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The ecology of the ciliated protozoa of Marion Lake, British Columbia Kool, Richard 1975

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THE ECOLOGY OF THE CILIATED PROTOZOA OF MARION LAKE, BRITISH COLUMBIA by RICHARD KOOL B.A., U n i v e r s i t y of New Hampshire, 1971  A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF • MASTER OF SCIENCE  i n the department o f X  \  Zoology We accept t h i s thesis as conforming to the required standard  THE UNIVERSITY OF BRITISH COLUMBIA September, 1975  In p r e s e n t i n g t h i s  thesis  an advanced degree at  further  for  freely  of  the  requirements  B r i t i s h Columbia, I agree  available  for  t h a t p e r m i s s i o n f o r e x t e n s i v e copying o f  this  representatives. thesis for  It  financial  this  The  that  thesis or  i s understood that copying or p u b l i c a t i o n gain s h a l l not be allowed without my  written permission.  Department  for  reference and study.  s c h o l a r l y purposes may be granted by the Head of my Department  by h i s of  agree  fulfilment  the U n i v e r s i t y of  the L i b r a r y s h a l l make it I  in p a r t i a l  of  U n i v e r s i t y of B r i t i s h Columbia  2075 Wesbrook P l a c e Vancouver, Canada V6T 1W5  0-  Abstract The population dynamics of the c i l i a t e d Protozoa i n Marion Lake sediment are examined.  2  D e n s i t i e s of c i l i a t e s range from 10-100/cm ,  2 w i t h the yearly mean being 51/cm  .  C i l i a t e density i s not c o r r e l a t e d  w i t h r a i n f a l l , but i s c o r r e l a t e d with temperature. data i s detrended, no c o r r e l a t i o n s appear.  However, when the  The number of i n d i v i d u a l s  and the number of species present i n a sample are c o r r e l a t e d , negative c o r r e l a t i o n i s found between c i l i a t e density and the i n t r i n s i c rate of increase at both 1 and £ meters depth.  A populations  I t i s concluded  that the c i l i a t e population cannot be c o n t r o l l e d by food l i m i t a t i o n as the c i l i a t e s cannot i n f l u e n c e the s i z e of the b a c t e r i a l population, and the predation rate i s not large enough to have a regulatory i n f l u e n c e on the c i l i a t e population. The c i l i a t e s make an energetic c o n t r i b u t i o n to higher t r o p h i c l e v e l s , but i t probably unimportant when compared to that of the b a c t e r i a and microalgae. unimportant.  For deposit feeders, the c i l i a t e s are e n e r g e t i c a l l y  However, benthic meiofaunal predators such, as cyclopoid  copepods and t h e i r n a u p l i i may- be supplied w i t h a considerable amount of t h e i r d a i l y energy needs by the c i l i a t e s .  iii Table of Contents  Abstract.  ..  i i  Table of Contents  ,  i i i  L i s t of Tables  v  L i s t of Figures  vi  The R e l a t i o n s h i p between C i l i a t e d Protozoa and t h e i r Predators i n Marion Lake Abstract  •  Introduction.  ....  1 2  Methods  3 1. Radiotracer experiments  ,  3  2. Predator a d d i t i o n experiments  4  Results  5 1. Predator a d d i t i o n experiments...  5  2. Radiotracer experiments.  5  3. Energetic c o n t r i b u t i o n of the c i l i a t e s to predators  11  Discussion  ,  12  Acknowledgements, References  , ,  ,  18 19  The Population of C i l i a t e s i n Marion Lake Abstract  ,.  22  Introduction  23  Methods  24 1. Sampling  24  2. A n a l y s i s  24  3. S l i d e preparation...  25  iv  5  4. Taxonomy  25  5. Physical parameters  26  Results..  *  26  1. General population data  26  2. Species composition  29-  3. Ciliate populations and meteorological factors  35  4. Population growth data  40  .  ..  Discussion.  45  1. Food limitation hypothesis.  45  2. Predator limitation hypothesis  49-  3. Conclusion  •  49.  Acknowledgements  52  References  53  V  L i s t of Tables The Relationship Between C i l i a t e d Protozoa and t h e i r Predators i n Marion Lake I.  Results o f . H y a l e l l a azteca a d d i t i o n experiments  6  II.  Percent of c i l i a t e population eaten per day by i n d i v i d u a l predator groups  9  C o r r e l a t i o n between c i l i a t e f i e l d density and predation r a t e . . . . . . . .  10  III.  The Population of C i l i a t e s i n Marion Lake I.  Taxonomic l i s t of species found i n Marion Lake  32  II.  Rank data f o r c i l i a t e s found at 1 meter  34  III.  Minimum and maximum d e n s i t i e s of c i l i a t e s reported i n the l i t e r a t u r e  37  IV. V. VI. VII. VIII. IX.  C o r r e l a t i o n s between c i l i a t e density and various environmental f a c t o r s  ,  38  Detrended c o r r e l a t i o n s between c i l i a t e density and various environmental f a c t o r s ,  .  39  S p e c t r a l c o r r e l a t i o n between c i l i a t e density and various p h y s i c a l f a c t o r s  41  I n t r i n s i c rate of increase of the c i l i a t e population at 1 meter  42  Values of r , b, and d, c a l c u l a t e d from the c i l i a t e population at 1 meter C o r r e l a t i o n between i n t r i n s i c rate of increase and c i l i a t e density.  •  43 50  The R e l a t i o n s h i p Between C i l i a t e d Protozoa and t h e i r Predators i n Marion Lake, B r i t i s h Columbia  Richard Kool I n s t i t u t e of Resource EcologyU n i v e r s i t y of B r i t i s h Columbia  C o n t r i b u t i o n to the Canadian I n t e r n a t i o n a l B i o l o g i c a l Programme  lb Abstract The c i l i a t e s make an energetic contribution to higher trophic l e v e l s , but i t i s probably unimportant when compared to that of the b a c t e r i a and microalgae. unimportant,  For deposit feeders, the c i l i a t e s are e n e r g e t i c a l l y  however, benthic meiofaunal predators such as cyclopoids  and t h e i r n a u p l i i may be supplied with a  considerable amount of t h e i r  d a i l y energy needs by the c i l i a t e s . Based on the experiments performed, we cannot conclude that there i s a density dependent predatory mechanism c o n t r o l l i n g the size of the c i l i a t e population.  2 Introduction C i l i a t e d protozoa have a cosmopolitan d i s t r i b u t i o n (Cairns and Ruthven, 1972), but reports of metazoans e a t i n g c i l i a t e s are uncommon. Maguire e_t ail, (1968) have demonstrated the importance of dipteran larvae eating c i l i a t e s i n H e l i c o n i a b r a c t s .  Gray (1952) observed a negative  c o r r e l a t i o n between chironomid and s i m u l i i d larvae and c i l i a t e numbers i n a B r i t i s h chalk stream.  More r e c e n t l y , Addicott (1974) found the  dipteran Wyeomyia sp. important i n determining the species d i v e r s i t y of the protozoan communities i n p i t c h e r p l a n t s .  Lawton (1970) has r e -  ported that i n s t a r s 2 and 3 of Pyrfhosoma nymphula (Odonata: Zygoptera) eat Paramecium caudatum and Stylonychia sp. i n feeding experiments. Thane-Fenchel (1968) observed a few genera of predatory marine r o t i f e r s eating c i l i a t e s , while Straarup (1970) gave instances of predation on c i l i a t e s by marine t u r b e l l a r i a n s . predation by marine nematodes.  Hopper and Meyers (1966) observed  Sushkina e_t a l . (1968) have used paramecia  as food f o r a l l stages of the cyclopoid copepod l i f e c y c l e .  Monakov  (1972), i n reviewing recent work on feeding of aquatic i n v e r t e b r a t e s , mentions a few groups which feed on c i l i a t e s , i n c l u d i n g b i v a l v e s , c y c l o p o i d s , r o t i f e r s , and chironomids. I have performed a s e r i e s of experiments concerned w i t h examining the r o l e predators have i n r e g u l a t i n g the s i z e of the c i l i a t e p o p u l a t i o n , and w i t h the energetic r e l a t i o n s h i p s between the c i l i a t e s and t h e i r predators.  This work was performed as part of a large s c a l e ecosystem  study of Marion Lake, c a r r i e d out under the auspices of the Canadian I n t e r n a t i o n a l B i o l o g i c a l Programme.  Other work done on Marion Lake i s  described by E f f o r d and H a l l ( i n p r e s s ) .  3  Methods 1. Radiotracer experiments These experiments were conducted i n small (diameter = 2 cm) undisturbed sediment cores taken from a depth of 1 m i n Marion Lake.  The cores  were transported from the lake to our laboratory w i t h a minimum of d i s t u r bance and allowed to stand f o r s e v e r a l days before use.  Incubation was  at e i t h e r 5, 1 0 , 15, or 20°C, whichever was c l o s e s t to the lake temperature.  H y a l e l l a azteca (Amphipoda) was added to some cores to ensure the  presence of t h i s grazer. A large number of healthy Paramecium b u r s a r i a ( C i l i o p h o r a ) were i s o l a t e d from c u l t u r e s and placed i n a small Stender d i s h w i t h 2 ml of lake water.  P. b u r s a r i a was chosen to be the t r a c e r c i l i a t e as i t harbours  p h o t o s y n t h e t i c a l l y a c t i v e z o o c h l o r e l l a e , which become l a b e l l e d when i n c u bated w i t h H-^C03 added to the c u l t u r e water.  The d i s h w i t h t r a c e r and  c i l i a t e s was sealed and placed i n the l i g h t at 20°C.  Periodically, a  few P_. b u r s a r i a were removed, r i n s e d and placed on a glass f i b e r f i l t e r to be counted f o r a c t i v i t y using l i q u i d s c i n t i l l a t i o n methods.  In a check  of the r i n s i n g procedures, i t was found that three r i n s e baths would r e move a l l but a very small amount of t r a c e r outside of the c i l i a t e s . When the F. b u r s a r i a were l a b e l l e d (greater than 1 0 0 cpm/individual) they were removed from the r a d i o a c t i v e l i q u i d , r i n s e d , and placed on top of the core sediment at the desired d e n s i t y .  I f a cold incubation was to  be used, the c i l i a t e s were acclimated at the lower temperature f o r 2 hr. A f t e r the incubation period i n the sediment core ( e i t h e r 4 or 6 h r ) , the  top 2 cm of mud and o v e r l y i n g water was removed from the core and  placed i n a b o t t l e , 10 ml of buffered f o r m a l i n added, q u i c k l y frozen.  When the sample was  and the sample  to be examined, the b o t t l e was thawed  and the organisms extracted using a sugar f l o t a t i o n method (M. Hoebel, pers. comm.).  The extracted organisms were then stained w i t h rhodamine-b  and examined using a d i s s e c t i n g microscope w i t h UV i l l u m i n a t i o n .  The  organisms were separated i n t o taxonomic groups, r i n s e d , and placed on glass fiber f i l t e r s .  In the case of small meiofaunal organisms, the f i l t e r s  were put d i r e c t l y i n t o Bray's s o l u t i o n . The l a r g e r organisms were ashed i n a tube furnace and the and Perez, 1974). method.  trapped using a toluene f l u o r  The samples were counted using a l i q u i d  (Burnison  scintillation  The a c t i v i t y of the sample was a d i r e c t i n d i c a t i o n of the number  of l a b e l l e d c i l i a t e s . eaten i n the incubation p e r i o d .  2.  Predator a d d i t i o n experiments  In J u l y , 1972, 5 cm diameter cores were taken at a depth of I m, 1/3 of these cores remained c o n t r o l s , w i t h only a t h i n screen placed over the top to prevent immigration or emigration of macrofauna.  To 1/3  the cores were added 10 times the normal density of H_. azteca. remaining  of  The  cores were covered so that water could c i r c u l a t e , but no l i g h t  could penetrate to the sediment surface. incubate f o r 45 days at a depth of 1 m.  The cores were allowed to A f t e r the incubation p e r i o d ,  the c i l i a t e s were removed and counted i n representative samples of the d i f f e r e n t treatments and the c o n t r o l . Marten (1975) discussed the design of t h i s experiment f u r t h e r , and a l s o described the r a d i o t r a c e r studies done a f t e r the incubation p e r i o d . In August, 1972, I placed 40 ml of sieved surface sediment i n t o  each of three dishes.  One remained a control and the others had f i v e  times the normal density of H_. azteca added.  A f t e r 48 hr at 15°C, the  c i l i a t e d e n s i t i e s were determined and compared against the i n i t i a l values. A s i m i l a r experiment was done i n December, 1972.  However, at that time,  a small dish was used and ten times the normal density of H_. azteca was present as the treatment, with no macrofauna present i n the control. In'May, 1973, I added 25 cyclopoid copepods to a 2 cm sediment core ( t h i s being f i v e times the normal spring density of cyclopoids).  After  a f i v e day incubation period, the number of c i l i a t e s i n the core was determined, and the predation rate calculated from a radiotracer experiment (see section 1).  Results 1. Predator addition experiments The f i r s t experiments were done by adding E.  azteca to either i n t a c t  cores or mixed sediment and allowing them to incubate for a varying number of days.  In a l l cases, the number of c i l i a t e s present i n the treatment  was lower than i n the controls (Table 1), but when a median test performed  was  (Sokal and Rolf, 1969), the treatments were a l l found to be  insignificant. In  the cyclopoid addition experiment, the treatment a c t u a l l y had  more c i l i a t e s i n i t than did the c o n t r o l , but again the treatment not a s i g n i f i c a n t  was  one.  2. Radiotracer experiments The predation r e s u l t s can be broken into two groups; l ) a f a l l / w i n t e r  Table I Results of H y a l e l l a azteca a d d i t i o n experiments, using 10 times the normal density. Data i s expressed as numbers of c i l i a t e s / c m ^ . Date August, 1972  Control 123  September, 1972  39  December, 1972  26  134  Treatment 105  108  34 27  27  16  group, and 2) a spring/summer group (Table 2, F i g . 1).  The winter group  had _H. azteca and cyclopoid copepods as the major predators, w i t h the former the most important.  Minor predators included nematodes, mites,  cyclopoid n a u p l i i and l a t e i n s t a r chironomid l a r a v e .  The only t u r b e l -  l a r i a n found i n a l l the samples had eaten two l a b e l l e d c i l i a t e s .  The  average predation r a t e expressed as percent of the population l o s t to predators per day was about 5%/day (Table 2). The spring group had a much higher predation r a t e than the winter group.  During t h i s p e r i o d , the major predators were the c y c l o p o i d cope-  pods (mainly Cyclops sp., M. Hoebel, pers. comm.), which ate an average of 14% of the c i l i a t e population/day.  This f i g u r e corresponded  of a l l the c i l i a t e s eaten i n t h i s time p e r i o d .  to 65%  One d i f f i c u l t y w i t h t h i s  f i g u r e i s that i t i s an estimate of the c y c l o p o i d population predation r a t e per core, however, the number of i n d i v i d u a l predators v a r i e d i n d i f ferent cores.  In most cases, a l l of the cyclopoids were counted f o r  a c t i v i t y together.  In the one case where the cyclopoids were counted  i n d i v i d u a l l y f o r a c t i v i t y , only two out of eleven had eaten l a b e l l e d ciliates. H. azteca ate more c i l i a t e s i n the spring (5% of the than i n the f a l l (1.2% of the population/day).  population/day)  But the p r o p o r t i o n of the  t o t a l population i n the spring was l e s s , dropping from 40% of the t o t a l eaten/day i n the winter to 17%/day i n the s p r i n g .  When the  chironomid  larvae were separated i n t o e a r l y and l a t e i n s t a r stages, only the l a t e i n s t a r s were found to have t r a c e r i n them.  They were probably deposit  feeding i n the same manner as H_. azteca. In December, 1972 and February, 1973, I performed experiments to see  To f a c e  Page 8  Figure 1 Percent of t o t a l c i l i a t e s eaten per season by various predators, based on radiotracer experiments.  j  ! ,;"  °/ I  8  0  of t o t a l ciliates eaten p e r season, fall, winter, spring  Table  &  Percent of c i l i a t e population eaten per day by i n d i v i d u a l predator groups, w i t h the t o t a l percent eaten per day f o r each experiment. harpactacoid 24 Sept  "72  cyclopoid  nematode  0.72  14 Nov  2.4  1-2  1.9  1.9  '73  1.9  15 March 8 May 11 May  naup- c h i r o n l i i • omid  1.3  12 Oct  14 Feb  mite  4.0  1.5  0.72  0.72  1.9  amphipod  turbellarian  total %  0.4  1.7  2.2  5.7  2.4  6.0  0  3.8  11.0  1.9  1.9  3.8  7.6  18.0 '  6.0  1.9  26.0  0  20.0  3.0  9.0  21.0  3.0  3.0  15.0  16.0  17 May  9.0  28 June  3.0  3.0 •  Table I I I C o r r e l a t i o n of c i l i a t e f i e l d density and predation r a t e Date  Density  Predation  21 Sept '72  10  1.7%  12 Oct '72  30  5.7  14 Nov '72  30  6.0  14 Feb '73  40  11.4  15 March '73  65  7.6  8 May '73  80  26  11 May  80  20  17 May * 73  60  21  28 June '73  50  15  '73  r = 0.81, p < .01  (individuals/cm ), 2  11  i f i t would be p o s s i b l e to induce higher predation rates by adding l a r g e r numbers of P_. b u r s a r i a to cores.  I n the December experiments,  although  fewer c i l i a t e s were eaten i n the low density cores than i n cores w i t h f i v e times the number of c i l i a t e s , the predation r a t e was the same i n both cores (5%/day and 6%/day).  This was owing to the predation of R.  azteca which being a non-selective predator, removed only a f i x e d proport i o n of the prey present. A l l of the predation experiments were done on lake sediment that had n a t u r a l c i l i a t e population d e n s i t i e s ranging from very low (20/cm ) to z  very h i g h (80/cm ).  I f some sort of density dependent regulatory mechanism  was r e g u l a t i n g the s i z e of the c i l i a t e population, we would expect to see higher predation rates when the c i l i a t e populations were high, and lower predation rates when the population was low.  Predation and c i l i a t e  f i e l d d e n s i t i e s at the time of experimentation were s i g n i f i c a n t l y correl a t e d ( r = 0.81, p 4. .01; Table 3 ) . This r e s u l t i s contrary to the experimental r e s u l t s described above, and would imply some sort of d e n s i t y dependent predation a c t i n g on the c i l i a t e population. 3.  Energetic c o n t r i b u t i o n of the c i l i a t e s  to predators  Work has been done on the b i o e n e r g e t i c s of the two major c i l i a t e predators i n Marion Lake; H. azteca and cyclopoid copepods.  From the  work of Mathias (1971) and Shushkina et al_. (1968) we can estimate the p o t e n t i a l c o n t r i b u t i o n of the c i l i a t e s  to the d a i l y energy needs of these  predators. The f o l l o w i n g c a l c u l a t i o n s are based on the assumption of a s i n g l e g c i l i a t e weighing 10 6000 c a l o r i e s .  grams dry weight, and one gram of c i l i a t e s e q u a l l i n g  12  Shushkina e_t a l . (1968) derived a r e g r e s s i o n that r e l a t e s body weight of c y c l o p o i d copepods to t h e i r O2 QQ  2  = 0.134  requirements: W  +  0  '  8  4  ,  where  O2 = ml 02/hour W = grams wet  weight.  The average cyclopoid i n Marion Lake benthos weighs 10  grams wet  weight, and would consume 7 X 10 ^ ml 02/day.  From Hargrave (1971) 1 ml 0^ = _3 4.8 c a l , so a cyclopoid would need about 3.57 X 10 cal/day. Assuming a 2 conservative predation r a t e of 4% of the c i l i a t e population i n a 3 cm 2 core/day/cyclopoid, and a c i l i a t e d e n s i t y of 80/cm , a s i n g l e predator  would eat 10 c i l i a t e s per day.  This would equal 6 X 10 ^ cal/day, which  i s equal to about 20% of the cyclopoids d a i l y energy need.  As c y c l o p o i d  copepods have a very high a s s i m i l a t i o n e f f i c i e n c y (90%) , t h i s may be a r e a l i s t i c estimate of the energy c o n t r i b u t i o n to them by the Mathias  ciliates.  (197l) has shown that during the warmer part of the year,  H. azteca needs about 1 cal/day.  I have shown that an i n d i v i d u a l H. azteca 2  can crop at most 4% of the c i l i a t e p o p u l a t i o n ' i n a 3 cm would equal 6 X 10 ^'cal/day, or about  core/day.  This  .06% of the enrgy needed d a i l y .  However, Hargrave (1971) has pointed out that H. azteca has a very low a s s i m i l a t i o n e f f i c i e n c y (15%) so t h i s value must be a d d i t i o n a l l y  lowered.  Discussion In the Marion Lake benthos, a l l meiofauna w i t h the exception of r o t i f e r s , t a r d i g r a d e s , and g a s t r o t r i c h s , have been shown to be p o t e n t i a l predators on the c i l i a t e s .  The most important of these are the cyclopoid  13  copepods.  As these copepods are v i s u a l hunters who  search and s t r i k e at  moving o b j e c t s , they could be s i g n i f i c a n t predators and could act i n a density dependent fashion when c i l i a t e numbers are high.  However, although  the c o r r e l a t i o n does e x i s t between predation rate and f i e l d d e n s i t y , the predation r a t e at high prey d e n s i t i e s i s not n e a r l y enough to c o n t r o l the growth of the c i l i a t e population.  This may  i n d i c a t e 1) that the cyclopoid  predation a b i l i t y i s e a s i l y saturated at r e l a t i v e l y low c i l i a t e d e n s i t i e s , or 2) that the complexity of the environment makes hunting very d i f f i c u l t . So many refuges may slightly  e x i s t f o r the c i l i a t e prey that the predators can only  respond to even high c i l i a t e d e n s i t i e s .  - I think that the l a t t e r explanation best f i t s the a v a i l a b l e data. M. Hoebel (pers. comm.)'has performed a feeding experiment w i t h Cyclops  sp.,  i n which he placed a few animals i n a d i s h w i t h no sediment, and then added a l a r g e number of l a b e l l e d _P_. b u r s a r i a . poid could eat 2 c i l i a t e s / h o u r .  He found that an i n d i v i d u a l c y c l o -  This f i g u r e of 24 c i l i a t e s / d a y i s more  than twice the number I a r r i v e d at from the predation experiments i n n a t u r a l sediment.  Since Hoebel's experiment was done without refuges f o r the prey,  i t may be that the complexity of the sediment surface o f f e r s s u b s t a n t i a l refuges f o r the c i l i a t e s from predators. H_. azteca has been reported by Hargrave (1970) to eat r o t i f e r s ,  as  w e l l as microalgae and b a c t e r i a . This i s the f i r s t report of H_. azteca eating c i l i a t e s .  As i s c l e a r from the amount of energy i t gets from  c i l i a t e s , H. azteca i s not gaining much by e a t i n g them.  As a deposit feeder  e a t i n g d e t r i t u s w i t h b a c t e r i a and microalgae, H. azteca w i l l probably a c i l i a t e only by accident.  eat  I t seems u n l i k e l y that they could a c t u a l l y  hunt f o r c i l i a t e s , therefore i t i s a l s o u n l i k e l y that H. azteca could have  14  much of an i n f l u e n c e on the s i z e of the c i l i a t e population. My data on chironomid (Marion Lake Report, 1970)  feeding i s counter to that reported by MacCauley and Lawton (1970), and others.  the e a r l y i n s t a r s feed on c i l i a t e s .  They s t a t e that  In a l l cases, the only larvae having  t r a c e r i n them were l a t e i n s t a r c l a s s e s , which probably are deposit feeding. However, as the number of chironomids seen w i t h l a b e l l e d c i l i a t e s i s low, I may have missed e a r l y i n s t a r predation. The H a l a c a r i d mites are p r i m a r i l y predators, but according to E f f o r d (pers. comm.) have not been known t o eat c i l i a t e s .  This would be due to  the l a c k of i d e n t i f i a b l e remains i n the guts of the predators, i n p a r t i c u l a r as these mites suck t h e i r food out of the prey. The only d i r e c t observation of a nematode e a t i n g c i l i a t e s i s by Hopper and Meyers (1966).  They observed j u v e n i l e Melonicholaimus  sp. (a marine ,  nematode) feeding on c i l i a t e s which were growing next to a decomposing worm.  They noticed a decrease i n number of c i l i a t e s and an increase i n the  s i z e of young worms.  Perkins  (1958) found that nematodes could survive  longer i f grown i n c u l t u r e medium c o n t a i n i n g b a c t e r i a and c i l i a t e s than i f kept i n pure sea water.  Webb (1956), even though she includes nematodes  as c i l i a t e predators, f a i l e d to see any d i r e c t predation by t h i s group. In Marion Lake, a small number of nematodes were found to have eaten c i l i ates. T u r b e l l a r i a n s are r e l a t i v e l y uncommon i n Marion Lake, and probably are i n s i g n i f i c a n t as predators on c i l i a t e s .  However, the one t u r b e l l a r i a n  found i n the r a d i o t r a c e r experiments had eaten c i l i a t e s .  This confirms  Straarups (1970) observation that some t u r b e l l a r i a n s eat c i l i a t e s . (1956) a l s o mentions that rhabdocoels may eat c i l i a t e s .  Webb  15  In the only core where P i s i d i u m (Mollusca) was found, i t appeared that one c i l i a t e was eaten.  P i s i d i u m i s reported t o eat b a c t e r i a and  algae (Efford and Tsumura, pers. comm.), and Monakov (1972) reports that "many Sphaerium and P i s i d i u m draw small I n f u s o r i a i n t o the mantle c a v i t y and r e j e c t b i g ones when feeding on c i l i a t e d plankton."  Fenchel (1969)  i m p l i e s that marine lamellibranchs must eat c i l i a t e s when eating sediment or siphoning surface water, but he had no evidence that t h i s was the case. Shushkina at a l . (1968) fed Paramecium to cyclopoid n a u p l i i as part of a study i n the b i o e n e r g e t i c s of cyclopoid copepods.  This study a l s o  i n d i c a t e s that c i l i a t e s are p o t e n t i a l prey f o r the n a u p l i i . We are now able t o r e f u t e Muus's (1967) contention that the c i l i a t e s do not play any traceable r o l e i n the food chain leading to higher animals. Picken (1937) a l s o mentions "The protozoa are e c o l o g i c a l l y a very i n t e r e s t i n g group inasumch as they have very few metazoan enemies... and t h e i r communities are not therefore l i n k e d up w i t h metazoan forms".  As t h i s  study has shown, at l e a s t nine d i f f e r e n t groups of metazoa prey on c i l i a t e s . C i l i a t e s may make up an important part of the energy input i n the c a r n i v orous cyclopoid copepods, a p o i n t which was stressed by Monakov and Sorokin (1971). This study has ignored the r o l e of predatory c i l i a t e s i n the p o s s i b l e r e g u l a t i o n of the t o t a l c i l i a t e population.  Predatory c i l i a t e s found i n  Marion Lake are D i l e p t u s sp., Lacrymaria sp., Loxophyllum sp., and Stentor spp.  Due to the nature of these experiments,  the importance of these predators.  i t was impossible to examine  From my population data, i t appears  as i f 10% of the species of c i l i a t e s found and 9% of the i n d i v i d u a l s found at 1 m i n Marion Lake are predatory.  This i s very s i m i l a r to Fenchel'  16  (1969) r e s u l t s , where he found about 10% of the c i l i a t e s he examined i n a marine i n t e r s t i t i a l environment to be predatory. There has been l i t t l e work done i n the r o l e of predators i n r e g u l a t i n g the s i z e of n a t u r a l populations of c i l i a t e s .  The only f i e l d work  of t h i s s o r t i s by Hairston (1967), examining the population dynamics of Paramecium a u r e l i a i n a small seep i n a hardwood f o r e s t .  He concluded  that the death r a t e observed i n the population was constant, and the popu l a t i o n was responding to changes i n the d i v i s i o n r a t e .  These changes i n  d i v i s i o n r a t e , he concluded, were based upon varying l e v e l s of food. maintains that since the "observed  He  l o s s rates (were not) r e l a t e d t o the  density of paramecia a t the s t a r t of the relevant observation periods", density dependent predation could not be invoked as the regulatory mechanism.  Webb (1956) b r i e f l y s t a t e s " c i l i a t e populations are apparently  l i t t l e r e s t r i c t e d by the attack of metazoan predators". In the f a l l and w i n t e r , the c i l i a t e population i n Marion Lake i s 2 r e l a t i v e l y s t a b l e at about 25 c i l i a t e s / c m . The measured predation r a t e i s very c l a s e t o the population growth r a t e , 8%/day (Stachurska, 1975). When the water temperature i s low and l i g h t a v a i l a b i l i t y i s reduced by clouds and i c e , lake production i s reduced, and by a combination of a l l these f a c t o r s ( i f growth r a t e and predation r a t e are the same) and low food a v a i l a b i l i t y , we would expect a s t a b l e population s i z e .  Luckinbill  (1973, 197A) has performed a s e r i e s of experiments that i n d i r e c t l y t e s t t h i s hypothesis.  A f t e r examining the s t a b i l i t y p r o p e r t i e s of a Paramecium—  Didinium system, he concluded that "enrichment of predator prey systems creates i n s t a b i l i t y " .  H i s studies have shown that a coexistence of pre-  dator and prey w i t h small predator-prey o s c i l l a t i o n s i s p o s s i b l e under  17  low food d e n s i t i e s f o r the prey.  This s i t u a t i o n may be what i s c o n t r o l -  l i n g the c i l i a t e population during the w i n t e r , and i s not due to density dependent predation. In the summer, predation i s at l e a s t 2-3 times greater than i n the w i n t e r , but the growth r a t e of the c i l i a t e s i s almost 10 times greater than what i t was i n the winter.  With the warmer temperatures the c i l i a t e  growth r a t e goes up (Stachurska, 1975), and we could a l s o expect the bact e r i a l growth r a t e to go up.  With the c i l i a t e population seemingly unbound  by predation, we would expect to see o s c i l l a t i o n s between c i l i a t e s and i t s b a c t e r i a l food, s i m i l a r to what L u c k i n b i l l (197.3, 1974) creased the number of paramecia.  However, Stachurska  found when he i n (pers. comm.) has  shown that even at high c i l i a t e d e n s i t y , the b a c t e r i a l population i n the sediment i s not a f f e c t e d by c i l i a t e grazing.  She concludes that she  has  not been able to show that the c i l i a t e populations are c o n t r o l l e d by a food l i m i t a t i o n .  I have not been able to show that the c i l i a t e s are con-  t r o l l e d by a predatory mechanism. Based on the data of Stachurska, i t seems u n l i k e l y that predation can have much of an i n f l u e n c e on the c i l i a t e population at temperatures above 10°C.  The population i n t r i n s i c  r a t e of increase at 15°C  i s r = 0.315,  which i s a higher r a t e of increase than m o r t a l i t y due to predation.  The  maximum predation observed (20%/day) i s much lower than the p o t e n t i a l r a t e of growth which may be between 50-70%/day.  However, a problem w i t h the  data i s that the growth r a t e of the population was measured i n the l a b oratory i n c u l t u r e s w i t h lake sediment. or lower values of r .  F i e l d c o n d i t i o n s may  give higher  Acknowledgements I am indebted to Dr. Ian E f f o r d f o r the opportunity to work w i t h the Marion Lake group.  Ideas, advice and assistance were received from Drs.  Gerry Marten, Teresa Stachurska, Ken H a l l , P i e r r e K l e i b e r , Ken and Mr. Mike Hoebel and Rob  Powell.  Burnison,  19  References A d d i c o t t , J.F.i Predation and prey community s t r u c t u r e :  An experimental  study of the e f f e c t of mosquito l a r v a e on the protozoan of p i t c h e r p l a n t s . Burnison, B.K., 1 4  communities  Ecology 55, 475-492 (1974)  Perez,'K.P.: A simple, method f o r the dry combustion of  C - l a b e l l e d materials.  Ecology 55, 899-902 (1974)  C a i r n s , J , Ruthven, J.A.: A study of the cosmopolitan d i s t r i b u t i o n of freshwater protozoa.  Hydrobiologia 3_9_, 405-427 (1972)  E f f o r d , I.E., H a l l , K.J.: Marion Lake- an a n a l y s i s of an ecosystem. Proceedings of the Royal Society of Canada ( i n press) Fenchel, T.: The ecology of marine microbenthos. IV.  The s t r u c t u r e and  f u n c t i o n of the benthic ecosystem, i t s chemical and p h y s i c a l f a c t o r s , and the microfauna communities w i t h s p e c i e a l reference to the c i l i a t e d protozoa.  Ophelia  1-182  (1969)  Gray, E.: The ecology of the c i l i a t e fauna of Hobsons Brook, a Cambridges h i r e chalk stream. J . Gen. Micro. H a i r s t o n , N.G.:  Studies on the l i m i t a t i o n of a n a t u r a l population of  Paramecium a u r e l i a . Hargrave, B.T.:  108-122 (1952)  Ecology 48, 904-910 (1967)  An energy budget f o r a deposit feeding amphipod.  Limnol.  Oceanog. 16, 99-103 (1971) Hargrave, B.T.:  The e f f e c t of a deposit feeding amphipod on the metabolism  of benthic m i c r o f l o r a .  Limnol. Oceanog. _15, 21-30  (1970)  Hopper, B.E., Meyers, S.F.: Observations on the bionomics of the marine nematode, Melonicholaimus ;sp.  Nature 209, 899-900 ( 1966)  20  Lawton, J.H.:  Feeding and food energy a s s i m i l a t i o n i n l a r v a e of the damsel-  f l y PyjrrJm £Ojiia nympjnila_ (Sulz.) (Odonata: Zygoptera). r  J.  Anim. E c o l .  39, 669-689 (1970) L u c k i n b i l l , L.S.:  Coexistance i n laboratory populations of Paramecium  a u r e l i a and i t s predator, Didinium nasutum.  Ecology 5_4, 1320-1327  (1973) L u c k i n b i l l , L.S.: The e f f e c t s of space and enrichment on a predator-prey system.  Ecology 55, 1142-1147 )1074)  Maguire, B., Belk, D., W e l l s , G.: mosquito l a r v a e . Marten, G.G.:  C o n t r o l of community s t r u c t u r e by  Ecology 4£, 207-210 (1968)  ,  The e f f e c t of grazing by a sediment feeding amphipod.  (unpublished, Mathias, J.A:  1975)  Energy flow and secondary production of the amphipods  H y a l e l l a azteca and Crangonyx richmondensis Lake, B.C. Monakov, A.V.:  J.  o c c i d e n t a l i s i n Marion  F i s h . Res. Bd. Can. 28, 711-726 (1971)  Review of studies on feeding of aquatic i n v e r t e b r a t e s  conducted at the I n s t i t u t e of Biology of Inland Waters, Academy of Science, USSR. Monakov, A.V.,  J.  F i s h . Res. Bd. Can. 29_, 363-383 (1972)  Sorokin, Y.I.: Role of I n f u s o r i a as food of Cyclopoida of  Rybinsk Reservoir.  Trans. I n s t . B i o l . Inland Waters, Acad. S c i .  USSR 21, 37-42 (1971) Muus, B.J.:  The fauna of Danish e s t u a r i e s and lagoons.  Hauv. 5, P e r k i n s , E.J.:  9-316  Fisk.  (1967)  The food r e l a t i o n s h i p s of the microbenthos w i t h p a r t i c u l a r  reference to that found at Whitestable, Kent. 12,  Medd. Dan.  Ser. 10, 37-42 (1958)  Ann. Mag. Nat. H i s t .  21  P i c k e n , L.E.R.; The s t r u c t u r e of some protozoan communities.  J . Ecol.  25, 368-384 (1937) Shushkina, E.A., Anisimov, S.I., Klekowski, R.Z.: C a l c u l a t i o n of production e f f i c i e n c y i n p l a n k t o n i c copepods.  P o l . Arch. H y d r o b i o l . 15, 251-261  (1968) Sokal, R.R., R o l f , S.F.: Biometry, 775pp. San F r a n c i s c o , C a l i f o r n i a : W.H. Freeman and Company 1969 Stachurska, T: The ecology of c i l i a t e d protozoa i n Marion Lake, B.C. I . (unpublished, 1975) Straarup, B-J.: On the ecology of t u r b e l l a r i a n s i n a s h e l t e r e d b r a c k i s h water bay. Ophelia ]_, 185-216 (1970) Thane-Fenchel,  A.: The ecology and d i s t r i b u t i o n of nonplanktonic r o t i f e r s  from Scandinavian waters. Ophelia 5_, 273-297 (1968) Webb, M.G.: An e c o l o g i c a l study of b r a c k i s h water c i l i a t e s . E c o l . 25, 148-175 (1956)  J . Anim..  The Population of C i l i a t e s i n Marion Lake, B r i t i s h Columbia  Richard Kool I n s t i t u t e of Resource Ecology U n i v e r s i t y of B r i t i s h Columbia  Contribution to the Canadian I n t e r n a t i o n a l B i o l o g i c a l Preogramme  22b Abstract The population dynamics of the c i l i a t e d Protozoa i n Marion Lake sediment are examined.  2  D e n s i t i e s of c i l i a t e s range from 10-100/cm ,  2 with the y e a r l y mean being 51/cm  .  C i l i a t e density i s not c o r r e l a t e d  with r a i n f a l l , but i s c o r r e l a t e d w i t h temperature. data i s detrended, no c o r r e l a t i o n appears.  However, when the  The number of i n d i v i d u a l s  and the number of species present i n a sample are c o r r e l a t e d . c o r r e l a t i o n i s found between c i l i a t e  density and the  A negative  populations  i n t r i n s i c rate of increase at both 1 and 4 meters depth.  I t i s concluded  that the c i l i a t e population cannot be c o n t r o l l e d by food l i m i t a t i o n as the c i l i a t e s cannot i n f l u e n c e the s i z e of the b a c t e r i a l population, and the predation rate i s not large enough to have a regulatory influence on the c i l i a t e population. r e g u l a t i o n i n c i l i a t e populations  The mechanism of population  i s s t i l l unkown.  Introduction. As part of the l a r g e s c a l e ecosystem study of Marion Lake (see E f f o r d , 1967, H a l l and Hyatt, 1975, and E f f o r d and H a l l , i n press, f o r a d d i t i o n a l information about Marion Lake), I have studied the temporal and s p a t i a l d i s t r i b u t i o n of the c i l i a t e d Protozoa i n the s u b l i t t o r a l sediment. The major alms of t h i s research were to determine the r o l e of the c i l i a t e s i n the sediment ecosystem, and to examine mechanisms c o n t r o l l i the dynamics of  the c i l i a t e s populations.  Methods 1 • Sampling Mud samples f o r q u a n t i t a t i v e studies of c i l i a t e density were taken using a g r a v i t y core designed by M. Hoebel.  The core has an i n s i d e  diameter of 2 cm., and the top 2 cm. of sediment plus the o v e r l y i n g water was saved f o r examination. Ten cores were taken at every s t a t i o n , w i t h each s t a t i o n being an area enclosed by a c i r c l e around a f i x e d p o i n t .  (diam. 2 meters)  A l l ten samples were mixed together i n a b o t t l e and  taken back to the laboratory f o r enumeration.  Stations were along  an east-west transect at the northern end of the l a k e , at depths of 1, 2, and 4 meters depth. 2 . Analysis In the l a b , the j a r s with sediment and water were kept at lake temperatures, and the sediment allowed to s e t t l e f o r at l e a s t one hour before a n a l y s i s was begun. The supernatant water was c a r e f u l l y pipetted o f f l e a v i n g only .25 cm. of water.  The sediment was then thoroughly mixed and 5 ml. was removed  The sample was then placed i n t o an e x t r a c t i o n column made of d i f f e r e n t s i z e d Nitex f i l t e r s ( 405 um, 253 urn, and 130 urn). The funnels were arrainged i n a s e r i e s , and the sediment washed through with 35 ml. of filtered  lake water.  The f i l t r a t e was c o l l e c t e d i n a beaker and the  volume determined. C i l i a t e s were counted by removing 0.5 ml. of the mixed  filtrate  w i t h a mouth p i p e t t e , to a 1 ml. hemispherical glass depression s l i d e well.  Eighteen 0.5 ml. samples were counted.  The number of  ciliates  in each depression was determined, and each i n d i v i d u a l i d e n t i f i e d and  25  removed f o r l a t e r s l i d e p r e p a r a t i o n . Using t h i s method, we could estimate the number of c i l i a t e s i n our o r i g i n a l sample of 5 ml.  However, because there i s good evidence that  i n mud bottom sediments, at l e a s t 90% of a l l the c i l i a t e s are i n the top centimeter (Cole, 1955, Goulder, 1971a), and as we wished to express 2 our r e s u l t s i n c i l i a t e s / c m  , we divided the answer by 2.5 r a t h e r than  by 5. 3• S l i d e preparation The i s o l a t e d c i l i a t e s were concentrated w i t h a f i n e micropipette and placed on a clean glass s l i d e . stain-fixative  The N i g r o s i n - HgC^-  formalin  (Borror, 1968a) was used, and the s l i d e s were dehydrated  i n the normal f a s h i o n . The f i n i s h e d s l i d e s were then examined and the c e l l s were i d e n t i f i e d , measured, and the contents of t h e i r food vacuoles recorded. 4^ Taxonomy A l l c i l i a t e s were examined l i v e using a Wild M-5 microscope.  dissecting  Most magnifications were 40X, thus small organisms were  hard to i d e n t i f y .  U n l i k e most phytoplankters, benthic algae or meiofaunal  organisms, c i l i a t e s do not, i n general, withstand f i x a t i o n very w e l l . For every type of f i x a t i v e , there w i l l be a d i f f e r e n t p r o p o r t i o n of the c i l i a t e fauna destroyed.  Therefore complete morphometric data i s not  a v a i l a b l e f o r a l l species. The i d e n t i f i c a t i o n from l i v e m a t e r i a l s makes accurate i d e n t i f i c a t i o n to species very d i f f i c u l t i n most cases. easy to d i s t i n g u i s h ,  In some genera, species are  such as Paramecium, Spirostpmum and Blepharisma.  In many smaller organisms (e.g. Coleps, Metopus and many s m a l l hypotrichs) genera can e a s i l y be assigned, but s p e c i f i c i d e n t i f i c a t i o n i s d i f f i c u l t .  26  F i n a l l y , i n some genera (e.g. Prorodon) taxonomy i s not c l e a r .  Unless  the species was c l e a r l y i d e n t i f i e d , the generic name i s used only.  The  monograph by Kahl (1930-1934) was used as the b a s i s of the nomenclature. 4 . P h y s i c a l parameters Continuous temperature records were kept at 1 and 4 meters depth by the use of Ryan temperature r e c o r d e r s . P r e c i p i t a t i o n ; data was taken from the records of the UBC Research Forest Spur #17, located on a ridge about two mile from Marion Lake.  Results 1. General population data The trend of the population at 1 meter i s c l e a r , w i t h two population maxima during the year. tendency f o r the peak  The f i r s t maxima was at the end of May, w i t h the d e n s i t i e s during the summer to be l e s s than the peak  at the end of May ( F i g . 1 ) . The population density remained low during the f a l l and e a r l y winter u n t i l the i c e l e f t the lake i n e a r l y Febuary. At that time the population "bloomed", and then d e c l i n e d , only to r i s e again i n May back to the c h a r a c t e r i s t i c summer density.  The mean density.  2 2 of c i l i a t e s at 1 meter i s 50/cm , with a range of 6/cm i n l a t e September 2 to a high of 100/cm  i n e a r l y June.  species at 1 meter show  The population trends of important  s i m i l a r trends, w i t h high d e n s i t i e s i n s p r i n g  and summer, and low d e n s i t i e s i n f a l l and winter ( F i g . 2 ) . The 4 meter population also shows a c l e a r increase i n the e a r l y summer, but the number of c i l i a t e s seems to o s c i l l a t e throughout the f a l l and never reaches the low d e n s i t i e s of the 1 meter population i n w i n t e r .  *3  To  face  Page  27  Figure 1  P o p u l a t i o n dynamics o f c j l i a t e s a t 1 meter depth i n M a r i o n Lake, u n i t s e x p r e s s e d as c i l i a t e s / c m . Bars i n d i c a t e 95% c o n f i d e n c e l i m i t s o f sample  To  f a c e Page  28  Figure 2 Population dynamics of^golepsMetropus, 'Prorodon and Paramecium b u r s a r i a at 1 meter depth., i n Marion Lake, u n i t s expressed as c i l i a t e s / c m 2 .  29 A ."bloom" at 4 meters i n Febuary i s s i m i l a r to the 1 meter bloom ( F i g . 3 ) . 2 Themean density of c i l i a t e s ' a t 4 meters i s 52/cm , w i t h a range of 2 2 13/cm i n l a t e J u l y to 96/cm i n e a r l y May (. F i g . 4). 2, Species ,  composition  T h i r t y two genera of c i l i a t e s were found i n Marion Lake.  Of these,  the most common were Coleps, Prorodon and an unkown c i l i a t e (put i n the Gymnostomatida, but p o s s i b l y Cinetochilum s p . ) .  Coleps contributed  about 30% of the t o t a l number of c i l i a t e s found at 1 meter (Tables 1 and 2 ) . Following the scheme of Grabaka (1971), the c i l i a t e s can be  classified  i n t o four groups of species: 1) very frequent- found i n 51-100% of the samples 2) frequent - found i n 21-50% of the samples 3) rare - found i n 11-20% of the samples 4) very rare  - found i n <^10%  of the samples.  Based on t h i s scheme, only f i v e species of c i l i a t e s were very frequently found i n Marion Lake (Coleps, Prorodon, Unid. gymnostome, Metopus, and an Unid. h y p o t r i c h ) . These species contributed most to the o v e r a l l v a r i a b i l i t y of the population at 1 meter ( F i g . 2 ) .  Grabaka (1971) found  a s i m i l a r number of frequent species i n the f i n g e r l i n g ponds she studied (Coleps, Prorodon, Cinetochilum, Uroleptus and A s p i d i s c a ) . About 50% of the species found i n Marion Lake were very r a r e ( F i g . 5 ) . These species were always found i n low numbers and do not i n d i v u d u a l l y have a large impact on the s i z e of the c i l i a t e population.  This i s  also s i m i l a r to Grabaka's (1971) data, where she found 50% of the species to be very r a r e . There i s a c o r r e l a t i o n between the number of i n d i v i d u a l s and numbers of species present at 1 meter i n Marion Lake (r=.55, p^.,01).  This would  i n d i c a t e that as the number of c i l i a t e s i n c r e a s e s , more rare species are  To  f a c e Page  30  Figure 3 Population dynamics of the c i l i a t e s at 4 meters depth i n Marion Lake, u n i t s expressed as c i l i a t e s / c m . Bars i n d i c a t e 9.5% confidence l i m i t s f o r the sample. 2  To f a c e Page 31.  Figure 4 Population dynamics of Coleps and Metopus at 4 meters i n Marion Lake, u n i t s expressed as c i l i a t e s / c m • z  32  Table I  Taxonomic l i s t of species found i n Marion Lake Order  Gymnostomatida Prorodon spp. Prorodon v i r i d i s Coleps spp. D i l e p t u s spp. Holophrya sp. Loxophyllum sp. Mesodinium sp. Lacrymaria sp. Placus sp. Loxodes magnus Nassula sp.  Order  Hymenostomatida Tetrahymena sp. Paramecium a u r e l i a P_. caudatum P_. b u r s a r i a Frontonia e l l i p t i c a F_. accuminata l Monochilum frontatum Cinetochilum margaritaceum e  u  c  a  s  Order O l i g i t r i c h i d a Strombidium sp. Halteria chlorelligera Order P e r i t r i c h i d a V o r t i c e l l a sp, E p i s t y l i s sp. Order H e t e r o t r i c h i d a Spirostomum ambiguum S. minor S. teres Stentor r o e s e l i S_. m u l l e r i S. coerulus Metops spp. Blepharisma muscorum B u r s a r i a sp. Condylostoma sp. Order Odontostomatida Caenomorpha sp.  Order Hypotrichida Euplotes sp. 8xytricha  sp.  Stylonychia mytilus Parurostyla weissei Uroleptus violaceus A s p l d i s c a sp. xHolostlcha sp.  Table I I Rank data f o r c i l i a t e s found at 1 meter i n Marion Lake Rank 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 3940 41 42  Name Coleps unid. gymnostome Prorodon unid. hypotrich Metopus Paramecium b u r s a r i a Loxophyllum Frontonia leucas unid. gymnostome #2 Holophrya Spirostomum Blepharisma muscorum Lacrymaria Stentor Dileptus Vorticella Stromidium Aspidisca Spirostomum minor Stentor igneus unid. hymenostome Paramecium a u r e l i a Loxodes Spirostomum teres unid. h e t e r o t r i c h Spirostomum ambiguum Uroleptus violaceus Holosticha Frontonia accuminata F. e l l i p t i c a Halteria chlorelligera Caenomorpha Nassula Homalozoon Parurostylaxweissei unid. pleuronematine Tetrahymena Euplotes Blepharisma . Bursaria unid. hymenostome #2 Strombidium  Number found 580 218 206 150 132 73 61 51 44 42 36 34 34 33 30 30 28 25 23 22 19 19 18 18 16 15 12 11 98 7 7 7 6 5 5 4 4 4 3.4 3 2  % of T o t a l 27.8 10.4 9.9 7.2 6.3 3.5 2.9 2.4 2.1 2.0 1.7 1.6 1.6 1.6 1.4 1.4 1.3 1.2 1.1 1.0 .92 .92 ,90 .89 .78 .71 .56 .51 ,45 ,36 .35 .35 .35 .29 .24 .24 .21 .21 .21 .16 .15 .11  35 added to the enumeratable population.  There i s also a c o r r e l a t i o n between  the number of Coleps and the t o t a l number of c i l i a t e s number of Prorodon and number of c i l i a t e s and the number of c i l i a t e s  (r=.75, p<  .01),  (r=.61, p< .01), and Metopus  (r=.5, p<.01).  3 . C i l i a t e populations and meteorological f a c t o r s The c i l i a t e population i n Marion Lake i s s i m i l a r to other c i l i a t e populations, i n that the d e n s i t i e s remain roughly w i t h i n an order of magnitude l e s s than the highest reported value (Table 3).  Given the  p o t e n t i a l rate of increase of the c i l i a t e s  Stachurska,  (Fenchel, 1968,  1975), these populations vary l i t t l e throughout the year. One p o s s i b l e way to evaluate patterns we saw i n population dynamics was to look f o r c o r r e l a t i o n s between p h y s i c a l f a c t o r s such as temperature and r a i n f a l l , and c i l i a t e d e n s i t y .  No c o r r e l a t i o n e x i s t s between  c i l i a t e density and r a i n f a l l , as reported by Hairston (1968).  A  p o s i t i v e c o r r e l a t i o n however e x i s t s between c i l i a t e density and temperature at 1 meter (Table 4). By using a modified s i g n test (Marten, pers. comm.), we can examine the short term c o r r e l a t i o n between population density and  temperature.  In the Marion Lake data, there was no short term c o r r e l a t i o n between these two v a r i a b l e s (Table 5 ) , (Greundling, 1971)  Temperature may  a f f e c t primary p r o d u c t i v i t y  and t o t a l benthic r e s p i r a t i o n (Hargrave, 1969), but i t  was not a primary f a c t o r i n f l u e n c i n g the c i l i a t e populations. This compares w e l l w i t h Fenchel's  (1969) data, as he a l s o found  no c o r r e l a t i o n between c i l i a t e density and temperature, e i t h e r i n the long or short run. This l a c k of c o r r e l a t i o n might be expected, however, as most e c o l o g i c a l f a c t o r s w i l l i n v o l v e some l a g periods before the population i s able to  To f a c e Page 36  Figure 5 D i s t r i b u t i o n of species found i n samples i n Marion Lake  36  1 Meter  201814106214-  2 Meters  12-  CO  8-  spec  10-  6-  H—  number  o  42-  4 Meters  1814106 -  10  ^"3  20 3 0 4 0 5 0 6 0 ° / samples found Q  70  80 90  100  37 Table I I I Minimum and maximum d e n s i t i e s of c i l i a t e s reported i n the l i t e r a t u r e , values are the maximum reported i n that paper.  Single  Author  Density  Goulder (1971a)  2500-8000/cm  Eutrophic l a k e , 3m, England  Grabaka (1971)  500-5000/cm  F e r t i l i z e d f i s h pond, Poland  Fenchel (1969)  900-4000/cm  I n t e r s t i t i a l sand beach Denmark  Fenchel (1975)  60-100/cm  A r c t i c tundra pond Alaska, USA  Pieczynska (1972)  30-r550/cm  2  E u l i t t o r a l eutrophic l a k e , Poland  A r l t (19-73)  20-200/cm  2  Subtidal i n t e r s t i t i a l sand, Germany  Borror (1963)-  54/cm  I n t e r t i d a l sand, F l o r i d a , USA  Moore  51/cm  Anaerobic profundal muck, Michigan, USA  (1939)-  Kool (present study).  Location  2  2  2  2  2  2  10-100/cm  2  Sublittoral oligotrophic l a k e , B.C., Canada  Table  IV  C o r r e l a t i o n c o e f f i c i e n t s (Spearman's r') between c i l i a t e density and various environmental f a c t o r s . Factor  Depth  r'  n  P  Temperature  1 meter  ,45  51  <.01  Temperature  4 meters  .18  20  n.s.  Rainfall  1 meter  .2  25  n.s.  Rainfall  4 meters  .06  23  n.s.  Table .V  Detrended (sign t e s t ) c o r r e l a t i o n s between c i l i a t e density and various p h y s i c a l f a c t o r s ( c o r r e l a t i o n as chi-square) Factor  Depth  n  P  Temperature  1 meter  .72  51  n.s.  Temperature  4 meters  .06  20  n.s.  Rainfall  1 meter  1.5  25  n.s.  Rainfall  4 meters  3.86  23  n.s.  40 respond to the environmental change.  I have examined the importance  of time lags by using s p e c t r a l c o r r e l a t i o n a n a l y s i s on detrended data (data which has had a t h i r d degree poynomial f i t t e d through i t ) ( F i g . 6 ) . The c o r r e l a t i o n i s done on the matched p a i r s of r e s i d u a l s from the polynomial and the c o r r e l a t i o n can be performed w i t h any l a g p e r i o d of one v a r i a b l e desired ( Marten, pers. comm., Blackman and Tukey, 1958). There was no c o r r e l a t i o n between c i l i a t e d protozoan density and e i t h e r temperature, r a i n f a l l or lake discharge r a t e , at any l a g period (Table 6 ) .  S i m i l a r l y , when s p e c t r a l a n a l y s i s was done on the data of  Fenchel (1969), no lagged c o r r e l a t i o n s appeared between c i l i a t e density and temperature. 4,. Population growth data Tables 7 and 8 give the c a l c u l a t e d values of r , the population i n t r i n s i c rate of increase f o r 1 and 4 meters.  The equation  N =N e t ° was used to c a l c u l a t e the value of r between the two sample dates, N r t  o and N » t  The i n t r i n s i c r a t e of increase i s made up of two components,  the b i r t h rate b, and the death rate d.  From Kool (1975), I can  estimate the predation rate (equal to d) f o r various times of the year. I f r and d are known, then the b i r t h r a t e can be c a l c u l a t e d , b=r+d (Table 7). The b i r t h r a t e c a l c u l a t e d f o r the f i e l d data can then be compared w i t h the data of Stachurska (1975) f o r c i l i a t e s grown i n the l a b o r a t o r y i n lake sediment at d i f f e r e n t temperatures.  Table 8 gives the value f o r  r , b, and d of the f i e l d data (when r i s p o s i t i v e ) , and then compares those values w i t h Stachurska's at the equivalent temperature.  Al Table  VI  S p e c t r a l c o r r e l a t i o n between c i l i a t e density and various p h y s i c a l f a c t o r s ( c o r r e l a t i o n i s Product-moment r ) Factor  Depth  r  n  p  Temperature  1 meter  .lA  51  n.s.  Rainfall  1 meter  -.18  25  n.s.  Table V I I I n t r i n s i c rate of increase Marion Lake.  ( r ) f o r the c i l i a t e population at 1 meter i n  Date  r  8 May '72 18 May 25 May 30 May 8 June 24 June 30 June 7 July 16 J u l y 26 J u l y 4 August 18 August 24 August 3 September 18 September 2 October 19 October 30 October 27 November 29 December 12 January '73 26 January 14 Febuary 27 Febuary 14 March 4 April 18 A p r i l 30 A p r i l 7 May 18 May 25 May  -.015 .024 .12 .089 -.02 -.05 -.028 .074 -.11 .083 .022 -.024 -.086 -.097 .05 -.054 .074 .003 -.015 .003 •T.OI  .035 .06 ^.034 ^.031 .03 -.02 .105 r.04 .04 -.016  Table VIII Values of r, b, and d calculated from the ciliate population at 1 meter in Marion Lake, contrasted with the lab data from Stachurska (1975). T is generation time in days..  Dates  Field data Temp.  r  b  d  T  25-30 May, '72  15 9 C.  .12  .25  ,13  2.7  8-16 July  15 °C  .07  ,15  .08  26 July-4 August  20°C  .08  .17  18 September-2 October  10°C  .06  19-30 October  5°C  14-27 Febuary, '73 30 A p r i l s May  b  T  .32  2,2  4.5  ,32  2.2  .08  4.1  .51  1.4  .09  .03  8.1  .19  3.7  .07  .11  .03  6.5  .12  5.6  5°C  .06  .14  .08  5.1  .12  5.6  10°C  .11  .21  .10  3,3  ,19-  3,7  -  To f a c e Page 4 4  Figure 6 An example of a t h i r d degree polynomial f i t t e d through, the data f o r May, June and J u l y , 1972.  temperature  45 Discussion 1 . Food l i m i t a t i o n hypothesis  of population r e g u l a t i o n  A f t e r a review of the l i t e r a t u r e regarding population r e g u l a t i o n of the c i l i a t e d Protozoa, i t seems c l e a r that the general consensus of workers i n the f i e l d i s that food l i m i t a t i o n i s the most l i k e l y f a c t o r involved. Hairston (1968) f e e l s that food l i m i t a t i o n i s the prime f a c t o r f o r two reasons; 1) that the dates of the major population peaks i n h i s study occur at a l l times of the year (as happens i n Marion Lake), thus e l i m i n a t i n g weather as an important f a c t o r , and 2) the observed l o s s rate i n the population i s independent of density at the s t a r t of the  observation  p e r i o d , thus e l i m i n a t i n g the density dependent predation argument.  He  found that the population increases were at times associated with r a i n f a l l , and he could d u p l i c a t e t h i s e f f e c t by watering an area with a garden hose.  The increase i n density of Paramecium was  due, he  to the presence of more food c a r r i e d by the water from the  maintains,  surrounding  s o i l to the small seep he studied. Gray (1952) also reported that the c i l i a t e s were found to "increase i n numbers a f t e r heavy rains or during prolonged drought, when the banks (of the stream) tend to crumble."  He f e l t that the c i l i a t e  population  was regulated by the q u a l i t y and quantity of b a c t e r i a i n the water, but that they are "made a v a i l a b l e as food by c l i m a t i c c o n d i t i o n s . . . " Johnson (1941) b r i e f l y reports that "the studies (of protozoan population growth) seems to i n d i c a t e that a depletion of the food supply i s more important as a l i m i t i n g f a c t o r i n population growth than are waste  products."  Grabaka (1971) and Goulder (1971a) imply that food i s the most important f a c t o r i n determining  the s i z e of c i l i a t e populations.  Grabaka (1971)  46  found the highest d e n s i t i e s of c i l i a t e s i n f i n g e r l i n g ponds to which the greatest amount of f e r t i l i z e r had been added, while the lowest d e n s i t i e s were found i n the c o n t r o l ponds.  Goulder (1971a) states that  the eutrophic c o n d i t i o n of one lake studied was the cause of the greater c i l i a t e density found there than i n a l e s s eutrophic pond. Pieczynska (1972) reports that a f t e r a l a r g e mass of planktonic algae was washed up on a sandy shore of a P o l i s h l a k e , the c i l i a t e 2 population increased from 292/10 cm  2 to 2880/10 cm  i n three days.  This  i s a population growth rate of .76, w i t h a generation time of .9 days; Stachurska  (1975) found a maximum mean generation time of 1.03 days f o r  c i l i a t e s growing at 25°C.  Pieczynska (1972) also states that a f t e r a  short time, the algae had been decomposed and the numbers of c i l i a t e s decreased. Fenchel (1969) , i n the most s i g n i f i c a n t study on the ecology of the c i l i a t e s done to date does not d i r e c t l y adress the question concerning what f a c t o r s c o n t r o l the s i z e of the microfaunal populations.  However, he  does i n d i c a t e h i s preference f o r the food l i m i t a t i o n hypothesis i n a number of ways.  In h i s d i s c u s s i o n of laboratory ecosystems, a l l references to  blooms of c i l i a t e s are associated w i t h d e s c r i p t i o n s of diatom or b a c t e r i a blooms, and never w i t h the decrease i n number of predators, or a decrease i n t h e i r rate of feeding on the c i l i a t e s . Fenchel (1968) demonstrates how the i n t r i n s i c rate of increase ( r ) of A s p i d i s c a v a r i e s w i t h concentration of food.  This would i n d i c a t e that  the growth rate of the population i s dependent on the food supply, which i s contrary to the r e s u l t s of Stachurska  (1975).  She found that  i n c r e a s i n g the amount of b a c t e r i a offered to Stylonychia growing i n lake sediment only increased the c a r r y i n g capacity of the sediment, but  47 did not increase the growth rate of the c i l i a t e s .  However, Fenchel's  work was done at very h i g h concentrations of b a c t e r i a growing i n proteose peptone, w h i l e Stachurska's was done under more r e a l i s t i c conditions w i t h much lower concentrations of food.  Fenchel (1969) concludes that  "the growth r a t e of the populations are lower than t h e i r p o t e n t i a l r a t e i n pure c u l t u r e " , and t h i s i s probably due to food l i m i t a t i o n . Stachurska (1975) performed experiments examining the p o s s i b l e r o l e of food l i m i t a t i o n i n r e g u l a t i n g the population of c i l i a t e s i n Marion Lake.  She found that only 2% of the t o t a l b a c t e r i a present i n the lake  were a v a i l a b l e f o r consumption by the c i l i a t e s .  A f t e r l a b e l l i n g sediment  14 bacteria with  C-glucose, she allowed  on 0.1 ml of the labeled sediment. individual c i l i a t e .  e i t h e r 20 or 50 c i l i a t e s to graze  Each day she she determined the  dpm/  A f t e r four days, she removed a l l the c i l i a t e s , and  then added the o r i g i n a l number back to the already grazed sediment and repeated her procedure.  She found much l e s s r a d i o a c t i v i t y i n the  l a t t e r groups as compared to the former.  The consumption rate (of  r a d i o a c t i v e m a t e r i a l ) declined 37% i n the sample w i t h 20 c i l i a t e s , and declined 61% i n the sample w i t h 50 c i l i a t e s .  She concluded that p o s s i b l y  "the consumption r a t e was lower as the amount of a v a i l a b l e food decreased". Another method f o r examining the p o s s i b i l i t y of food l i m i t a t i o n i n Marion Lake sediment i s to estimate the number of b a c t e r i a i n a volume of sediment, and then compare t h i s w i t h the number of b a c t e r i a the c i l i a t e s may eat i n a day.  H a l l and Hyatt (1974) using unpublished data of  P. Fraker, W. Ramey and B.K. Burnison, estimated that at l e a s t 2X10 2 b a c t e r i a l cells/cm are present i n the sediment, while Perry (1975) c a l c u l a t e d that there are between 5X10 9 and 1.6X10 10 bacteria/cm 2. Tezuka (1974) c a l c u l a t e d that Paramecium caudatum consumes 4.2X10^  g  48 bacteria/day, or 1700/hour.  Fenchel (1975) found Tetrahymena to consume  500-600 bacteria/hour during logarithmic growth, but during the stationary phase only 180-200 bacteria/hour. If 75% of the c i l i a t e s at 1 meter eat b a c t e r i a , and they eat roughly 1000 bacteria/hour (based on the above data), the summer density of ciliates  2 6 2 (80/cm ) would consume 1.9X10 bacteria/day/cm . 9  a density of 2X10  I f we assume  2 bacteria/cm  , and according to Stachurska  (1975) only  2% of these are a v a i l a b l e , then the c i l i a t e s could consume 4X10^ b a c t e r i a / 2 day / cm . Based on these c a l c u l a t i o n s , the c i l i a t e s could eat only 5% of the available bacteria/day, and only 0.1%  of the t o t a l bacteria/day.  In  radiotracer experiments done to examine the carbon flow i n the Marion Lake sediment (Marten, 1975), we have estimated that the c i l i a t e s were taking 0.5% of  of the t o t a l bacteria/day (see also Marten et a l , 1975,  f o r methods  analysis). Fenchel (1975) has presented a picture of the carbon flow i n a  small tundra pond. and microalgae  He based h i s estimates of carbon flow from b a c t e r i a  to c i l i a t e s by calculating from measured feeding r a t e s .  -He found that the c i l i a t e s ate only .03% of the t o t a l b a c t e r i a l  population/day.  Even assuming that only 2% of the b a c t e r i a are available to the c i l i a t e s , they would s t i l l have eaten  only 1.4%  of the available b a c t e r i a .  Goulder (1972), i n a study of feeding of Loxodes magnus on the green algae Scenedesmus sp. calculated that the c i l i a t e could eat .68% of the alga's standing crop.  Although he maintains  at most  that "grazing  by a l l invertebrates could be s i g n i f i c a n t " , i t i s unlikely that L. magnus (the numerically dominant c i l i a t e i n h i s study) could influence the standing crop of Scenedesmus, and was not food l i m i t e d .  49 2 . Predation l i m i t a t i o n hypothesis of population r e g u l a t i o n There are a number of reports i n the l i t e r a t u r e of predation being important i n c o n t r o l l i n g the c i l i a t e s populations.  Gray (1952) reported  a negative c o r r e l a t i o n between i n s e c t larvae and c i l i a t e s i n a stream. Maguire et a l (.1968) and Addicott (1974) also demonstrated the importance of i n s e c t l a r v a e i n reducing the number of c i l i a t e s i n small aquatic environments (plant b r a c t s ) . Kool (1975) reviewed the l i t e r a t u r e regarding c i l i a t e predation, and presented evidence that although the predation rate may  equal the population  growth r a t e during part of the winter i n Marion Lake, during the summer months the predation rate i s much lower than the p o t e n t i a l rate of increase of the p o p u l a t i o n , as determined by Stachurska  (1975).  I f density dependent predation was involved i n r e g u l a t i n g the population, then, according to Hairston (1968), we should f i n d a c o r r e l a t i o n between r (population i n t r i n s i c rate of increase) and the population density p r i o r to a d e c l i n e .  No c o r r e l a t i o n was  found (r=.07); the same  r e s u l t that Hairston found. . However, some s o r t of density dependent f a c t o r must be i n v o l v e d , as there are h i g h l y s i g n i f i c a n t negative c o r r e l a t i o n s between population density and r i n Marion Lake at both 1 and 4 meters.  When the data of Fenchel  (1969)  and Grabaka (1971) i s put to the same a n a l y s i s , a negative c o r r e l a t i o n i s also found (Table 9).  Tanner (1966) , while examining records of population  growth, performed c o r r e l a t i o n s as described above, and found that i n 47 out of 66 populations examined, a s i g n i f i c a n t negative c o r r e l a t i o n existed. 3.. Conclusion I have t r i e d to apply three standard mechanisms of population  /  Table  IX  C o r r e l a t i o n (Spearman's r') between the i n t r i n s i c rate of increase ( r ) and c i l i a t e density. The Helsing^r l o c a t i o n i s from Fenchel (1969), and the P o l i s h l o c a t i o n i s from Grabaka (1971). Location  r  n  Marion Lake 1 meter  -.36  32  Marion Lake 4 meters  -.7  20  <  .01  Helsing^r  -.38  27  <  .025  Poland  -.96  7  < .001  P  .025  51  r e g u l a t i o n , i e . weather and density independent f a c t o r s , and food and predation, to e x p l a i n the dynamics of the populations of c i l i a t e s i n Marion Lake.  A l l three explanations are u n s a t i s f a c t o r y by themselves,  and each cannot s u f f i c i e n t l y e x p l a i n the observations. I t seems h i g h l y u n l i k e l y that the c i l i a t e s can deplete t h e i r food supply, and Fenchel (19751 c a l c u l a t e s that a l l benthic invertebrates can consume only 50% of the b a c t e r i a present i n the sediment. rather than quantity of b a c t e r i a may  P o s s i b l y the q u a l i t y  i n f l u e n c e the growth, of the c i l i a t e s .  The. sediment b a c t e r i a may have to have an extremely adaptable to deal w i t h the sporadic inputs of organise^matter  biochemisty  ( K l e i b e r , pers. comm),  and consequently may be of higher n u t r i t i o n a l q u a l i t y at c e r t i a n times of the year, while of poorer q u a l i t y at other times. Waste product i n h i b i t i o n was not examined as a p o s s i b l e f a c t o r i n c o n t r o l l i n g the c i l i a t e population.  I t was u n l i k e l y that at the r e l a t i v e l y low  d e n s i t i e s present i n the f i e l d (compared to d e n s i t i e s common i n c u l t u r e s ) and the r a p i d f l u s h i n g of the lake ( E f f o r d , 19.671 that an i n h i b i t i n g concentration of waste products could ever b u i l d up. Although the predation rate seems to be to low to be able to c o n t r o l the p o t e n t i a l r a t e of reproduction of the c i l i a t e s , i f the f i e l d reproductive r a t e i s lower than the r a t e measured by Stachurska  (1975).  i n the l a b , then predation may be more important i n c o n t r o l l i n g the population than I now assume. The data i n d i c a t e that f a c t o r s c o n t r o l l i n g the population act i n a density dependent fashion. do not seem to apply.  However, the standard density dependent mechanisms  P o s s i b l y some i n t e r a c t i o n between the various f a c t o r s  not yet studied are responsible f o r the observed population dynamics.  Acknowlegements I must thank Dr. Ian E f f o r d f o r h i s i n t e r e s t and assistance. Berger and Michael Hoebel gave most u s e f u l c r i t i c i s m .  Dr. Tom  k i n d l y provided the data from h i s 1969 paper.  Dr. A.C.  gave me the ideas f o r the e x t r a c t i o n process.  Dr. Teresa  Dr. Jim Fenchel  Borror f i r s t Stachurska,  Dr. Gerry Marten and Michael Hoebel a l l a s s i s t e d i n the planning and execution of the work, and made the time spent very pleasant.  53 References A d d i c o t t , J.F.: Predation and prey community s t r u c t u r e :  An experimental  study of the e f f e c t of mosquito larvae on the protozoan of p i t c h e r p l a n t s .  communities  Ecology 55, 475-492 (1974)  A r l t , G.: V e r t i c a l and h o r i z o n t a l m i c r o d i s t r i b u t i o n of the meiofauna i n the Greifswalder Bodden. Blackman, R.B., Tukey, J.W.: New York, N.Y.  Oikos (suppl) 15_, 105-111 (1973)  The measurement of power s p e c t r a . Dover P r e s s ,  (1958)  Borror, A.C.: Morphology and ecology of the benthic c i l i a t e d Protozoa of A l l i g a t o r Harbor, F l o r i d a .  Arch. 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