Porter, 1984. the Energetic Cost Response to Blue-green Algal Filaments by Cladocerans

8/10/2019 Porter, 1984. the Energetic Cost Response to Blue-green Algal Filaments by Cladocerans.

1/5

Notes

365

Llmnoi. Oceanogr, 29(2),

1984, 365-369

G 1984, by the American

Society of Limnology and Oceanography, 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 al-

gal filaments were examined as a possible cause

of the shift from large- to small-bodied cladocer-

ans during eutrophication and seasonal succes-

sion. Mandible rate increased with body size

among species and was maximal and indepen-

dent of filament concentration within a species.

Carapace gape increased with body size among

species and was independent of filament concen-

tration for

Daphnia parvula, Ceriodaphnia la-

custris,

and

Bosmina longirostris

while it de-

creased with increasing concentration for Daphnia

magna.

An increase in

Anabaena

filament con-

centration caused a significant increase in rejec-

tion and respiration rates only for the largest

species,

D. par&a.

Numerous hypotheses have been pro-

posed to explain the shift from large- to

small-bodied zooplankton that occurs dur-

ing 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 cladocer-

ans, such as Daphnia, often coincides with

an increase in blue-green algal filaments

(Gliwicz 1977; Pace and Orcutt 198 1; Ed-

mondson and Litt 1982; Richman and Dod-

son 1983). The inhibitory effect may be di-

rect through a greater ability of larger species

to filter the filaments which clog append-

ages, are toxic, or are nutritionally inade-

quate (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 re-

sources (Infante and Abella in prep.) or for-

tuitous.

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 Ogle-

thorpe Limnological Association. R.McD. was sup-

ported by a fellowship from the College Work Studies

Program of the University of Georgia.

Anabaena filament concentration on the

major feeding behaviors and energy expen-

diture 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 rein-

hardi) and to a toxic species of Anabaena

(Porter and Orcutt 1980; Porter et al. 1982).

Three feeding behaviors are reported: man-

dible 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 re-

sults in lowered ingestion (e.g. Burns and

Rigler 1967; Burns 1969; Gliwicz 1980; Gli-

wicz and Siedlar 1980). This reduction in

food intake is commonly proposed as the

mechanism by which blue-greens lower fe-

cundity in the field (Gliwicz 1977) and lab-

oratory (Webster and Peters 1978; Porter

and Orcutt 1980). However, elevated res-

piration rate also accompanies increased re-

jection (Porter et al. 1982) and this energy

expenditure reduces net assimilation effi-

ciency, 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 re-

productive abilities of larger species are re-

duced in the presence of blue-green fila-

ments.

We thank Y. S. Feig for technical assis-

tance and R. Bargmann for the numerical

analyses.

Daphnia magna (2.7 + 0.04 mm) was

obtained from a long-standing, clonal, lab-

oratory culture; D. parvula (1.3 + 0.04 mm),

C. lacustris (0.66 -+ 0.004 mm), and B. lon-

girostris

(0.4 1 * 0.0 1 1 mm) were from cul-

tures originally isolated from Lake Ogle-

thorpe, Georgia, a 30-ha monomictic,

eutrophic impoundment. Animals were cul-


2/5

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 Ana-

baena

sp. were axenic strains grown in a

vitamin-enriched Woods Hole culture me-

dium (see Porter et al. 1982 for details of

culture and handling). Suspensions of An-

abaena were concentrated and cleaned by

stirring and filtering through glass Micro-

fiber filters (GFC) using 0.22~pm Milli-

pore-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 fila-

ments.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 Or-

cutt 1980; Porter et al. 1982). Daphnia

magna was observed at 25 X, and D. par-

vula, 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 concen-

tration 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 de-

termined 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-cali-

brated 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 produc-

tion exceeded animal respiration. There-

fore, a 1Op5M concentration of DCMU was

added to the algal suspensions to inhibit

photosynthesis and allow for accurate de-

termination 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 pre-

liminary determinations of respiration rates

in particle-free water. Initial and final oxy-

gen concentrations were measured in ten

replicates for each species at each concen-

tration of algae and in three controls con-

taining algae alone. Statistical analyses of

the behaviors were separate from those of

the respiration rates because they were mea-

sured on different groups of animals.

Differences among species and concen-

tration 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 in-

termediate and equivalent for D. parvula

and C. lacustris with no detectable differ-

ences 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 concentra-

tion. Rejection rates are highest for D. par-

vula

and equivalent for the other three

species; D. parvula showed the greatest ef-

fect of filaments, with significant differences

among rates at all filament concentrations,

and B. longirostris the least. Weight-specific

respiration rates are highest for B. longi-

rostris, lowest for D. magna, and interme-

diate and equivalent for D. parvula and C.

lacustris. Daphnia parvula is the only species

that shows a significant increase in respi-

ration rate with increasing filament concen-

tration.

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 blue-

green filaments. In our comparison of three

co-occurring species we also found the

greatest increase in rejection rates with in-

creasing filament concentration in the larg-

est species, D. parvula, with less response

by the smaller species. We saw few filaments


3/5

Notes

367

-

00

1,~ 80

- t

E

f

Q: 60

lr

t

%

- 1

-I 40

2

1 I

-; 0.04-

T

r

s

2 0.03-

0,

a

ON

5 o.oz-

t

9

d

i

4

4

FILAMENT CONCENTRATION

(filaments cme3)

Fig. 1.

Mandible 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:

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.


4/5

368

Notes

-z

. %

0.6 -

Oa5+ t + + +

+ +

0.4-

0.31

L-ii

I I I

1

0

10 102

103

104

IO5

IO6

10.0

t

8.0 -

c

k

2

6.0 -

0

$ 4.0-

z:

g 2.0- +

r

7

AZ

; 0.7-

E

.-

E 0.6-

$ 0.5 -

2

0.4 -

I= 0.3-

t

E

2 0.2-

LT

t

t

I I

%+ Id 102 163 10Gco6

1 I

- ,b ,& A3 104 105 lb6

PARTlCLE CONCENTRATION (particles 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 fila-

ments 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 cham-

ber; this would not occur with free-swim-

ming B. longirostris. The small B. longiros-

tris may be able to swim between the

filaments as in a patchy environment (Web-

ster 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 in-

creasing filament concentration: this sug-

gests that there is an energetic cost associ-

ated with the filtration of filaments, which

may be due to energy expended in the pro-

cess 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 jlos-

aquae (NRC-44- 1) filaments and cells (Por-

ter 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 fil-

tering chamber and clog their filtering ap-

pendages by regulating carapace gape (Gli-

wicz 1980; Gliwicz and Siedlar 1980).

However, no change of gape is seen in re-

sponse 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. fil-

aments than in the presence of

Chlamydom-

onas (Fig. 2). This reduction in gape may

have ameliorated the responses in rejection

and respiration in the large D. magna. Re-

jection rates of both toxic and nontoxic


5/5

NC es

369

strains of Anabaena are higher than those

of Chlamydomonas and are proportional to

particle concentration rather than to parti-

cle volume or toxicity, confirming the sug-

gestion of Porter and Orcutt (1980) that re-

jection 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 ma-

nipulating behavior and indicate a further

energetic cost rather than increased inges-

tion.

We have shown that increasing filament

concentration disproportionately stresses the

largest species of cladocerans. Higher rejec-

tion and respiration rates may, therefore,

significantly reduce the energy available to

larger cladocerans for growth and repro-

duction in eutrophic lakes and thereby en-

hance 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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Submitted: I1 January 1983

Accepted: 8 July 1983

Documents

Porter, 1984. the Energetic Cost Response to Blue-green Algal Filaments by Cladocerans