Experimental methods for measuring the effect of light acclimation on vertical migration by Daphnia in the field

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1 638 Notes Limnol Oceunogr., 38(3), 1993, , by the American Soctety of Limnology and Oceanography, Inc Experimental methods for measuring the effect of light acclimation on vertical migration by Daphnia in the field Abstract-A new method is developed and tested for measuring vertical migration behavior by zooplankton in the field by means of acrylic columns with conical traps. Migration behavior in columns by different species and by different individuals of the same species is similar to migration behavior in the lake. We further show that acclimation to light intensity can be a factor in determining the amplitude of vertical migration in Daphnia p&curia. Although diel vertical migration behavior in zooplankton has received much attention, the behavior itself has been subjected to little direct field experimental work (Johnsen and Jakobsen 1987; Leibold 1990; Neil1 1990). In large part this is due to the need for an inexpensive and convenient method to assay the behavior of known individuals in a replicated and manipulatable way in the field. Laboratory studies in small containers (e.g. Calaban and Makarewicz 1982; Dodson 198 8; De Meester and Dumont 1988) have problems of scale because behavior that occurs on a scale of meters in the field is generally measured on a scale of centimeters in the lab. Temperature, food, oxygen, and other gradients are also often lacking in these small-scale experiments. Large laboratory containers, i.e. plankton towers (e.g. Enright and Hammer 1967; Bohrer 1980; Huntley and Brooks 1982) that solve many of these problems suffer from being artificial and expensive; such experiments are often unreplicated or lack simultaneously run controls. Experimental studies using field bag enclosures suffer least from these problems (e.g. Neil1 1990; Johnsen and Jakobsen 1987) but are not always convenient due to their size and the effort required to use them. They often have additional problems because plankton Acknowledgments We are grateful for the assistance and advice of Alan Tessier throughout and to Kevin Geedey for data on natural distributions of Daphnia in Lawrence Lake. This research was supported by NSF BSR 9 l and by a University of Chicago Block Grant. that are not protected from their predators may appear to show different behaviors due to selective mortality (e.g. Leibold 1990; Arts et al ; Raess and Maly 1986). They also must be sampled carefully to avoid the confounding impacts of sampling on densities (e.g. Dumont 1972) and to avoid bias due to potential variation in sampling efficiency on plankton with different behaviors (e.g. animals that are near the bottom of the enclosures). We have designed, constructed, and tested a more convenient field apparatus for measuring the behavior of controlled zooplankton populations and used them to test directly for the effects of light acclimation on the magnitude of upward nighttime migration by Daphnia pulicaria. Although the influence of light has long been known to affect the timing of vertical migration (reviewed by Huntley 1986) and also suggested as influencing its amplitude (Haney and Hall 1973, little work has been done on its effects in situations where migration occurred in strongly stratified environments. We hypothesized that acclimation and imprinting (intragenerational responses) might affect the amplitude of migration behavior. Our columns (Fig. 1) consist of four sections of acrylic tubing. Sections have a circular 6.25 cm2 window at the midpoint with screening that allows exchange of chemicals and small particulates with the ambient water (more windows could be used but this makes the columns more fragile). These sections alternate with short sections containing conical traps and 6.25-cm2 circular Nitex screens that serve to drain the tubes and trap zooplankton when the columns are lifted out of the water. For measuring upward migrations the uppermost trap section is fitted with a removable screen that prevents animals from migrating out of the top of the column. The lowermost trap section is fitted to a removable windowless acrylic bucket that holds the animals at the beginning of the experiment and ensures that the columns are filled by water flowing in

2 Notes 639 through windows located above the conical traps. This bucket section can also be fitted with a small weight to ensure that the columns remain vertical. The columns are inverted to measure downward migration so that the bucket section is at the top and the screen at the bottom. We used nontoxic polyethylene tape to hold sections together, but mechanical clips could also be used. The columns are deployed in the field by placing a small population of animals in the lower bucket; we typically used near-ambient densities ranging from 20 to 200 individuals (per 33.5-liter column), although we found little evidence for an effect of density per se on behavior in these short-term experiments. The first conical section is then attached to the bucket. Alternating tubes and trap sections are then attached as the column is slowly lowered into the water. Water enters the column through the windows located above the conical traps. In visual observations with SCUBA we did not see any animals entrained out of the lower bucket section during the deployment process. After this assembly, the column is suspended from a float at a specified depth. We selected this depth so that the uppermost trap section was at a depth of 2 m and the column extended from the shallow epilimnion well into the hypolimnion of the lake. Thus animals trapped in each section are representative of their distributions integrated over five successive 2-m intervals and of a sixth section representing animals that remain in the lowermost bucket that may have not migrated or would have tended to move downward. The columns are allowed to stay in the lake for a specified time interval during which the animals can move in one direction (up or down depending on the orientation of the columns) but are impeded from returning in the opposite direction by the conical traps. We generally left the columns out overnight when estimating upward nocturnal migrations and from midmorning to late afternoon when measuring daytime migrations. After this incubation period, the animals in each trap section in the column are collected by slowly lifting the column, disassembling each section, and rinsing animals trapped in each of the small sections into prelabeled vials. We also rinsed the tube sections to collect an- Fig. 1. Design of experimental columns (detailed description given in text). imals that had adhered to the walls during emptying. If the columns are used to measure downward movement, the column would first be rotated 180 by releasing the top of the column from the float and pulling up on the bottommost section of the column with a previously attached rope. Animals remaining in the lowermost trap section are also collected and visually inspected to verify that they are still alive. Deployment and recovery of the columns generally takes 20 min per column. The traps act as effective barriers to the downward movement of Daphnia. Visual inspection with SCUBA of water flow during this process with dyes indicates that most of the water from each section flows out of the win- dows above the conical traps at the bottom of the section rather than flowing into the next

3 640 Notes PROPORTION PROPORTION 01 I 02 I 03 I 04 I 05 I 06 I 07 I 08, 0,l 0,i 0,3 0;4 0,5 0,6 0;7 0,8 Fig. 2. Nighttime vertical distributions of Daphnia pulicaria (left) and Daphnia galeata mendotae (right). Crosshatched bars show the distribution in the columns; open bars show the distribution in the lake estimated from a series of Schindler traps. Two-way confidence intervals illustrate 1 SE for the mean proportion at each depth interval across replicate columns. section through the opening in the trap. We migration behavior. During the day, most inalso observed that most animals tended to dividuals are found in the hypolimnion but at move downward along the sides of the col- night D. pulicaria is found in both the epilimumns and were less likely to move through the nion and the hypolimnion; thus some individtrap opening in the center of the column. uals appear to be entirely hypolimnetic where- We tested the performance of the columns as others migrate (Leibold and Tessier 199 1). in the field by comparing the estimates of up- We collected D. p&curia from Gull Lake at ward nighttime migrations of two Daphnia night ( EST) separately from the species collected from Lawrence Lake (see Lei- epilimnion (O-8-m depth) and hypolimnion bold 1990) in three replicated columns with (25-l 5-m depth) with a self-closing Wisconsin their nighttime distributions in the lake. Zoo- bucket net (80-pm mesh). The animals were plankton used in the columns were collected held in the lab at 12 C and fed a generous in late afternoon (1700-l 800 EST) from ver- amount of Ankistrodesmus falcatus until the tical tows with a Wisconsin bucket net (80 pm next afternoon. They were then ( mesh) and immediately transferred to the col- EST) transferred to replicate columns (two repumns as described above. To estimate the licate columns per subpopulation) and incunighttime vertical distribution of lake popu- bated in Lawrence Lake. The columns were lations we used a Schindler trap (20 liters, net retrieved the next morning ( EST) with 80-pm mesh) to sample at 2-m intervals and the animals preserved and enumerated as between 2200 and 2400 EST. Columns were described above. The experiment was repeated taken down the next morning ( EST). 4 d later for a total of four replicates per sub- Animals collected from the Schindler traps and population. from the columns were preserved in cold sug- Finally we conducted a third experiment to ar-formalin. The samples were enumerated test for the effects of acclimation to light. Repand classified by species and life-history stage. licate sample populations of migratory D. puli- We conducted a second experiment with the curia from the epilimnion of Gull Lake were columns to determine whether the behavior of kept in the lab for 2 1 d under laboratory conindividuals in a population with variable mi- ditions (2O C, 12 : 12 L/D cycle, regularly fed gration behavior was constant from day to day. A. falcatus at - 15,000 cells ml- ). These pop- D. pulicaria in Gull Lake exhibits variation in ulations were then kept in the lab at one of

4 Notes 641 Table 1. Mean depth (m) of separate life-history classes and species of Daphnia in columns and in Schindler trap series taken on the same night. Standard errors (m) are also shown for estimates among three columns and P-values for one-sample t-test comparison with Schindler series. Schmdler Mlgratlon columns traps Species/Class (depth) Depth SE t P D. galeata mendotae Juveniles >0.2 Gravid females Barren females >0.2 >0.2 D. pulicaria Juveniles >0.2 Gravid females >0.2 Barren females co.05 two different light levels for 6-l 2 d; half were kept continuously in low light (1 PEinst mp2 s-l) and the other half at high daytime light (12 PEinst m-2 s-l) on a photoperiod of 16 : 8. One replicate of each of these treatments was assayed for upward nighttime migration with the columns on each of five different nights. Our experiment thus consisted of a blocked (by date) experiment with two treatments (light vs. dark acclimation). Comparisons of the distributions of Daphnia from Lawrence Lake as determined from a series of Schindler trap samples with their EPILIMNION HYPOLIMNION HABITAT SOURCE Fig. 3. Average depth of juvenile (hatched bars) and adult (open bars) Daphnia pulicaria collected from the epilimnion and hypolimnion of Gull Lake. Error bars denote SE of each mean E 40 z W I f DARK ACCLIMATION LIGHT TREATMENT Fig. 4. Average depth of juvenile (hatched bars) and adult (open bars) Daphnia pulicaria acclimated to dark and light regimes. Error bars denote SE of each mean. distributions in the columns shows that the columns had little effect on migration behavior (Fig. 2). The mean depths of different life-history stages for each of the species in the columns compared with their distributions (Table 1) reveal no significant differences between the columns and the lake samples except that nongravid animals were 0.8 m deeper in the lake than in the columns. In all of these comparisons the standard error for estimates of the mean depth of individuals was between 0.2 and 0.5 m, indicating that mean depth estimates from the columns have a statistical resolution of 0.5-l m. The behavior of D. pulicaria is also relatively stable from day to day (Fig. 3). Juvenile and adult D. pulicaria collected as migrants in Gull Lake continued to migrate in the columns in Lawrence Lake. Similarly, nonmigrating D. pulicaria collected from Gull Lake stayed in the hypolimnion in the columns in Lawrence Lake. The difference between migrant and nonmigrant behavior was 3-4 m and highly significant (P < for juveniles and adults with a one-way ANOVA). In our final experiment comparing the migration behavior of D. pulicaria raised under low light with animals raised under high light conditions we found that light acclimation-imprinting had a significant effect on migration behavior (Fig. 4) of adults (F = 9.29, df = 9,

5 642 Notes P = with one-way ANOVA), although the magnitude was fairly small (- 1 m). Although juveniles showed a similar trend, there was no significant difference in their average depth (F = 1.25, df = 8, P = 0.30). There was no significant block (i.e. date) effect in this experiment (F = 1.45, P > 0.2 for adults; F = 0.77, P > 0.5 for juveniles) and this effect was ignored in the analyses described above. Our comparisons of the migration behavior of animals in the columns and in the lake (Table 1) show that the columns have little effect on the migration behavior of two species of Daphnia. Although some subtle differences may be due to enclosure effects in the columns, they may be equally ascribed to possible bias in comparisons with the estimates from the Schindler series for two reasons. First, the migrations as estimated from Schindler traps represent distributions at one particular time during the night whereas migration behavior in the columns is more likely to represent behavior expressed over the duration of the entire night. Deeper distribution of D. pulicaria in the Schindler series than in columns might reflect the possibility that D. pulicaria upward migrations were not at their maximum when the Schindler samples were taken. Second, for various reasons, Daphnia captured during the day with a vertical net tow are likely to represent a biased sampling of individuals compared to individuals captured at night with the Schindler trap. These potential effects notwithstanding, our data indicate that they are small and that the columns can accurately measure migration behavior of Daphnia. More importantly, the columns allow precise characterization of animal populations with known differences in behavior. Animals with substantially different behavior in one lake faithfully maintained differences in their behavior when placed in the columns in a different lake. Further, the data demonstrate that this method can detect differences of < 1 m in the average depth of Daphnia with as few as three replicates. Finally we found that acclimation to light could significantly alter the vertical distribution of D. pulicaria adults. In both adults and juveniles this effect was small and resulted in a change in average depth of only - 1 m. Acclimation to light thus appears to be a weak regulator of migration amplitude in D. puli- caria. However, other potential acclimation factors (e.g. temperature, oxygen levels, etc.) may also be important. The columns allow manipulative field experiments over a natural spatial scale on factors influencing vertical migration of zooplankton. However, there are several potential problems with the use of these columns for studying migration behavior. First, there might be altered distributions of food and chemicals in the columns. During the filling process, water enters the columns from all of the windows that are underwater and a certain amount of mixing of water from different depths occurs during the filling process. The presence of windows that allow some exchange of chemicals and small particles with the ambient water mitigates this somewhat, but some differences are almost inevitable. One solution is to close all of the windows except the lowermost one with tape. However the extra work with SCUBA required to remove the tape after deployment makes this somewhat impractical. In our case we also found that it had little effect on the behavior of our organisms. Second, there could be overcrowding of animals and consequent effects of density on vertical distributions. We found it was best to use > 10 individuals of any group (i.e. species and life-history stage) to obtain reliable estimates of their distributions. Although we were generally able to do so without using artificially high densities, we imagine that studies of organisms with lower densities might require use of artificially high numbers of individuals. Finally, there is possible bias due to complex migration behavior. Distributions estimated with our columns are probably best interpreted as measures of maximum movement by groups of individuals over the defined time interval, which may not be the same as the average distribution of organisms when there is complex migration behavior such as midnight sinking (Haney and Hall 1975). Care in choosing a relevant time interval for the deployment of the columns could help overcome this problem. Mathew A. Leibold Colin T. West Department of Ecology and Evolution University of Chicago

6 Notes E. 57th St. Chicago, Illinois References ARTS, M. T., E. J. MALY, AND M. PASITSCHNIAK The influence of Acilius (Dytiscidae) predation on Daphnia in a small pond. Limnol. Oceanogr. 26: BOHRER, R Experimental studies on vertical migration. Am. Sot. Limnol. Oceanogr. Spec. Symp. 3: 11 I-121. New England. CALABAN, M.J., AND J.C. MAKAREWICZ Theeffect of temperature and density on the amplitude of vertical migration of Daphnia magna. Limnol. Oceanogr. 27: DE MEESTER, L., AND H. J. DUMONT The genetics of phototaxis in Daphnia magna: Existence of three phenotypes for vertical migration among parthenogenie females. Hydrobiologia 162: DODSON, S The ecological role ofchemical stimuli for the zooplankton: Predator avoidance behavior in Daphnia. Limnol. Oceanogr. 33: 143 l-l 439. DUMONT, H. J A competition-based approach of the reverse vertical migration in zooplankton and its implications, chiefly based on a study of the interactions of the rotifer Asplanchna priodonta (Gosse) with several Crustacea Entomostraca. Int. Rev. Gesamten Hydrobiol. 57: l-38. ENRIGHT, J. T., AND W. M. HAMNER Vertical diurnal migration and endogenous rhythmicity. Science 157: HANEY, J. F., AND D. J. HALL Diel vertical migration and filter-feeding activities of Daphnia. Arch. Hydrobiol. 75: HUNTLEY, M Experimental approaches to the study of vertical migration of zooplankton. Contrib. Mar. Sci. 27(Suppl.): 7 l-90. p, AND E. BROOKS Effects of age and food availability on diel vertical migration of Calanus pac$cus. Mar. Biol. 71: JOHNSEN, G. H., AND P. J. JAKOBSEN The effect of food limitation on vertical migration in Daphnia longispina. Limnol. Oceanogr. 32: LEIBOLD, M. A Resources and predators can affect the vertical distribution of zooplankton. Limnol. Oceanogr. 35: , AND A. J. TESSIER Contrasting patterns of body size for Daphnia species that segregate by habitat. Oecologia 86: NEILL, W. E Induced vertical migration in copepods as a defence against invertebrate predation. Nature 345: RAESS, F., AND E. J. MALY The short term effects of perch predation on a zooplankton prey community. Hydrobiologia 140: 155-l 60. Submitted: 20 May 1992 Accepted: 7 October 1992 Revised: 12 November 1992 Limnol Occano ~r, 3X(3), 1993, , by the American Society of Limnology and Occanographb, Inc Resuspension of sediment by focused groundwater in Lake Banyoles Abstract - Resuspension of sediment by subterranean springs occurs in karstic, multibasin Lake Banyoles, Spain. The sediment at the bottom of one of the basins was consolidating when intrusion of groundwater caused resuspension. Here, the luto- Cline rose nearly 20 m over 10 months. During this episode temperature profiles, sediment size distributions, bulk density, and settling rates showed that the jet-generated turbulence produced strong mixture in the central core of the conic depression forming the basin. Data from another basin where the sediment was always in suspension are presented for comparison. Here, the stratification in density and settling rate of the particles suggest sorting out of the aggregates, with the largest floes occupying the deepest parts of the basin. Resuspensions of unconsolidated sediment are a common phenomena in inland, estuarine, and coastal waters (Wolanski et al. 1988). The sediment is entrained from the bottom and is mixed upward by turbulence induced by wind-driven, surface gravity waves, tidal currents, plunging inflows, etc. The entrainment laws are still poorly understood, but depend strongly on the type of sediment, the degree of consolidation and many other variables (Mehta et al. 1989). Once the sediment is entrained, the water column can be divided as two fluids-a fairly clear upper layer and a turbid bottom layer -separated by a lutocline (a sharp step structure in suspended sediment concentration). Suspension of lake sediment by groundwater is a feature of Lake Banyoles Acknowledgments We are indebted to Jiirg Imberger for comments on an early draft of the manuscript, to R. E. Stauffer for critical that has not been described elsewhere. revision of the manuscript, and to David Brusi for assis- In Table 1 averages of meteorological data tance in the graphical representation of Fig. 1. collected over 40 yr are presented (Llamazares

Population dynamics and body-size selection in Daphnia

LIMNOLOGY AND OCEANOGRAPHY January 12 Volume 37 Number 1 Limnol. Oceanogr., 37(l), 12, 1-13 0 12, by the American Society of Limnology and Oceanography, Inc. Population dynamics and body-size selection