Notes

Llmnoi. Oceanogr,
29(2), 1984, 365-369
Society of Limnology
G 1984, by the American

and Oceanography,

365

Inc

The energetic cost of response to blue-green algal filaments

by cladocerans l
Abstract-Specific differences in behavior and
energy expenditure in response to blue-green algal filaments were examined as a possible cause
of the shift from large- to small-bodied cladocerans during eutrophication
and seasonal succession. Mandible rate increased with body size
among species and was maximal and independent of filament concentration within a species.
Carapace gape increased with body size among
species and was independent of filament concentration for Daphnia parvula, Ceriodaphnia lacustris, and Bosmina longirostris while it decreased with increasing concentration for Daphnia
magna. An increase in Anabaena filament concentration caused a significant increase in rejection and respiration rates only for the largest
species, D. par&a.

Numerous hypotheses have been proposed to explain the shift from large- to
small-bodied zooplankton that occurs during seasonal succession and eutrophication.
Size selective predation (Brooks 1969),
higher rates of increase in smaller forms
when food is not limiting (Hall et al. 1976;
Hrbacek 1977; Lynch 1980) and a shift in
food to small bacteria and detritus (Gliwicz
1969; Pace et al. 1983) may all act to favor
smaller species. The loss of larger cladocerans, such as Daphnia, often coincides with
an increase in blue-green algal filaments
(Gliwicz 1977; Pace and Orcutt 198 1; Edmondson and Litt 1982; Richman and Dodson 1983). The inhibitory effect may be direct through a greater ability of larger species
to filter the filaments which clog appendages, are toxic, or are nutritionally
inadequate (Webster and Peters 1978; Porter and
Orcutt 1980; Lampert 198 1; Starkweather
1981; Holm et al. 1983). It may also be
indirect through inhibition
of other resources (Infante and Abella in prep.) or fortuitous.
We examine here the effect of increasing
Research was supported by NSFgrant DEB 8203254
to K.G.P. This is Contribution
17 of the Lake Oglethorpe Limnological
Association. R.McD. was supported by a fellowship from the College Work Studies
Program of the University of Georgia.

Anabaena filament

concentration
on the
major feeding behaviors and energy expenditure of three co-occurring
cladocerans

Daphnia parvula, Ceriodaphnia lacustris,

and Bosmina longirostris. The responses of
Daphnia magna to Anabaena filaments is
also examined and compared with those to
a high quality food (Chlamydomonas reinhardi) and to a toxic species of Anabaena
(Porter and Orcutt 1980; Porter et al. 1982).
Three feeding behaviors are reported: mandible rate, which along with food bolus size
determines ingestion rate (Porter et al. 1982);
carapace gape, which may be decreased to
exclude filaments (Gliwicz 1980; Gliwicz
and Siedlar 1980); and the rate of rejection
from the filter appendages and food groove.
Rejection of blue-green filaments often results in lowered ingestion (e.g. Burns and
Rigler 1967; Burns 1969; Gliwicz 1980; Gliwicz and Siedlar 1980). This reduction in
food intake is commonly proposed as the
mechanism by which blue-greens lower fecundity in the field (Gliwicz 1977) and laboratory (Webster and Peters 1978; Porter
and Orcutt 1980). However, elevated respiration rate also accompanies increased rejection (Porter et al. 1982) and this energy
expenditure reduces net assimilation
efficiency, growth, and reproduction (Porter et
al. 1983). We propose that the energetic cost
of selective (i.e. rejective) feeding behavior
is a primary mechanism by which the reproductive abilities of larger species are reduced in the presence of blue-green filaments.
We thank Y. S. Feig for technical assistance and R. Bargmann for the numerical
analyses.
Daphnia magna (2.7 + 0.04 mm) was
obtained from a long-standing, clonal, laboratory culture; D. parvula (1.3 + 0.04 mm),
C. lacustris (0.66 -+ 0.004 mm), and B. longirostris (0.4 1 * 0.0 1 1 mm) were from cultures originally isolated from Lake Oglethorpe, Georgia, a 30-ha monomictic,
eutrophic impoundment. Animals were cul-

366

Notes

tured in aged tapwater saturated with CaCO,

at 20 * 1C in a 16:8 L:D (cool-white)
fluorescent light cycle and fed C. reinhardi.
The C. reinhardi and a filamentous Anabaena sp. were axenic strains grown in a
vitamin-enriched
Woods Hole culture medium (see Porter et al. 1982 for details of
culture and handling). Suspensions of Anabaena were concentrated and cleaned by
stirring and filtering through glass Microfiber filters (GFC) using 0.22~pm Millipore-filtered aged tapwater saturated with
CaCO,. Rinsed filaments were diluted with
the filtered aged tapwater, counted in a
Sedgwick-Rafter cell, and diluted to final
concentrations
of 102, 103, and 1O4 filaments.cmp3. Filaments averaged 0.37 1 k
0.039 mm long with 69.08 + 7.22 cells per
filament. Vegetative filament cells were
about 3.5 pm in diameter and ranged in
length from 3 to 8 pm.
Behavior of adults was observed with a
Zeiss inverted microscope (Porter and Orcutt 1980; Porter et al. 1982). Daphnia
magna was observed at 25 X, and D. parvula, C. lacustris, and B. longirostris were
observed at 100 x . Each animal was fixed
by its head shield to a glass rod with silicone
grease under a dissecting microscope, placed
in 50 cm3 of appropriate Anabaena concentration in a 5- x 5- x 5-cm glass chamber,
and acclimated for 15-20 min (Porter et al.
1983). Then carapace gape was measured
and mandible and rejection rates were determined during 3- and 1O-min intervals for
11 animals of each species.
Oxygen consumption
was measured at
20C for 4 h at midday with an air-calibrated YSI oxygen meter. Groups of 15 adult

D. magna, 25 D. par&a,

3 5 C. lacustris,

or 60 B. longirostris were measured and

placed in 130 + 0.17-ml Pyrex BOD bottles
containing the appropriate algal suspension
in air-saturated aged tapwater. Preliminary
experiments showed that algal O2 production exceeded animal respiration. Therefore, a 1Op5M concentration of DCMU was
added to the algal suspensions to inhibit
photosynthesis and allow for accurate determination
of the animals respiration.
DCMU at that concentration is reported to
have no effect on animal metabolism (C.
Black pers. comm.) as we confirmed in preliminary determinations of respiration rates

in particle-free water. Initial and final oxygen concentrations were measured in ten
replicates for each species at each concentration of algae and in three controls containing algae alone. Statistical analyses of
the behaviors were separate from those of
the respiration rates because they were measured on different groups of animals.
Differences among species and concentration means were detected with univariate
analyses of variance and Roy-Scheffe tests
(Cochran and Cox 1957; analyses available
on request). Duncans multiple range tests
were then performed and are reported in
Fig. 1. Mandible rates are highest for D.
magna, lowest for B. longirostris, and intermediate and equivalent for D. parvula
and C. lacustris with no detectable differences among concentrations of Anabaena.
Carapace gape is significantly
different
among species due to body size differences

(D. magna > D. par&a > C. lacustris >

B. longirostris). Daphnia magna is the only
species that shows a detectable decrease in
gape with increase in filament concentration. Rejection rates are highest for D. parvula and equivalent for the other three
species; D. parvula showed the greatest effect of filaments, with significant differences
among rates at all filament concentrations,
and B. longirostris the least. Weight-specific
respiration rates are highest for B. longirostris, lowest for D. magna, and intermediate and equivalent for D. parvula and C.
lacustris. Daphnia parvula is the only species
that shows a significant increase in respiration rate with increasing filament concentration.
Previous studies show that an increase in
blue-green algal filament concentration can
produce an increase in rejection rate in large
cladocerans such as Daphnia but that the
rejection response is less for smaller species
because fewer filaments enter the carapace
and require rejection. Reduced ingestion
rates also accompany increases in filament
concentrations and may explain the reduced
fecundity of Daphnia in the presence of bluegreen filaments. In our comparison of three
co-occurring
species we also found the
greatest increase in rejection rates with increasing filament concentration in the largest species, D. parvula, with less response
by the smaller species. We saw few filaments

Notes

100
-!

1,~ 80
E
t

1I

Q: 60
lr

-;

367

0.04-

T
r

s
2 0.030,
a

ON
5 o.oz-

4
i4

%
-I
2-

40
1

FILAMENT

CONCENTRATION

(filaments

cme3)

rates, carapace gapes, respiration rates, and rejection rates of Daphnia magna (x), Daphnia
parvula (0), Ceriodaphnia Iacustris (A), and Bosmina longirostris (0) in different concentrations of Anabaena
sp. filaments. Vertical bars-means
k SE (n = 11). Differences determined by Duncans multiple range tests (all
P < 0.05; where DM2 = D. magna at lo2 filaments.cm-3, etc.) are:
Fig. 1. Mandible

carapace gape--L4

BL3 BL2 CL2 CL3 CL2 DP4 DP3 DP2 DM4 DM3 DM2;

mandible

rate--L4

BL2 BL3 CL2 DP2 DP3 CL3 DP4 CL4 DM2 DM4 DM3;

rejection

rate-CL2

DM2 BL3 CL3 DM3 BL2 CL4 DM4 BL4 DP2 DP3 DP4;

respiration

rate--M2

DM3 DM4 CL2 CL3 DP2 DP3 CL4 DP4 BL2 BL3 BL4.

368

Notes

r
-z
0.6 .!%
Oa5+

104

IO5

0.4-

0.31

L-ii0

10

102

103

IO6

10.0

7
AZ

t
c
k
2

0.7-

8.0 -

.-E
E

0.6-

6.0 -

$
2
5

0
$
z:
g

0.5 -

0.4 -

4.02.0-

%+

Id

I
I
102 163 10Gco6
PARTlCLE

CONCENTRATION

2I= 0.3E
2 0.2LT

- 0
(particles

,b

,&

1 I
A3 104 105 lb6

cm-31

Fig. 2. Carapace gapes, mandible rates, rejection rates, and respiration rates of Daphnia magna in different
concentrations of Chlamydamonas reinhardi cells (-) and Anabaena sp. filaments (x). Rejection rates were also
measured in toxic Anabaena flos-aquae (NRC-44-l)
filaments m) and cells (0). Vertical bars-means
+ 95%
C.I.

entering the carapace of the smallest species,

B. longirostris, due to the size of the filaments in relation to the animals carapace
gape. Active rejection occurred primarily in
response to filaments that built up on the
outside of the carapace while animals were
in the fixed position in the viewing chamber; this would not occur with free-swimming B. longirostris. The small B. longirostris may be able to swim between the
filaments as in a patchy environment (Webster and Peters 1978) and may be able to
deflect filaments with its rostrum as it swims.
The respiration rates of the larger D. parvula
also showed the greatest increase with increasing filament concentration:
this suggests that there is an energetic cost associated with the filtration of filaments, which
may be due to energy expended in the process of rejection.
Data on behavioral and respiration rate

collected under equivalent conditions for D.

magna in the presence of a high quality food
(C. reinhardi) and of toxic Anabaena jlosaquae (NRC-44- 1) filaments and cells (Porter and Orcutt 1980; Porter et al. 1982) can
be compared with those in Fig. 2 to clarify
certain responses. Cladocerans reduce the
number of filaments that can enter the filtering chamber and clog their filtering appendages by regulating carapace gape (Gliwicz 1980; Gliwicz
and Siedlar 1980).
However, no change of gape is seen in response to excess collection of high quality
food that also stimulates rejection (Burns
1969; Porter et al. 1982). Gape becomes
smaller in the presence of Anabaena sp. filaments than in the presence of Chlamydomonas (Fig. 2). This reduction in gape may
have ameliorated the responses in rejection
and respiration in the large D. magna. Rejection rates of both toxic and nontoxic

NCZes
strains of Anabaena are higher than those
of Chlamydomonas and are proportional to
particle concentration rather than to particle volume or toxicity, confirming the suggestion of Porter and Orcutt (1980) that rejection
is proportional
to encounter
probability.
The higher respiration rate in
the presence of filaments than in that of
Chlamydomonas implies an energy cost to
the animals. Mandible rates are higher for
Anabaena sp. than for Chlamydomonas;
however, in the previous study ingestion
rates were lower on Anabaena (Porter and
Orcutt 1980). The high mandible rates are,
therefore, probably the result of an overall
stimulator-y effect of filaments on food manipulating behavior and indicate a further
energetic cost rather than increased ingestion.
We have shown that increasing filament
concentration disproportionately
stresses the
largest species of cladocerans. Higher rejection and respiration rates may, therefore,
significantly reduce the energy available to
larger cladocerans for growth and reproduction in eutrophic lakes and thereby enhance the shift toward smaller species.

Karen Glaus Porter

Robert McDonough
Department of Zoology and
Institute of Ecology
University of Georgia
Athens 30602

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STARKWEATHER,

Submitted: I1 January 1983

Accepted: 8 July 1983