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JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 9 j PAGES 1095–1103 j 2004 Diel cycle in the percentage abundance of parthenogenetic females with embryos of different developmental stages in four species of marine cladocerans C. KIM WONG*, CHANGHAI JI AND TONY H. M. NIP DEPARTMENT OF BIOLOGY, THE CHINESE UNIVERSITY OF HONG KONG, SHATIN, HONG KONG, CHINA *CORRESPONDING AUTHOR: [email protected] Received March 3, 2004; accepted in principle April 8, 2004; accepted for publication May 26, 2004; published online June 10, 2004 The diel cycle in the percentage abundance of parthenogenetic females carrying embryos of different developmental stages in the marine cladocerans Penilia avirostris, Pseudevadne tergestina, Pleopis polyphymoides and Pleopis schmackeri was studied at the edge of an artificial rocky shore area in a semi-enclosed bay in Hong Kong. Females carried embryos during both day and night, but females with fully-developed embryos were found predominantly at night. The diel cycle in the abundance of females with mature embryos was most pronounced in P. tergestina, and less prominent, but still clearly noticeable in P. avirostris, P. schmackeri and P. polyphymoides. The absence or scarcity of females with mature embryos during daytime could be caused by both selective predation by visual predators and nocturnal maturation and release of embryos. Juveniles of Acanthopagrus schlegeli (black seabream) were the most abundant planktivorous fish in the study area in spring. Stomach content analyses revealed that these daytime predators fed intensively on marine cladocerans and exhibited a strong selection for females with mature embryos. On the other hand, the gradual decline in the percentage of females with advanced embryos during the latter part of the night, when feeding by visual predators presumably had not yet begun, suggests that there was a tendency for nocturnal release of neonates in marine cladocerans. INTRODUCTION Some marine cladocerans exhibit a diel cycle in the development and release of parthenogenetic embryos. Onbé (Onbé, 1974) reported that Pseudevadne tergestina and Evadne nordmanni in the Inland Sea of Japan released their mature embryos in darkness between midnight and sunrise. No females with mature embryos remained in the population during the day. Nocturnal maturation and release of embryos has also been described for podonids in the Caspian Sea (Rivier, 1969), for P. tergestina in Chesapeake Bay (Bryan, 1979) and in the Gulf of Mexico (Mullin and Onbé, 1992). Penilia avirostris from the Inland Sea of Japan and the Gulf of Mexico carried mature embryos during both day and night, but showed a strong tendency to release embryos at night (Mullin and Onbé, 1992). Marine cladocerans are preyed upon by planktivorous fishes (Young and Davis, 1990; Thiel, 1996). Many planktivorous fishes depend on light to discriminate among prey items and feed more efficiently on the larger and more conspicuous prey (Brooks and Dodson, 1965). Marine cladocerans are almost transparent. For podonids, the pigmented eye is the most visible part of the body. In E. nordmanni, the eye becomes pigmented during the final stages of embryonic development (Platt and Yamamura, 1986). Because pigmentation increases the vulnerability of freshwater cladocerans to predation by fish (Zaret, 1972), it was hypothesized that marine cladocerans release their embryos before sunrise to avoid predation by visual predators (Mullin and Onbé, 1992). No data have been presented, however, to show that females containing mature embryos are exposed to higher predation risk than non-gravid females and females with small, unpigmented embryos. Penilia avirostris has a tiny eyespot, but enlargement of the carapace to accommodate the growing embryos may still increase the visibility of a gravid female to visual predators. doi:10.1093/plankt/fbh102, available online at www.plankt.oupjournals.org Journal of Plankton Research Vol. 26 No. 9 Ó Oxford University Press 2004; all rights reserved JOURNAL OF PLANKTON RESEARCH j VOLUME Four species of marine cladocerans occur in Tolo Harbour, a semi-enclosed bay in the northeastern part of Hong Kong. Penilia avirostris, the most abundant species, is present in the plankton during most of the year (Tang et al., 1995). Three podonids, P. tergestina, Pleopis polyphemoides and Pleopis schmackeri occur sporadically (Tam, 1998), although only Evadne tergestina and Podon schmackeri have been recorded in a previous study (Tang et al., 1995). Following the analyses of Gieskes (Gieskes, 1971) and Mordukhai-Boltovskoi (Mordukhai-Boltovskoi, 1978), E. tergestina has been moved to the genus Pseudevadne, and the genus Pleopis is used for P. polyphemoides and P. schmackeri. We report here on diel changes in the percentage abundance of parthenogenetic females carrying embryos of different developmental stages in P. avirostris, P. tergestina, P. polyphemoides and P. schmackeri in nearshore waters of Tolo Harbour. We also present data to show that cladoceran females with advanced embryos are more susceptible to fish predation than females with no embryos or with immature embryos. METHOD Marine cladocerans were collected from a sampling station at the edge of an artificial rocky shore area in the inner part of Tolo Harbour, Hong Kong. Water depth at the station was 3.5–4.0 m during high tide. For each species of marine cladoceran, diel changes in the percentage abundance of parthenogenetic females carrying embryos of different developmental stages were studied in two 24 h periods. Because marine cladocerans did not show clear seasonal patterns of occurrence in Tolo Harbour and abundances were low during most of the year (Tang et al., 1995), the strategy was to study each species when a large number of parthenogenetic females could be collected from the sampling station. P. avirostris, the only marine cladoceran with an almost year round occurrence in Tolo Harbour, was studied on 16 and 20 July 1998. P. tergestina was studied on 4 and 17 May 1999. The two rare species, P. schmackeri and P. polyphemoides were studied on 16 and 28 March 1999 and 4 and 16 April 1999, respectively. During each 24 h period, marine cladocerans were collected at intervals of 2 h by hauling a plankton net (0.25 m mouth diameter, 125 mm mesh size) vertically from 1 m above the bottom to the surface. The number of vertical hauls made at each sampling time ranged from two to six. The objective was to collect enough animals for determination of the percentage abundance of females carrying embryos of different development stages in the population. Once collected, the samples were preserved in 5% buffered formaldehyde. In the laboratory, samples collected at the same time were mixed together to form a single composite sample. 26 j NUMBER 9 j PAGES 1095–1103 j 2004 From each composite sample, 25 parthenogenetic females were sorted out randomly and without regard to size for examination of embryo development. For each species, a total of 300 individuals was examined for each 24 h period. Each female was dissected carefully with fine needles under a stereomicroscope and the embryos in the brood pouch were removed and examined. Following the approach of other investigators (Della Croce and Bettanin, 1965; Platt and Yamamura, 1986), embryonic development in marine cladocerans was divided arbitrarily into a series of stages based on easily distinguished external characteristics which can be found in all species. Stage 1 began with the appearance of parthenogenetic eggs in the brood chamber. As they developed, the eggs became slightly elongated. A head region appeared toward the end of stage 1 and the second antennae were clearly visible. Stage 2 began with the appearance of the first antennae. The second antennae continued to develop and became bifurcated. At least one thoracic segment was visible at the end of stage 2. The embryo elongated further at stage 3. The carapace and the thoracic appendages began to appear. In P. tergestina, P. polyphemoides and P. schmackeri the compound eye was visible, but no pigment was present. The eye became pigmented at stage 4. The carapace was complete and the embryo appeared to be fully developed. Stage 4 embryos of P. tergestina, P. polyphemoides and P. schmackeri often contained miniature parthenogenetic eggs in their own embryonic brood pouches. The twotailed Mann–Whitney test was used to test the null hypothesis that the percentage of parthenogenetic females carrying embryos of a particular developmental stage did not differ between day and night. Millions of Acanthopagrus schlegeli (black seabream) larvae and juveniles settle in the inshore areas of Tolo Harbour between January and March, shortly after spawning has taken place each year. A. schlegeli were collected for gut content analyses on 18 March 1999 when dense swarms of marine cladocerans appeared in the study area. Fish were captured at the sampling station between 1000 h and 1100 h by hauling a large dip net (1.8 1.8 m2, 0.3 mm mesh) from 2 m to the surface. Fish collected in the net were immediately preserved in 95% ethanol. Juveniles of A. schlegeli accounted for >80% of all fishes collected. Because many fish were able to avoid the net, the procedure did not provide quantitative information on the abundance of the fish population. In the laboratory, 15 A. schlegeli juveniles of 2.0–3.0 cm standard length were randomly chosen for stomach content analysis. Food objects in the oesophagus and stomach were removed with a fine needle and examined under a stereomicroscope at 50 magnification. Marine cladocerans were sorted and counted. Because many of the marine cladocerans in the 1096 C. K. WONG, C. JI AND T. H. M. NIP j DIEL REPRODUCTIVE CYCLE IN MARINE CLADOCERANS stomachs of A. schlegeli were partly digested, the percentage distribution of parthenogenetic females with embryos of different developmental stages was only estimated for stomachs (n = 12) in which >75% of the cladocerans could still be staged. The analysis was restricted to P. polyphemoides and P. tergestina because P. avirostris recovered from fish stomachs were usually badly damaged. Pleopis polyphemoides and P. tergestina from all 12 stomachs were sorted into a single composite sample. For each species, 50 individuals from the composite sample were randomly chosen for examination of embryo development. To decrease the likelihood of errors, parthenogenetic females were grouped into those with no embryos, those with small embryos (stages 1, 2 and 3), and those with large pigmented embryos (stage 4). Abundance of marine cladocerans in the water column was estimated from net samples collected immediately after fish sampling. For P. polyphemoides and P. tergestina, 50 individuals of each species were randomly chosen for determination of embryo development. Prey selectivity was analyzed using the a selectivity index of Chesson (Chesson, 1978), X a ¼ ðri =pi Þ= ðri =pi Þ where ri and pi are, respectively, the proportion of females of group i in fish stomachs and in the water column. The index varies between 0 and 1 and is unaffected by the relative abundance of food types. RESULTS The percentages of females with stage 1, stage 2 and stage 3 embryos did not differ significantly (P > 0.05) between day and night. The percentage of parthenogenetic females without embryos averaged 36.6 on 16 July 1998 and 23.3 on 20 July 1998 and also did not differ significantly between day and night (P > 0.05). Pseudevadne tergestina Pseudevadne tergestina was studied on 4 and 17 May 1999 when abundance in most net samples was 500 individuals m3. Parthenogenetic females of P. tergestina exhibited a pronounced diel cycle in reproduction (Fig. 2). A significant difference (P < 0.01) between day and night was found on both 4 and 17 May 1999 in the percentages of females with stage 1 and stage 4 embryos. The percentage of females with stage 1 embryos increased during the latter part of the night and constituted 50% of the population during the morning and early afternoon. The percentage of females with stage 4 embryos increased after sundown, attained a peak around midnight, and decreased between 0200 and 0800 h. No females with advanced stage 4 embryos remained in the population during daytime. No significant difference (P > 0.05) between day and night was found in the percentages of females carrying stage 2 and stage 3 embryos. Similarly, no significant difference (P > 0.05) between day and night was found in the percentage of females without embryos. Pleopis schmackeri Penilia avirostris The diel cycle in the percentage abundance of parthenogenetic females of P. avirostris carrying embryos of different developmental stages was studied on 16 and 20 July 1998 when abundance at the sampling station was 100 individuals m3. The percentage of females with advanced stage 4 embryos differed significantly (P < 0.01) between day and night on both sampling days (Fig. 1). Females with stage 4 embryos became less abundant between 0400 and 0800 h and were almost completely absent between 1000 and 1800 h. Accompanying the decline in the percentage of females with stage 4 embryos was an increase in the percentage of females with small stage 1 embryos. While females carrying stage 1 embryos could be found throughout the day, their percentages were highest in the hours around sunrise. Embryonic development appeared to be rapid. Females with stage 2 embryos increased in percentage throughout the morning and constituted the greatest portion of the population at around noon. The percentage of females with stage 3 embryos increased throughout the afternoon and reached a peak around sundown. Pleopis schmackeri exhibited no clear seasonal pattern of occurrence, and abundance in the study area was usually negligible. The species was studied on 16 and 28 March 1999 when abundance in the study area was 30 individuals m3. A significant difference (P < 0.05) between day and night in the percentage of parthenogenetic females with well-developed stage 4 embryos was found on both 16 and 20 July 1998 (Fig. 3). On both days, females with stage 4 embryos became less abundant during the latter part of the night and were absent during the morning between 0800 and 1200 h. Significant difference (P < 0.05) between day and night was also recorded in the percentage of females with stage 2 embryos on 28 March 1999. Pleopis polyphemoides Dense populations of P. polyphemoides appeared sporadically in the study during the period from February to May in both 1998 and 1999. The species was studied on 4 and 16 April 1999 when most net samples contained >2000 individuals m3. Pleopis polyphemoides did not show a clear diel cycle in the percentage abundance of parthenogenetic females carrying embryos of different developmental stages. 1097 JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 9 j PAGES 1095–1103 j 2004 Penilia avirostris 60 Stage 4 40 20 0 60 Stage 3 40 20 0 60 Stage 2 40 % 20 0 80 Stage 1 60 40 20 0 Non-gravid 80 60 40 20 0 0000 0200 0400 0600 0800 1000 1200 1400 1600 1800 2000 2200 Time Fig. 1. Diel change in the percentage abundance of parthenogenetic females of P. avirostris carrying embryos of different developmental stages on 16 ( ) and 20 (&) July 1998. Arbitrarily defined developmental stages were used in this study (see text). Each point was based on the observation of 25 females. . Females without embryos could be found during both day and night (Fig. 4). No statistically significant difference (P > 0.05) was found between day and night in the percentages of parthenogenetic females with embryos of different developmental stages. Females with small stage 1 embryos increased during the morning. No clear diel cycles were observed in the percentages of females with stage 2 and stage 3 embryos. Females with stage 4 embryos were found during both day and night, but their percentages were, on average, two to three times higher during the night than during the day. On 4 April 1998, <10% of the females collected between 1000 and 1400 h were carrying stage 4 embryos, compared with an average of 20.7% among females collected during the night. On 16 April 1998, <10% of the females collected between 0600 h and 1600 h contained stage 4 embryos. On both days, females with stage 4 embryos became less abundant during the latter part of the night and were completely absent at 1000 h. Fish predation Juveniles of A. schlegeli constituted >80% of the fishes collected in the study area on 18 March 1999. The stomach contents of 15 individuals were examined to estimate the extent to which marine cladocerans were preyed upon by fish (Table I). All 15 fish stomachs contained marine cladocerans. Pleopis polyphemoides constituted 90% of the cladocerans in the study area on 18 March 1999. Penilia avirostris and P. tergestina occurred in much lower numbers. 1098 C. K. WONG, C. JI AND T. H. M. NIP j DIEL REPRODUCTIVE CYCLE IN MARINE CLADOCERANS Pseudevadne tergestina 60 Stage 4 40 20 0 60 Stage 3 40 20 0 60 Stage 2 40 % 20 0 80 Stage 1 60 40 20 0 60 Non-gravid 40 20 0 0000 0200 0400 0600 0800 1000 1200 1400 1600 1800 2000 2200 Time Fig. 2. Diel change in the percentage abundance of parthenogenetic females of P. tergestina carrying embryos of different developmental stages on 4 ( ) and 17 (&) May 1999. Arbitrarily defined developmental stages were used in this study (see text). Each point was based on the observation of 25 females. . No P. schmackeri were found in the water column, so all Pleopis individuals found in fish stomachs were assumed to be P. polyphemoides. P. polyphemoides was found in all fish stomachs examined and comprised >50% of all prey objects in most fish. The number of P. polyphemoides per stomach averaged 53.4 and ranged from 12 to 102. The much lower numbers of P. avirostris and P. tergestina in fish stomachs probably reflected the relative scarcity of these species in the plankton. However, it must be noted that P. tergestina was eaten far less frequently by A. schlegeli juveniles than P. avirostris, even though the two species were present at almost comparable abundances. The proportion of P. polyphemoides females with advanced stage 4 embryos in the fish stomachs was much higher than would be expected on the basis of their proportion in the plankton (Table II). Accordingly, the value of a was much higher for females with stage 4 embryos than for females with immature embryos or without embryos. The a selectivity index could not be calculated for P. tergestina because females carrying stage 4 embryos were present in fish stomachs but absent in the water column. The percentage of females without embryos was lower than would be expected based on their percentage in the water column. DISCUSSION All four species of marine cladocerans exhibited diel cycles in the frequency distribution of females with embryos of different developmental stages. Parthenogenetic females carrying the most advanced embryos tended to be most abundant at night. The diel cycle in 1099 JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 9 j PAGES 1095–1103 j 2004 Pleopis schmackeri 60 Stage 4 40 20 0 40 Stage 3 20 0 60 Stage 2 40 20 0 % 100 Stage 1 80 60 40 20 0 Non-gravid 80 60 40 20 0 0000 0200 0400 0600 0800 1000 1200 1400 1600 1800 2000 2200 Time Fig. 3. Diel change in the percentage abundance of parthenogenetic females of P. schmackeri carrying embryos of different developmental stages on 16 ( ) and 28 (&) March 1999. Arbitrarily defined developmental stages were used in this study (see text). Each point was based on the observation of 25 females. . embryo development was most pronounced in P. tergestina. Only females collected between sunset and sunrise contained advanced embryos with pigmented eyes. Penilia avirostris, P. schmackeri and P. polyphemoides also carried advanced embryos predominantly at night, but the periodicity was not as well defined as that exhibited by P. tergestina. Diel changes in the frequency distribution of females with embryos of different developmental stages have been reported in populations of P. tergestina in Chesapeake Bay (Bryan, 1979), P. tergestina and E. nordmanni in the Inland Sea of Japan (Onbé, 1974), P. avirostris from the Inland Sea of Japan and the Gulf of Mexico (Mullin and Onbé, 1992) and various species of podonids in the Caspian Sea (Rivier, 1969). Observations reported in this paper confirm that diel cycles in reproduction are widespread among marine cladocerans and exhibit a high degree of constancy in geographical range. Tolo Harbour is an important spawning and feeding ground for a variety of pelagic fishes (Sadovy and Cornish, 2000). Between January and March, millions of young-of-the-year A. schlegeli aggregate in the artificial rocky shore areas of inner Tolo Harbour (Nip et al., 2003). The young fish grow rapidly on a diet of copepods and cladocerans, and disperse offshore to deeper waters as they become larger (Nip et al., 2003). The impact of fish predation on marine cladocerans cannot be estimated because no quantitative information is 1100 C. K. WONG, C. JI AND T. H. M. NIP j DIEL REPRODUCTIVE CYCLE IN MARINE CLADOCERANS Pleopis polyphemoides 60 Stage 4 40 20 0 60 Stage 3 40 20 0 60 Stage 2 40 % 20 0 100 Stage 1 80 60 40 20 0 60 Non-gravid 40 20 0 0000 0200 0400 0600 0800 1000 1200 1400 1600 1800 2000 2200 Time Fig. 4. Diel change in the percentage abundance of parthenogenetic females of P. polyphemoides carrying embryos of different developmental stages on 4 ( ) and 16 (&) April 1999. Arbitrarily defined developmental stages were used in this study (see text). Each point was based on the observation of 25 females. . available on the abundance of the fish populations. Nevertheless, data presented here show that the juveniles of A. schlegeli were feeding voraciously on marine cladocerans and showing strong preference for podonid females containing mature embryos. Many planktivorous fishes are visually dependent and select the largest and most conspicuous prey. Cladocerans counter visual predators by being small and invisible. All four species of marine cladocerans in Tolo Harbour are small. The body length of P. avirostris in our samples ranged from 0.38–1.04 mm. Podonids are smaller, with body size ranging from 0.26–0.85 mm for P. tergestina, 0.32–0.61 mm for P. schmackeri and 0.21–0.75 mm for P. polyphemoides. Nevertheless, females carrying mature embryos have enlarged brood chambers and are likely to appear more conspicuous to visual predators than females with no embryos. In several species of lake cladocerans, females carrying eggs are detected from greater distance (Tucker and Woolpy, 1984) and selected by fish over non-gravid females (Green, 1967; Zaret, 1972; Brancelj and Blejec, 1994). Enlargement of the brood chamber to accommodate the growing embryos presumably may increase the visibility of a gravid female to visual predators. Green (Green, 1967) found that the vulnerability of cladocerans to fish was influenced by the size of the brood pouch. Among marine species, egg-carrying females of Podon intermedius were more common in the stomachs of Baltic herrings than non-gravid females even though they were relatively rare in plankton samples (Flinkman et al., 1992). 1101 JOURNAL OF PLANKTON RESEARCH j VOLUME Table I: Number (mean¯ SD) of marine cladocerans in the stomachs of A. schlegeli (standard length 2.0–3.0 cm) collected at the study site on 18 March 1999 Marine cladocerans Water column Fish stomach (individuals m3) (n = 15) (individuals per stomach) Penilia avirostris 139¯ 74 29.5¯ 9.2 Pseudevadne tergestina 176¯ 39 6.9¯ 1.2 Pleopis polyphemoides 2405¯ 514 53.4¯ 11.7 Density of marine cladocerans (mean¯ SD) in the water column was estimated at the time of fish sampling. Table II: Selection by A. schlegeli (standard length 2.0–3.0 cm) on P. polyphemoides and P. tergestina carrying embryos of different developmental stages Water column Fish stomachs a (n = 12) Pleopis polyphemoides No embryos 10 (20%) 3 (6%) 0.07 Embryos in stages 31 (62%) 13 (26%) 0.09 9 (18%) 34 (68%) 0.84 1, 2 and 3 Embryos in stage 4 Pseudevadne tergestina No embryos Embryos in stages 9 (18%) 4 (8%) _ 41 (82%) 43 (86%) _ 3 (6%) _ 1, 2 and 3 Embryos in stage 4 0 A. schlegeli were collected at the study site on 18 March 1999. Cladocerans were collected from the water column at the time of fish sampling. Arbitrarily defined developmental stages were used in this study (see text). a is the standardized forage ratio (see text). Body size is not the only feature that determines the total visibility of cladocerans. It is well known that fish may detect some pigmented structure rather than the core body size of prey (Zaret and Kerfoot, 1975). For podonids, the large pigmented eye is the most visible part of the almost transparent body. Zaret (Zaret, 1972) has demonstrated that freshwater cladocerans with more heavily pigmented eye were removed more rapidly by fish. Parthenogenetic embryos of marine cladocerans are not heavily pigmented until the eye is fully developed. If the pigmented eyes of mature embryos enhance the visibility of the female during the final stage of embryonic development, it would be an advantage for females 26 j NUMBER 9 j PAGES 1095–1103 j 2004 to carry advanced embryos only at night (Bryan, 1979; Mullin and Onbé, 1992). The feeding efficiency of fish decreases as light intensity decreases (Vinyard and O’Brien, 1976), and some planktivorous fishes cease feeding at night (Zaret and Suffern, 1976). Onbé (Onbé, 1974) proposed that marine cladocerans use nocturnal maturation and release of neonates to decrease fish predation. This hypothesis is supported by our observation of a gradual decline in the percentage of females with advanced embryos during the latter part of the night, when feeding by visual predators had not yet begun, in all four species of marine cladocerans and, in the case of P. tergestinia and P. schmackeri, complete disappearance of females with advanced embryos from the plankton before sunrise. Onbé [in (Egloff et al., 1997)] observed that neonate release in podonids was triggered by darkness. However, it remains unknown whether marine cladocerans have an endogenous rthythm in reproduction. Two observations recorded in the present study suggest that selective predation by fish in the early part of the morning could account for the decline or disappearance of females with well-developed embryos in samples collected during the daytime. First, P. avirostris females with well-developed embryos did not disappear completely until at least 2 h after sunrise. Second, P. schmackeri and P. polyphemoides females with mature embryos became less abundant, but did not disappear completely, during the daytime. Further investigations are needed to determine the relative contributions of endogenous rhythm and selective predation by visual predators to the occurrence of diel changes in the percentage abundance of parthenogenetic females carrying embryos of different developmental stages in the marine cladocerans. ACKNOWLEDGEMENTS We would like to thank Y. H. Yung, P. Tse and Y. K. Kwok for assistance with field sampling and fish gut content analysis. P. F. Tam and K. C. Cheung assisted with data analysis. Constructive comments by K. H. Chu, Jefferson Turner and an anonymous reviewer improved the manuscript. Prof. Saywa Kim, Yong-In University, Korea, kindly confirmed the identification of the marine cladocerans. The study was supported by a Direct Grant for Research from The Chinese University of Hong Kong. REFERENCES Brancelj, A. and Blejec, A. 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