FEEDINC
RATE OF DAPHNIA
MAGNA STRAUS IN DIFFERENT
FOODS LABELED
WITH RADIOACTIVE
PHOSPIIORUSL
J. W. McMahon”
Dcpartmcnt
of Zoology,
University
and F. Il. Ri&r
of Toron to, ‘Toronto,
Ontario
The f&cling
rntc of Unphnia mqp~
was studied by measuring the radioactivity
of
animals Ecd on pure cultures of Escherichia
coli, Saccharomyces
cwevuisicw, Chlorella vull?yrifornzis labclcd with radioactive
phosphorus.
Uclow a certain
guris, and Tetruhymena
concentration
of each food, the feeding rate is proportional
to conccntrntion
of food. Above
that concentration,
feeding rate is indcpcndcnt
of concentration.
Starved animals, when
placed in a nonlimiting
conccntmtion
of food, bchavc temporarily
as if it wcrc limiting and
for a few minutes filter at the maximum rate. Although the maximum volume of the various foods eaten in unit time is not the same, it is probably dctcrmincd more by digestibility
than by size of the food cells.
Filtering
efficiency
of Daphnia mcrglzn is indcpcnclcnt
of the size of food cells bctwccn
0.9 pL3and 1.8 X 10’ #.
Log-phc
ChZorelZa vzrlgwis was not obscrvcd to inhibit feeding, but scncsccnt 41s
GluScd Duphniu magnu to dccrcnsc the filtering
rntc and its maximum feeding r&.
( 1963)) during studies of the behavior of
Dqdanin
magna in an observation chamber,
The first purpose of this work was to
found
that
the relation between feeding
investigate the possibility
that log-phase
of both SacckaChlore,& vulgaris cells inhibit the feeding of rate and concentration
romyczrs
cerevisiae
and
ChZoreZZa
vulgaris
Daphnia magna. This inhibitory cffcct was
was
the
same
as
that
described
by
Rigler
postulated by Ryther ( 1954) to explain two
(
19Glh).
Since
their
cstimatcs
of
the
volobservations. The first was that in concentrations of ChZoreZZuvulgaris above 2 x lo5 ume of food boluses swallowed wwc subcells/ml, the feeding rate of Duphnia magna jective, it scemcd desirable to make careful
quantitative mcasurcmcnts of the feeding
was not proportional to food concentration,
rate
of Daphrzia magna in both of thcsc
although it continued to increase with insince the Fact that
creasing concentration. The validity of this foods. Furthcrmorc,
observation as evidence of inhibition
was fcoding behavior in Sacchnromyces cere,visine and Chloretla vuZguris was dcmonqucstioncd by Rigler ( 19Glb), who showed
stratcd to be the same could bc interprctcd
that when D. magna is fed Saccharomyces
cereuisine, the relationship between Eccd- equally well as showing either that Snccharomyces cerevisiae is toxic or that C1%Zoing rate and food concentration
is that
relka vulgaris is not, two additional foods
which might bc expected bctwecn any biowere
studied. One was a small bacterial
logical process and a factor capable of
limiting that process, Below a critical con- cell (Escherichin coli) and the other a much
larger ciliated protozoan
( Tetrdzymenu
centration, or, according to Fry’s ( 1947)
pyriformis ) .
terminology, below the ‘incipient
limiting
The second observation considcrcd by
level,” the feeding rate is proportional
to
Ryther to be consistent with his hypothesis
concentration; above this level, they are inwas that animals previously fed on bacteria
dependent.
Then McMahon
and Riglcr
and detritus consumed the same number of
ChZoreZZa vuZgaris cells in 1 hr as starved
1 This work was supported by rcscnrch grants
From the National
Rcscarch Council
of Can&
animals, whereas those previously fed on C.
ancl from the University
of Toronto Advisory Comvulgaris consumed fcwcr.
He reasoned
mittcc on Scientific
Rcscarch.
It form&l part of
that since a starved animal ate as much as
n doctoral thesis prcscntcd by J. W. McMahon.
an animal previously fed on bacteria and
2 Present address: Chalk River Nuclear Laboratories, Chalk River, Ontario, Canada.
detritus, the feeding rate is unaffected by
105
INTRODUCTTON
106
J. W.
Mc,MAIION
the amount of food in the animal’s gut.
the reduced feeding by animals
t)rcviously fed C. vulgaris was cvidencc
that they had been poisoned during the
prior feeding perio,d. However, McMahon
and Rigler (1963) found evidence suggesting that feeding rate is affected by the
amount of food in the animal’s gut, and
they also were unable to demonstrate any
cumulative inhibition of feeding even after
24 hr in C. vzrZ,~@s cultures. Although we
have not fully resolved these diffcrcnccs,
WC will present additional evidence that a
starved animal consumes more food in 1 hr
than a fed animal when both are in non1imiting concentrations of C. vulgnris.
Finally, Ryther (1954) observed that
Ikphnin
magna ,did not survive on a diet
of senescent Chlorella vulgaris and that
fewer senescent cells than log-phase cells
wcrc eaten. Since WC had been unable to
obtain any unambiguous cvidencc that logphase C. vulgaris was toxic or inhibitory, it
sccmcd desirable to reinvestigate his hypothesis that senescent cells were more
toxic than log-phase cells.
IIc~Mx,
MATERIALS
AND
MIXTIIODS
Daphnia magna were cultured by the
method described by McMahon and Riglcr
(1963), and mature females 2.8-3.3 mm long
(0.22-0.34 mg dry wt) were used in all cxpcrimcnts. Axenic cultures of Sacchzromzjces
cerevitiae were grown in acratcd dextrose
medium (Riglcr 1961b). Chlorellu vulgaris,
obtained from Dr. R. C. Starr, Indiana Univcrsity, was culturccl by the method of
McMahon and Riglcr ( 1963). Escherichia
COGwas maintained on Difco nutrient agar
plates. Axenic cultures of E. COG were
grown in Difco nutrient broth at 37C for
12-14 hr. Tetrahymew
pyriformis
strain
T. C. 105, obtained from Dr. I. Tallan, Univcrsity of Toronto, were cultured at 20C
for 48-60 hr in the following medium: 1
liter of deionized distilled water containing
10 g proteosc peptonc, 5 g @@one, 1 g
sodium acetate, 1 g potassium dihydrogm
phosphate, 0.005 g thiamine HCl, 0.1 g
yeast extract, and 0.1 g liver extract. The
AND
P. II.
RIGLER
~11 was adjusted to 7.2-7.4 with 1 n/r sodium
hydroxide.
When radioactive
food was required,
carrier-free Pn2 was added to the culture
medium. Radioactive algal, yeast, or bacterial cells were centrifuged twice and rcsuspended in membrane-filtered,
dechlorinatcd tap water before they were used in
feeding experiments. Radioactive T. pyriformis to be used for feeding were transferrcd from the medium to filtered tap
water by the clectromigration
technique
described by Van Wagtendonk,
Simonsen, and Zill ( 1952), because the cultures
often contained particulate
matter that
could not conveniently be separated from
the protozoans by centrifugation
or filtration.
Concentrations of yeast and algae were
then measured by counting 1,000 or more
cells in a hemacytometcr.
The concentration of bacteria was determined with a
Pctroff-IIauscr
bacterial counting chamber
under a phase-contrast microscope. The
concentration of Tetrahymena was detcrmined with a Model R Coulter particle
counter cquippcd with a 200-p-aperture
tube. Suspensions were then diluted with
filtered tap water to the desired conccntrations. Samples were examined with a phasccontrast microscope and discarded if contaminants were present.
Unless otherwise stated, animals were
previously fed for 1 hr in nonradioactive
food at the same concentrations as the radioactive food to which they were to be exposed. The experiment was begun when
the animals were transferred by net to the
radioactive food suspension. The volume
of water per animal was adjusted so that
feeding would reduce the concentration of
the cells by less than 10%. Water tcmpcraturc was constant at 20 + 1C. Feeding cxpcriments wcrc limit& to a 20-min period
to avoid loss of radioactive food from the
animal’s gut through defecation.
At the
end of the feeding cxpcriment, the animals
wcrc removed from the food suspension,
rinsed for a few seconds in tap water,
blotted gently on filter paper, and dried on
FEEDING
planchcts.
Their
sured as rcportcd
RATE
OP
DAPZZNZA
radioactivity
was mcaby Riglcr ( 1961u).
msuLTs
foocls
1.0
2.0
3.0
$
5.0
40
MILLIONS
I
6.0
7.0
6.0
OF CELLS/ML
I
9.0
I
10.0
0
0.5 0
/,
0.4
Chlorella
I/
0.3 i
0
I3
vulgoris
.
.
Socchoromyces
0
OI
”
02
0.3
”
05
04
MILLIONS
cerevisiae
1.1
”
06
07
0.6
OF CELLS/ML
09
’
I .o
107
FOODS
feeding
TAULE 1. Maximum
magna (2.8-3.3 mm) on foods
organism
To check the relationship between the
feeding rate of Daphnia rnngna and the conccntration of food, feeding rates were measurcd in different concentrations of four
foods. One hundre,d animals were used at
each of seven concentrations of ChZoreZlrL
wu&ris, 50 at each of five concentrations
OPSacchuromyces cerevisiae, 20 at each of
seven concentrations of Escherichia coli,
.I
DCPlWlEWT’
l?OOd
FeetZing rate in different
3
IN
of
I)aphnia
cclls/l1r)
5.6
0.005
34
34
0.50
0.027
0.017
0.001
66
0.25
0.016
x 10"
0.0028
0.051
0.9
Maximum
fwding
riltc (mil-
sixes
Volume
of
l-oocl ccrlsiunccl pci
animal
(rnm~/hr)
Cdl
v01u1nc
(N’)
Escherichia
coli
ChZoreZZu vu2 6 nris
Log-phase
Scncsccnt
Scrccharomycas
cerevisine
Tetrahymenn
j@formb
1.8
rale
of tliffcrent
lions
of
and 100 at each of six concentrations of
Tetrahymena pyriformis.
The feeding behavior of Daphnia magncl
was essentially the same in each of the four
foods ( Fig. 1). Above a certain concentration of food cells, feeding rate was no
longer proportional to concentration but remained constant. The incipient limiting
concentration decreased as the size of the
food cells increased. With the largest ccl],
Tetrahymenn
pyriformis,
it occurred at
about lo3 cells/ml, whereas it was above
lo6 cells/ml when Escherichia coli was the
food. Consequently, the maximum volume
of the various foods catcn was similar, although maximum rates cxprcsscd as cells
hr-’ differed trcmcndously (Table 1). The
maximum volume ingested was not indcpendent of the nature of the food, bccausc
the volume of Tetrahymena
pyriformis
catcn was 10 times that of Escherichia co&
although the volumes of Chtoretlu vulgwis
and Saccharomyces cerevisiae catcn were
similar and intermediate bctwccn the other
foods.
FeecZing rate of starvetl anal prefe(Z c~nimds
“I
THOUSANDS
0F
cELts/ML
3
FlG. 1. Feeding rate of Daphnia magna on the
food organisms Escherichia coli, Chlorella vulgaris,
Snccharomyces
cerevkiae,
and Tetrahymenn
pyriformis.
Since the range of concentrations
was so
tliffcrcnt
for Escherichia
co2i and Tetruhymonn
pyriformis,
they wcrc plotted on separate graphs.
To give an idea of the actual relationship,
Sncchuromyces cerevisiae
and Chlorella
vulgaris
were
plotted to scale on Graph A.
From direct observations of the feeding
behavior of Daphnia magna, McMahon and
Rigler ( 1963) concluded that a starved animal, when exposed to a nonlimiting
concentration of food, feeds for a short time at
an abnormally high rate. To test this conclusion, the, feeding rates of starved and fed
D. magnu were measured as follows: One
group of starved animals and one group of
108
0.6-
J. W.
McMAHON
A
?
f
TIME-MINUTES
FIG.
2.
Cells consumed by starved and previously fed Daphnia magna in concentrations of
5 x 10’ and 5 x 10” cells per ml of log-phase
Clzlorelk~ vulgaris.
Each point represents the average of 100 animals.
S'J
/
animals previously fed in 5 x lo4 cells/ml
of Chlorella vulgaris were placed in a suspension of 5 x lo4 cells/ml of radioactive
C. vulgaris. At intervals, subsamples of 20
animals were removed from the radioactive
algal suspension and assayed for radioactivity. Two other groups, one starved and one
fed in 5 x lo’) cells//ml, were placed in a suspension of 5 x 1V cells/ml of radioactive
algae and sampled at intervals. The two
concentrations of algae, 5 X 104 cells/ml
and 5 x 10” cells/ml, were chosen because
they were, respectively, well below and well
above the incipient limiting concentration
of food. This experiment was repeated and,
although they are similar, the results of both
‘tests are presented (Fig. 2) because the slight
difference between them is of interest.
When Daphnia magna was exposed to a
limiting
concentration
(5 X 10” cells/ml)
of algae, there was no difference between
the feeding rate of starved and fed animals
(Fig. 2). When exposed to a nonlimiting
concentration (5 x lo5 cells/ml), the starved
animals initially ingested algae more rapidly
than the fed animals. Comparison of the
initial feeding rates of starved animals in a
suspension of 5 x lo” cells/ml with the
feeding rate in 5 x 104 cells/ml shows that
the starved animals were feeding at the
AND
F. H. RIGLER
maximum possible rate. They consumed
1.77 x 10” cells/hr,
as compared with
1.71 x 10” cells/hr eaten by animals in the
more dilute suspension (average of A and
B, Fig. 2). Thus, a tenfold increase in food
supply caused a tenfold increase in feeding
rate, a result possible only if the starved
animals in 5 X lo5 cells/ml
temporarily
abandoned all regulation of collecting and
ingesting rates.
The difference between the two experiments was that the fed animals given 5 x
lo5 cells/ml fed more rapidly in experiment
B than in experiment A (Fig. 2). The feeding rates calculated from the slopes of the
uptake curves between 5 and 30 min were
0.31 x 10” cells/hr in A and 0.65 x 10”
cells/hr in B. Since the filtering rates were
the same in the two experimen&!the
difer?%ce-Z&EitG
that-the ?naZ~rnumft!%drate
i’- ing rate can vary while the filtering
below
the
incipient
li-miting
level
remains
__--__
-I
\
\ cons&.nt. ,ZG average size of the Chlorella
vulgaris cells used in the two experiments
was not measured, so the difference may
merely indicate that the algal cells used in
experiment A were twice the size of those:
in B. However, we have never detected a
change of this magnitude in the average
volume of our C. vulgaris. Possibly, therefore, the maximum volume eaten by Daphniu magna may be influenced by factors
other than the nature of the food.
LI
The effect of senescent Chlorella
on feeding behavior
vulgaris
Our previous experiments involved only
C. vulgaris cells taken from cultures in the
logarithmic growth phase. In these experiments, we were unable to demonstrate conclusively an inhibition
of feeding by logphase C. vulgaris.
Consequently,
we
questioned Ryther’s ( 1954) conclusion that
the inhibitory action of senescent cells was
greater than the inhibitory
action of logphase cells. This conclusion was derived
primarily from his observation that Daphnia
magna invariably ingested fewer senescent
than log-phase cells in 1 hr. Since most of
his measurements of feeding in senescent
cells appeared to have been done above the
FEEDING
RATE
OF DAPZZNZA IN DIP~ERENT
incipient limiting level (Fig. 3)) one might
describe, his results by saying that the maximum feeding rate on senescent cells was
lower than on log-phase cells. A variation
in maximum feeding rate apparently dots
take place in the absence of variation of
cell size ( l?ig. 2), and, in this case, a rcduction of maximum feeding rata could bc
attributed to a toxic effect of the food.
lIowcvcr,
the maximum feeding rate is
nearly inversdy proportional to volume 0E
food cells (Table l), and since Fogg ( 1953)
reported that senescent ChZoreZZa cells arc
larger than log-phase cells, the possibility
that Ryther’s observation was the result of
a size effect was investigated.
Preliminary tests showed that thcrc was
no difference between the size of logphase and senescent C. m&ark cells grown
Both had an average
in our laboratory.
diamctcr of 4.1 p. However, Ryther’s algae
could have bchavcd like Fogg’s rather than
like ours, and the possibility still remained
that his results were caused by a size differcnce. Thcreforc,
using scncsccnt cells
known to bc the same size as our log-phase
cells, WC repeated Ryther’s mcasurcment of
‘,‘r-----
CHLORELLA
I
0.2
I
0.4
I
0.6
MILLIONS
I
0.8
I
1.0
0.2
OF CHLORELLA
0.4
0.6
0.8
1.0
CELLS/ML
FIG. 3.
Left: Thcorctical
values of the number
of Chbdla
dgaris
cc& consumed by Daphnia
magna &ring
a 1-hr fccccling cxpcrimcnt
calculated from results in Fig. 2. Right:
Ryther’s cxwkncntal
results ulottccl to the same scale.
109
l?OODS
Fee&g
rate of Daphnia magna in
@ferent conccntrcltions of senescent Clllorclla
TABLE 2.
vulgaris
Conccntrntion
(millions
of
ccll,s /ml)
\
0.001
\ ‘~
0.01
0.1
0.2
0.4
0.0
Cells consmxd
per animal
(thousnnds/hr)
0.8
5.4
27.0
20.0
32.0
30.0
the feeding rate in diffcrcnt concentrations
of scncscent cells. Six groups of Dnphrkz
mugnn were fed for 1 hr in senescent ChZOW&Z wzcZ@s and then transferred to a radioactive algal suspension of the same conccntration for 20 min. The feeding rate,
calculated from the radioactivity
of the
Dnph.nia magna, is shown in Table 2. The
sencsccnt Chlorella wuZ,garis had a pronounced effect both on the filtering rate
below the incipient limiting concentration
an d on the maximum feeding rate. The
normal filtering rate in log-phase cells is
from 2.7-3.4 ml/hr ( SEX Table 4)) but in
scncsccnt cells it was only 0.7 ml/l-n. Even
more pronounced was the effect on the
maximum feeding rate, which was rcduccd
to 3 X 10” cells/hr from a usual value of
30-60 x W cclls/hr.
Direct observation of the behavior of animals exposed first to 5 x 10;’ cells/ml of
log-phase C. wuZgaris and then to the same
concentration of senescent cells showed the
mechanism by which food intake is rcstrictcd and suggested the location of the
inhibitory stimulus. In log-phase cells, the
thoracic appendages beat 132 times per
minute. This rate is to be cxpccted at this
concentration and is the minimum rate observed in acceptable foods (McMahon and
Rigler 1963). However, when the animal
was cxposcd to senescent cells, the rate of
m\ovcmcnt of the thoracic
appendages
dropped over a period of 15 min to 74
cycles/min. Thus, one mechanism restrict- ing food intake in senescent C. wulgaris is
reduction of the rate of filtering water.
TIE slow resnonse and the reduction of
1.10
J. W.
McMAIION
AND
‘rh131x
3.
The feeding rate in log-phase Cldorclla
vnlgxris of animal.3 previously feel in either senescent C. vulgaris or in log-phase C. vulgnris
Cells
Concentration
(millions
of
cc~lls/ml)
I’rcfcd
consumccl
(millions/hr)
log-phnsc
ChlOWZZ~
0.05
0.3
0.s
0.21
0.54
0.48
per
animal
Prdccl
scncac~n
ChZomZZa
t
0.13
0.22
0.21
pumping rate, a mechanism previously suggcstcd by McMahon and Riglcr (1963) to
1)~ under the control of sensory receptors
in the gut, suggest that inhibition
is not
merely a taste phenomenon associated with
stimulation of external chcmoreccptors but
is caused by stimulation of internal reccptors or, perhaps, an adverse physiological
cEfcct of the absorbed materials.
Confirmation
of the above conclusion
came from an experiment in which one
group of Daphnia magna were fed for 2 hr
on senescent ChZoreZZa vuZgnris cells and
another group was fed for the same time
on log-phase algae. Both groups were then
transferred to radioactive, log-phase C. vulgaris, and their feeding rates were measured during the first 20 min in this suspension. The experiment was repeated
with three different concentrations of algal
cells, two of which were nonlimiting.
The rationale of this experiment was as
follows: The animals fcoding in scncsccnt
C. vuZgaris would eat at an abnormally low
rate and when transferred to the suspcnsion of radioactive, log-phase cells would
have less food in their gut than those which
had fed on log-phase cells. If the inhibitory
cffcct of senescent algae were mcdiatcd by
cxtcrnal chemoreceptors only, these animals
would bc expected to behave as partially
starved animals for a short time after immersion in radioactive
algae and thus
would consume more cells in 20 min than
those previously fed in log-phase cells.
Convcrscly, if the scnesccnt algae acted intcrnally, they would remain in the gut and
cxcrt their adverse cffcct for some time al&r
the animals were transfcrrcd to the lognh:~so cells. IIcncc. animals 1XYXiously fed
F. I-1. RIGLER
senescent a.lgae would consume fewer cells
than the control animals,
The experiment (Table 3) showed that
at each concentration, the animals previOUSTS fed senescent C. vulguris ate fewer Iogphase cells than tho controls, a result that
is consistent with the postulated internal
action of sencsccnt C. vzclgnris.
DISCUSSION
It is now clear that the relationship bctwecn the concentration of food and the
feeding rate of Daphnia magna is similar
for a variety of foods. In every case, a
maximum feeding rate was attained, and a
further increase of availability of food did
not influence feeding rate. The same observation was made by Reeve ( 1963a), who
measured the fce,ding rate of Artemia
sulina on three spccics of food organisms.
Thus, Ryther’s observation that the rate of
increase of feeding rate decreases above a
certain concentration of log-phase ClzZoreZZ~
vuZgaris can no longer be considcrcd to bc
evidence that this food inhibits the feeding
of Daphnia magna. However, two problems concerning the interpretation
of Ryther’s results still exist. They concern, first,
why the animals previously fed on ChZoreZZa
ate fewer cells in 1 hr than starved animals
or animals previously fed “bacteria and dctritus,” and, second, why the feeding rate
of starved animals continued to incrcasc as
the concentration of C. vuZgnris incrcascd.
In an attempt to answer the first qucstion, McMahon
and Riglcr ( 1963) and
and Reeve ( 1963a) suggested that Ryther’s
animals that were fed bacteria and detritus
had actually previously been feeding at a
very low rate and thus behaved as star&
animals when given an excess of C. vulgaris.
However, those that had been fed algae
had full guts when transferrod to C. VUZg&s suspensions, and they thus limited
their food intake during the cntirc cxpcrimental period, We have now measured the
differcncc bctwcen feeding rate of starved
and fed animals and have shown that
starved animals, in a nonlimiting concentration of food, bchavc as if food wcrc limiting and, for some time, filter water at the
FEEDINC,
,
RATE
OF nAZ-‘ZINZA
maximum rate ( Fig. 2). With this information, one can estimate the amount of food
that a starved animal would eat during 1
hr in any concentration of food and make a
direct comparison of the differcncc
cxpetted between a starved and a fed animal
caused by the rapid initial feeding of the
starved animal and the difference observed
by Ryther (1954).
To calculate the amount of food eaten by
a starved animal in 1 hr, we made the simplifying approximation
that a starved animal feeds at the maximum rate until it has
FiTliif its g u t and then immediately reduces
its rate to that characteristic of a fed animal. That this is not correct is obvious
from Fig. 2, but the error introduced by
this approximation will tend to exaggerate
the difference between starved and fed
animals. To estimate the number of algal
cells in a full gut, we assumed that the
abrupt cessation of uptake of Pg2 by the
starved animals in Fig. 2B indicates the beginning of defecation of radioactive cells
and hence that a full gut contained approximately 0.55 x 10” cells. The fact that the
fed animals feeding in 5 x 10” cells/ml in
the same experiment consumed this number of cells in 48 min, a time: close to that
given by Bourne ( 1959) and Rigler (196lb)
as the minimum time for a food cell to pass
through the gut, is consistent with this assumption.
The food intake calculated from the results in Fig. 2A and B, arc shown in Fig, 3
beside Ryther’s results. Fig. 3 shows that a
starved animal in a nonlimiting
conccntration of food would be cxpectcd to eat considerably more cells in the first hour than a
fed animal and that the difference bctwecn
the two would increase as the conccntration of cells increases. However, in spite of
the fact that the difference is exaggerated
by the above approximation, it does not account for more than half of the difference
obscrvcd by Ryther. Therefore, unless an
altcrnativc explanation can be found to account for the residual differcncc, the hypothesis that log-phase Chlor&
vulgaris
can, at times, inhibit the feeding of l&r.phnicr. mngmz cannot hc rcjcctcd.
IN
DIPl?ElULN’~
FOODS
111
An ans,wer to the second question posed
by Ryther’s results is also suggested by Fig.
3, which shows that in the range of conccntrations studied by Ryther (up to 0.6 X 10”
cells/ml) the number of cells eaten by N
stawed animal in its first hour of feeding,
when plotted against the concentration of
cells, does not conform to the relationship
between the feeding rate of a fed animal
and the concentration of cells. It differs in
that the number of cells eaten continues to
increase with concentration above the incipicnt limiting concentration.
The only incontrovertible
indicts of the
desirability of a given species as food for
D. mqruz are growth and survival of D.
magna supplied with that food. However,
a given food might bc undesirable lmx~~sc
it a) inhibits feeding, b ) is toxic, c ) is indigestible, or d) is deficient in some esscntial nutrient. When D. magna are supplied
with a pure culture of an organism, undcsirable for any one of these reasons, the rcsult will be the same, reduced growth or
death. In nature, pure cultures are not
available, and the effects of indigestibility
or nutritional
inadequacy of one spccics
might be masked by the presence of other,
desirable foods. Conversely, an inhibitory
or toxic action of one species mig,ht affect
the animal in such a way that ingestion of
all species would be reduced. Therefore, it
would be useful to have a simple way of
determining whe.ther a given food is undcsirable because it is inhibitory or toxic or
because it is indigestible or nutritionally
incomplete.
Inhibitory or toxic foods should dccrcnsc
food intake, and thus they might bc dctectcd by their cffcct on tither filtering rate
below the incipient limiting concentration
or on the maximum food intake, providctl
that there is a standard with which any individual food can be compared. Table 4
shows that it will probably bc possible to
cstnblish the “normal” filtering rate of D.
mugnu. In four foods, the filtering rate was
approximately the same, although the smallcst (Esch&chia
coli) was 2-3 p long, ant1
the largest ( Tetdzymena
pyriformis)
was
37-68 /.A. If, xs Table 4 suggests, filtering
I12
TAnrAd 4.
J. W.
Filtering
McMAHON
AND
J?. II.
IUGLER
rates of 2.8-3.3-mm
Daphnia magna measured below the incipient
concentrntion
of CLwzridy of foods hetzwen 18 and 2OC
Source of measllroment
limiting
Filtering r:i tck
per aiiimnl
(1111/h)
rates arc indepcndcnt of food size, and if
care is taken to provide less than the incipient limiting concentration of a food organism, a measurement of filtering rate in only
one conccntra tion of foocl might be enough
to sho,w whether or not tllat species wcrc
toxic or inhibitory.
Thus, scncscent CM+
dh
ZX&ZT~S, which has been shown to bc
inhibitory by a variety of experiments, is
Ciltcrcd only one-quarter as rapidly as other
foods.
Although senescent C. v~@aris apparcntly ha,d an even greater cffcct on the
maximum volume of food ingested (Tables
1 and 3)) this is at present a less rcliablc
indication of inhibition or toxicity than the
cffcct on filtering rate. There is cvidencc
that feeding of some microcrustaceans is
ultimately limited by the maximum volume
of food the gut will pass (Ryther 1954,
Reeve 1963a, and Table 1) , but several obscrvations aro inconsistent with this simple
explanation. First, Daphnia magnu ingcs ted
10 times as much Tetrnhymena
p’yriformis as Escherichiu coli, although both
foods were acceptable as judged by the
filtering rate of Daphnia magnn in limiting
This tenfold
difference
concentrations.
might be attributed to a difference in the
digestibility of the two foods. Tetrahymena
pyriformis is large and easily ruptured. If
it is more digestible than Escherichia co&
and, if the residue is compacted into a
smaller volume than that of E. cc&, then
J’ig. 1
3.4
Fig. 1
Fig. 2
Fig. 2
Ryther ( 1954)
Table 3
Fig. 1
McMahon
( 1962 ), Table 1
McMahon
(1962), Tnblc XIIIa
McA&Aon
(1962), Table XTIIb
Riglcr ( 196117)
Fig. 1
2.7
3.0
3.4
3.3
0.7
2.2
2.2
3.2
3.1
2.6
3.0
the gut might pass a larger volume of
Tetrahymena pyrifwmis.
IIowcver, Reeve’s
( 19G3b) observation that Artemia sdinn
consumes a much larger volume of sand or
sand mixed with algae than it does of a
pure culture of algal cells is inconsistent
with this hypothesis. Thus, the maximum
volume ingested may be influenced by the
digestibility and nutritional value of a food
as well as by inhibitory or toxic properties.
Until more is known about the factors limiting the maximum intake of various foods,
the best and-most easily o,btainable Gidencc
of inhibition
_.-...-or-go-city is probably an abnorrrial$YJow filtering rate, mcasurcd either- as
an ingestion rate or as the rate of movement of thoracic appendages in a limiting
concentration of the food in question.
REPERGNCE,S
N. F. 1959. The dctcrminntion
of
carbon transfer from Chlorella udgaris Bcycrinck to Daphina magna Straus, using radionctivc carbon (04)
as a tracer. Ph.D. Thesis,
Univ. Toronto.
Fwc;,
G. E. 1953. Famous plants-Chlorella.
New Biol., Penguin Books, Ltd., 15: 99-116.
lby,
F. E. J. 1947. Effects of the cnvironmcnt
Publ. Ontario
Fisheries
on animal activity.
Kcs. Lab., No. 68, Univ. Toronto Press, 62 p.
1962. The feeding behaviour
MCMAIION,
J. W.
and feeding rate of Duphniu magna in difPh.D. Thesis,
fercnt conccntrntions
of foods.
Univ. Toronto.
1963. Mechanisms
-,
AND F. H. RIGLER.
regulating the feeding rate of Daphnia mngnn
Can. J. Zool., 41: 321-332.
S traus.
hUl~NE,
I~EEDING
RATE
OF DAPZZNZA
REEVE, M. 1~. 1963a.
The filter-feeding
of Artenria. I. In pure cultures of plant cells. J.
Exp. Biol., 90: 195-205.
-.
1963b. The filter-feeding
of Ademia. II.
In suspensions of various part&s.
J, Exp.
Biol., 40: 207-214.
RIGL~,
F. I-1. 1961a.
The uptake and r&ax
of inorganic
phosphorus by Daphnia magna
Straus.
Limnol. Oceanog., 6: 165-174.
-.
196~lb. The rclntion
bctwccn
conccntrntion of food and feeding rate of Daphnia
IN
DII+TRl~N’I
113
FOODS
magna
&-ails.
Can. J. Zool., 39: 857-868.
1954. Inhibitory
effects of phytoplnnkton
upon the feeding
of Daphnia
magna with rcfcrencc to growth, rcprodnction
and survivt?l.
Ecology, 35 : 522-533.
JIy’mm,
VAN
J. II.
WACTE:NUONK,
W.
J., D.
I-1. SIMONSEN,
AND
I,. I’. ZILL.
1952. The USC of clcctromigration tcchniqucs in washing and concentrating
cultnrcs of Pnromeccium awelicr. Physiol. Zool.,
25: 312-317.