Journal of Oceanography, Vol. 56, pp. 153 to 160. 2000

Diel Vertical Migration of the Marine Cladoceran leuckarti: Variations with Reproductive Stage

1 2 HIROAKI SAITO * and HIROSHI HATTORI

1Hokkaido National Fisheries Research Institute, 116 Katsura-koi, Kushiro, Hokkaido 085-0802, Japan 2Hokkaido Tokai University, Minami-ku, Sapporo 005-8601, Japan

(Received 8 February 1999; in revised form 17 May 1999; accepted 11 June 1999)

Diel vertical migration (DVM) of the marine cladoceran Podon leuckarti was investi- Keywords: gated with reference to their reproductive stages and size. Males and females, except ⋅ Podon leuckarti, for gamogenic females with an advanced resting egg (GA), aggregated at the near- ⋅ diel vertical bottom layer or at the surface during the day and dispersed into the water column at migration, ⋅ night. Both the near-bottom aggregation and the surface aggregation during daytime resting egg, ⋅ predation avoid- are suggested to be behavior that reduces the predation risk from visual predators. ance, However, GA aggregated in the near-bottom layer during daytime and avoided the ⋅ visibility. surface layer. The near-bottom aggregation might be more effective behavior for GAs to reduce risk of visual predation than the surface aggregation because of the con- spicuous resting egg they carried. These results show that carrying an advanced rest- ing egg influenced the DVM of P. leuckarti.

1. Introduction 1975; Buskey, 1994; Tsuda et al., 1998). Other important Zooplankton have adopted various strategies to mini- factors are size (Brooks and Dodson, 1965; O’Brien et mize the risk of predation, such as development of crests al., 1976) and motion (Buskey et al., 1993; Tiselius and or spines (Grant and Bayly, 1981; Havel and Dodson, Jonsson, 1997). The greater visibility of parthenogenic 1984), and decreasing daytime feeding activity (Bollens eggs of the freshwater cladoceran Daphnia increases the and Stearns, 1992; Tsuda et al., 1998). There is ample risk of visual predation (Gliwicz et al., 1981; Tucker and evidence that diel vertical migration (DVM) of Woolpy, 1984). Parthenogenic females of the marine zooplankton has a function in avoiding the risk of preda- cladoceran release embryos that have large tion (e.g., Lampert, 1993). Predation risk can influence pigmented eyes just before dawn, and they carry only the magnitude and properties of DVM. Larger or embryos with non-pigmented eyes during daytime (Onbé, pigmented species, which are more vulnerable to visual 1974; Bryan, 1979). This reproductive cycle is another predatory fish, show more extensive DVM than do smaller strategy, like DVM, to reduce the chance of being recog- or transparent species (O’Brien, 1975; Zaret and Suffern, nized by visual predators. 1976; Hays et al., 1994). The extent of the DVM increases Gamogenic females of cladocerans carry resting with increasing fish number (Bollens and Frost, 1989; eggs, which are dark colored and larger than the Frost and Bollens, 1992) or due to the presence of chemi- pigmented eyes of the embryos. Mellors (1975) showed cal exudates of fish (Loose et al., 1993). However, that freshwater cladoceran Daphnia spp. with resting eggs zooplankton cease DVM in predator-free environments were selected more by fish than females without resting (Gliwicz, 1986; Neil, 1990). Reverse DVM, i.e., upward eggs. Therefore, it is expected that gamogenic females migration during the day and downward migration at would show a different DVM pattern from parthenogenic night, is observed when predators such as chaetognaths females and males. In the present study, we examined the and euphausiids, which undergo the usual pattern of effects of reproductive stage, sex and size on the DVM DVM, are dominant (Ohman et al., 1983). of the marine cladoceran Podon leuckarti, and discuss Visibility is an important factor influencing the prey the factors influencing vertical distribution of P. leuckarti. selectivity of visual predators (e.g., Zaret and Kerfoot, 2. Materials and Methods Sampling was carried out at the center part of * Corresponding author. E-mail: [email protected] Akkeshi Bay, on the eastern coast of Hokkaido, Japan, Copyright © The Oceanographic Society of Japan. on 14Ð15 October, 1992 (Fig. 1). Bottom depth was 15Ð

153 16 m. Zooplankton were collected every 4 hours at 0, 2.5, ocular micrometer and up to 50 specimens in each sam- 5, 7.5, 10, and 14 m using an NIPR-sampler which was ple. designed to collect plankton using electronic screw-in- The concentration of breakdown products of algal duced water flow (Fukuchi et al., 1979). The sampler was pigments (pheopigments) in their guts was analyzed fitted with 330-µm mesh netting. Zooplankton were col- fluorometrically, as described previously (Saito and lected twice in each sampling layer. One sample was used Taguchi, 1996). Gut pigment contents increase propor- for enumeration (4.65 m3 filtered volume) and another tionally with ingestion rate if the gut evacuation rate con- (1.55 m3) was used for gut pigment analysis. Samples used stant is unchanging (e.g., Mackas and Bohrer, 1976). Al- for enumeration were preserved with buffered 5% (v/v) though gut evacuation rate constants increase with tem- formalin-seawater. Podon leuckarti were sorted from perature (e.g., Irigoien, 1998), they have been reported these samples by sex, and for females, by reproductive for copepods to be less variable by the time of day and by stages. Five reproductive stages of females were defined gut pigment contents (Ellis and Small, 1989; Durbin et based on the developmental status of the embryo or rest- al., 1990; Hattori and Saito, 1997). In the present study, ing eggs that they carried (Table 1). Females with uni- we assume gut pigment contents to be an indicator of in- dentified embryo/resting eggs due to a broken brood gestion rate due to invariant water temperature during the chamber or undeveloped embryo/resting egg (U) were not observation (see Results). The validity of gut content as used in the subsequent investigations. Measurements of an indicator of ingestion rate has been confirmed for body length were made to the nearest 10 µm using an copepods (Peterson et al., 1990), amphipod (Pakhomov and Perissinotto, 1996), euphausiids (Perissinotto and Pakhomov, 1996) and fish (Arrhenius and Hansson, 1994). For each gut pigment analysis, 20 to 30 were used. The materials in the guts of selected specimens were ex- amined with a scanning electron microscope (SEM).

3. Results The water column was not greatly stratified and the vertical difference in temperature was 0.6°C (Fig. 2). The chlorophyll a concentrations were higher than 5 mg mÐ3 in the upper 10 m, and the concentration at the near-bot- tom layer was lowest (Fig. 2). Podon leuckarti was dominant in cladoceran assem- blages and a small number of Evadne nordmanni were present. Sex ratios (females: males) of P. leuckarti were between 2.0 and 6.9 (Table 2). Parthenogenic females accounted for 36.0 to 52.4% of the total females. All of Fig. 1. Location of the station in Akkeshi Bay. these females carried one embryo. Gamogenic females

Table 1. Abbreviations for reproductive stages of females used in this study.

154 H. Saito and H. Hattori Table 2. Composition of sexes and reproductive stages of females. % female is the percentages of females in the total Podon leuckarti in the water column.

Sampling duration % female Percentages of the reproductive stages of female PE PA GE GA U Oct. 14 15:06Ð15:59 66.7 20.0 32.4 22.6 19.6 5.4 18:37Ð09:32 87.4 14.0 23.6 25.7 27.1 9.6 22:17Ð23:07 75.1 15.9 32.0 12.6 29.2 10.2 Oct. 15 02:23Ð03:08 83.4 29.0 19.0 19.5 20.3 12.3 06:26Ð07:20 72.6 20.8 20.8 22.7 22.2 13.6 10:29Ð11:15 69.2 23.0 19.9 24.3 23.0 9.9 14:34Ð15:16 70.1 17.6 18.4 22.6 28.2 13.3

Fig. 2. Vertical distribution of temperature (°C) and chloro- phyll a concentration (mg mÐ3).

accounted for between 39.8 and 52.8% of total females. One of these carried two resting eggs in its brood cham- ber, and all the others carried only one. During daytime, males aggregated in the near-bot- Fig. 3. Vertical distribution of Podon leuckarti by sex and by tom layer on 14 October and both in the surface and near- reproductive stage of females. Shaded graphs mean bottom layers on 15 October, and they dispersed into the nighttime distributions. For an explanation of reproductive water column at night (Fig. 3). The highest density at night stages, see Table 1. was observed between 2.5 and 5 m. Parthenogenic females with an early embryo (PE) and with an advanced embryo (PA), and gamogenic females with an early resting egg egg (GA) also aggregated in the near-bottom layer dur- (GE) showed a DVM pattern that was similar to that of ing daytime, their surface aggregation was less obvious the males. The highest densities of these reproductive than males and other reproductive stages of females. stages at night were observed in the 7.5 and 10 m layers, During daytime, 4.7% of GA were distributed in the layer which were deeper than the layers occupied by the males. shallower than 2.5 m. On the other hand, males and other Although gamogenic females with an advanced resting reproductive stages of females that distributed in this layer

Diel Vertical Migration of Podon leuckarti 155 Fig. 6. Diel change in gut pigment content (ng individ.Ð1) at Fig. 4. Diel change in the median depths of males and each each sampling layer. Open and closed bars mean daytime reproductive stage of females. Open and closed bars mean and nighttime, respectively. daytime and nighttime, respectively.

layers (Fig. 5). However, the differences in body length between depths were less than 4% of the mean. Gut pigment contents were highest at midday and lowest during the period between midnight to morning (Fig. 6). Gut pigment contents in the near-bottom layer were lower than that of P. leuckarti in shallower layers. Especially in midday and evening, they were 1/2 to 1/3 of those in the shallower layers. Centric diatoms domi- nated the gut contents for all the reproductive stages of females. Most diatoms in the gut were less than 10 µm in diameter. Pennate diatoms and silicoflagellates were mi- nor components. No zooplankton remains were identified in the gut contents.

4. Discussion During daytime, Podon leuckarti aggregated at the near-bottom layer, where the chlorophyll concentration Fig. 5. Vertical change in the body length of Podon leuckarti. was lowest in the water column, and dispersed into the ± Open and closed circles show the mean 1 S.E. (bars) at water column at night. The gut pigment content of the P. each sampling depth during daytime and nighttime, respec- leuckarti that aggregated at the near-bottom layer was tively. lower than that of P. leuckarti in the shallower layers. Although the near-bottom layer, where the light level was 0.27% of that at the surface (Saito and Hattori, 1997), were accounted for 14.4 to 26.6% of each group. Median was not sufficiently dark to prevent the visual predation depths (MDs) of GA during the day were deeper than those of fish (Marcy et al., 1998), reducing the possibility of of other reproductive stages and males (Fig. 4). After sun- being recognized by visual predator (Confer et al., 1978; set, GA migrated into the intermediate layers. The verti- O’Brien, 1979; Batty et al., 1990). A part of the popula- cal distribution and MDs of GA at night were similar to tion of P. leuckarti might chose to stay in the dimly lit those of the other stages of females. near-bottom layer during daytime to reduce the preda- The day-night difference in body length at each sam- tion risk, in spite of the lower food availability of this pling depth (Fig. 5) was insignificant (one-way ANOVA, layer. The near-bottom aggregation as a result of the trade p > 0.05). During nighttime, the P. leuckarti that were off between foraging and reducing mortality has also been distributed at the near-bottom layer (14 m) were signifi- reported in copepods (Saito and Hattori, 1997). cantly larger than those at the intermediate layers (2.5, 5, On the other hand, females, except for GA, and males 7.5 m). During the day, the animals that aggregated at the also aggregated at the surface during daytime on 15 Oc- surface were also larger than those in the intermediate tober. Surface aggregation during daytime is widely ob-

156 H. Saito and H. Hattori served both for marine (Bosch and Taylor, 1973; Onbé, phototaxis are thought to be advantageous for foraging 1974; Checkley et al., 1992) and freshwater cladocerans but vulnerable to visual predators (De Meester, 1993a), (Ratzlaff, 1974; Butorina, 1986; Johnsen and Jakobsen, and vice versa for cladocerans with negative phototaxis. 1987). Young (1978) reported that freshwater cladoceran However, no single genotype was most fit to various en- formed surface swarms in which “immi- vironments (Weider, 1985). Thus, the bimodal vertical nently sexual” females were dominant, and suggested that distribution, probably dependent on genetic diversity, may the swarms were for the successful fertilization. The sur- be advantageous for the risk dispersion of the population face layer might be suitable for mating because males need in the temporally and spatially variable environments of visual stimuli for efficient copulation (Goulden, 1966). Akkeshi Bay (Motoda et al., 1977). In the present study, however, the surface aggregation was Surface aggregation was not observed on 14 Octo- not composed only of animals seeking a mating partner. ber. Jakobsen and Johnsen (1988) showed that swarming Butorina (1986) also reported that the surface swarms of behavior did not occurred when food concentration within pediculus were formed by various reproduc- the swarm was limiting. In the present study, however, tive stages of females, including parthenogenic females, food concentrations at the surface were high and did not newly born, and gamogenic females with developed rest- vary much throughout the observation (4.2Ð5.8 mg chlo- ing eggs. In the present study, it is apparent that other rophyll a mÐ3). The formation of the surface aggregation factors than successful fertilization related to the surface of cladoceran was influenced by various environmental aggregation. factors, e.g., light, waves, current, etc. (Ratzlaff, 1974; Fish attack transparent prey distributed near the wa- Butorina, 1986). Different weather conditions between ter surface from outside of Snell’s window (a nadir angle two days (more windy and cloudy on 14 October than on of 49°) because the relative position of fish to prey in- 15 October) were possibly related to the presence and creases the contrast of the prey (Janssen, 1981). Prey out- absence of the surface aggregation. side of the fish’s Snell’s window reflects and refracts light Only gamogenic females with an advanced resting that pass through the prey’s own Snell’s window, and the egg (GA) did not aggregate at the surface during day- background of prey is dark because the water surface re- time. On the other hand, the nighttime median depths of flects light from the dark water. However, if a prey dis- GAs were similar to those of males and females of the tributes very near the water surface, the prey often van- other reproductive stages. SEM observations revealed that ishes in the Snell’s window because waves distort and GA fed on diatoms, as did the other reproductive stages. fragment the edge of the window. Thus, the near-surface These results show GA was not an inactive stage, just distribution of cladoceran would decrease the mortality awaiting the release of a resting egg. Mellors (1975) by visual predation. Although finer vertical distribution showed that a certain fish fed Daphnia with resting eggs than 2.5 m is unknown in the present study, it has been more selectively than females without resting eggs, and reported that freshwater cladoceran Polyphemus pedicu- the selectivity to females with resting egg increased with lus often aggregated at the top 5-cm of the water column irradiance. The fish’s selectivity was higher on females (Butorina, 1986). The strategy of near-surface distribu- with advanced resting eggs than those with early resting tion to decrease the predation risk is more effective for eggs. This suggests that the aggregation in the dimly lit less pigmented animals because animals with a pigmented near-bottom layer might be a more effective strategy for body are visible to fish both outside and inside the fish’s GAs to reduce the risk of visual predation compared to Snell’s window. the surface aggregation. Thus, P. leuckarti avoid the sur- Swarming behavior also reduce predation risk from face layer when they are carrying a large and dark-colored visual predators (e.g., Neill and Cullen, 1974). Unfortu- resting egg, the most vulnerable period for visual preda- nately, it is unknown whether P. leuckarti formed swarms tion. or not during the observation. However, surface swarms It has been observed that larger animals occur in of freshwater cladocerans to decrease visual predation deeper layers than do smaller animals during daytime to were observed (Jonsen and Jacobsen, 1987; Vetti Kvam reduce the chance of recognition by visual predators and Kleiven, 1995). It is suggested that disparate vertical (Duncan et al., 1993). In the present study, the mean body habitats of P. leuckarti during daytime, near-bottom layer length of specimens aggregated in the near-bottom layer and near-surface layer, were selected for the identical and in the surface layer was statistically larger than the purpose of reducing the risk of visual predation. mean body lengths in the intermediate layers (Fig. 5). The observed variety in the daytime habitat was pos- However, the differences were small and the ranges of sibly related with genetic differences in P. leuckarti. Even body lengths in the different layers greatly overlapped. in the same species, variations in phototaxis depending Such small differences in body length between depths on genetic differences were observed in cladocerans (De have negligible influence on the risk of visual predation Meester, 1993a, b). In general, cladocerans with positive (O’Brien, 1979, his figure 1). Zaret and Kerfoot (1975)

Diel Vertical Migration of Podon leuckarti 157 showed that visibility of prey is a more important selec- tion of an estuarine cladoceran, Podon polyphemoides, in tive factor for fish than prey size. Therefore, the size may the Chesapeake Bay. Mar. Biol., 19, 172Ð181. not be an important factor in the vertical distribution of Brooks, J. L. and S. I. Dodson (1965): Predation, body size, P. leuckarti. and composition of plankton. Science, 150, 28Ð35. The diel feeding rhythm (DFR), like DVM, is one of Bryan, B. B. (1979): The diurnal reproductive cycle of Evadne tergestina Claus (, Podonidae) in Chesapeake Bay, the most common behaviors of zooplankton, and is U.S.A. Crustaceana, 36, 229Ð236. thought to be a behavior for decreasing visual predation. Buskey, E. J. (1994): Factors affecting feeding selectivity of In the present study, gut pigment contents increased in visual predators on the copepod Acartia tonsa: locomotion, the afternoon and decreased at midnight (Fig. 6). The in- visibility and escape responses. Hydrobiol., 292/293, 447Ð crease in ingestion rate at midday is inconsistent with the 453. predation avoidance hypothesis. Chisholm and Stross Buskey, E. J., C. Coulter and S. Strom (1993): Locomotory (1975) showed a similar pattern of DFR for arctic Daphnia patterns of microzooplankton: Potential effects on food se- which responded to the diel temperature cycle. In the lectivity of larval fish. Bull. Mar. Sci., 53, 29Ð43. present study, however, the diel temperature change was Butorina, L. G. (1986): On the problem of aggregations of small. For cladocerans, although the usual pattern of DFR planktonic Polyphemus pediculus (L.), was observed (Haney, 1985; Kleppel et al., 1988; Uye Cladocera. Arch. Hydrobiol., 105, 355Ð386. Checkley, D. M., Jr., S. Uye, M. J. Dagg, M. M. Mullin, M. and Onbé, 1993), reverse DFR (Bainbridge, 1958; Omori, T. Onbé and M.-Y. Zhu (1992): Diel variation of Starkweather, 1978), phase-shifted DFR (Rodriguez et al., the zooplankton and its environmental at neritic stations in 1991), and continuous feeding (Uye and Onbé, 1993) were the Inland Sea of Japan and the north-west Gulf of Mexico. also observed. Although both the swimming and gut con- J. Plankton Res., 14, 1Ð40. tents associated with feeding activity increase the risk of Chisholm, S. W. and R. G. Stross (1975): Environmental and visual predation, the increase in the visibility due to gut intrinsic control of filtering and feeding rates in Arctic contents may be less important because of the larger Daphnia. J. Fish. Res. Board Can., 32, 219Ð226. pigmented eyes of P. leuckarti than their gut. DFR of Confer, J. L., G. L. Howick, M. H. Corzette, S. L. Kramer, S. cladoceran may be controlled not only by the avoidance Fitzgibbon and R. Landesberg (1978): Visual predation by of visual predation but also by other factors. planktivores. Oikos, 31, 27Ð37. De Meester, L. (1993a): The vertical distribution of Daphnia magna genotypes selected for different phototactic behav- Acknowledgements iour: Outdoor experiments. Arch. Hydrobiol. Beih. Ergebn. We thank Mr. N. Muroya and the captain and crew Limnol., 39, 137Ð155. of the F.R.V. Tankai-Maru for their field assistance, and De Meester, L. (1993b): Genotype, fish-mediated chemicals, anonymous reviewers for their constructive criticisms. Dr. and phototactic behavior in Daphnia magna. Ecology, 74, J. Raymond kindly corrected the English and improved 1467Ð1474. the manuscript. This study was supported partly by the Duncan, A., C. Guisande and W. Lampert (1993): Further trade- Comprehensive Program of Research for Agro-Ecologi- offs in Daphnia vertical migration strategies. Arch. cal System and Optimum Control (BCP-99-IV-A-6). Hydrobiol. Beih. Ergebn. Limnol., 39, 99Ð108. Hokkaido National Fisheries Research Institute Contri- Durbin, A., E. G. Durbin and E. Wlodarczyk (1990): Diel feed- bution B-646. ing behavior in the marine copepod Acartia tonsa in rela- tion to food availability. Mar. Ecol. Prog. Ser., 68, 23Ð45. Ellis, S. G. and L. F. Small (1989): Comparison of gut-evacua- References tion rates of feeding and non-feeding Calanus marshallae. Arrhenius, F. and S. Hansson (1994): In situ food consumption Mar. Biol., 103, 175Ð181. by young-of-the-year Baltic Sea herring Clupea harengus: Frost, B. W. and S. M. Bollens (1992): Variability of diel verti- a test of predictions from a bioenergetics model. Mar. Ecol. cal migration in the marine planktonic copepod Prog. Ser., 110, 145Ð149. Pseudocalanus newmani in relation to its predators. Can. Bainbridge, V. (1958): Some observations on Evadne nordmanni J. Fish. Aquat. Sci., 49, 1137Ð1141. Lovén. J. Mar. Biol. Ass.U.K., 37, 349Ð370. Fukuchi, M., A. Tanimura and T. Hoshiai (1979): NIPR-I, a Batty, R. S., J. H. S. Blaxter and J. M. Richard (1990): Light new plankton sampler under sea ice. Bull. Plankton Soc. intensity and the feeding behavior of herring, Clupea Japan, 26, 104Ð109. harengus. Mar. Biol., 107, 383Ð388. Gliwicz, Z. M. (1986): Predation and the evolution of vertical Bollens, S. M. and B. W. Frost (1989): Predator-induced diel migration in zooplankton. Nature, 320, 746Ð748. vertical migration in a planktonic copepod. J. Plankton Res., Gliwicz, Z. M., A. Ghilarov and J. Pijanowska (1981): Food 11, 1047Ð1065. and predation as major factors limiting two natural Bollens, S. M. and D. E. Stearns (1992): Predator-induced populations of Daphnia cucullata Sars. Hydrobiol., 80, 205Ð changes in the diel feeding cycle of a planktonic copepod. 218. J. Exp. Mar. Biol. Ecol., 156, 179Ð186. Goulden, C. E. (1966): Co-occurrence of moinid Cladocera and Bosch, H. F. and W. R. Taylor (1973): Diurnal vertical migra- possible isolating mechanisms. Verh. int. ver. Limnol., 16,

158 H. Saito and H. Hattori 1669Ð1772. whether schooling by their prey affects hunting behavior of Grant, J. W. G. and I. A. E. Bayly (1981): Predation induction cephalopod and fish predators. J. Zool., Lond., 172, 549Ð of crests in morphs of the Daphnia carinata King complex. 569. Limnol. Oceanogr., 26, 201Ð218. O’Brien, W. J. (1975): Some aspects of the limnology of the Haney, J. F. (1985): Regulation of cladoceran filtering rates in ponds and lakes of the Noatak drainage basin, Alaska. Verh. nature by body size, food concentration, and diel feeding Int. Ver. Limnol., 19, 472Ð479. patterns. Limnol. Oceanogr., 30, 397Ð411. O’Brien, W. J. (1979): The predator-prey interaction of Hattori, H. and H. Saito (1997): Diel change in vertical distri- planktivorous fish and zooplankton. Am. Sci., 67, 572Ð581. bution and feeding activity of copepods in ice-covered Reso- O’Brien, W. J., N. A. Slade and G. L. Vinyard (1976): Appar- lute Passage, Canadian Arctic, in spring 1992. J. Mar. Sys., ent size as the determinant of prey selection by bluegill sun- 11, 205Ð219. fish (Lepomis macrochirus). Ecology, 57, 1304Ð1310. Havel, J. E. and S. I. Dodson (1984): Chaoborus predation on Ohman, M. D., B. W. Frost and E. B. Cohen (1983): Reverse typical and spined morphs of Daphnia pulex: Behavioral diel vertical migration: An escape from invertebrate preda- observations. Limnol. Oceanogr., 29, 487Ð494. tors. Science, 220, 1404Ð1407. Hays, G. C., C. A. Proctor, A. W. G. John and A. J. Warner Onbé, T. (1974): Studies on the ecology of marine cladocerans. (1994): Interspecific differences in the diel vertical migra- J. Fac. Fish. Anim. Husb., Hiroshima Univ., 13, 88Ð179 (in tion of marine copepods: The implications of size, color, Japanese). and morphology. Limnol. Oceanogr., 39, 1621Ð1629. Pakhomov, E. A. and R. Perissinotto (1996): Trophodynamics Irigoien, X. (1998): Gut clearance rate constant, temperature of the hyperiid amphipod Themisto gaudichaudi in the South and initial gut contents: a review. J. Plankton Res., 20, 997Ð Georgia region during late austral summer. Mar. Ecol. Prog. 1003. Ser., 134, 91Ð100. Jakobsen, P. J. and G. H. Johnsen (1988): The influence of food Perissinotto, R. and E. A. Pakhomov (1996): Gut evacuation limitation on swarming behaviour in the waterflea Bosmina rates and pigment destruction in the Antarctic krill longispina. Anim. Behav., 36, 991Ð995. Euphausia superba. Mar. Biol., 125, 47Ð54. Janssen, J. (1981): Searching for zooplankton just outside Peterson, W., S. Painting and R. Barlow (1990): Feeding rates Snell’s window. Limnol. Oceanogr., 26, 1168Ð1171. of Calanoides carinatus: a comparison of five methods in- Johnsen, G. H. and P. J. Jakobsen (1987): The effect of food cluding evaluation of the gut fluorescence method. Mar. limitation on vertical migration in Daphnia longispina. Ecol. Prog. Ser., 63, 85Ð92. Limnol. Oceanogr., 32, 873Ð880. Ratzlaff, W. (1974): Swarming in Moina affinis. Limnol. Kleppel, G. S., D. Frazel, R. E. Pieper and D. V. Holliday (1988): Oceanogr., 19, 993Ð995. Natural diets of zooplankton off southern California. Mar. Rodriguez, V., F. Echevarria and B. Bautista (1991): In situ diel Ecol. Prog. Ser., 49, 231Ð241. variation in gut pigment contents of Ceriodaphnia sp. in Lampert, W. (1993): Ultimate causes of diel vertical migration stratification and destratification periods. J. Plankton Res., of zooplankton: New evidence for the predator-avoidance 13, 187Ð196. hypothesis. Arch. Hydrobiol. Beih. Ergebn. Limnol., 39, 79Ð Saito, H. and H. Hattori (1997): Diel vertical migration and 88. feeding rhythm of copepods in a shallow, food-abundant Loose, C. J., E. von Elert and P. Dawidowicz (1993): Chemi- embayment. Plankton Biol. Ecol., 44, 13Ð29. cally-induced diel vertical migration in Daphnia: a new Saito, H. and S. Taguchi (1996): Diel feeding behavior of neritic bioassay for kairomones exuded by fish. Arch. Hydrobiol., copepods during spring and fall blooms in Akkeshi Bay, 126, 329Ð337. eastern coast of Hokkaido, Japan. Mar. Biol., 125, 97Ð107. Mackas, D. and R. Bohrer (1976): Fluorescence analysis of Starkweather, P. L. (1978): Diel variation in feeding behavior zooplankton gut contents and an investigation of diel feed- of Daphnia pulex. Influences of food density and nutritional ing patterns. J. Exp. Mar. Biol. Ecol., 25, 77Ð85. history on madibular activity. Limnol. Oceanogr., 23, 307Ð Marcy, W. K., S. J. Sutherland and E. G. Durbin (1998): Ef- 317. fects of zooplankton size and concentration and light inten- Tiselius, P. and P. R. Jonsson (1997): Effects of copepod forag- sity on the feeding behavior of Atlantic mackerel Scomber ing behavior on predation risk: An experimental study of scombrus. Mar. Ecol. Prog. Ser., 172, 89Ð100. the predatory copepod Pareuchaeta norvegica feeding on Mellors, W. K. (1975): Selective predation of ephippial Daphnia Acartia clausi and A. tonsa (Copepoda). Limnol. Oceanogr., and the resistance of ephippial eggs to digestion. Ecology, 42, 164Ð170. 56, 974Ð980. Tsuda, A., H. Saito and T. Hirose (1998): Effect of gut content Motoda, S., T. Kawamura and S. Nishizawa (1977): Akkeshi on the vulnerability of copepods to visual predation. Limnol. Bay. p. 223Ð265. In Productivity of Biocenoses in Coastal Oceanogr. 43, 1944Ð1947. Regions of Japan, ed. by K. Hogetsu, M. Hatanaka, T. Tucker, R. P. and S. P. Woolpy (1984): The effect of partheno- Hanaoka and T. Kawamura, University of Tokyo Press, genic eggs in Daphnia magna on prey location by the Tokyo. bluegill sunfish (Lepomis macrochirus). Hydrobiol., 109, Neil, W. E. (1990): Induced vertical migration in copepods as a 215Ð217. defense against invertebrate predation. Nature, 345, 524Ð Uye, S. and T. Onbé (1993): Diel variation in gut pigments of 526. marine cladocerans in the Inland Sea of Japan. Bull. Plank- Neill, S. R. St. J. and J. M. Cullen (1974): Experiments on ton Soc. Japan, 40, 67Ð69.

Diel Vertical Migration of Podon leuckarti 159 Vetti Kvam, O. and O. T. Kleiven (1995): Diel horizontal mi- cyclic parthenogen. Freshw. Biol., 8, 279Ð281. gration and swarm formation in Daphnia in response to Zaret, T. M. and W. C. Kerfoot (1975): Fish predation on Chaoborus. Hydrobiol., 307, 177Ð184. Bosmina longirostris: Body-size selection versus visibility Weider, L. J. (1985): Spatial and temporal genetic heterogene- selection. Ecology, 56, 232Ð237. ity in a natural Daphnia population. J. Plankton Res., 7, Zaret, T. M. and J. S. Suffern (1976): Vertical migration in 101Ð123. zooplankton as a predator avoidance mechanism. Limnol. Young, J. P. W. (1978): Sexual swarms in Daphnia magna, a Oceanogr., 21, 804Ð813.

160 H. Saito and H. Hattori