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

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Diel Vertical Migration of the Marine Cladoceran Podon Leuckarti: Variations with Reproductive Stage Journal of Oceanography, Vol. 56, pp. 153 to 160. 2000 Diel Vertical Migration of the Marine Cladoceran Podon 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 Evadne 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 14–15 October, 1992 (Fig. 1). Bottom depth was 15– 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 animals 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 m–3 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 15:06–15:59 66.7 20.0 32.4 22.6 19.6 5.4 18:37–09:32 87.4 14.0 23.6 25.7 27.1 9.6 22:17–23:07 75.1 15.9 32.0 12.6 29.2 10.2 Oct. 15 02:23–03:08 83.4 29.0 19.0 19.5 20.3 12.3 06:26–07:20 72.6 20.8 20.8 22.7 22.2 13.6 10:29–11:15 69.2 23.0 19.9 24.3 23.0 9.9 14:34–15:16 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 m–3). 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.–1) at Fig. 4. Diel change in the median depths of males and each each sampling layer.
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