Diel Changes in Vertical Overlap Between Cyclops Strenuus Ž/Copepoda; Cyclopoida and Its Prey in Oligotrophic Lake Toya, Hokkaido, Japan

Journal of Marine Systems 15Ž. 1998 139±148

Diel changes in vertical overlap between Cyclops strenuus ž/Copepoda; Cyclopoida and its prey in oligotrophic Lake Toya, Hokkaido, Japan

Wataru Makino ), Syuhei Ban Biological Oceanography, Faculty of Fisheries, Hokkaido UniÕersity, 3-1-1 Minato-machi, Hakodate, Hokkaido 041, Japan Revised 30 March 1997; accepted 26 September 1997

Abstract

The vertical distribution of Cyclops strenuus and its prey, and the gut contents of C. strenuus were investigated at 3 h intervals over 24 h periods in the pelagic area of oligotrophic Lake Toya in May, August and October 1992. C. strenuus showed slight diel vertical migrationŽ. DVM in May, but did not migrate and was always distributed below 15 m in August and October, the thermally stratified period. This suggests that the DVM is strongly influenced by the development of the thermocline, which the copepod may not be able to cross. Gut content analyses revealed that in Lake Toya it is omnivorous, and that the dominant prey are cladocerans and Filinia longiseta. The number of prey remains in the gut varied with time, and the diel changes did not follow changes in prey density that take the vertical overlap between predator and prey into account. We argue that very low prey density associated with the oligotrophic nature of the lake would mask the relationship between prey density and the number of prey in the gut of the predator. q 1998 Elsevier Science B.V. All rights reserved.

Keywords: Copepoda; cyclopoid copepoda; diel vertical migration; overlap; feeding; gut content analysis; oligotrophic lakes

1. Introduction predation rates of cyclopoids on its prey generally depend on prey densityŽ e.g. Brandl and Fernando, Based on gut content analysesŽ. e.g. Fryer, 1957 1978; Zankai, 1984; Williamson, 1986. although and feeding experimentsŽ e.g. Brandl and Fernando, Â prey morphology and escape responses, and the 1978. , cyclopoid copepods, especially adult females hunger level of cyclopoids, may also play an impor- Ž.Williamson and Magnien, 1982 are known to be tant roleŽ. Williamson, 1983, 1986 . Hence, the im- predatory, and planktologists consider that cy- pact of cyclopoids on their prey communities will clopoids may have a substantial impact on the sur- depend largely on the spatial and temporal overlap vivorship of their prey, such as cladocerans and between themŽ. Williamson and Magnien, 1982 . rotifers, in natural lakesŽ Brandl and Fernando, 1978, Diel vertical migrationŽ. DVM of zooplankton is 1979; Karabin, 1978. . Many studies have shown that a characteristic feature of both herbivorous and car- nivorous species. It is known that the larger carnivo- ) Corresponding author. Tel.: q81-138-405543. Fax: q81- rous elements of the zooplankton generally perform 138-405542. E-mail: [email protected] a much more pronounced DVM than do smaller

0924-7963r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved. PII S0924-7963Ž. 97 00073-0 140 W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148 ones, such as rotifersŽ. Hutchinson, 1967 . The differ- except for adult males which feed very littleŽ Wil- ences in the extent of DVM between predators and liamson and Magnien, 1982. . Among the zooplank- their prey can place the predators in food environ- ton, we treated cladocerans and rotifers as potential ments that differ in both quantity and quality over a `prey'. For the purpose of defining vertical distribu- 24 h periodŽ. Williamson and Magnien, 1982 . How- tion, abundances for each species were calculated as ever, few studies deal with vertical distribution of the number of individuals per cubic meter in each both cyclopoids and their prey together with gut depth stratum. The absolute abundance for each content analysis of the cyclopoids over 24 h periods. species was standardized by converting to the per- Cyclops strenuus Ž.Fischer is a cyclopoid copepod centage of the total population of that species occur- widely distributed in a broad range of freshwater ring in each depth stratum. habitats. In Japan it often inhabits large, oligotrophic The vertical overlap Ž.Oi between late cope- lakes and is rarely found in shallow, eutrophic habi- podites and prey animals i was determined using the tatsŽ Mizuno and Miura, 1984; Mizuno and Taka- equation given in Williamson et al.Ž. 1989 and hashi, 1991. . In the oligotrophic Lake Toya, it is the Williamson and StoeckelŽ. 1990 , only copepod in the plankton, and is found throughout the yearŽ. authors' unpubl. data . In this study, we mmm s P r P investigated the vertical distribution of both C. OizizzizÝÝÝŽ.N nm Ž.Ž.N n strenuus and its prey over 24 h periods, and exam- ½5½5zs1 zs1 zs1 ined the diel changes in vertical overlap between them. Gut contents of C. strenuus were also ana- where N and n are the predator and prey density, lyzed over 24 h periods in order to elucidate the respectively, z is a given depth stratum, and m is the relationship between the extent of vertical overlap number of depth strata sampled. Values of less than and foraging behaviour. one reflect a negatively correlated distribution between the predator and prey populations, and the theoretical lower limit representing no overlap is zero. Values greater than one represent a positively 2. Methods correlated distribution between the predator and prey populations, and the theoretical upper limit is defined We conducted three observations during 27±28 by the number of depth strata sampledŽ Williamson May, 5±6 August, and 21±22 October 1992 at a and Stoeckel, 1990. . station in Lake Toya where the lake is 170 m deep. The different DVM patterns of C. strenuus and its Details of the site and the lake are given by Makino prey place it in areas of different prey availability, in et al.Ž. 1996 . terms of numbers. In order to know more accurately During each observation period, zooplankton the density available for C. strenuus, taking into samples were collected at 3 h intervals over 24 h consideration the overlap between the copepod and P periods with vertical discrete net hauls using a clos- its prey, the weighted densityŽ. WDii , n O iof prey ing netŽ. mouth opening, 20 cm; mesh size, 0.1 mm . species i was calculated. Depth ranges sampled included 0±5, 5±10, 10±15, For gut content analyses, 25±30 individuals of C. 15±20, 20±25, 25±30, 30±40, 40±50, 50±60, 60±80 strenuus Žmostly adult females and a few of C5 and 80±100 m. Collected zooplankton was anaes- stage. were sorted at each sampling time from the thetized with carbonated water and fixed in 5% successive strata in which more than 90% of C. formaldehyde solution with sugar addedŽ Haney and strenuus from the whole population throughout the Hall, 1973. . water column were distributed, and put into an Animals were counted under a dissecting micro- ethanol±glycerol mixtureŽ 10% glycerol and 90% scope. C. strenuus was grouped into three develop- ethanol, see Dussart and Defaye, 1995. . The animals mental stages: nauplii, early copepoditeŽ. C1±3 and were left for a few hours until the alcohol had late copepodite stagesŽ. C4±6, except adult male . evaporated, then transferred to a 30% glycerol solu- We regarded the late copepodite stages as predators, tion. The entire gut tube was dissected from each W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148 141 animal and transferred to a small drop of 30% sampling time to 25 and 40% of the WD at the prior glycerol solution on a slideglass. The isolated gut sampling time to get a modified WD that was more tube was covered with a coverglassŽ. 5=5 mm , and representative of gut passage timeŽ 3±4 and 4±5 h, a few drop of 5% sodium hypochlorite solution were respectively. . added to the edge of the coverglass in order to dissolve the organic matter and reveal any rotifer trophiŽ. Williamson, 1984; Schoeneck et al., 1990 . 3. Results The gut contents were observed under a microscope with phase contrast illumination at 600= magnifica- The mean abundance of C. strenuus and its poten- tion. All rotifer trophi were identified to species and tial prey during each observation period is summa- counted. Cladoceran and copepod remains were rized in Table 1. The abundance of late copepodite scored as one prey item unless evidence of more stages of C. strenuus was low in May, but increased than one was found in a single gutŽ Schoeneck et al., one order of magnitude in August, and remained at 1990. . Then we estimated the average number of this level in October. animals eaten per copepod Ž.Pi for prey species i at Two cladocerans, Daphnia longispina and each sampling time. Bosmina coregoni occurred in the lake. In May and We examined the relationship between P and August D. longispina was more abundant than B. WD because predation rates of cyclopoids are den- coregoni. Although the abundance of large D. sity dependent, as described above. If gut passage longispina Ž.)1 mm body length without tail spine time is less than our sampling intervals of 3 h, we exceeded small Ž.-1 mm individuals in August, we can examine the relationship between WD and P at did not treat the large individuals as potential prey every sampling time. If passage time is longer than 3 since it is widely accepted that the large-size prey h, however, we must modify the WD with the one at are more difficult to capture because of escape re- a prior sampling time. WilliamsonŽ. 1984 showed sponses and handling problems. Balseiro and Vega that more than 80% of trophi of Brachionus calyci- Ž.1994 showed that Daphnia middendorffiana with a florus had passed out of the midgut of Mesocyclops body length greater than 1.1 mm frequently escaped edax after 3±4 h. The best estimate of his study for from the predatory copepod Parabroteas sarsi.We the time that most trophi spent in the gut is 3±5 h. lumped the small D. longispina and B. coregoni as Thus, we added 75 and 60% of the WD at a given one category, `cladocerans', in order to summarize

Table 1 Average zooplankton abundanceŽ ind. my3 .Ž. and standard deviation SD at a fixed station in Lake Toya during each observation period Species 27±28 May 5±6 August 21±22 October average SD average SD average SD Predator Cyclops strenuus C4±6Ž. except C6 male 28.4 6.8 259.8 48.6 221.4 56.5

Prey Cladocera Daphnia longispina Ž.)1 mm 185.3 142.9 263.4 90.5 137.8 44.1 Daphnia longispina Ž.-1 mm 479.9 388.0 154.1 63.6 239.2 62.8 Bosmina coregoni 110.9 61.7 169.9 55.4 566.8 143.4 Rotifera Filinia longiseta 14.5 4.7 21.5 13.2 121.7 45.1 Asplanchna herricki 0 440.6 324.5 67.0 40.5 Polyarthra Õulgaris 0 96.1 131.8 65.1 20.9 Conochilus unicornis 0 0 3807.4 1075.0 142 W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148 the results of gut content analyses, because often we quency, 50%. . Its abundance decreased again in could not identify cladoceran remains to species, as October. Conochilus unicornis did not occur in May described below. The abundance of the potential and August, but became the most numerous prey prey cladocerans was high in May and October, but species in October. Polyarthra Õulgaris occurred in its relative frequency decreased from MayŽ. 98% to August and October, and its abundance was low. OctoberŽ. 17% due to an increase in the number of Late copepodites of C. strenuus performed a rotifers. Filinia longiseta was scarce in May and slight nocturnal DVM in MayŽ. Fig. 1A . They began August and increased about 6-fold in October, though to ascend just after sunsetŽ. 20:15 , and some individ- its relative frequency was constantŽ. ca. 2.5% . As- uals reached to the surface and stayed until early planchna herricki did not occur in May but became morningŽ. 5:00 , although more than 70% of the the most numerous prey in AugustŽ relative fre- population was below 10 m even at night. The part

Fig. 1. Diel changes in vertical distribution of late copepoditesŽ. C4, C5 and C6 female of Cyclops strenuus over 24 h sampling periods, and vertical profiles of water temperature on 27±28 MayŽ. A , 5±6 August Ž. B , and 21±22 October 1992 Ž. C at a fixed station in Lake Toya. Scale of each histogram is shown in far right for each time period. Horizontal bars represent the night. W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148 143 of the C. strenuus population above 5 m seemed to begin to descend before dawn, between 23:00 and 2:00. The entire population was dispersed between 10 and 60 m depth during the daylight period. In August and October, however, C. strenuus showed no evidence of migrationŽ. Fig. 1B, C . It was broadly distributed between 15 and 50 m depth in August, while more than 75% of the population was restricted between 15 and 25 m in October. These vertical distributions roughly corresponded to the vertical profiles of water temperature in August and October. C. strenuus tended to avoid the warm epilimnion. In May, the vertical overlaps Ž.O for both cladocerans and F. longiseta varied from 1 to 2, but their diel changes differedŽ. Fig. 2A . O for cladocerans had two maxima at 23:00 and 11:00 when O for F. longiseta was at its minimum, while a peak of O for F. longiseta was at 5:00 when O for cladocerans reached its minimum. This discrepancy in diel changes of O was associated with their vertical distribution pattern. Cladocerans showed nocturnal DVM but F. longiseta did not migrate and stayed continuously in the 20±60 m strata. Since the timing of DVM differed between cladocerans and C. strenuus, the O between them was not constant. In August, O for A. herricki, P. Õulgaris and F. longiseta were almost constant at -0.2, ca. 1 and about 2, respectively, over a 24 h periodŽ. Fig. 2B . The differences of O for rotifers were associated with their unique distribution patterns. O for A. herricki, the most numerous prey in August, was very low because it was continuously restricted above 20 m in the warm epilimnion. F. longiseta had a Fig. 2. Diel changes in overlap value for each prey over 24 h sampling periods on 27±28 MayŽ. A , 5±6 August Ž. B , and 21±22 high O value because it was distributed in the same October 1992Ž. C at a fixed station in Lake Toya. Horizontal bars strata as C. strenuus 24 h a day while for P. Õulgaris represent the night. O value was around 1 because this species was almost homogeneously distributed throughout the water column. Contrary to the rotifers, O for clado- creased. As in August, O for F. longiseta was cerans was not constant because these animals per- always high but fluctuated from 2 to 4. F. longiseta formed nocturnal DVM. was distributed in the same strata as C. strenuus 24 In October, O for F. longiseta was continuously h a day as in August, but both animals inhabited a high, more than 2, and O for A. herricki and P. narrower range than in August. The small differences Õulgaris was continuously low, less than 1 and in their mode of distribution caused the fluctuation around 1, respectively, as shown in AugustŽ Fig. of O for F. longiseta in October. 2C. . O for cladocerans and C. unicornis, the most More than 700 C. strenuus were dissected, and numerous prey in October, decreased from 14:00 to very few guts were emptyŽ. Table 2 . Animal remains 17:00, kept a low level until 11:00 and then in- consisted mainly of cladocerans in May, cladocerans 144 W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148

Table 2 Total number of each food item found in the gut of C. strenuus. Relative frequency of individuals that contained brown-coloured mush, individuals that had empty guts, and the number of C. strenuus examined are also shown Months Animals Empty guts Animals with stomach Food items examinedŽ. % containing brown-coloured mush CS CL FL AH PV CU UAR DIA DIN POL Ž.No. Ž. % NP COP May 216 3 91 0 2 20 2 0 0 0 10 2685 227 277 August 267 14 61 2 0 18 13 0 0 0 14 1856 210 13 October 225 9 90 1 0 9 13 2 0 7 27 355 35 9

CSsC. strenuus;NPsnauplii; COPscopepodites; CLscladocerans; FLsF. longiseta;AHsA. herricki;PVsP. Õulgaris;CUsC. unicornis; UARsunidentifiable animal remain; DIAsdiatoms; DINsdinoflagellates; POLspollen grains.

Fig. 3. Diel changes in WDŽ.Ž. lines and symbols and P histograms of cladocerans and F. longiseta over 24 h sampling periods on 27±28 MayŽ. A , 5±6 August Ž. B , and 21±22 October 1992 Ž. C . Asterisks denote no occurrence in the gut. Horizontal bars represent the night. W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148 145 and F. longiseta in August, and cladocerans, F. cycle, nor were they parallel to the changes in their longiseta and C. unicornis in October. Some of the WD, though we found a just significant positive cladoceran remains were identified as B. coregoni relationship between WD and P for cladocerans in by the morphology of the second antennae or postab- OctoberŽ. Table 3 . The maximum P for both prey dominal claw, but other body partsŽ e.g., feeding categories was mostly observed when the WD was appendages. could not be identified with certainty. relatively small. The remains of F. longiseta consisted of trophi, its There was no relationship between modified WD, entire three setae, and sometimes both, but no eggs considering a gut passage time longer than 3 h, and were found. Only trophi of C. unicornis was found. P for either of the two prey categories, even in the C. strenuus occasionally preyed on its own juveniles case of cladocerans in October for which we found a and on A. herricki, but P. Õulgaris was never found positive relationship between crude WD and P ŽTa- in the guts. Additionally, diatoms, dinoflagellates ble 3. . Therefore, we could not find any valid rela- and pollen grains were found in the gut. The large tionship between these two values assuming longer number of diatoms found may be associated with gut passage times than our sampling interval. their higher densityŽ 3±4 orders of magnitude, Y. Takebe, unpubl.. than zooplankton. In the three periods between 60 and 90% of C. strenuus examined contained indeterminate, brown-coloured mush which 4. Discussion may have been derived from soft-bodied organisms Ž.Fryer, 1957 , or may have been mineral matter FryerŽ. 1957 studied the gut content of C. strenuus Ž.TothÂ et al., 1987 . and C. strenuus abyssorum Ž.sC. abyssorum , and Diel changes in both P and WD were traced for determined Cyclops to be a carnivore. On the other two dominant prey species, cladocerans and F. hand, ElbournŽ. 1966 showed that several kinds of longiseta Ž.Fig. 3 . The remains of cladocerans andror phytoplanktonŽ including diatoms and dinoflagel- F. longiseta in the gut were found at almost all lates. , ciliates and soft parts of animals were found sampling times, and P for both prey categories in the gut of C. strenuus but no recognizable animal varied considerably with time. Diel changes of P for remains in the form of skeletal parts were found, and both prey were not associated with the light±dark concluded that C. strenuus was basically a herbivore that feeds on a variety of phytoplankton with an animal supplement. GhilarovŽ. 1976 obtained an in- Table 3 termediate result that C. strenuus feeds on crus- Summary of regression analyses between P and WD for two tacean zooplankton and rotifers, as well as phyto- dominant prey categories planktonŽ. mainly diatoms and dinoflagellates . Our Prey animals Month Gut passage Slope rp2 timeŽ. h Ž=10y3 . results were in good agreement with Ghilarov's re- sultsŽ. Ghilarov, 1976 . C. strenuus from Lake Toya - y Cladocerans May 3 0.022 0.115 0.372 Ž. 3±4 y0.019 0.062 0.551 fed both zooplankton crustacean and rotifer and 4±5 y0.016 0.039 0.639 phytoplanktonŽ. diatoms and dinoflagellates , suggest- August -3 y0.110 0.108 0.388 ing that C. strenuus is an omnivore, even in adult 3±4 y0.072 0.053 0.583 females. One can speculate that the phytoplankton in 4±5 y0.076 0.055 0.577 the gut of the predator came from the gut of ingested October -3 0.071 0.482 -0.05 3±4 0.086 0.445 0.071 prey. In this study, however, that was not necessarily 4±5 0.093 0.369 0.110 the case because we often found the gut that con- Filinia longiseta August -3 y0.991 0.257 0.164 tained only phytoplankton. Evidence has been accu- 3±4 y0.990 0.208 0.257 mulating that omnivory is a common phenomenon in 4±5 y1.022 0.229 0.231 planktonic cyclopoidsŽ e.g. Karabin, 1978; Toth and - y Â October 3 0.146 0.252 0.168 . 3±4 y0.207 0.239 0.218 Zankai,Â 1985; Adrian and Frost, 1992, 1993 . As 4±5 y0.207 0.196 0.273 zooplankton communities are often confronted with limited food resources, omnivory appears to be an 146 W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148 advantageous feeding strategyŽ Adrian and Frost, prefer larger-size preyŽ. Brooks and Dodson, 1965 , 1992.Ž. . Adrian and Frost 1993 showed that the and the DVM of the cladocerans in Lake Toya can survival and reproduction of three cyclopoids, be considered to be predator-avoidance behaviour Tropocyclops prasinus mexicanus, Diacyclops Ž.Makino et al., 1996 . This suggests that diel changes thomasi and Mesocyclops edax, were substantially in vertical overlap between C. strenuus and clado- enhanced by the addition of invertebrate prey to an cerans may depend indirectly on vertebrate preda- algal diet. tors. In this study, C. strenuus performed a slight In this study, cladocerans and F. longiseta were DVM in May when the thermocline had not yet ingested by C. strenuus in similar amounts in Au- developed, whereas it did not migrate vertically in gust and October although WD of the cladocerans August and October, the thermally stratified period. was almost an order of magnitude higher than that of These results suggest that the DVM of C. strenuus is F. longiseta. This selective feeding on F. longiseta strongly influenced by the development of the ther- may be attributed to the smaller size, more vulnera- mocline, which it may not be able to cross. Inhibi- ble body wall without theca, and less effective es- tion of DVM by increasing surface water tempera- cape ability of rotifers than of cladocerans. Although ture has often been observedŽ. e.g. Tappa, 1965 . On Filinia, Hexarthra and Polyarthra are known to the other hand, evidence has been accumulating on exhibit a jump escape response using their movable the role of predation as a major driving force of appendagesŽ Williamson, 1983; Stemberger and DVMŽ. see Lampert, 1993 . Two planktivorous fishes, Gilbert, 1987. , there are some controversial studies kokanee Ž.ŽOncorhynchus nerka and pond smelt Hy- on the escape ability of Filinia. For example, Roche pomesus transpacificus nipponensis., inhabit Lake Ž.1987 found that F. terminalis exhibited no jump Toya. The most effective predator-avoidance be- escape response and simply raised its two anterior haviour may be for C. strenuus to stay in deep layers spines above its corona in response to the predator during the thermally stratified period. In addition, Acanthocyclops robustus. Stemberger and Gilbert not only a relatively dense prey population ŽF. Ž.1987 mention that little is known about the me- longiseta, major diet of the copepod. but also a chanics and effectiveness of the escape responses of relatively dense chlorophyll a concentrationŽ see Filinia. Fig. 2 in Makino et al., 1996. was observed within We could not find a positive relationship between the living-space of C. strenuus, even in the daylight WD and P, except for cladocerans in October. A period. We consider that the vertical distribution of possible explanation for this lack would be irregular C. strenuus may be basically determined by the changes in the gut passage time over 24 h. Elbourn vertical temperature profiles, and it remains in deep Ž.1966 found that the gut passage time for C. strenuus water because food is relatively plentiful there. was faster when the copepods were continuously The vertical temperature profiles may also have feeding than when they did not feed. In this study, influenced the vertical distribution of rotifers in this we could almost always find either zooplankton or study. A. herricki and C. unicornis inhabit the warm phytoplankton in the gut of C. strenuus, and the epilimnion, but F. longiseta inhabits the cold deep proportion with empty guts was very low. Since C. hypolimnion. Many studies have shown that water strenuus often fed continuously on various food temperature regulates the vertical distribution of ro- items, we think that gut passage time did not vary tifersŽ. e.g. Mikschi, 1989; Radwan et al., 1989 . It is greatly with time. probable that diel changes in vertical overlap be- There is much evidence that zooplankton, espe- tween C. strenuus and rotifers was indirectly regu- cially herbivores, show feeding rhythms. It is widely lated by water temperature. On the other hand, diel accepted that feeding rhythms often occur irrespec- changes in O for cladocerans could not be explained tive of diel changes in the amount of ambient food by water temperature alone because these animals resources, and planktologists consider that feeding migrated across the thermocline. Compared with the rhythms may be the result of recurrent environmental rotifers, cladocerans are more susceptible to fish stimuli, such as light and darkness, or due to internal predation because visually oriented planktivorous fish circadian oscillations as entrained by exogenous W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148 147 stimuliŽ. e.g. Haney and Hall, 1975 . Carnivores have oligotrophic environments, where zooplankton abun- received less attention, but Schoeneck et al.Ž. 1990 dance is generally low. investigated diel changes in the gut contents of Mesocyclops edax and found a periodical, strong increase in the number of ingested prey per copepod Acknowledgements within a one day cycle. They attributed such an increase of gut contents to a true diel periodicity in We are very grateful to Dr. H. Ueda and Mr. H. the intensity of predatory activity, because it could Haruna, Toya Lake Station for Environmental Biol- not be explained by diel changes in ambient prey ogy, Hokkaido University, for their encouragement density, taking vertical overlap between the copepod and kind support. We are also grateful to Dr. N. and the prey into consideration. In this study, P was Kitoh, Hokkaido University of Education, Hakodate not constant over a one day cycle, but we could not Branch, for his helpful comments about pollen grains. find any kind of feeding rhythm of the copepod. We also thank H. Kagawa, M. Kondoh, K. Ozaki However, we could not rule out the possibility that and H. Watanabe for assistance with sampling, and each individual C. strenuus had its own feeding Dr. J.R. Bower for correction of our English. rhythm, including a light±dark cycle, which was not synchronized within the population. There is some evidence that the feeding rhythm of Daphnia is not References necessarily identical in all individuals of a popula- tionŽ. Chisholm et al., 1975; Starkweather, 1983 . Adrian, R., Frost, T.M., 1992. Comparative feeding ecology of Tropocyclops prasinus mexicanus Ž.Copepoda, Cyclopoida . J. Since cyclopoids are often abundant in meso- and Plankton Res. 14, 1369±1382. eutrophic systemsŽ e.g. Matsumura-Tundisi et al., Adrian, R., Frost, T.M., 1993. Omnivory in cyclopoid copepods: 1990. , almost all studies, to our knowledge, on their comparisons of algae and invertebrates as food for three, feeding have been conducted in meso- and eutrophic differently sized species. J. Plankton Res. 15, 643±658. lakes, where zooplankton abundance is generally Balseiro, E.G., Vega, M., 1994. Vulnerability of Daphnia middendorffiana to Parabroteas sarsi predation: the role of the high. The density-dependent, functional responses in tail spine. J. Plankton Res. 16, 783±793. predation rates of cyclopoids are widely accepted Brandl, Z., Fernando, C.H., 1978. Prey selection by the cyclopoid from feeding experiments in which the range of prey copepods Mesocyclops edax and Cyclops Õicinus. Verh. Int. density examined was also much higherŽ more than Ver. Limnol. 20, 2505±2510. 10 up to 1000 individuals per litre.Ž Williamson, Brandl, Z., Fernando, C.H., 1979. The impact of predation by the Ž. .Žcopepod Mesocyclops edax Forbes on zooplankton in three 1986 than were observed in this study less than 3 lakes in Ontario, Canada. Can. J. Zool. 57, 940±942. individuals per litre. . This low density is associated Brooks, J.L., Dodson, S.I., 1965. Predation, body size, and com- with the oligotrophic nature of Lake Toya, and infor- position of plankton. Science 150, 28±35. mation on cyclopoid feeding in oligotrophic environ- Chisholm, S.W., Stross, R.G., Nobbs, P.A., 1975. Environmental ments is limited. This study may be the first chal- and intrinsic control of filtering and feeding rates in Arctic Daphnia. J. Fish. Res. Bd. Can. 32, 219±226. lenge to deal with such an issue. It is probable that Dussart, B.H., Defaye, D., 1995. Copepoda: Introduction to the an extremely low prey density may obscure density- Copepoda. SPB Academic Publishing BV, Amsterdam, 277 dependence in predation rates, because the encounter pp. probability with prey may vary much among individ- Elbourn, C.A., 1966. Some observations on the food of Cyclops uals in such circumstances due to small-scale patchi- strenuus strenuus Ž.Fischer . Ann. Mag. Nat. Hist. 9, 227±231. Fryer, G., 1957. The food of some freshwater cyclopoid copepods ness. Copepods that encounter patchily distributed and its ecological significance. J. Anim. Ecol. 26, 263±286. prey may ingest many items. Therefore, we consider Ghilarov, A.M., 1976. Feeding of Cyclops strenuus Žcopepoda, that an extremely low prey density may mask the crustacea.Ž. in the Glubokoye Lake Moscow distinct in sum- relationship between available prey density and the mer time. Zool. Zh. 55, 294±296, in Russian, with English number of prey in the gut of C. strenuus in this abstract. Haney, J.F., Hall, D.J., 1973. Sugar-coated Daphnia: A preserva- study. A future topic of study will be how to deal tion technique for Cladocera. Limnol. Oceanogr. 18, 331±333. with the patchiness problem in the quantitative anal- Haney, J.F., Hall, D.J., 1975. Diel vertical migration and filter- ysis of prey±predator relationships, especially in feeding activities of Daphnia. Arch. Hydrobiol. 75, 413±441. 148 W. Makino, S. BanrJournal of Marine Systems 15() 1998 139±148

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