Jpn.J.Lirnnol.,4G:3,185一 一191,1985.

Effect of Temperature in the Laboratory Studies on Growth, Egg Development and First Parturition of Five Species of

Takayuki HANAZATO and Masayuki YASUNO

Abstract

Effect of temperature on growth, egg development and age at first parturition of five cladoceran species ( longispina, Moina micrura, Diaphanosoma brachyurum, Bosmina longirostris and Bosmina fata- lis) were investigated in the laboratory. The relationships between egg development time of these species and temperature, and between age at first parturition and temperature, were expressed by an equation (ln D=ln a+b(ln T)2). M. micrura and Diaphanosoma brachyurum seemed to have adapted to relatively higher temperature, while Daphnia longispina, B. longirostris and B. fatalis showed their adaptation to lower temperature. However, the results did not necessarily agree with the seasonal succession of the appearance of these species in the field.

the distribution or the seasonal succession of 1. Introduction species. WINBERG (1971) reviewed the methods to estimate the production of zooplankton. These 2. Materials and Methods methods require in principle the data on the B. longirostris and Daphnia longispina were duration of egg, juvenile and adult stages at obtained from Lake Yunoko, which is a eutrophic different temperatures. It is difficult to deter- alpine lake situated in Nikko National Park. In mine these parameters from field observations summer, the former species was abundant in for natural populations of cladocerans which re- the epilimnion, where the maximum water tem- cruit continuously. Therefore, it is vital to de- perature reached about 20°C and the latter was termine growth rate, egg development time and found in the hypolimnion, where the water age at first parturition at various temperatures temperature was about 12°C (HANAZATO,YA- under laboratory conditions for production SUNo and HosoMI, 1984). M. micrura, Diapha- estimation. nosoma brachyurum and B. f atalis were collected The effect of temperature on the egg develop- from eutrophic Lake Kasumigaura. They ap- ment time of various cladocerans in the labora- peared in summer, when the mean water tem- tory has been reported by many authors (HALL, perature was about 25°C and the maximum 1964; BOTTRELL,1975; KERFOOT,1975; KWIK became above 30°C (HANAZATOand YASUNO, and CARTER,19/5; MUNRO and WHITE, 1975; 1985). ALLAN, 1977; VIIVERBERG,1980). However, All of the species had been reared with the there are very few studies on Moina micrura alga, Chlorella sp., in the laboratory for more and Bosmina f atalis. The present report includes than two months. Chlorella sp. used here was these two species, and Daphnia longispina, Dia- cultured in log-phase-growth with MC medium ph.anosom brachyurum and Bosmina iongirostris. (medium for Chlorella ellipsoidea; WATANABE, The distribution or the seasonal succession of 1960) at 23°C under continuous fluorescent cladoceran species can be explained by the dif- illumination of 40001ux. Algal cells rinsed with ference or change of water temperature in many dechlorinated tap water by centrifugation were cases (TAPPA, 1965; ALLAN, 1977). In the pre- provided for the cladocerans. sent study, temperature adaptation of caldocerans Experiments were conducted at 15°C, 20°C, was inferred from laboratory data in relation to 25°C and 30°C under a 16-8 LD photocycle. 186 HANAZATO and YASUNo

Additional experiments at 10°C and 12°C were conducted for Daphnia longispina. Daphnia 3. Results longispina, M. micrura and Diaphanosoma bra- Growth chyurum were reared individually in a 50 ml M. micrura and Diaphanosoma brachyurum beaker, while B. longirostris and B. f atalis were could reproduce well even at a high temperature reared individually in a test tube (20 ml). The (30°C), but Daphnia longispina and B. longiro- vials were kept at temperatures of ±0.5°C in stris could not survive at this temperature. a water bath controlled with a thermostat. The B. f atalis also could not survive at 30°C, al- culture medium for the was prepared though this species was abundant in summer with dechlorinated tap water suspending Ghlo- in Lake Kasumigaura, when the water tempera- rella at a concentration of 1 x 106 cells ml-'. ture reached 30°C. Growth curves of five clado- This algal density was above the "incipient ceran species in the mean body length at different limiting level" of food for cladocerans studied temperatures are shown in Fig. 1. here (unpublished data). The culture medium Daphnia longispina was about 0.6 mm in body for the animals was changed for a fresh one length when it was born and grew to about every other day. 1.9 mm after 25 days at 15, 20 and 25°C. There Before the experiments, animals were reared are no significant differences in the body length for several days under the respective experi- at these temperatures. However, it took about mental conditions and young born within 24 hr 40 and over 60 days to reach the maximum body from them were used for the experiments. At length at 12 and 10°C, respectively. each temperature, ten to twelve young of Daphnia ion gispina, M. micrura and Diaphanosoma bra- chyurum were reared respectively. The growth of these young was followed daily by measuring the total body length (top of the head to pos- terior of carapace) under a binocular microscope with a micrometer eyepiece to the nearest 0.025 mm. For these three species, the mature size, which is the body length when a female bears eggs first in her brood chamber, was determined. Since B. ion girostris and B. f atalis were intolerant of handling for measurement of body length, individuals of these species were discarded after measurement. Thus, 64 to 91 replicates were prepared for each temperature for these species, and 3-16 individuals of each species were dis- carded everyday. Any newborns from each were recorded and removed daily. Accordingly, the duration of egg development in days was determined as the time from the release of one brood to the next. The age in days at first parturition was taken as the first release of brood. To relate the duration of egg development and age at first parturition to temperature, the following regression equation of BoTTRELL(1975) was used, In D-1n a+b(ln T)2 Fig. 1. Growth of five cladoceran species as mean where D is the duration of egg development or body length at various temperatures. 30°C age at first parturition in days and T is tempera- (o), 25°C (A), 20°C (0), 15°C (s), ture (°C). 12°C (®•), and 10°C (x). Temperature on growth, egg development and age at first parturition of five cladoceran species 187

The body length of M. micrura newborns was 0.55 mm in maximum, respectively. The growth about 0.45 mm. The maximum body length was curves at 15 to 25°C were approximately equal. about 1.2 mm after 15 days at 20°C. The growth This result was similar to that of Daphnia at 25 and 30°C could not be followed after the longispina. ninth day, because they had all died. The body In general, mature size is negatively correlated length of the animals by the eighth day at 20, with water temperature. In the present study, 25 and 30°C did not differ significantly. M. Daphnia longispina matured at a relatively micrura showed a similar growth rate between smaller size at 20°C and 25°C, M. micrura did 20°C and 30°C, while that at 15°C was ap- so at 30°C, and Diaphanosoma brachyurum at parently lower. 25°C and 30°C (Table 1). The newborn of Diaphanosoma brachyurum was about 0.4 mm in body length, and the Duration of egg developmemnt maximum was about 0.95 mm, which did not Duration of egg development of cladocerans differ between the temperatures. The growth at different temperatures is shown in Table 2 curves at 20, 25 and 30°C were nearly the same, and Fig. 2. The duration became shorter with but the slope of the curve at 15°C was flatter. rising temperature. The relationship between The temperature-growth relationship was similar the duration and temperature can be described to that of M. micrura, yet there was a difference by a logarithmic equation (Table 3). The in the survival rate between the two species at curves are shown in Fig. 2. At 30°C, the eggs higher temperatures, at which the rates of of M, micrura and Diaphanosoma brachyurum Diaphanosoma brachyurum were higher than developed fast and became young after 24 hours. those of M. micrura. The differences in the duration of egg develop- The body lengths of B. longirostris and B. ment among the five cladocerans were smaller f atalis newborns were about 0.21 mm and 0.25 at a higher temperature (20-25°C), but larger mm, and eventually reached about 0.50 mm and at a lower temperature (15°C). The duration

Table 1. Mature size (mm) of Cladocera at different temperatures. Mean±S.D. Number of observations in parentheses.

Table 2. Duration of egg development in days (mean±S.D.) of five cladoceran species at different temperatures. Number of observations in parentheses. 188 HANAZATO and YASUNO

Table 3. Coefficients for the regression equation relating the egg development time of five cladoceran species to temperature.

* N .S. (95% CL of b contains zero).

soma brachyurum>Daphnia longispina>B. lon- girostris and B. f atalis. The egg development time was almost the same between M. micrura and Diaphanosoma brachyurum and betwen B. longirostris and B. f atalis at the temperatures examined.

Age at first parturition With the rise in temperature, the age at first parturition of the cladocerans was younger (Table 4 and Fig, 3). At higher temperatures (25°C and 30°C), M. micrura had first parturi- tion at a younger age than in the other species. At a lower temperature (15°C), however, B. longirostris reached the age earlier than the others. B. f atalis was almost the same as B. longirostris as for the age at first parturition as well as the duration of egg development. Fig. 2. Mean duration of egg development of cla- Diaphanosoma brachyurum, on the other hand, docerans at various temperatures. Daph- gave the first parturition at 2-5 days older nia longispina (©, • • • •), Moina micrura age than M. micrura between 15°C and 30°C, (A, -), Diaphanosoma brachyurum although the egg development time of the (D, - • -S), Bosmina longirostris (0, former species was similar to that of the latter (-- -), and Bosmina f atalis (•, ) species at these temperatures. The relationships between the age and temperature for the five of the five cladoceran species at 15°C was in species were fitted to a logarithmic equation the following order: M. micrura and Diaphano- (Table 5). The curves are shown in Fig. 3,

Table 4. Age at first parturition in days (median) of five cladoceran species of different temperatures. Number of observations in parentheses.

* mean value . Temperature on growth, egg development and age at first parturition of five cladoceran species 189

Table 5. Coefficients for the regression equation relating the age at first parturition of five cladoceran species to temperature.

* N .S. (95% CL of b contains zero)

MURUGAN(1975), but shorter than LEWIS' data (1979) at 25°C. The egg development time for Diaphanosoma brachyurum in the present study was slightly shorter than that reported by VIJVERBERG(1980). As for B. longirostris, the egg development time in the present data was close that in the literature (KERFOOT, 1975; ALLAN, 1977; VIJVERBERG,1980. However, KWIx and CARTER (1975) reported a longer egg de- velopment time for this species. The egg de- velopment time of B. f atalis was shown only in LEWIS' report (1979). He put the development time from the field data at 25°C, which was similar to the result at the same temperature in the present findings. The growth rates of Daphnia longispina did not differ between 15°C and 25°C. Those of M. micrura and Diaphanosoma brachyurum were the same between 20°C and 30°C, respec- tively, but the age at first parturition became younger with a rise in the temperature. This resulted not only from shortening the duration Fig. 3. Age at first parturition in days of clado- of egg development but also from reducing the cerans at various temperatures. Daphnia mature size at higher temperature. The growth longispina (QQ, •), Moina micrura (i, rates of Daphnia longispina were temperature- ---), Diaphanosoma brachyurum (tx , dependent between 10°C and 15°C, and those -.-) , Bosmia longirostris (0, ---), and of M. micrura and Diaphanosoma brachyurum Bosmina f atalis (•, ) . were also suppressed by lowering the tempera- ture to between 15°C and 20°C. Still, except 4. Discussion for Daphnia longispina at 10°C, their mature Egg development time of Daphnia longispina sizes did not change at these lower temperatures. in the present study agreed with the data by This result indicates that the older age at first ELSTER and SCHWOERBEL(1970) and MUNRo parturition at lower temperature was affected and WHITE (1975), and was similar to Daphnia by the lower growth rate and the longer dura- galeata mendotae (HALL, 1964), Daphnia am- tion of egg development but not by any change bigua (ALLAN, 1977) and Daphnia hyalina in the mature size. (VIJVERBERG,1980). The duration of egg de- From the growth curve at 15°C, the clado- velopment for M. micrura in the present investi- ceran species can be classified into two groups. gation at 30°C was the same as the result by The one includes M, micrura and Diaphanosoma 190 HANAZATO and YASUNO brachyurum, which showed an apparently lower growth rate at 15°C than at higher temperature 摘 要 (20-30°C). These species reproduced at 30°C and could be regarded as the species adapting 枝 角 類5種(Daphnialongispina,Moinamicrura, to higher temperatures. This finding agrees with Diaphan・ ∫omα ろ7m勿 π7～m,BosminaJ・ngirostris, the fact that these two species become predomi- Bosminafatalis)を 実 験 室 内 で 飼 育 し,そ れ ら の 成 長 nant in Lake Kasumigaura in summer. Another ,胚 の 発 育 期 間,お よ び 最 初 の 産 仔 ま で に 要 す る 日数 group includes Daphnia longispina, B. longiro- に 対 す る 温 度 の 影 響 を 調 べ た. stris and B. f atalis, which showed the same 1)Daphnialongispina,B,longirostris,B,fata- growth curve at 15°C as at higher temperatures lisは,そ れ ぞ れ の 種 に つ い て15-25。Cで ほ と ん ど 同 (20-25 ° C). These species seemed to adapt to じ様 な 成 長 速 度 を 示 した.一 方,ルf.rrticruraと1)is一 lower temperatures. B. ion girostris, which 効mo50m8brachyurumlよ,そ れ ぞ れ の 種 で24-30 。Cで 同 じ様 に 成 長 した が showed the shortest egg development time and ,15。Cで は 明 ら か に 成 長 earliest age at first parturition among the five 速 度 の 低 下 が み ら れ た. species at 15°C, has an advantage in the com- 2)胚 の 発 育 期 間 や 最 初 の 産 仔 ま で に 要 す る 日数 petition with other species at lower tempera- は,水 温 が 上 昇 す る に つ れ て 短 く な り,そ れ ら の 時 間 tures. BHAJAN and HYNES (1972) also showed (日 数,1))と 温 度(T)と の 関 係 は,InD=lna+b experimentally that B. longirostris populations (lnT)2の 式 で 表 わ す こ と が で き た. fared better at lower temperatures. However, 3)実 験 水 温 に お け る 胚 の 発 育 期 間 で は,B.tongi- the adaptation of B, f atalis to lower temperature rustrisとB.ノ 認 α薦 の 問,お よ びM.m∫6剛mと did not agree with the field observations as to Diaphanosomabachyurumの 間 で ほ と ん ど 相 違 が み its abundance in Lake Kasumigaura in summer, when the water temperature reaches 30°C ら れ ず,さ ら にBosmina2種 の 間 で は 最 初 の 産 仔 ま で に 要 す る 日数 で も似 た 値 が 得 ら れ た. (HANAZATOand YASUNO, 1985). The seasonal succession from B. ion girostris 4)本 実 験 の 結 果 か ら 推 察 さ れ た 枝 角 類 の 温 度 適 性 to B. f atalis in early summer and from B, f atalis だ け で は,霞 ケ 浦 に お け るB.fatalisの 出 現,B.lan- to B, longirostris in the fall in Lake Kasumiga- girostrisとB.fatalisの 季 節 変 化,湯 の 湖 に お け る ura as reported in our previous study (HANAZATO Daphnialongispinaの 垂 直 分 布 を 説 明 す る こ とが で et al., 1984) could not be explained by the dif- きず,そ れ ら の 季 節 変 化 や 分 布 に は 温 度 以 外 の 要 因 が ference in the optimal temperature between the 関 与 し て い る こ と が 示 唆 され た. two species, because the growth, egg develop- ment time and age at first parturition of these References species at various temperatures were almost the same. This fact suggests that succession is as- ALLAN, J. D. (1977) : An analysis of seasonal sociated with other factors such as the change dynamics of a mixed population of Daphnia in the algal species as food (HANAZATOet al., and the associated cladoceran community. 1984). Freshwat. Biol., 7: 505-512. Daphnia longispina is found in the hypolim- BHAJAN, W. R. and H. B. N. HYNES (1972) : nion in Lake Yunoko where the water tempera- Experimental study on the ecology of Bosmina longirostris (d. F. MULLER) (Cladocera). ture was 12°C. Since it was shown in the present Crustaceana, 23: 133-140. study that the egg development and the first BOTTRELL, H. H. (1975) : The relationship be- parturition of this species at 12°C took more tween temperature and duration of egg de- than twice as long as at 20°C. The hypolimnion velopmnt in some epiphytic Cladocera and of this lake in summer is not necessarily favour- Copepoda from the River Thames, Reading, able to the population of this species. Such a with a discussion of temperature functions. discrepancy may suggest the presence of some Oecologia, 18: 63-84. factors other than temperature governing the ELSTER, H. J, and J. SCHWOERBEL (1970) : vertical distribution. Further studies are needed Beitrage zur Biologie and Populationsdynamik to clarify these factors in the future. der Daphnien im Bodensee. Arch. Hydrohiol. Suppl., 38: 18-72. HALL, D. J. (1964) : An experimental approach to the dynamics of a natural population of Temperature on growth, egg development and age at first parturition of five cladoceran species 191

Daphnia galeata mendotae. Ecology, 45: 94- England. Oecologia, 20: 157-165. 112. MURUGAN, N. (1975) : Egg production, develop- HANAZATO,T. and M. YASUNO (1985) : Popu- ment and growth in Moina micrura Kurz lation dynamics and production of cladoceran (1984) (Cladocera: Moinidae). Freshwat. zooplankton in the highly eutrophic Lake Biol., 5: 245-256. Kasumigaura. Hydrobiologia, 124: 13-22. TAPPA, D. W. (1965) : The dynamics and the HANAZATO, T., M. YASUNO and M. HOSOMI association of six limnetic species of Daphnia (1984) : Vertical migration of zooplankton in Aziscoos Lake, Maine. Ecol. Monogr., 35: in Lake Yunoko. (in Japanese). Commemo- 395-423. rative Issue for Retirement of Prof. Toshihiko VIJVERBERG, J. (1980) : Effect of temperature Mizuno, 113-121. in laboratory studies on development and HANAZATO, T., M. YASUNO, T. IWAKUMA and growth of Cladocera and Copepoda from N. TAKAMURA(1984): Seasonal changes in Tjeukemeer, The Netherlands. Freshwat. Biol., the occurrence of Bosmina longirostris and 10: 317-340. Bosmina fatalis in relation to Microcystis WATANABE, A. (1960) : List of algal strains in bloom in Lake Kasumigaura. Jap.J. Limnol., collection at the institute of applied micro- 45: 153-157. biology, University of Tokyo. J. Gen. Appl. KERFOOT, W. C. (1975) : Seasonal changes of Microbiol., 6: 238-292. Bosmina (Crustacea, Cladocera) in Frains WINBERG, G. G. (ed.) (1971) : Methods for the Lake, Michigan: Laboratory observations of estimation o f production of aquatic animals. phenotypic changes induced by inorganic fac- Soviet National Committee of IBP, Minsk. tors. Freshwat. Biol., 5: 227-253. Trans. A. Duncan, Academic Press, London, KWIK, J. K, and J. C. H. CARTER (1975) : Popu- 175 pp. lation dynamics of limnetic Cladocera in a beaver pond. J. Fish. Res. Board Can., 32: (著者:花 里孝幸 ・安野正之,国 立公害研究所 生物 341-346. 環 境 部,〒305筑 波 郡 谷 田部 町小 野 川16-2; Taka- LEWIS, W. M. Jr. (1979) : Zooplankton Com- munity Analysis. Springer-Verlag, New York, yuki HANAZATO and Masayuki YASUNO, Division 163 pp. of Environmental Biology, National Institute for MUNRO, I. G. and R. W. G. WHITE (1975) : Environmental Studies, Yatabe, Tsukuba 305.) Comparison of the influence of temperature on the egg development and growth of Daph- Received: 9 August 1984 nia longispina O. F. MULLER (Crustacea: Accepted: 15 March 1985 Cladocera) from two habitats in southern