t h e r was d e t e r m i n a t i o n o f the t e m p o r a l v a r i a t i o n o f taxa c o m p o s i t i o n . T o estimate the effect o f e n v i r o n m e n t a l factors on the d y n a m i c s o f a m i c r o p h a g o t r o p h c o m m u n i t y , data f r o m two series o f o b s e r v a t i o n s in periods with different c o m b i nations o f w a t e r t e m p e r a t u r e a n d litter d e c o m p o s i t i o n degree were c o m p a r e d .
M a t e r i a l s and M e t h o d s
Sampling Method A 5-month experiment was conducted from December 1979 to May 1980 at Mizutori-no-numa Pond in the National Park for Nature Study, which is attached to the National Science Museum in Tokyo. The pond is surrounded by dense vegetation with trees. Deciduous trees shed leaf litter into the water from November to December, and evergreen trees shed in May. The pond water is supplied only by rainfall and is eutrophicated by the input of leaf litter [7]. Water depth was about 30 cm at the sampling station where leaf litter had been deposited from the last autumnal leaf fall. A detailed description of this pond was given in a previous paper [6]. Collection of microphagotrophs was made with a litter-vessel method [11]. Litter of Idesia polycarpa was collected just after the leaf fall in November 1979, and cut to even disks (47 mm in diameter). These were dried in a desiccator with silica-gel for more than a month. The dry
Seasonal Succession o f Microphagotrophs
57
5mm-mesh net , -
| V ,~............... ~, ~ . . . . . . . . . . . . . _~
.............. ~,
~ l i t t e r disks 0.5 mm-mesh n e
~
litter vessel
red loam
t
~
T control vessel
Fig. l. Experimental device of plastic vessels with litter disks of Idesia polycarpa (litter vessels) and without litter (control vessels). The vessels were placed on the litter layer underwater, and collected at intervals o f I or 2 weeks.
weight of a litter disk was about 100 rag. Three litter disks and 40 ml o f loam were put in each vessel (Fig. 1). A stainless steel net o f 0.5 m m mesh was placed between the loam and the litter disks, and the open top of the vessels was covered by a 5 m m mesh net to retain the leaf disks. To compare the effect of litter freshness on a microphagotroph community, two series of observations were made. For the winter-spring (WS) series, the vessels were placed on the pond bottom on December 25, 1979, whereas for the spring (S) series vessels were placed on March 25, 1980. In both series, organisms in the litter vessels were observed at intervals of 1 or 2 weeks until the end of May. Vessels without litter disks were also placed at the same time to obser;ce the microphagotrophs in the pond water (Fig. 1). At each sampling time, two litter vessels and one control vessel were taken from the pond following underwater replacement of the 5 m m mesh net with a watertight lid. The samples were kept at 5~ until microscopic examination in the laboratory within 8 hours after sampling. Water temperature was measured with a maximum-minimum thermometer placed on the pond bottom. The midday value was recorded together with the maximum and minimum values from the previous sampling. The dry weight o f litter disks was measured after drying at 80*(2 for 24 hours.
Counting of Organisms Species of microphagotrophs were identified using a stereoscopic, a phase contrast (x 100-1,000), and a scanning electron microscope (• 1,000-5,000). The species and their food habits were described in another report [10]. Counts were made of each taxon, consisting o f one or more species, which could be easily distinguished from others even at low magnification ( • 40-80). Unidentified species were discriminated and tentatively designated by capital letters. Unidentified small holotrichs (UNSCX, 20iC)
litter feeders active bacteria bacteria ~ active active sapropel I increased | bacteria increased
sapropel deoxidized
mIVAGILETYPE FREESWIMMINGTYPEI
sapropelic small holotrichs I Ispecies hypotrichs dominated I [ increase, and nematodes replaced
I
~pre
datoryII
eiliates
increasedl
Fig. ft. Summary of causal relationships between seasonal factors and the dynamics of a microphagotroph community. litter surface. Instead, a few sapropelic species ofMetopus, Caenomorpha, and Brachonella appeared. T h e effect o f detritus could not be distinguished as a statistically independent c o m p o n e n t , but was shown to be related to the fauna and taxa diversity (Fig. 7). In the course o f annual seasonal succession, water t e m p e r a t u r e was the most influential factor affecting the dynamics o f m i c r o p h a g o t r o p h s in the pond. However, high t e m p e r a t u r e (25-30~ is not necessarily the direct cause o f the s u m m e r absence o f m i c r o p h a g o t r o p h s [6]. Although it was not possible to examine whether the effect o f water temperature operated on microphagotrophs directly, it probably affected t h e m indirectly through its effect on food availability and physical habitat conditions. It does cause the dynamics o f microphagotrophs to be m o r e variable as c o m p a r e d with the gradual change in seasonal weather. M a n y species have the ability to encyst or to produce tolerant eggs, guaranteeing their growth during the next favorable condition [4]. Thus the repetition o f seasonal succession o f m i c r o p h a g o t r o p h s can be roughly predicted from i n f o r m a t i o n o f the allogenic factors. H o w e v e r , o m n i v o r o u s taxa at high levels o f the food chain do not d o m i n a t e during a definite period o f each yearly cycle [6]. Since the result o f interspecific interactions m a y always be delicately affected by allogenic factors, it is m o r e difficult to predict the autogenic replacements. For the future study o f a u t o g e n i c succession in natural conditions, physically spatial heterogeneity within a given habitat should be considered as a factor affecting interspecific interactions.
Acknowledgments.We are particularly grateful to N. Hisai, the National Park for Nature Study of The National Science Museum, for allowing us to carry out the present study at Mizutori-no-numa
66
H. Kusano et al.
Pond. We would also like to thank S. Takii, Department of Biology of Tokyo Metropolitan University, for a constructive critique of the manuscript.
References 1. Bick H (1963) Vergleichende Untersuchung der Ciliatensukzession beim Abbau von Pepton und Cellulose (Modellversuche). Hydrobiologia 30:353-373 2. Bick H (1973) Population dynamics of protozoa associated with the decay of organic materials in fresh water. Am Zool 13:143-160 3. Bick H, Schmerenbeck W (1971) Vergleichende untersuchung des Peptonabbaus und der damit verknfipften Ciliatenbesiedlung in Strrmenden und stagnierenden Modellgewiissern. Hydrobiologia 37:409-446 4. Corliss JO, Esser SC (1974) Comments on the role of the cyst in the life cycle and survival of free-living protozoa. Trans A m Micros Sue 93:578-593 5. H a m m A (1964) Untersuchungen uber die Okologie und Variabili~t yon Aspidisca costata (Hypotricha) im Belebtschlamm. Arch Hydrobiol 60:286-339 6. Hatano H, Watanabe Y (1981) Seasonal change of protozoa and micrometazoa in a small pond with leaf litter supply. Hydrobiologia 85:161-174 7. Hisai N, Sugawara T, Tanaka N (1974) Report on the qualities of water at ponds and springs in the National Park for Nature Study. Miscellaneous Reports of the National Park for Nature Study No. 5:1-7 8. Jackson KM, Berger J (1984) Survival of ciliate protozoa under starvation conditions and at low bacterial levels. Microb Ecol 10:47-59 9. Johaness RE (1964) Phosphorus excretion and body size in marine animals: microzooplankton and nutrient regeneration. Science 146:923-924 10. Kusano H (1985) List of microphagotrophs and their food habits in Mizutori-no-numa Pond. Rept lnst Nat Stu 16:99-112 11. Kusano H (1986) A sampling method for field survey o f a microphagotroph community in a lentic litter layer: a litter-vessel method. Jap J Eeol 36:99-104 12. Miinch yon F (1970) Der Einfluss der Temperature auf den Peptonabbau und die damit verkniipfte Organismensukzession unter besondere Berficksichtigung der Populationsdynamik der Ciliaten. Int Revue ges Hydrobiol 55:559-594 13. Pielou EC (1969) An introduction to mathematical ecology. John Wiley & Sons, New York 14. Porter KG, Pace ML, Battey J F (1979) Ciliated protozoans as links in freshwater planktonic food chains. Nature 277:563-565 15. Sheath PH, Sokal R R (1973) Numerical taxonomy. WH Freeman & Company, San Francisco 16. Taylor W D (1978) Growth responses of ciliate protozoa to the abundance of their bacterial prey. Microb Ecol 4:207-214
Seasonal Succession of a Microphagotroph Community in a Small Pond During Litter Decomposition H. Kusano, T. Kusano, and Y. Watanabe Departmentof Biology,TokyoMetropolitanUniversity,Fukazawa2-1-1, Sctagaya-ku,Tokyo 158 Japan Abstract. Temporal dynamics of a lentic microphagotroph community were studied during leaf litter decomposition from December to May. Small plastic vessels containing leaf litter were placed on a pond bottom. They were sampled periodically to collect microphagotrophs. Three abiotic factors and abundance of two food items were also measured to analyze the autogenic and allogenic phenomena during a microphagotroph succession. Three behavior types were recognized in dominant taxa: a free-swimming type, a vagile (creeps on substratum, sometimes swims) type, and a voluntarily fixed type. Dominant taxa changed from the free-swimming to the vagile type up to mid-March, and the reverse change occurred from midApril. Principal component analysis (PCA) indicated four factors affecting the dynamics of the community: water temperature as a seasonal factor, detritus Volume on the litter surface as a habitat factor, and densities of bacteria and small flagellates as food factors. Taxa replacement appeared to occur through two mechanisms. (1) Dominance of small holotrichs, a free-swimming type, was brought about by a high bacterial density caused by seasonal events, i.e., leaf fall in December and detritus formation by litter feeders in mid-April. This is an allogenic aspect of community dynamics. (2) The free-swimming type was replaced by the vagile one during the period with high taxa diversity. This replacement occurred through intertaxa competition for scarce food and/or selective predation by larger microphagotrophs. It is an autogenic process within the community.
Introduction
Microphagotrophs, such as protozoans and rotifers, have been implicated as important in nUtrient regeneration [9] and in food chains [ 14]. They commonly show periodic changes in lentic environments, called "seasonal succession.'" Seasonal succession ofmicrophagotrophs involves both autogenic and allogenie aspects; the former occurs through the interspecific interactions in a community, while the latter depends on seasonal weather factors such as a shift in water temperature. The pattern of seasonal change in microphagotrophs is generally determined by some conditions characteristic of a given aquatic environment, e.g., seasonal fluctuation of water temperature or source of organic matter. A
56
H. Kusano et al.
m i c r o p h a g o t r o p h c c o m m u n i t y d e p e n d s on bacteria a n d microalgae as a f o o d resource. In habitats where h e t e r o t r o p h i c o r g a n i s m s d e p e n d on a l l o c h t h o n o u s organic matter, it is expected that the frequency a n d a m o u n t o f supplied organic m a t t e r strongly control the d o m i n a n c e o f m i c r o p h a g o t r o p h s . T h e r e p l a c e m e n t o f d o m i n a n t p r o t o z o a after an input o f organic m a t t e r has been studied u n d e r l a b o r a t o r y conditions with different a m o u n t s o f v a r i o u s nutrients [1, 2]. T h e p o p u l a t i o n growth o f each species was f o u n d to be regulated b y bacterial density, d e c o m p o s i t i o n product, a n d interspecific relations. In the course o f such a process o f organic m a t t e r d e c o m p o s i t i o n , relatively small ciliates d o m i n a t e d just after high bacterial density. As bacterial density decreased, the n u m b e r o f p r o t o z o a n species increased a n d small ciliates were replaced by o t h e r larger species [ 1]. As m o r e organic m a t t e r was a d d e d a n d as w a t e r t e m p e r a t u r e was increased, sapropelic species, tolerant to a n a e r o b i c conditions, a p p e a r e d after the occurrence o f high bacterial density [12]. W i t h a low bacterial density, c o m p e t i t i v e d o m i n a n c e o f m i c r o p h a g o t r o p h s c a n n o t be d e t e r m i n e d b y their growth rates b u t b y the food level threshold necessary for growth [ 16] a n d the ability to endure s t a r v a t i o n [8]. W h e n organic m a t t e r supplied as a single e v e n t brings a b o u t the r e p l a c e m e n t o f d o m i n a n t m i c r o p h a g o t r o p h species, it is an autogenic process and independent o f seasonal factors. Since the seasonal change in w e a t h e r is so slow c o m p a r e d with the generation t i m e o f m i c r o p h a g o t r o p h s , it is difficult to distinguish w h e t h e r the c o m m u n i t y d y n a m i c s results f r o m the interspecific interaction or the w e a t h e r factors prevailing in the field. T h e p u r p o s e o f the present study was to analyze the relation between autogenic a n d allogenic factors in the r e p l a c e m e n t o f d o m i n a n t m i c r o p h a g o t r o p h s . T h e field survey was c o n d u c t e d in a lentic litter layer, a c o m m o n habitat for m i c r o p h a g o t r o p h s . It has been s h o w n that they play a role in the f o o d link between bacteria a n d larger p h a g o t r o p h s [ 10]. In the present study, two m e t h o d s were applied. O n e was the artificial p l a c e m e n t o f l e a f litter to control tree species f r o m which litter was d e r i v e d a n d degree o f d e c o m p o s i t i o n . T h e o t h e r was d e t e r m i n a t i o n o f the t e m p o r a l v a r i a t i o n o f taxa c o m p o s i t i o n . T o estimate the effect o f e n v i r o n m e n t a l factors on the d y n a m i c s o f a m i c r o p h a g o t r o p h c o m m u n i t y , data f r o m two series o f o b s e r v a t i o n s in periods with different c o m b i nations o f w a t e r t e m p e r a t u r e a n d litter d e c o m p o s i t i o n degree were c o m p a r e d .
M a t e r i a l s and M e t h o d s
Sampling Method A 5-month experiment was conducted from December 1979 to May 1980 at Mizutori-no-numa Pond in the National Park for Nature Study, which is attached to the National Science Museum in Tokyo. The pond is surrounded by dense vegetation with trees. Deciduous trees shed leaf litter into the water from November to December, and evergreen trees shed in May. The pond water is supplied only by rainfall and is eutrophicated by the input of leaf litter [7]. Water depth was about 30 cm at the sampling station where leaf litter had been deposited from the last autumnal leaf fall. A detailed description of this pond was given in a previous paper [6]. Collection of microphagotrophs was made with a litter-vessel method [11]. Litter of Idesia polycarpa was collected just after the leaf fall in November 1979, and cut to even disks (47 mm in diameter). These were dried in a desiccator with silica-gel for more than a month. The dry
Seasonal Succession o f Microphagotrophs
57
5mm-mesh net , -
| V ,~............... ~, ~ . . . . . . . . . . . . . _~
.............. ~,
~ l i t t e r disks 0.5 mm-mesh n e
~
litter vessel
red loam
t
~
T control vessel
Fig. l. Experimental device of plastic vessels with litter disks of Idesia polycarpa (litter vessels) and without litter (control vessels). The vessels were placed on the litter layer underwater, and collected at intervals o f I or 2 weeks.
weight of a litter disk was about 100 rag. Three litter disks and 40 ml o f loam were put in each vessel (Fig. 1). A stainless steel net o f 0.5 m m mesh was placed between the loam and the litter disks, and the open top of the vessels was covered by a 5 m m mesh net to retain the leaf disks. To compare the effect of litter freshness on a microphagotroph community, two series of observations were made. For the winter-spring (WS) series, the vessels were placed on the pond bottom on December 25, 1979, whereas for the spring (S) series vessels were placed on March 25, 1980. In both series, organisms in the litter vessels were observed at intervals of 1 or 2 weeks until the end of May. Vessels without litter disks were also placed at the same time to obser;ce the microphagotrophs in the pond water (Fig. 1). At each sampling time, two litter vessels and one control vessel were taken from the pond following underwater replacement of the 5 m m mesh net with a watertight lid. The samples were kept at 5~ until microscopic examination in the laboratory within 8 hours after sampling. Water temperature was measured with a maximum-minimum thermometer placed on the pond bottom. The midday value was recorded together with the maximum and minimum values from the previous sampling. The dry weight o f litter disks was measured after drying at 80*(2 for 24 hours.
Counting of Organisms Species of microphagotrophs were identified using a stereoscopic, a phase contrast (x 100-1,000), and a scanning electron microscope (• 1,000-5,000). The species and their food habits were described in another report [10]. Counts were made of each taxon, consisting o f one or more species, which could be easily distinguished from others even at low magnification ( • 40-80). Unidentified species were discriminated and tentatively designated by capital letters. Unidentified small holotrichs (UNSCX, 20iC)
litter feeders active bacteria bacteria ~ active active sapropel I increased | bacteria increased
sapropel deoxidized
mIVAGILETYPE FREESWIMMINGTYPEI
sapropelic small holotrichs I Ispecies hypotrichs dominated I [ increase, and nematodes replaced
I
~pre
datoryII
eiliates
increasedl
Fig. ft. Summary of causal relationships between seasonal factors and the dynamics of a microphagotroph community. litter surface. Instead, a few sapropelic species ofMetopus, Caenomorpha, and Brachonella appeared. T h e effect o f detritus could not be distinguished as a statistically independent c o m p o n e n t , but was shown to be related to the fauna and taxa diversity (Fig. 7). In the course o f annual seasonal succession, water t e m p e r a t u r e was the most influential factor affecting the dynamics o f m i c r o p h a g o t r o p h s in the pond. However, high t e m p e r a t u r e (25-30~ is not necessarily the direct cause o f the s u m m e r absence o f m i c r o p h a g o t r o p h s [6]. Although it was not possible to examine whether the effect o f water temperature operated on microphagotrophs directly, it probably affected t h e m indirectly through its effect on food availability and physical habitat conditions. It does cause the dynamics o f microphagotrophs to be m o r e variable as c o m p a r e d with the gradual change in seasonal weather. M a n y species have the ability to encyst or to produce tolerant eggs, guaranteeing their growth during the next favorable condition [4]. Thus the repetition o f seasonal succession o f m i c r o p h a g o t r o p h s can be roughly predicted from i n f o r m a t i o n o f the allogenic factors. H o w e v e r , o m n i v o r o u s taxa at high levels o f the food chain do not d o m i n a t e during a definite period o f each yearly cycle [6]. Since the result o f interspecific interactions m a y always be delicately affected by allogenic factors, it is m o r e difficult to predict the autogenic replacements. For the future study o f a u t o g e n i c succession in natural conditions, physically spatial heterogeneity within a given habitat should be considered as a factor affecting interspecific interactions.
Acknowledgments.We are particularly grateful to N. Hisai, the National Park for Nature Study of The National Science Museum, for allowing us to carry out the present study at Mizutori-no-numa
66
H. Kusano et al.
Pond. We would also like to thank S. Takii, Department of Biology of Tokyo Metropolitan University, for a constructive critique of the manuscript.
References 1. Bick H (1963) Vergleichende Untersuchung der Ciliatensukzession beim Abbau von Pepton und Cellulose (Modellversuche). Hydrobiologia 30:353-373 2. Bick H (1973) Population dynamics of protozoa associated with the decay of organic materials in fresh water. Am Zool 13:143-160 3. Bick H, Schmerenbeck W (1971) Vergleichende untersuchung des Peptonabbaus und der damit verknfipften Ciliatenbesiedlung in Strrmenden und stagnierenden Modellgewiissern. Hydrobiologia 37:409-446 4. Corliss JO, Esser SC (1974) Comments on the role of the cyst in the life cycle and survival of free-living protozoa. Trans A m Micros Sue 93:578-593 5. H a m m A (1964) Untersuchungen uber die Okologie und Variabili~t yon Aspidisca costata (Hypotricha) im Belebtschlamm. Arch Hydrobiol 60:286-339 6. Hatano H, Watanabe Y (1981) Seasonal change of protozoa and micrometazoa in a small pond with leaf litter supply. Hydrobiologia 85:161-174 7. Hisai N, Sugawara T, Tanaka N (1974) Report on the qualities of water at ponds and springs in the National Park for Nature Study. Miscellaneous Reports of the National Park for Nature Study No. 5:1-7 8. Jackson KM, Berger J (1984) Survival of ciliate protozoa under starvation conditions and at low bacterial levels. Microb Ecol 10:47-59 9. Johaness RE (1964) Phosphorus excretion and body size in marine animals: microzooplankton and nutrient regeneration. Science 146:923-924 10. Kusano H (1985) List of microphagotrophs and their food habits in Mizutori-no-numa Pond. Rept lnst Nat Stu 16:99-112 11. Kusano H (1986) A sampling method for field survey o f a microphagotroph community in a lentic litter layer: a litter-vessel method. Jap J Eeol 36:99-104 12. Miinch yon F (1970) Der Einfluss der Temperature auf den Peptonabbau und die damit verkniipfte Organismensukzession unter besondere Berficksichtigung der Populationsdynamik der Ciliaten. Int Revue ges Hydrobiol 55:559-594 13. Pielou EC (1969) An introduction to mathematical ecology. John Wiley & Sons, New York 14. Porter KG, Pace ML, Battey J F (1979) Ciliated protozoans as links in freshwater planktonic food chains. Nature 277:563-565 15. Sheath PH, Sokal R R (1973) Numerical taxonomy. WH Freeman & Company, San Francisco 16. Taylor W D (1978) Growth responses of ciliate protozoa to the abundance of their bacterial prey. Microb Ecol 4:207-214
