Lack of Endogenous Rhythmicity in Daphnia Diel Vertical Migration

Lack of Endogenous Rhythmicity in Daphnia Diel Vertical MigrationAuthor(s): Carsten J. LooseSource: Limnology and Oceanography, Vol. 38, No. 8 (Dec., 1993), pp. 1837-1841Published by: American Society of Limnology and OceanographyStable URL: http://www.jstor.org/stable/2838459 .

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Notes 1837

tonic copepod, Calanus pacificus Brodsky: Laboratory observations. J. Exp. Mar. Biol. Ecol. 74: 53-66.

SMITH, P. E., M. D. OHMAN, AND L. E. EBER. 1989. Anal- ysis of the patterns of distribution of zooplankton aggregations from an acoustic doppler current profiler. Calif. Coop. Oceanic Fish. Invest. Rep. 30: 88-103.

WONG, C. K. 1988. The swimming behavior of the copepod Metridia pacifica. J. Plankton Res. 10: 1285- 1290.

ZARET, T. M. 1972. Predators, invisible prey, and the

nature of polymorphism in the Cladocera (Class Crus- tacea). Limnol. Oceanogr. 17: 171-184.

1980. Predation and freshwater communities. Yale.

Submitted: 5 November 1992 Accepted: 23 April 1993 Revised: 21 June 1993

Limnol Oceanogr, 38(8), 1993, 1837-1841 ? 1993, by the Amencan Society of Limnology and Oceanography, Inc

Lack of endogenous rhythmicity in Daphnia diel vertical migration

Abstract-A population of Daphnia galeata x hyalina was induced to perform diel vertical migration (DVM) by the addition of fish-kairomones to a large plankton tower. Vertical profiles of zooplankton abundance were measured every 12 h. When the tower was covered to shield the water column from the light, DVM ceased, and vertical distributions were not statistically different from the night profiles that had been observed before the tank was covered. This result suggests that endogenous rhythms do not trigger DVM, but that a change in light intensity must occur.

The ultimate causes of zooplankton diel vertical migration (DVM) have received much attention since the phenomenon was discov- ered (see Lampert 1989, 1993). The predator avoidance hypothesis (Kozhov 1963; Zaret and Suffern 1976) has gained recent strong support from studies showing that DVM can be induced by chemical exudates from predators (Dodson 1988; Neill 1990; Dawidowicz and Loose 1992; Loose 1993).

However, the proximate causes triggering migration every morning and evening have received less attention, and the question of endogenous vs. environmental control remains unanswered. Early work of Ringelberg (1964)

Acknowledgments Thanks to Winfried Lampert, Bill DeMott, Herwig Sti-

bor, and three anonymous reviewers for comments which improved the manuscript, and to Nancy Zehrbach for lin- guistic help.

showed that a phototactic reaction is provoked by relative changes in light intensity that cross a certain threshold. This phototactic response was later shown to be enhanced by exudates from predators (Ringelberg 1991 a,b; De Mees- ter 1993). This proximate mechanism requires a change in light intensity for migration to occur (Ringelberg 1993). Another mechanism could be endogenous rhythms that provide a regular internal trigger on a diel basis without external stimuli being active. A signal by an internal clock would then cause the animals to migrate. These rhythms have indeed been found in the phototactic responses (Rimet 1960; Ringelberg and Servaas 1971) and in the vertical distribution of Daphnia in small-scale laboratory columns (Harris 1963; Young and Watt 1993). A large-scale experiment with marine zooplankton revealed endogenous rhythms in some taxa and environmental control in others (Enright and Hamner 1967).

Previous research has not directly tested whether an internal clock governs DVM in Daphnia or whether a relative change in light intensity is necessary. I performed a simple large-scale experiment to test the hypothesis that DVM in Daphnia is controlled by an endogenous rhythm.

The experiment was conducted in one of the plankton towers at the Max Planck Institute for Limnology in Plon. A detailed description of the plankton towers is given by Lampert and Loose (1992). The tower (stainless steel, 11.2 m high, 85.8-cm diam) was filled with 10-



1838 Notes

,um-filtered water from the nearby mesotroph- ic Schohsee. The temperature distribution in the tower (20?C in the epilimnion and 1 0?C in the hypolimnion) was kept stable throughout the experiment (Fig. 1). Natural daylight, enhanced by three lamps (Osram HQI-TS 70 W/NDL), illuminated the tank from above (long day, 16: 8 L/D cycle). Light intensities at the surface during the day were 100-150 AEinst m-2 s-i and 5-8 in the thermocline (LiCor Quantumsensor).

I used a clonal population of Daphnia galeata x hyalina, which was originally established from an animal collected in Lake Constance (Bodensee). These hybrids are known to perform strong diel vertical migrations in Lake Constance in summer (Weider and Stich 1992).

Scenedesmus acutus grown in batch cultures served as food for the daphnids. The food concentration in the epilimnion was continuously kept above the incipient limiting level (0.26 mg C liter- 1; Muck and Lampert 1984) to pre- vent changes in Daphnia vertical distribution due to food limitation (see Johnsen and Ja- kobsen 1987). Food quantity decreased below the thermocline (Fig. 1). The amount of food available for the Daphnia population in the tank was measured daily by two methods. First, a vertical profile of particle volumes (<30 gm) was measured with a CASY particle counter. Particle volume was converted to particulate organic carbon (POC) with a regression established in previous experiments (r2 = 0.92, P < 0.001, n = 18; Loose 1993). Second, water from three different depths was mixed, screened through 30-,gm gauze, filtered through What- man GF/F, and analyzed for POC. The algal concentration was then calculated and the re- quired amount of Scenedesmus was added to the epilimnion each day.

The vertical distribution of the Daphnia population (initially - 70,000 animals) was measured with the flow-through traps de- scribed by Lampert and Loose (1992). Twelve of these traps were installed at vertical inter- vals of -0.5 m. For measuring one Daphnia depth profile, all traps were run simultaneously for 5 min. The animals were counted under a dissecting microscope. Daphnids that were re- moved (-4% of the population per sampling) were not replaced.

Previous experiments showed that fish-kairomones are needed to induce DVM in the

* POC (mg C liter-1)

0.0 0.2 0.4 0.6

20 ,_j

D4-

5-

6-

, I , I I

10 12 14 16 18 20 a Temperature (0C)

Fig. 1. Temperature and food conditions (POC) in the plankton tower throughout the experiment (means of the five daily measurements ?95% C.I.).

plankton towers (Loose 1993). An aquarium (100 liters) containing four adult fish (Leucas- pius delineatus, Cyprinidae; body size, 5 cm) was placed near the top of the tower. The fish were fed frozen midge larvae every second day. Water was continuously pumped out of the tower from near the surface through a 1 00-Am mesh which Daphnia could not penetrate and into the aquarium at a rate of 2 liters min-'. Passive outflow was directed from the aquarium back into the tower at a depth of 2 m. The flow provided complete circulation of the epi- limnetic water through the aquarium in - 12 h. This technique ensured a "chemical presence" of the predators via fish-exuded kairomones dissolved in the water (Loose et al. 1993).

The experiment started after 1 week of ad-



Notes 1839

Abundance (%) 25 0 25 50 25 0 25 50 75 25 0 25 25 0 25 25 0 25

0 0

2 2 2

=4 4 -~~~~~~~~~~~~~~~~~

6 6 6

8 * *8

| Day/nightrhythm 16:8 L/D 3 continuousdarkness

Fig. 2. Vertical distribution of a Daphnia population in the plankton tower on five consecutive days. The first five profiles were measured during a day-night cycle and the last five profiles under continuous darkness. Dark curves are profiles taken at midnight. Open curves are profiles taken at noon under daylight. Shaded curves are profiles taken at noon in the darkened plankton tower. Significant differences between midnight and noon profiles are marked with an asterisk (rank sum test, P < 0.001). Horizontal line indicates the depth of the thermocline.

aptation to the prevailing conditions. The depth distribution of the Daphnia population was then measured every 12 h (noon and midnight) for five consecutive days. A 16: 8 L/D cycle was maintained for the first 2 d. Then, after the third midnight sampling, the tower was covered with thick black, light-impenetrable plastic-foil and the artificial light sources above the towers were turned off. After darkening the tank, the tower was again sampled every 12 h for the next 3 d.

The presence of fish kairomones and a light/ dark cycle induced diel vertical migration in the Daphnia population. The animals stayed deeper during the day, showing strong surface avoidance, and scattered throughout the epilimnion at night (Fig. 2). As in previous experiments in the plankton towers, the animals did not penetrate the thermocline into the deep hypolimnion, but stayed around the thermo-

cline (Loose 1993). On both days before cov- ering the tower, there was a highly significant difference between the day and night distributions (rank sum test, P < 0.001).

The daphnids in the tower stopped their DVM behavior immediately after the tower was covered. Without a "sunrise," no daytime surface avoidance reaction took place and the animals stayed in the epilimnion, although the kairomones that induce migratory behavior were still present. There was no significant difference between day and night distributions on the last three consecutive days (rank sum test; P = 0.62, P = 0.66, and P = 0.39, respectively). A nonparametric ANOVA showed no significant difference when comparing all six profiles in total darkness (Kruskal-Wallis, P = 0.37).

The results of this experiment in the plankton tower show no influence of internal rhythms on DVM behavior. Of course, this outcome



1840 Notes

does not prove that endogenous rhythms do not exist in Daphnia. Different investigators have shown that these rhythms are present in phototactic reactions (Rimet 1960) or in small- scale laboratory columns (Young and Watt 1993). Sometimes prolongation of the diel rhythm to 28 h is observed after switching to continuous conditions (Harris 1963; Rin- gelberg and Servaas 1971). However, such a phase shift would still have invoked a daytime response of the Daphnia population at the samplings 12 and 36 h after darkening the towers.

Thus, my results show that endogenous rhythms did not influence the DVM behavior of this clone in a natural-scale experiment. Pre- vious studies in the plankton towers demon- strated that the Daphnia clone used in this experiment does not undergo DVM without fish-kairomones (Loose 1993). The present study shows that if kairomones are present, but the animals are deprived of a change in light intensity, no migration takes place. Thus, for the Daphnia clone tested here, two stimuli must be present for the display of DVM: a chemical stimulus by fish-exuded kairomones (Loose et al. 1993; Loose 1993) and a change in relative light intensity (Ringelberg 1964). Ringelberg (1991lb) proposed a mechanism by which a basic phototactic response is triggered only if a certain threshold in kairomone concentration is surpassed. Indeed, an enhancement of phototaxis in the presence of fish-exuded kairomones was measured in different Daphnia clones by Ringelberg (1991a,b) and De Meester (1993). My study further supports Ringelberg's (1991b) hypothesis that both chemical and light stimuli are needed to evoke DVM.

Carsten J. Loose' Max Planck Institute for Limnology Department of Physiological Ecology P.O. Box 165 24302 Plon, Germany

I Present address: Alfred Wegener Institute for Polar and Marine Research, P.O. Box 12 01 61, 27515 Bre- merhaven, Germany.

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1991 a. Enhancement of the phototactic reaction in Daphnia hyalina by a chemical mediated by ju- venile perch (Perca fluviatilis). J. Plankton Res. 13: 17-25.

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Notes 1841

, AND H. SERVAAS. 1971. A circadian rhythm in Daphnia magna. Oecologia 6: 289-292.

WEIDER, L. J., AND H. B. STICH. 1992. Spatial and tem- poral heterogeneity of Daphnia in Lake Constance: Intra- and interspecific comparisons. Limnol. Ocean- ogr. 37: 1327-1334.

YOUNG, S., AND P. WATT. 1993. Behavioral mechanisms controlling vertical migration in Daphnia. Limnol. Oceanogr. 38: 70-79.

ZARET, T. M., AND J. S. SUFFERN. 1976. Vertical migration in zooplankton as a predator avoidance mechanism. Limnol. Oceanogr. 21: 804-813.

Submitted: 2 June 1993 Accepted: 8 September 1993

Revised: 6 October 1993



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Lack of Endogenous Rhythmicity in Daphnia Diel Vertical Migration