Metabolic Costs During Predator-Induced Diel Vertical Migration of Daphnia

Metabolic Costs During Predator-Induced Diel Vertical Migration of DaphniaAuthor(s): Piotr Dawidowicz and Carsten J. LooseSource: Limnology and Oceanography, Vol. 37, No. 8 (Dec., 1992), pp. 1589-1595Published by: American Society of Limnology and OceanographyStable URL: http://www.jstor.org/stable/2838054 .

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LIMNOLOGY AND

OCEANOGRAPH December 1992

Volume 37

Number 8

Limnol. Oceanogr., 37(8), 1992, 1589-1595 ? 1992, by the American Society of Limnology and Oceanography, Inc.

Metabolic costs during predator-induced diel vertical migration of Daphnia

Piotr Dawidowiczl and Carsten J. Loose Max Planck Institute for Limnology, Department of Physiological Ecology, P.O. Box 165, W-2320 Pl6n, Germany

Abstract Life-history parameters were determined for a cohort of 60 clonal Daphnia magna grown in-

dividually in thermally stratified, 1 -m-long flow-through tubes under a constant high-food regime (2.0 mg C liter-'). The individuals could migrate freely in the tubes and their depth was noted at regular intervals. Half of the tubes received water from a reservoir containing a fish. The animals in these tubes stayed deep during the day and higher at night, thus showing a "normal" diel vertical migration behavior. The other half of the tubes was supplied with the same water, but free of fish. The individuals in this set exhibited no diel migration, but stayed in the warm upper strata day and night. The migrating animals in the fish-treated set grew at rates (0.21 d-') only a third those of individuals in the no-fish treatment (0.57 d-'). Most of the difference between the treatments can be attributed to the lower temperatures experienced by the migrating individuals. However, an experiment with no thermal stratification showed that the chemical presence of fish in the water can significantly retard Daphnia growth.

The hypothesis that diel vertical migration (DVM) behavior of zooplankton is a predator avoidance strategy (Kozhov 1963; Zaret and Suffem 1976; Stich and Lampert 1981; Gliwicz 1986) has received strong support from laboratory and field studies showing that DVM can be chemically induced by the presence of predators. This induced DVM has been reported for various planktonic prey species responding to different predator taxa in both freshwater and marine environments (copepods: Bollens and Frost 1989; Neill 1990; cladocerans: Dodson 1988; Ringelberg 1991; Loose 1993; Chaoborus: Dawidowicz et al. 1990; Da- widowicz 1993; Tjossem 1990).

The widely accepted hypothesis to ex- plain these periodic migrations is that the

'Permanent address: Department of Hydrobiology, University of Warsaw, Nowy Swiat 67, 00 046 War- saw, Poland.

Acknowledgments We thank Joanna Pijanowska, Barbara Taylor, and

Winfried Lampert for improving the manuscript with their comments, and Nancy Zehrbach for linguistic help.

metabolic costs of swimming to and staying in suboptimal depth strata throughout the day are balanced by reduced risk of predation (see Lampert 1989). The cost of swimming itself has been found to be neg- ligible in DVM of Daphnia (Dawidowicz and Loose 1992), whereas the costs due to lower temperature and poorer food conditions in deep waters have proved to be considerable (Stich and Lampert 1984; Orcutt and Porter 1983). Kerfoot (1985) stated that temperature costs are most important and probably cannot be compensated for by food quantity.

In the experimental setups of Stich and Lampert (1984) and Orcutt and Porter (1983), the animals did not really migrate. They were forced to grow under fluctuating temperature and food regimes, thus only simulating the conditions experienced by migrating and nonmigrating animals, but not the metabolic costs of actual migration.

We developed an experimental design in which single Daphnia could move freely in a controlled laboratory system. We were able to track the vertical migration behavior of

1589



1590 Dawidowicz and Loose

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Fig. 1. The experimental setup. Sixty flow-through tubes were put into a water bath where a defined thermal stratification was kept constant (see graph). Water was continuously pumped from the reservoirs into the tubes, which were screened with gauze on the bottom to keep the animals inside. Half the tubes received water from the reservoir containing a fish and the other half served as a no-fish control.

every individual (see Schallek 1942). The presence or absence of chemical cues exuded by a fish served to divide a clonal cohort of animals into two groups that differed in migratory pattern. Consequently, we could attribute the differences in individual life-history data directly to the metabolic costs of different DVM patterns induced in Daphnia by fish.

Materials and methods The experiments were performed with a

clone of Daphnia magna originating from Grosser Binnensee, a hypertrophic, shallow, brackish lake in north Germany. The fish community in the lake consists mainly of cyprinids (Lampert 199 1). The water for the

experiments originated from mesotrophic Sch6hsee (north Germany), but had been stored for several weeks in a fishless 6.5-m3 stainless steel tank. The water was filtered through a 0.45-,gm membrane filter and en- riched with chemostat-grown Scenedesmus acutus to a final concentration of 2.0 mg C liter-'.

The experimental setup consisted of 60 Perspex flow-through tubular chambers (1 m long, 1.5-cm diam) placed vertically into a. transparent water bath (2.5 x 0.25 x 1.1 m, Fig. 1). The system was illuminated with a set of 12 halogen lamps (Osram Halostar KLR 51, 20 W, 12 V) shining overhead through a frosted glass screen to provide homogeneous and diffuse irradiance. Dur-



Costs of Daphnia D VM 1591

ing "sunrise" (0330-0430) and "sunset" (1930-2030) the lamp voltage was changed linearly between 0 and 12 V, which resulted in a sigmoid change in light intensity. The light intensity ranged from 17.9 ,uEinst m-2 s-' at the top of chambers to 1.3 at the bottom (LiCor quantum sensor).

Two experiments were conducted. In the first, we maintained a constant temperature distribution in the water bath, with 22.5?C at the top and 9.5?C at the bottom, to mimic a summer thermal stratification (Fig. 1). In the second experiment, the temperature was kept at 20?C throughout all depths.

In the stratification experiment both treatments consisted of 30 tubes with one animal per tube, whereas in the unstratified experiment every treatment included six tubes containing three animals per tube. Ev- ery tubular chamber had an inflow at the top with a constant flow rate of 0.33 (first experiment) and 1.0 liter d-I (second experiment) via a multichannel peristaltic pump that was fed by a 10-liter reservoir. The per capita flow rate was the same for all tubes in both experiments. The outflow at the bottom of the tubes was screened with 250-,um mesh to keep the animals inside (Fig. 1). Both experiments consisted of a fish treatment and a no-fish control. In the fish treatment, an adult Leucaspius delineatus (Cyprinidae; body size, 5 cm) swam in the 10-liter glass reservoir, which supplied the fish-treated flow-through chambers. The fish was fed 30 adult D. magna of the same Bin- nensee clone every day before daily cleaning and water exchange in the reservoir. Air bubbling prevented sinking of the algae in the reservoir. The control treatment was treated identically, but the reservoir con- tained no fish. The fish-treated tubes and the control tubes were alternated in the water bath.

To determine the depth of the animals at night, we illuminated the tubes individually with a vertical 1-m-long luminescent lamp screened with a red gelatin filter (Kodak No. 25 Wratten). The filter allowed only wave- lengths >610 nm to pass.

In the stratification experiment, a cohort of 60 Daphnia was placed individually in the tubes when the animals were 41 h old. The initial body length and dry weight were

determined with a subsample of 15 individuals taken from the same cohort. The mothers of the experimental animals were sisters from the same clutch of one female. The experimental animals consisted of a subset of the third clutch of their mothers. Both tubing and chambers were flushed for 12 h before adding animals. In the unstratified experiment, 12 tubes with three individuals per tube were used. The animals were reared under the same conditions as in the stratification experiment.

The vertical position of each individual was noted every 3 h during the stratification experiment and at noon and midnight in the unstratified experiment. The experiments lasted 4 d, then the animals were har- vested and the following parameters were determined for every individual. Body length was measured under a dissecting mi- croscope to the nearest 0.01 mm. Dry weight was determined to the nearest 0.2 jig with a Sartorius ultramicro-balance after drying the animals for 12 h at 60?C. Egg number was noted and the state of maturity was determined according to the method of Ed- mondson and Litt (1982). The total growth rate gw of the animals (d-1) was computed with the formula

gw= [ln(WV) - ln(Wo)]/(t1 - to)

where W0 and W1 are the dry weights at the beginning (to) and the end (tl) of the experiment. In the second experiment the eggs were carefully detached from the body and weighed separately. The somatic growth rate was calculated with the dry weights of the body only. The mean temperature experienced by each animal was calculated by av- eraging the temperature values determined from the depth-temperature relationship (Fig. 1) for each observation.

Results All Daphnia exposed to fish-free water

stayed in the upper, warm part of the tubes throughout the entire stratification experiment. Although some individuals occasion- ally visited deeper strata, they never crossed the thermocline at 40 cm (Fig. 2). Conse- quently, all the Daphnia individuals raised in no-fish water experienced a high average temperature throughout the experiment,




0 10

20

30 -

80 -

9n 0 -50 (D

60 6 70

80 90

0 12 24 36 48 60 72 84 96

0 10 20 30

E o40

. 50 o60-

70-

90-

0 12 24 36 48 60 72 84 96

elapsed time (h)

Fig. 2. Swimming tracks of the Daphnia individuals in the no-fish treatment (above) and in the fish treatment (below) in the stratification experiment. Thick lines reflect the average population depth. The day/ night cycle is indicated by the bars at the top of the panels.

ranging from 19.6?C to 21.7?. The mean depth of the 30 fish-free Daphnia did not show any regular diel changes. On the fourth day of the experiment a short-term migration (3-9 h) into deeper strata was observed in individuals that had just laid the first clutch of eggs into their brood chambers (Fig. 2).

The behavioral pattern of the Daphnia exposed to the fish cue was different. Im- mediately after being placed into the fish- treated tubes, the animals migrated downward. This trend was interrupted during the first night. The next day, the animals again migrated downward until almost all individuals reached the bottom (Fig. 2). Throughout the entire experiment the fish- treated population showed the normal pattern of DVM, moving up at night and staying deep during the day. However, even at night the mean depth of the population never moved above 60 cm, thus persisting below the thermocline both day and night.

There was considerable behavioral vari-

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0.6 -

0.5 -

. 0.4 -

002 040@ 0.0

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0.0 , , , , , i 8 10 12 14 16 18 20 22

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Fig. 3. Total growth rate of Daphnia individuals from the no-fish set (0) and from the fish set (0) vs. mean depth (above) and vs. mean ambient temperature (below) for the experiment with thermal stratification.

ability in the fish-treated set of animals; some individuals migrated up to the very surface, while others remained at the bottom. Thus, in the fish-treated set the average depth of the individuals throughout the experiment ranged from 60.6 cm to 93.1. As a consequence of the individual migration pattern, the animals were exposed to different average ambient temperatures, which varied between 9.60 and 13. 1C.

The behavioral differences between the fish-treated and the control Daphnia were accompanied by marked differences in the individual development rates. The animals staying in fish-free water grew on average 2.8 times faster (0.57 d-t) than those exposed to the fish cue (0.27 d-l). The cor- relations in the fish-treated set between growth rates and both individual mean depth and individual mean temperature were found to be highly significant (r = 0.647, P = 0.001 and r = 0.680, P = 0.001, respec-



Costs of Daphnia DVM 1593

tively; Fig. 3). All fish-free Daphnia laid eggs on the sixth day after birth. Only 52% of the fish-treated animals displayed the mor- phological characters indicating maturity at the end of the experiment and none pro- duced eggs.

In the experiment without thermal stratification, the basic patterns of Daphnia behavior in both sets were the same as in the stratification experiment (Fig. 4). Again, the fish-treated population spent the day lower in the water column and migrated toward the surface at night, whereas the fish-free Daphnia permanently occupied the surface strata. Although all were exposed to the same constant temperature, the individual sizes and body weights were still significantly larger in animals grown in no-fish water (Ta- ble 1). Furthermore, we found a different resource-allocation pattern between treatments. The individuals experiencing the chemical presence of fish invested more en- ergy into reproduction and had larger clutches with smaller eggs than fish-free Daphnia (Table 1).

Discussion We conducted our experiments with ge-

netically identical D. magna females of the same age. Though separated, they all faced the same abiotic environment and food conditions. However, we observed within this very uniform group of animals two different patterns of behavior, which were as- sociated with the presence or absence of a fish-originated chemical cue (Loose et al. 1992). The behavioral difference between the fish-treated set and the control set con- firms that onset of DVM in this Daphnia

0~ 10 -

20

30-

E 40 -

50-

70 -

80-

90

0 12 24 36 48 60 72 84

elapsed time (h)

Fig. 4. Average population depths of the Daphnia from the no-fish treatment (0) and from the fish treatment (0) during the second experiment. Error bars indicate 95% C.I.

clone did not require any genetic shift caused by selective predation, but was controlled by phenotype alone.

The warm, food-rich subsurface strata are optimal for maximizing the metabolic rate. Planktonic animals that spend more time at the surface are in a better physiological state (higher fecundity, higher protein content) than those lower in the water (Stich and Lampert 1984; Guisande et al. 1991). However, surface-dwelling zooplankton ob- viously suffer from severe fish predation. Hence, the optimal strategy for maintaining high individual growth would be to simply remain at the surface permanently (Stich and Lampert 1984). Indeed, in our study all the no-fish Daphnia remained at the surface and displayed little variation in their habitat choice.

The individuals exposed to the fish cue,

Table 1. Growth and resource allocation in Daphnia magna raised at identical food and temperature conditions (nonstratification experiment) in the presence and in the absence of chemical fish cues (P-values were calculated with nested one-way ANOVA, df = 1, n = 18).

No fish With fish

Mean SD Mean SD P

Length (mm) 2.90 0.081 2.67 0.092 <0.0001 Somatic wt (,g) 213 19 176 12 <0.0001 Total clutch wt (,g) 92.8 13 100 8.7 0.0182 Total wt (,g) 305 25 276 14 0.0004 Egg No. 14.7 1.9 18.6 1.3 <0.0001 Single egg wt (,g) 6.43 0.58 5.39 0.50 <0.0001 Somatic growth rate (d-') 0.435 0.024 0.386 0.019 <0.000 1 Total growth rate (d-') 0.529 0.022 0.503 0.013 0.0005




however, avoided the favorable surface strata at least during the day. These behavioral differences directly contributed to differences in life-history parameters. The migrating individuals of the experimental population had much lower growth rates than the nonmigrating ones. Food effects can be ruled out as a cause for the difference in growth, because the algae were homogeneously distributed in the flow-through chambers and were kept at constant con- centrations during the experiment. Depth- dependent differences in temperature were the primary reason for the delayed development of the fish-treated animals. "Cou- rageous" individuals that regularly migrated to the surface at night experienced a higher average ambient temperature and grew faster than the "timid" ones that stayed deep in the cold most of the time (Fig. 3). In the field, where low temperatures in deep waters are often correlated with low food quantity and quality, depth-dependent differences in metabolic rates might be even more extreme. Even if a subsurface chlorophyll maximum lies in the cold hypolimnion, the disadvantage due to low temperature is not likely to be overcome by the better food quality (Kerfoot 1985).

Thus, even if the death rate is not directly enhanced by predation, the mere presence of a fish predator can slow the population growth rate of zooplankton by inducing a shift in behavior (i.e. migration into a suboptimal habitat). This indirect predator effect, although described in many other predator-prey systems (see Sih 1987), has not yet been suggested for planktonic populations because predator-induced changes in zooplankton behavior were not recognized until relatively recently (Dodson 1988).

The fish-induced decrease in the average temperature of D. magna individuals was not solely responsible for the decrease in growth rate we observed. The response to the chemical presence of fish seems to be more complex, including both behavioral and physiological shifts. Our estimates of the metabolic cost in terms of growth rate could be influenced by the observed predator-induced switch in resource allocation, a pattern that was reported and discussed by Machacek (1991) and Stibor (in press)

for Daphnia galeata. Indeed, individuals exposed to the fish cue allocated more en- ergy for egg production relative to somatic growth than did individuals in the no-fish treatment. Moreover, the total biomass production (i.e. body plus eggs) of those animals grown in fish-free water was significantly higher than the production of fish- treated animals, even without temperature or food differences between treatments (Ta- ble 1). One possible mechanism to account for the difference in total production could be that fish-treated animals produce their first clutch more quickly (Stibor in press). The part of the biomass represented by the eggs in the brood pouch does not contribute further to the production of the animal. A delay in egg production would therefore result in enhanced total production.

If the DVM behavior is assumed to be evolutionarily stable, metabolic costs of downward migration to lower temperatures must be balanced by fitness gains (Gabriel and Thomas 1988). In our case, the benefits are most likely linked to the vertebrate predation risk, which can be reduced by migrating into darker deep zones where visu- ally oriented fish are less efficient in detecting prey (Kozhov 1963; Zaret and Suffem 1976).

In the presence of a predator, however, our Daphnia appeared to be inaccurate in choosing the optimal behavioral tradeoff and exhibited a much wider range of different space-use modes than fish-free individuals. Though genetically identical and exposed to the same environmental conditions, fish- treated Daphnia displayed several behavioral patterns, which in turn led to diverse individual growth rates. Hence, not only the general pattern of the population behavior was affected by the presence of the fish cue, but the behavioral variability between individuals of the same clone also increased.

Field observations indicate that planktonic cladoceran populations are often widely distributed throughout the water column of lakes (e.g. Pijanowska and Dawido- wicz 1987). This distribution may reflect variability in habitat choices (Pearre 1979). It seems possible that single Daphnia individuals cannot precisely assess the balance between risks and gains of DVM and therefore do not express the optimal behav-



Costs of Daphnia D VM 1595

ioral response. Another possibility is that different migration strategies result in only small differences in terms of payoff. In an extreme case, both "normal" DVM and nonmigration behavior could coexist in the same population, which (under certain pa- rameter constellations) was indeed predict- ed by the ESS model of Gabriel and Thomas (1988). The selective forces in such a case would be too weak to maintain low behavioral variability in the population.

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RINGELBERG, J. 1991. A mechanism of predator-me- diated induction of vertical migration in Daphnia hyalina. J. Plankton Res. 13: 83-89.

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Submitted: 30 April 1992 Accepted: 21 October 1992 Revised: 9 November 1992



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Metabolic Costs During Predator-Induced Diel Vertical Migration of Daphnia