Download Diel cycle in the percentage abundance of

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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
*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
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DEPARTMENT OF BIOLOGY, THE CHINESE UNIVERSITY OF HONG KONG, SHATIN, HONG KONG, CHINA
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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.
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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
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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.
26
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DIEL REPRODUCTIVE CYCLE IN MARINE CLADOCERANS
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.
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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
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Penilia avirostris
60
Stage 4
40
20
0
60
Stage 3
40
20
0
60
%
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.
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Stage 2
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Pseudevadne tergestina
60
Stage 4
40
20
0
60
Stage 3
40
20
0
60
%
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
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Stage 2
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Pleopis schmackeri
60
Stage 4
40
20
0
40
Stage 3
20
0
60
Stage 2
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
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Pleopis polyphemoides
60
Stage 4
40
20
0
60
Stage 3
40
20
0
60
%
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).
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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
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
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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.
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