Download relation between filtering rate, temperature, and body size in four

RELATION
BETWEEN FILTERING
RATE, TEMPERATURE,
AND BODY SIZE IN FOUR SPECIES OF DAPHNIA
Carolyn W. Bums1
Department
of Biology, Osborn Memorial
Laboratories,
New Haven, Cormecticut
06520
Yale University,
ABSTBACT
Filtering rates of four species of Daphnia were measured at 15, 20, and 2%. Maximum
filtering rattc increased with increasing temperature
and increasing body size of the animal
in all species, but a general equation relating filtering
rate to body length could not bc
derived.
When filtering
rates were expressed on a unit body weight basis, the species
differed.
Filtering
rates of adult D. sch@dZeri and D. pulex were similar and at 20C were
slightly higher than their rates at 15 and 25C. In contrast, filtering rates of D. magna and
D. galeata mendotas increased with increasing temperature
and at 20 ancl 25C were more
than twice their rates at 15C.
INTHODUCTION
The filtering
rates of two freshwater
cladocerans, Daphnia magna Straus 1820
and Daphnia rosea Sars 1862, have been
shown to increase with increasing tempcrature below 20C (McMahon
1965; Burns
and Riglcr 1967). Above this temperature,
the filtering behavior of the two species
differed.
In several species of Daphnia, filtering
rates have been shown to increase with increasing body size (Ryther 1954; Richman
1958). Filtering rates of D. magna feeding
in dilute suspensions of food were roughly
proportional to the square of body length
( McMahon
1965), whereas rates of D.
rosea, measured under similar conditions,
were proportional
to the cube of body
length ( Burns and Rigler 1967).
In the following study, the relation bctwecn filtering rate, temperature, and body
size is cxamincd in Daphnia magna Straus
1820, Daphnia schgdleri Sars 1862, Daphnia pulex Leydig 1860, and Daphnia galeata Sars 1864 mendotae Birgc 1918. The
investigation
had two purposes: first, to
determine whether, at temperatures char’ I am grateful to Dr. J. L. Brooks for supporting this research on his National Science Foundation Grant GB-6004 and for critically
reading the
manuscript.
Present address : Zoology
Department,
University of Otago, P.O. Box 56, Dunedin,
New
Zealand.
actcristic of the epilimnion of tempcratc
lakes during summer, there arc diffcrenccs in filtering rate bctwccn similar-sized
Daphnia belonging to different
species;
and, second, to detcrminc whether maximum filtering rates of several species of
Daphnia are more nearly proportional
to
the square or to the cube of their body
lengths.
METHODS
Laboratory populations of D. pulex and
D. galeata were established from adults
collected in several Connecticut lakes. D.
sch@dZeri had been cultured in the laboratory for approximately two years since its
collection
in New England.
Daphnia
magna was obtained from long-established
laboratory cultures.
All Daphnia were raised in spring water
in constant temperature chambers (15, 20,
and 25C; 12-hr light and 12-hr dark per
day) for several weeks before they were
used in experiments.
Because temperatures above 2% rarely occur in tempcratc
lakes inhabited
by the species studied,
cxpcrimcnts were not carried out at higher
temperatures.
Algae from cultures (Ezcglena gracilis, Chlamydomonas reinhardtii,
or Selenastrum sp.) were added daily as
food.
Measurement
of
body sixe
Body length is the most easily measured
index of body size in Daphnia, but differ693
694
CAROLYN
cnces between species in the degree of
roundness or flatness of the body and
temporal differences within the same species ( cyclomorphosis ) may decrease the
usefulness of body length as a measure of
body size when several species of Daphnia
are being compared. Body weight, as an
index of body size, varies with the nutritional state of Daphnia (Berg 1936)) and
with reproductive condition ( Green 1956).
To find the most satisfactory index of
body size for the Daphnia used in these
expcrimcnts,
the relation between body
length and body weight was determined.
Daphnia were rinsed in deionized distilled
water and placed on a slide where body
length (from the base of the tail spine
to the top of the helmet) and carapace
length (from the base of the tail spine
to the middle of the insertion of the locomotory antennae) were measured. Animals
were placed in weighed aluminum boats,
dried for 24 hr at 6OC, cooled for 1 hr
in a desiccator, and weighed immediately
on a Cahn Ratio Electrobalance.
For *he
smaller instars of a species, several individuals of the same length, and frequently
from the same brood, were weighed
together.
--W.
----mel5UJANS
solution could be considered negligible in
these experiments,
Laboratory studies had shown that at
concentrations of yeast below an incipient
limiting concentration filtering rates of D.
rosea and D. magna were maximal and
independent of concentration
( McMahon
and Rigler 1965; Burns and Rigler 1967).
A concentration of 0.25 x lo5 yeast cells/
ml is well below an incipient limiting concentration for D. magna of 1.25-3.5 mm in
body length and feeding at temperatures
between 5 and 35C ( McMahon
1965).
This concentration is also below an incipicnt limiting concentration for D. rosea of
0.64-1.60 mm in body length and feeding
at 20C (Burns and Rigler 1967). On the
assumption that this concentration would
be below an incipient limiting conccntration for the other species of Daphnia,
comparable in body size to D. rosea, used
in these experiments, all measurements of
filtering rate were carried out in the light
in a suspension of 0.25 x 10S cells/ml. Procedures were the same for all experiments.
About 120 Daphnia, representing the range
in body sizes of a species raised at one
temperature, were rinsed by allowing them
to swim freely for 10 min in membranefiltered, aerated spring water. Between 60
Measurement of filtering rate
and 80 first and second instar animals,
and 20-30 individuals of each of the larger
Filtering rates were measured by allowing Daphnia to feed on 32P-labeled yeast size categories were used in an experiment.
Feeding was in 4,000-ml beakers contain( Rhodotorula
glutinis)
cells. Unlabeled
yeast for prefeeding was prepared by sus- ing 1,000 ml of feeding suspension. Rapid
pending cells harvested from agar slopes in transfer of animals from one beaker to
another was achieved in a Plexiglas cylinmembrane-filtered
(Millipore filter, 0.45-pdiam pores) spring water. Labeled cells der (30.5-cm length x 12.5-cm ID) over
were prepared by adding radioactive phos- the bottom end of which No. 8 (0.203phorus in the form of carrier-free I-ISSZP04 mm2 aperture size) nylon netting had been
glued.
in water (New England Nuclear Corp.,
This cylinder, which had been placed in
Boston, Mass.) to a stock suspension of
a beaker of prefeeding suspension before
yeast cells in membrane-filtered water. Upof Daphnia, was lifted
take of the radioactive label by the cells the introduction
was maximal after 5 min. Preliminary ex- gently to an adjacent beaker of labeled
food. Although
most animals resumed
periments in which 150 adult Daphnia
were allowed to swim freely for 3 min in swimming almost immediately after transfer, early instars of lighter-bodied
species
a cell-free filtrate of a labeled feeding
sometimes became trapped in the surface
suspension indicated that any radioactivity
which might be acquired by the Daphnia
film. If bombardment with a drop of suspension from a pipette failed to submerge
through direct uptake of the 32P label from
FILTERING
d-*
BODY
k0
LENGrH
RATE,
I5
20
mm
TEMPERATURE,
m ’ ’
30
40
50
FIG. 1. Relation
between body weight
(W)
and body length (La) of immature and ovigerous
instars of four species of Daphnia
on a double
logarithmic
scale. The regression equation, W =
0.0116Lb”.G7, is indicated by a continuous line.
these individuals within 15 set of the start
of a feeding period, they were removed
from the experiment. Results of any experiments were discounted if more than
about 20% of the total Daphnia became
caught at the surface, or if the behavior of
the Daphnia
appeared abnormal
(e.g.,
frenzied swimming, cessation of antenna1
movements ) .
To minimize possible differences in feeding rates arising from differences in the
initial fullness of the gut of individual
Daphnia, animals were prefed on unlabeled yeast at the same concentration as
that of the labeled food. Since feeding
rates of D. magna after a 30-min prefceding period are not significantly
different
from rates after longer prcfeeding periods
( McMahon
1965), the Daphnia used in
these experiments were allowed to feed for
30-45 min in unlabeled yeast before they
were transferred to a labeled yeast suspension, in which they were allowed to
feed for 3 min. Animals were returned
AND
BODY
SIZE
695
OF DAPHNIA
to the unlabeled suspension for 1 min to
allow them time to ingest radioactive food
present in their food grooves at the end
of the feeding period in labeled food.
Feeding was terminated by plunging the
Daphnia into carbonated water (which
acts as an immediate anesthetic),
after
which they were prepared for measuremcnt of body length and radioactivity
as
described elsewhere (Burns and Riglcr
1967). Radioactivity
was measured in a
gas-flow counter equipped with automatic
sample changer and printer (Nuclear Chicago) until 2,560 counts had been recorded. All counts were corrected for
background (ca. 12 counts/min)
and for
of
radioactive decay of 32P. Radioactivity
the labeled yeast suspension was measured
by filtering a 5- or 2-ml sample of the
suspension through a Millipore filter (25mm diam, 0.45~p-diam pores).
Filtering rates, expressed as the volume
(ml) filtered per animal per hour, were
calculated from the average radioactivity
acquired by each animal during the period
in labeled yeast suspension and from the
radioactivity
of the yeast cells in suspension according to the equation,
Filtering rate
cotmt min-1 animal-l
(ml animal-1 = count min-l (ml
hr -I)
yeast suspension)-*
X
60
min spent in *
labclcd food
RESULTS
Measurement
of body size
The relation between body weight and
body length was most nearly linear when
data were plotted logarithmically
(Fig. 1).
The regression equation fitted to the data
by the least squares method is,
W = 0.0116Lb2.67,
or
log,, W = log,, 0.0116 + 2.67 log,, Lb,
where W is body weight in mg, and L, is
body length in mm.
The comparable equation for the regression of body weight on carapace length is,
W = 0.0223L,2.“2,
or
log,, W = log,, 0.0223 + 2.62 loglo L,.
Because the difference between the two
equations was small (sample standard de-
CAROLYN
immature
05
BODY
BURNS
adult
II
0.25
W.
IO
LENGTH
15
mm
III
20
30
-
40
5.0
I025
I
05
BODY
1-I
IO
LENGTH
15
mm
2.0
30
1
40
1
50
FIG. 2. Relation between log,, maximum filtering
rate (F) and loglo body length (LO) of four spcties of Duphnia at 15, 20, and 2%. Regression equations fitted to the data are indicated
by dashed
lines , Horizontal
bars indicate 95% confidence limits for the prediction
(from the regression equation)
of average maximum filtering rate for any body length. IIypothetical
curves describing filtering
rate as
squared (F m Las) and cubic (F a Lb3) functions of body length are shown by continuous lines.
vi&ions from regression 0.0954 and 0.0979
for body length and carapace length cquations, respectively), the more conventional
mcasuremcnt of body length was used in
this study.
Equations for the regression of body
weight on body length for each spccics of
Daphnia were derived as well (see Table
2) and used in later calculations.
Measurement
of filtering
rate
In all four species of Daphnia studied,
filtering
rate increased with increasing
body size. The relation between filtering
rates at 15, 20, and 25C and body length
is shown by the double logarithmic plots in
Fig. 2. The regression equations fitted to
the data by the method of lcast squares are
at 1X:
F = o.153LbZ*‘c’
(or, log,, F = loglo 0.153 + 2.16 log,, Lb);
at 20C:
F = 0.208 Lb=);
at 2%:
F = 0.202 L&y
where F is filtering rate (ml animal-l hr-l )
and Lb is body length in mm.
At SC, the :regrcssion coefficient (2.16)
is close to 2, so that filtering rate is roughly
proportional to the square of body length.
However, at 2CC, the regression coefficient
(2.80) approaches 3 and filtering rate bccomes more closely proportional
to the
cube of body length. At 25C, the regression coefficient (2.38) cannot be said to
approximate either the square or the cube
of body length.
In Fig, 2, the solid lines afford a gauge
for assessing the closeness of fit of the filtering rate data to the square or cube of
body length.
Maximum body size differed among the
FILTERING
immature
P ELlE
p, sch0dleri
+
Y
.
0.
PA%
0
gclledta
mL?iidXie
&
TEMPERATURE,
AND
adult
+
x
Q
BATE,
4
25 “C
o-
5 -
5 -
I -
5 -
p-IL-I
0.25
05
BODY
FIG.
2.
II0
LENGTH
30
I.5
20
mm
40
50
Continued
species of Daphnia studied. To compare
filtering rates of the four spccics at different temperatures, filtering rates were expressed on a unit body weight basis. Mean
values for the filtering rates of immature
and adult instars of a species at the three
temperatures were calculated. The gcncral
BODY
SIZE
OF Da4PIINIA
697
equation ( Table 1) and species-specific
equations (Table 2) were used to convert
filtering rates expressed as (ml filtered)
Daphnia-l hr-l to (ml filtered)
(mg dry
wt Daphnia)-1 hr-I. A mean filtering rate
value characteristic of a species at each
temperature was obtained by averaging filtering rates for all instars (Tables 1 and 2,
in parcnthescs) .
The differences between pairs of mean
values for each species in Tables 1 and 2
wcrc tested by analysis of variance using
the lcast significant difference as a criterion
for significance at the 5% level. Only those
differences between means which were significant in both tables were accepted.
At all three temperatures, the mean filtering rates of D. pulex and D. galeata
wcrc significantly
different.
Differences
between mean filtering rates of D. sch@Zeri and D. pulex were not significant at
any temperature used.
At 1X, D. schedkri and D. gaZeata filtered at a similar rate, but at 20 and 2X
filtering rates of D. galeata were significantly higher than those of D. schedleri.
Filtering rates of D. magna were significantly higher than those of D. puZex at 15
and 25C. At 2OC, the difference in mean
filtering rate between the two species was
not significant.
Howcvcr,
filtering
rate
data for D. magna at this temperature
1. Mean maximum filtering rates, ml (mg dry wt Daphnia)-1 hr-I, of immature (I) and adult
(A) insturs of four species of Daphnia at 15, 20, and 25C. Average filtering
rates of all instars are
given in parentheses.
The general equation, W = 0.0116L1F~G7, was used to convert body lengths to
bocly weights
TABLE
Temp (“C)
15
Spccics
D. magna
I
20
A
7.6
I
8.3
25
A
I
A
QlO
15-25C
23.4”
13.9*
(16.6)*
23.6
‘15.3
(19.0)
2.38
W)
D. schprdleri
15.9
9.2
(12.6)
12.5
18.2
(15.9)
10.1
12.5
(11.3)
0.90
D. pulex
13.2,
14.2
(13.6)
15.4
17.3
(15.9)
19.1
10.2
(12.8)
0.94
D. galeata
13.2
7.4
(10.3)
20.8
29.1
(24.3)
30.4
26.1
(27.9)
2.71
* Values calculnted from McMahon’s
(1962)
centration of 0.1 X 10” cells/ml, at 20C.
filtering
rate clnta for D. magna feeding
on log phase Chlorella
at a con-
698
TABLE
(A)
CAROLYN
W.
BURNS
2. Mean m&mum
filtering
rates, ml (mg dry wt Daphnia,F
hP, of immature (I) and adult
instars of four species of Daphnia at 15, 20, and 25C. Average filtering
rates of all instars are
given in parentheses.
Species-specific
equations (SS) were used to convert body lengths to
body weights
Temp (“C)
15
Species
I
20
A
I
25
A
I
A
-
QIO
ss
15-25C
D. magna
10.0
11.3
(10.7)
30.9”
18.5”
(22.1) *
31.0
20.9
(25.4)
2.38
w = 0.009 La2.e3
D. schedleri
18.7
7.6
(13.1)
12.7
14.3
(13.6)
11.2
9.7
(10.4)
0.80
w = o.010Lb3*10
D. pulex
13.2
14.4
(13.6)
15.0*
17.7
(15.7)
18.9
10.4
(12.9)
0.95
w = o.012Lb2~e3
D. galeata
10.6
16.6
24.8
(21.6)
25.5
22.5
(23.8)
2.80
w = o.014Lb2~64
6.4
(8*5)
* Values calculated from McMahon’s
(1962)
centration of 0.1 X 10” cells/ml, at 2OC.
filtering
rate data for D. magna feeding
were obtained from animals feeding in a
suspension of different food at a higher
cell concentration
( McMahon 1962) than
used in these experiments so that maximum
filtering rates may not have been measured
for all instars, in which case the mean
filtering rate value for D. magna would
be too low.
Although the mean filtering rates of D.
galeata at 20 and 25C were significantly
higher than those of D. magna when the
generalized equation was used to convert
body length to body weight ( Table 1))
the differences between the two means at
these temperatures were not significant
when the species-specific equations were
used (Table 2).
Differences between immature and adult
instars in their filtering rate values did not
follow a consistent pattern in any species.
DISCUSSION
Filtering
rates of the four species of
Daphnia studied agree well with rates determined by Monakov and Sorokin ( 1961)
for two sizes of Daphnia longispina feeding
in a dilute suspension of Chlorococcus cells
at 15C and by McMahon (1965) for D.
magna feeding on Chlorella at 20C.
When filtering rates measured in these
experiments are plotted graphically on a
double logarithmic scale, the points arc too
on log phase Chlorella
at a con-
widely scattered to permit the derivation
of a general expression relating filtering
rate to body length in all species of Daphnia. Filtering :rates ranged from approximating a squared function of body length
at 15C to approaching a cubic one at 20C.
To minimize the possible influence on
filtering rate of differences in physiological condition of the Daphnia used in this
study, filtering rates were measured intermittently over a period of about a year.
All the measurements at one temperature,
or on one species, were never carried out
at one time. Although these precautions
were taken, the scatter of points in Fig. 2
may reflect, in part, changes in filtering
rate that could have accompanied changes
in metabolic rate with age, reproductive
state, and nutritional
history (MacArthur
and Baillie 19129; Richman 1958; Blagka
1966). Since the inhalant current subserves
respiration, it is possible that changes in
the oxygen demands of Daphnia may lead
to changes in filtering rates as well.
The species-specific equation used to relate body weight to body length of D.
pulex in these experiments (Table 2) is
interesting in that the regression coefficient, 2.63, is very close to that of 2.64
obtained by Smith (1963) using Richman’s
data (1958) to relate weight to length of
this species.
FILTERING
BATE,
TEMPERATURE,
A comparison of filtering rates of the
four species, expressed on the basis of
body weight using species-specific equations for the conversion of length to weight
(Table 2), reveals two distinct types of
response to tcmpcratures above 15C.
Filtering rates of adult D. schedleri and
D. pulex at 20C were slightly higher than
rates at 15 and 25C. In this rcspcct, the
filtering behavior of these two species is
similar to that of D. rosea feeding at the
same temperatures and food concentrations ( Burns and Rigler 1967). The magnitude of the differences between rates of
filtration at 15, 20, and 25C is similar in
all three species.
In contrast, the filtering
rates of D.
magna and D. galeata increased with increasing temperatures over the range studied. At 25C, the mean filtering rates of
these two species were two to three times
higher than their rates at 15C ( Q10, Table
2). Results for D. magna accord well with
those obtained by McMahon (1965) who
found filtering rates of this species to increase with increasing temperatures up to
28C, above which rates declined rapidly.
Since each type of filtering rate response
was shown by a species that had recently
been brought into the laboratory (D. pulex
and D. galeata) as well as by one which
had been long-established
in laboratory
difcultures (D. magna and D. s&$dleri),
ferences in filtering rate in response to tcmpcrature could not be an outcome wholly
of the length of time the species had been
kept in culture.
Although
the results of these studies
accord well with observations on the ecology and distribution
of Daphnia, the following discussion should not be taken to
imply that responses of filtering rate to
temperature
play an important
role in
determining the zoogeography of Daphnia.
Competition and predation must outweigh
a physical factor such as temperature in
determining the distribution
of most species. Furthermore, temperature is only one
of a number of variables in nature known
to affect rates of filtration in Daphnia. The
concentration of particulate matter in sus-
AND
BODY
SIZE
OF DAPHNIn
699
pension has important effects on filtering
rate (Monakov and Sorokin 1961; Burns
and Rigler 1967) and some species of
algae have been shown to inhibit filtration
( McMahon and Rigler 1965; Burns 1968).
The four species studied can be grouped
by habitat prefcrcnce (Brooks 1957) into
those 1) chiefly confined to temporary
ponds ( D. magna); 2) chiefly in ponds,
sometimes in lakes (D. pulex, D. schadleri,
D. rosea); and 3) restricted to lakes ( D.
galeata).
For D. magna, an ability to filter more
rapidly at temperatures as high as 24-28C,
which occur in some of the Danish ponds
( Berg 1931)) would seem to be a distinct
asset and is perhaps a compensation for an
inability to exist in permanent bodies of
water where piscine predation could prove
fatal to this large-bodied species. Further
proof of the ability of D. magna to tolerate
both high temperatures and sudden increases in temperature similar to those
characterizing
shallow ponds on a sunny
day comes from an accidental rise in tempcrature of the 20C growth chamber. Over
a 4-hr period, the room temperature rose
to 40C. Mortality among the D. pulex and
D. schadleri cultures was lOO%, slightly
less than this among D. galeata, and insignificant among D. magna. Conditions of
feeding, density of the animals, and volume of the vessel had been the same for
all spccics.
The remarkable similarity between D.
pulex,
D. sch@dleri, and D. rosea in their
habitat preferences and wide geographic
distribution
in North America2 is heightencd by the similarity
of their filtering
rates. The filtering behavior of these species at tempcraturcs between 15 and 25C
suggests they would filter equally fast
(other things being equal) over the range
of temperatures characterizing
their summer habitats.
Some species of Daphnia appear more
2 Since the publication
of the monograph
by
Brooks ( 1957 ), the range of D. rosea in North
America has been extended eastwards to a lake
near the western short of Lake Ontario, Canada
( Burns and Rigler 1967 ).
700
CAROLYN
successful than others in occupying the
warm epilimnctic
waters of temperate
lakes in summer. Frequently D. gdeuta is
one of these ( Hall 1964; Tappa 1965).
One hypothesis attributes their success to
a better avoidance of predators as an outcome of morphological
changes involving
reduction in body size and the development of a helmet ( Brooks 1965). Results
of my experiments and a consideration of
the geographic range of this species, which
extends south into Mexico and Central
America, suggest that a higher tempcrature threshold for maximum filtration may
be involved as well.
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0. F. Miiller
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-*
the Cladocera
illustrated
by the weight
of
the animals.
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Metabolism
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BLA~KA, P.
1966.
cultured
populations
of Daphnia
related to
Intern. Vcr. Theorct.
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Angew. Limnol. Verhandl.,
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1965.
-*
Proc. Natl.
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1968.
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-,
AND F. H. RIGLER. 1967. Comparison
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W.
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-,
1965. Some physical factors influencing
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-,
AND F. I-1. RIGLER. 1965. Feeding rate
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