Diel variation of zooplankton in the tropical coral-reef waterof Tioman Island, Malaysia
Ryota Nakajima Æ Teruaki Yoshida ÆBin Haji Ross Othman Æ Tatsuki Toda
Received: 14 January 2008 / Accepted: 1 August 2008 / Published online: 15 August 2008
� Springer Science+Business Media B.V. 2008
Abstract Zooplankton was sampled at 3-h intervals
for a 48-h period from a coral reef of Tioman Island,
Malaysia. It was size-fractionated into three size
classes: 100–200, 200–335, and [335 lm using
different sieves with different mesh sizes. Total
zooplankton ([100 lm) abundance and biomass in
the water column were high later at night (0300 h),
not just after sunset as previously described in other
studies. Only the largest size-fraction ([335 lm) of
zooplankton significantly differed in biomass and
abundance between day and night. The increase in the
large zooplankton later in the night is suggested to be
caused by the advection of pelagic species into the
reef. This work has provided a measurement of the
variation of zooplankton community over coral reef
that can exist on a scale of hours.
Keywords Day/night change � Size-fraction �Copepods � Pelagic � Reef associated
Introduction
Nocturnal ascent is one of the most noticeable char-
acteristics of zooplankton migratory behavior in
marine ecosystem. This feature is also known from
various coral reefs (e.g., Ohlhorst 1982; Roman et al.
1990; Madhupratap et al. 1991; McFarland et al. 1999;
Yahel et al. 2005a, b). Daytime visual predation by the
planktivorous fish is interpreted to be the ultimate
factor of this avoidance behavior (De Robertis 2002).
The nocturnal emergence in coral reefs is also consid-
ered as a mechanism for avoiding the intense near-
bottom predation by highly abundant sedentary zoo-
planktivores such as corals. Corals and other sedentary
zooplanktivores use tentacles to capture zooplankton
prey primarily during the night (Sebens et al. 1998),
and the nocturnal bottom avoidance is suggested to
be one of the ultimate causes shaping the temporal
variation of zooplankton abundance above coral reefs
(Yahel et al. 2005b). Moreover, coral-reef zooplank-
ton is reported to show intense nocturnal emergence
early in the dark, e.g., soon after sunset when prey-
capture efficiency of many diurnal planktivorous fish is
greatly decreased and corals have not yet expanded
their tentacles (Yahel et al. 2005b). In fact, several
studies have observed high zooplankton abundance in
the water column in the early hours of night from
various coral reefs (Glynn 1973; McFarland et al.
1999; Yahel et al. 2005b). However, there are some
reports of coral-reef zooplankton showing their peak
abundance later in the night (e.g., Sorokin 1993), and
R. Nakajima (&) � T. Toda
Department of Environmental Engineering for Symbiosis,
Faculty of Engineering, Soka University, Tangi-cho,
Hachioji, Tokyo 192-8577, Japan
e-mail: [email protected]
T. Yoshida � B. H. R. Othman
Marine Ecosystem Research Centre, Faculty of Science &
Technology, Universiti Kebangsaan Malaysia, 43600
Bangi, Selangor, Malaysia
123
Aquat Ecol (2009) 43:965–975
DOI 10.1007/s10452-008-9208-5
there is also a report of no peak in abundance at night
(Heidelberg et al. 2004). Thus, these temporal varia-
tions of zooplankton during the night are not
unequivocal. At present, quantitative data on diel
variation in the coral-reef zooplankton with one to
several hour intervals are scarce. Investigations with
sampling at short-time intervals provide important
additional information to help interpret the variation
patterns in zooplankton emergence.
The nocturnal increase in zooplankton abundance
in shallow water as the coral reefs inhabit can be
attributed to two factors: (1) the migration of reef-
associated zooplankton living in or on the benthic
substrate by daytime and migrating into the water
column at night (Alldredge and King 1977) and (2)
the onshore advection of pelagic zooplankton which
have diel migration offshore (Yahel et al. 2005a).
Reef-associated zooplankton is at risk of being
captured by benthic planktivores if they stay near
bottom during the night, so they possibly move into
the water column earlier in the night. On the other
hand, pelagic zooplankton, which performs diel
migration offshore, would be in the surface waters
offshore early in the night and could advect into the
reef area with the tide later in the night.
In this study, we collected zooplankton at 3-h
intervals for a 48-h period at a coral reef in Tioman
Island, Malaysia. The objective of this study was (1)
to examine the temporal variation of coral-reef
zooplankton on a diel basis and (2) to examine the
significance of zooplankton origin (reef associated or
pelagic) and its influence in the temporal variation.
We hypothesize that the zooplankton peak early in
the night is due to emergence of reef-associated
zooplankton, while the peak later in the night is due
to onshore advection of pelagic zooplankton. In this
study we fractionated zooplankton into various size
classes. Such a size-fractionation of the zooplankton
communities simplifies a complex community
composition (Magnesen 1989) and will provide
information on what size-class chiefly contributes to
the diel variation.
Materials and methods
Study site
This study was carried out at Tioman Island, Malay-
sia (2�5000000 N; 104�1000000 E), located 32 km off
the east coast of Peninsular Malaysia (Fig. 1). The
island forms a typical fringing coral reef, with live
coral coverage that ranged from 35% to 69% with a
dominance of Acropora corals (Harborne et al. 2000;
TiomanIsland
104° 09’E
04° 49’N
100 m
Jetty
Sampling site
PeninsularMalaysia
The Straits of Malacca
South China Sea
Indonesia
Fig. 1 Map of the
sampling site in Tioman
Island off the east coast of
Peninsular Malaysia
966 Aquat Ecol (2009) 43:965–975
123
Toda et al. 2007). Zooplankton sampling was con-
ducted at a jetty in the marine park located at the west
side of the island (Fig. 1). The water depth varied
from 6.5 to 11.0 m depending on the tide. The bottom
of the sampling site is covered with fine-to-medium
carbonate sand with small patches of live corals of
Acropora spp.
Sampling and analysis
We collected zooplankton every 3 h, starting at
1200 h on 20th of October 2003 and with last
sampling at 0900 h on 22nd October. The timing of
sunrise was 0647 h and of sunset 1850 h. The total
number of the sampling time (n) was 16 because we
collected samples every 3 h for a 48-h period. Within
the 16 sampling times, eight samples represent
samples taken during the day (0900, 1200, 1500, and
1800 h for two daytimes) and another eight for the
night sampling (2100, 0000, 0300, and 0600 h for two
nighttimes). Therefore, the number of replicates was 8
for both day and night samples resulting in 16 for total.
Zooplankton was collected by five gentle vertical
tows of a plankton net (mesh size, 100 lm; diameter,
30 cm; length, 100 cm) with a flowmeter from the
water column of 1 m above the sea bottom to the
surface. The samples were pooled and immediately
brought back to the laboratory of the marine park
within 5 min.
Prior to the zooplankton collection, water was
sampled with a 10-l Niskin bottle at three depths: 1, 3,
and 6 m. Water temperature and salinity were measured
for samples from each depth. Also, these were pre-
filtered through a 100-lm mesh screen and combined
for chlorophyll a (Chl. a) determinations. The pre-
filtered seawater (\100 lm) was filtered onto GF/F
filters (Whatman), which were placed in 90% acetone
for pigment extraction and stored in a refrigerator for
24 h. Chl. a concentration was determined using a
spectrophotometer according to Parsons et al. (1984).
The net-collected samples ([100 lm) were size-
fractioned into three size-classes (100–200, 200–335,
and [335 lm) by mesh screens of 200 and 335 lm.
The three fractions were each divided into two aliquots
with a Folsom plankton splitter (Omori and Ikeda
1984). One aliquot was used for taxonomic analysis
and the other for weight determination as organic
carbon. The aliquot for taxonomic analysis was
fixed in 5% formalin seawater, and zooplankton was
characterized into different groups such as phylum,
subphylum, class, subclass, and order and counted
under a dissecting microscope. Copepod adults were
identified to species level whenever possible. The
aliquot for weight determination was immediately
filtered onto a GF/A filter (Whatman), which was
pre-combusted at 500�C for 4 h and pre-weighed. The
filters were dried for 24 h at 60�C, and the organic
carbon weight was measured following Nagao et al.
(2001), using a CN analyzer (Fisons model EA 1108
CHNS/O). The measured organic carbon is seston
mass, included zooplankton, detritus, and larger
phytoplankton. We also measured the organic carbon
contents of the detritus/larger phytoplankton and
subtracted its value from the total seston mass as
carbon for obtaining the actual zooplankton biomass.
For this, we separated the detritus/larger phytoplank-
ton from the formalin samples by sorting all the
zooplankton including nauplii and measured their
carbon contents as described above.
The difference between day and night density and
biomass of zooplankton for each size-fraction was
determined using Mann–Whitney’s U-test.
Results
Environmental factors
Tide level was 6.5 m at 1200 h on 21st October but
gradually increased and reached 11 m at 0600 h on
22nd October. After that the tide level repeatedly rose
and fell until the final sampling time. The times of high
tide were at 0600, 0900, 1500, and 2100 h on 21st
October and 0600 h on 22nd October. The times of
low tide were at 1200 and 1800 h on 21st October and
0000 and 0900 h on 22nd October. The mean water
temperature and salinity at 1-, 3-, and 6-m depth varied
from 27.0 to 28.5�C (average = 27.3 ± 0.05�C) and
from 33.0 to 35.0 PSU (average = 34.0 ± 0.08 PSU),
respectively. Chl. a concentration varied from 0.16 to
0.57 mg m-3 (average = 0.36 ± 0.21 mg m-3).
Day/night change of zooplankton abundance,
biomass, and composition
We carried out our sampling by vertical tows of the
entire water column (1 m above the bottom to the
surface) and not depth-discrete sampling. Therefore,
Aquat Ecol (2009) 43:965–975 967
123
the result stated here is the biomass of zooplankton
throughout the water column (depth ca. 7–11 m
depending on the tide).
The total biomass (mg C m-3) of zooplankton
([100 lm) in the water column was significantly
higher during the night (P \ 0.01) (Fig. 2a), being
2.1 times as high (4.56 ± 1.66 mg C m-3) as during
the day (2.22 ± 0.66 mg C m-3). The total average
density at night (4,629 ± 1,685 inds. m-3) was also
higher than at daytime (3,168 ± 1,450 inds. m-3),
but the difference was not statistically significant
(P = 0.093), because of an increase during the day at
1200 h due to the addition of nauplii in the small
fraction (100–200 lm) and nauplii and calanoid
copepodites and Oithonidae in the mid fraction
(200–335 lm) (Figs. 2b, 3, and 4). The influence of
this day-increase was small for biomass.
At night, both biomass and abundance of total
zooplankton ([100 lm) attained peaks at 0300 h in the
water column (1 m above the bottom to the surface)
due to the addition of the large fraction ([335 lm)
mainly consisting of Paracalanus spp., copepodites of
calanoid and oithonidae, chaetognaths, and larvaceans
([45% of the total abundance of the large fraction).
The nocturnal increase in the total biomass of
zooplankton was highly associated with a correspond-
ing increase in the proportion of the large fraction
(Fig. 2c), constituting 67.3% of the total biomass,
which was numerically dominated by calanoid co-
pepodites (mostly Paracalanus spp. and Acartia spp.)
and Oithonidae, larvaceans, and chaetognaths
(Tables 1 and 2). Zooplankton in this large fraction
had lower biomass and density in the water column
during the day (1.13 ± 0.57 mg C m-3; 516 ± 515
inds. m-3), while at night it significantly increased 2.7-
fold for biomass (3.07 ± 1.22 mg C m-3; P \ 0.05)
and 2.1-fold for abundance (1,069 ± 614 inds. m-3;
P \ 0.01). Most zooplankters in this fraction showed
peaks at 0300 h but amphipods, other crustaceans
(mainly crab zoea), and polychaete larvae showed
peaks at 2100 h on either night.
The day and night biomass and abundance in the
smaller fractions (200–335 and 100–200 lm) did
not significantly differ (P = 0.093 and 0.059 and P =
0.834 and 0.345, respectively). The mid fraction
(200–335 lm) was numerically dominated by nauplii
and copepodites of Oithonidae and calanoid (mostly
Paracalanus spp.). The average biomass was 0.65
(a)
Time (hours)
(b)
(c)
1800
0000
0600
1200
1800
0000
0600
1200
Abu
ndan
ce (
inds
. m-3
)
1800
0000
0600
1200
1800
0000
0600
1200
(d)
0
2000
4000
6000
8000
0
1000
2000
3000
>335 µm
200-335 µm
100-200 µm
Bio
mas
s (m
g C
m-3
)
>335 µm
200-335 µm
100-200 µm
0
2
4
6
0
2
4
6
8
Fig. 2 Diel variation in abundance and biomass of total (a, b) and size-fractionated zooplankton (c, d), respectively, at Tioman
Island. Black bars indicate hours of night. Dotted vertical lines indicate the time of sunset
968 Aquat Ecol (2009) 43:965–975
123
(±0.12) mg C m-3 at day and 0.92 (±0.35) mg C m-3
at night. The average density was 1,096 (±449)
inds. m-3 at day and 1,609 (±607) inds. m-3 at night.
The small fraction (100–200 lm) was dominated by
nauplii, with a mean biomass of 0.43 (±0.26) mg
C m-3 during daytime and 0.57 (±0.29) mg C m-3 at
night; and the density was 1,565 (±768) inds. m-3
during daytime and 1,950 (±824) inds. m-3 at night.
The copepods (adult + copepodites) in all frac-
tions were about two times more abundant at night
than during the daytime. Adult copepods and copepo-
dites were the most dominant taxa in the large and mid
fractions, constituting 63.5% and 57.9% of the total
abundance in each fraction, respectively (Table 1),
and were responsible for the temporal variation in
these size-fractions (Fig. 3c, f). In the small fraction,
Adult copepods and copepodites
Chaetognaths
Echinoderm larvae
Larvaceans
0
2
4
6
8
10
12
100-200 µm
200-335 µm
>335 µm
1800
0000
0600
1200
1800
0000
0600
1200
1800
0000
0600
1200
1800
0000
0600
1200
1800
0000
0600
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1800
0000
0600
1200
Time (hours)
Abu
ndan
ce (
in
ds. m
-3)
3
(a)
(b) (c)
(e) (f) (g)
Hydrozoans
Polychaete larvae
Ostracods
Amphipods
Other crustaceans
(d)
Polychaete larvae
Adult copepods and copepodites
Nauplii
Larvaceans
Hydrozoans
Polychaete larvae
Adult copepods and copepodites
Other crustaceans
Nauplii
Ostracods
Chaetognaths
Larvaceans
14
16
0
2
4
6
8
10
12
14
16
0
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0
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0
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12
14
16
0
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6
8
10
12
14
16
0
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14
16
Fig. 3 Diel variation in abundance of common zooplankton taxa in the three size-fractions (a: 100–200 lm; b, c, d: 200–335 lm;
e, f, g: [335 lm) at Tioman Island. Black bars indicate hours of night. Dotted vertical lines indicate the time of sunset
Aquat Ecol (2009) 43:965–975 969
123
OithonidaeOithonidae copepodites
ParacalanusCalanoid copepodites
OithonidaeOithonidae copepodites Microsetella
Saphirella-like copepodsPoecilostomatoid copepodites
ParacalanusCalanoid copepodites
AcartiaSubeucalanusLabidocera
Clausocalanus
Temora
CentropagesParacalanusCalanopia
Poecilostomatoid copepodites
OncaeaCorycaeus
FarranulaPoecilostomatoid copepodites
100-200 µm
200-335 µm
>335 µm
1800
0000
0600
1200
1800
0000
0600
1200
1800
0000
0600
1200
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Time (hours)
Abu
ndan
ce (
inds
. m-3
)3
(a) (b) (c) (d)
(e) (f) (h)(g)
(i)
(j) (k) (l) (m)
(n) (o) (p)
Harpacticoid copepodites
Harpacticoid copepodites
MicrosetellaEuterpina
AcrocalanusPseudodiaptomsCalanoid copepodites
OithonidaeOithonidae copepodites
Macrosetella
MicrosetellaEuterpinaHarpacticoid copepodites
Corycaeus
Farranula
1800
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Fig. 4 Diel variation in abundance of common copepod taxa in the three size-fractions (a–d: 100–200 lm; e–i: 200–335 lm;
j–p: [335 lm) at Tioman Island. Black bars indicate hours of night. Dotted vertical lines indicate the time of sunset
970 Aquat Ecol (2009) 43:965–975
123
nauplii were the most abundant (59.8%), followed by
adult copepods and copepodites (39.4%). Nauplii
determined the zooplankton variation due to the
dominance, but adult copepods and copepodites
demonstrated more explicit day/night difference.
The copepod taxa which significantly increased at
night in the large fraction were Acartia spp., Centro-
pages spp., Subeucalanus spp., Paracalanus spp.,
Calanopia spp., Labidocera minuta, Pseudodiapto-
mus spp., Temora discaudata, Microsetella norvegica,
and calanoid copepodites including Acartia and
Paracalanus (Table 2). The day and night differences
of Oithonidae and their copepodites in the large
fraction were statistically not significant (P = 0.248
and 0.141, respectively), but clear nocturnal increases
were observed (Fig. 4n). In the mid fraction, Para-
calanus spp., Oithonidae and its copepodites, and
Oncaea conifera increased significantly at night
(P \ 0.05). In the small fraction, Paracalanus spp.
and copepodites of Paracalanus and Oithonidae
significantly increase at night (P \ 0.05). Most adult
copepods and copepodites showed a significant noc-
turnal increase at 0300 h, but Pseudodiaptoms spp.
peaked at 2100 h on both nights (Fig. 4m).
Origin of zooplankton
Our net sampled all zooplankton in the water column,
including both the reef-associated and pelagic type.
We characterized our zooplankton by origin as reef-
Table 1 Average abundance and percent composition (%) of common zooplankton taxa in different size-fractions at Tioman Island
Size-class (lm) Zooplankton Origin Abundance (inds. m-3)
Day n % Night n % P Total n %
100–200 Polychaete larvae 5 ± 6 8 0.2 11 ± 9 8 0.4 * 8 ± 8 16 0.5
Adult copepods and
copepodites
499 ± 315 8 23.5 886 ± 526 8 34.1 ns 693 ± 464 16 39.4
Nauplii 1,058 ± 629 8 76.2 1,045 ± 513 8 65.1 ns 1,052 ± 554 16 59.8
Larvaceans 2 ± 4 8 0.1 6 ± 5 8 0.2 ns 4 ± 5 16 0.2
200–335 Hydrozoans 14 ± 13 8 1.3 8 ± 10 8 0.5 ns 11 ± 11 16 0.8
Polychaete larvae 31 ± 33 8 2.8 33 ± 23 8 2.1 ns 32 ± 28 16 2.4
Ostracods 17 ± 37 8 1.5 9 ± 6 8 0.5 ns 13 ± 26 16 0.9
Adult copepods and
copepodites
521 ± 379 8 47.5 1,046 ± 622 8 65.0 * 784 ± 567 16 57.9
Other crustaceans 14 ± 19 8 1.2 13 ± 11 8 0.7 ns 11 ± 13 16 0.8
Nauplii 438 ± 169 8 40.0 428 ± 271 8 26.6 ns 433 ± 218 16 32.0
Chaetognaths 14 ± 13 8 1.3 15 ± 7 8 0.9 ns 15 ± 10 16 1.1
Echinoderma larvae 7 ± 10 8 0.6 2 ± 3 8 0.1 ns 4 ± 7 16 0.3
Larvaceans 41 ± 21 8 3.8 56 ± 24 8 3.4 ns 48 ± 23 16 3.6
[335 Hydrozoans Ra 10 ± 17 8 1.9 19 ± 8 8 1.5 * 13 ± 12 16 1.7
Polychaete larvae PRb 2 ± 2 8 0.4 21 ± 13 8 2.0 ** 11 ± 13 16 1.5
Ostracods Rb,c,d 2 ± 1 8 1.6 11 ± 10 8 0.6 ** 6 ± 9 16 0.8
Adult copepods and
copepodites
PR 310 ± 339 8 58.8 680 ± 461 8 65.4 ** 495 ± 435 16 63.5
Amphipods (Gammaridae) Rb,d 0.1 ± 0.2 8 0.01 9 ± 16 8 0.9 ** 4 ± 12 16 0.6
Other crustaceans (mainly
of crab zoea)
PRd 7 ± 20 8 1.4 35 ± 23 8 3.4 ** 21 ± 25 16 2.7
Chaetognaths Pc,d 47 ± 49 8 9.8 101 ± 52 8 9.4 * 74 ± 56 16 9.5
Echinoderma larvae Pc,d 74 ± 27 8 14.1 59 ± 32 8 5.7 ns 66 ± 30 16 8.5
Larvaceans Pc,d 54 ± 69 8 11.9 120 ± 85 8 11.0 * 87 ± 82 16 11.2
n means number of samples. P values pertain to the abundance differences between day and night (* P \ 0.05; ** P \ 0.01; ns, not
significant). Zooplankton origin indicates whether the zooplankton are pelagic (P), reef associated (R), or both (PR) based on
literatures (see aMcFarland et al. 1999; bJacoby and Greenwood 1988; cSorokin 1993; dHeidelberg et al. 2004)
Aquat Ecol (2009) 43:965–975 971
123
Table 2 Average abundance and percent composition (%) of common copepods taxa in different size-fractions at Tioman Island
Size-class (lm) Copepod taxa Origin Abundance (inds. m-3)
Day n % Night n % P Total n %
100–200 Calanoid
Paracalanus spp. 5 ± 8 8 1.0 12 ± 7 8 1.1 * 8 ± 8 16 1.1
Copepodites 48 ± 29 8 9.0 110 ± 64 8 10.9 * 79 ± 58 16 10.2
Cyclopoid
Oithonidae spp. 22 ± 24 8 4.1 59 ± 51 8 5.8 ns 40 ± 43 16 5.2
Copepodites 202 ± 210 8 37.6 401 ± 255 8 39.4 * 301 ± 248 16 38.8
Harpacticoid
Microsetella norvegica 171 ± 85 8 31.8 317 ± 191 8 31.2 ns 244 ± 161 16 31.4
Copepodites 29 ± 13 8 5.3 28 ± 26 8 2.7 ns 28 ± 20 16 3.6
Poecilostomatoid
Saphirella-like copepods na 8 8 ± 11 8 0.8 * 4 ± 9 16 0.5
Copepodites 54 ± 44 8 10.1 81 ± 46 8 7.9 ns 67 ± 46 16 8.7
200–335 Calanoid
Paracalanus spp. 29 ± 28 8 5.1 105 ± 72 8 8.7 * 67 ± 66 16 7.6
Copepodites 156 ± 132 8 27.8 343 ± 246 8 28.5 ns 249 ± 214 16 28.3
Cyclopoid
Oithonidae spp. 52 ± 75 8 9.2 153 ± 108 8 12.7 * 102 ± 104 16 11.6
Copepodites 176 ± 151 8 31.4 377 ± 246 8 31.4 * 277 ± 223 16 31.4
Harpacticoid
Microsetella norvegica 60 ± 51 8 10.7 76 ± 26 8 6.4 ns 68 ± 40 16 7.7
Euterpina actifrons 11 ± 12 8 2.0 26 ± 20 8 2.2 ns 19 ± 18 16 2.1
Copepodites 18 ± 12 8 3.2 27 ± 28 8 2.3 ns 23 ± 21 16 2.6
Poecilostomatoid
Oncaea conifera 1 ± 3 8 0.2 5 ± 5 8 0.4 * 3 ± 4 16 0.3
Corycaeus spp. 12 ± 9 8 2.2 7 ± 5 8 0.6 ns 10 ± 7 16 1.1
Furranula gibbla 6 ± 7 8 1.1 6 ± 5 8 0.5 ns 6 ± 6 16 0.7
Copepodites 38 ± 21 8 6.7 72 ± 51 8 6.0 ns 55 ± 41 16 6.2
[335 Calanoid
Acartia spp. Pa,b 0.3 ± 0 8 0.1 33 ± 35 8 4.2 ** 17 ± 29 16 3.0
Canthocalanus pauper Pa 1 ± 1 8 0.4 2 ± 1 8 0.2 ns 1 ± 1 16 0.2
Calocalanus spp. Pb 1 ± 1 8 0.2 2 ± 3 8 0.3 ns 1 ± 2 16 0.3
Clausocalanus spp. Pc na 8 4 ± 9 8 0.5 ns 2 ± 7 16 0.3
Centropages spp. Pc na 8 8 ± 8 8 1.0 ** 4 ± 7 16 0.7
Subeucalanus spp. Pa 0.2 ± 0 8 0.1 7 ± 7 8 1.0 * 4 ± 6 16 0.7
Paracalanus spp. Pa,b 20 ± 12 8 6.0 71 ± 59 8 9.1 * 45 ± 49 16 8.2
Acrocalanus spp. Pa 3 ± 2 8 1.0 6 ± 4 8 0.7 ns 4 ± 4 16 0.8
Calanopia spp. Pa,b 0.2 ± 1 8 0.1 3 ± 2 8 0.4 ** 2 ± 2 16 0.3
Labidocera minuta Pc na 8 2 ± 2 8 0.2 ** 1 ± 2 16 0.2
Pseudodiaptomus spp. Ra,d na 8 2 ± 3 8 0.3 ** 1 ± 3 16 0.2
Temora dicaudata Pb 0.3 ± 0 8 0.1 1 ± 1 8 0.2 * 1 ± 1 16 0.2
Tortanus spp. Pc na 8 1 ± 1 8 0.2 ns 1 ± 1 16 0.1
Copepodites PR 84 ± 115 8 25.1 231 ± 142 8 29.6 ** 157 ± 146 16 28.2
972 Aquat Ecol (2009) 43:965–975
123
associated and pelagic zooplankton based on litera-
ture (Jacoby and Greenwood 1988; Sorokin 1993;
Heidelberg et al. 2004; Shimode and Shirayama
2004), and a study of offshore, pelagic copepod
samples near the study site (Yoshida unpublished
data). Since the large fraction demonstrated clear
nocturnal increase in both biomass and abundance,
we characterized the origin of the zooplankton in this
fraction (Tables 1 and 2). Using our classifications,
about 64.0% of the zooplankton was pelagic in origin,
and 6.0% was reef associated. However, if we assume
the calanoid copepodites as pelagic in origin because
they included mainly of Acartia and Paracalanus, the
proportion of the pelagic zooplankton would exceed
80%. Therefore, the pelagic zooplankton obtained in
our study site had a much higher proportion.
Discussion
This study describes the temporal variation of size-
fractionated zooplankton communities on a diel basis
at 3-h intervals in a coral reef of Malaysia. We
obtained the organic carbon biomass of zooplankton
by subtracting the value of the organic carbon
contents of the detritus/larger phytoplankton from
the organic carbon contents of total seston mass. The
detritus/larger phytoplankton was sorted from the
formalin fixed samples in this study. The organic
carbon content of zooplankton samples fixed in
formalin is known to decrease slightly over time
(Omori 1978), and the same effect may be true for on
the detrital and larger phytoplankton samples. How-
ever, we did not take into account the carbon loss in
this study, since we do not know the extent of carbon
decrease for the detrital and larger phytoplankton.
The diel variation in total biomass of zooplankton
([100 lm) is mainly due to the largest size-fraction
([335 lm), particularly copepodites of both calanoid
(mostly Paracalanus spp. and Acartia spp.) and
Oithonidae, larvaceans, and chaetognaths. However,
comparing with the coarse fraction, the diel variations
in the smaller fractions (100–200 and 200–335 lm)
appear to be obscure.
The increase in total biomass at night was
caused mainly by the larger-sized zooplankton,
which increased 2.7 times in biomass but only 2.1
times in density. This means that relatively heavier
Table 2 Average abundance and percent composition (%) of common copepods taxa in different size-fractions at Tioman Island
Size-class (lm) Copepod taxa Origin Abundance (inds. m-3)
Day n % Night n % P Total n %
Cyclopoid
Oithonidae spp. PRa,b 20 ± 26 8 5.9 64 ± 68 8 7.8 ns 42 ± 55 16 7.5
Copepodites PRa,b 63 ± 117 8 18.9 109 ± 140 8 14.0 ns 86 ± 127 16 15.4
Harpacticoid
Microsetella norvegica Pc 55 ± 50 8 16.5 96 ± 57 8 12.4 ns 75 ± 56 16 13.5
Macrosetella gracilis Pc 1 ± 1 8 0.4 6 ± 5 8 0.8 * 4 ± 4 16 0.7
Euterpina actifrons Pc 8 ± 11 8 2.4 18 ± 13 8 2.4 ns 13 ± 13 16 2.4
Benthic harpacticoids Rd 2 ± 3 8 0.6 1 ± 1 8 0.1 ns 1 ± 2 16 0.3
Copepodites PR 12 ± 9 8 3.6 20 ± 9 8 2.6 ns 16 ± 10 16 2.9
Poecilostomatoid
Oncaea conifera Pb,c 3 ± 5 8 0.9 3 ± 4 8 0.3 ns 3 ± 4 16 0.5
Corycaeus spp. Pc 30 ± 30 8 9.1 43 ± 30 8 5.6 ns 37 ± 30 16 6.6
Farranula gibbla Pc 15 ± 11 8 4.6 28 ± 20 8 3.6 ns 22 ± 17 16 3.9
Saphirella-like copepods R? 0.4 ± 1 8 0.1 1 ± 1 8 0.1 ns 1 ± 1 16 0.1
Copepodites PR 12 ± 16 8 3.6 16 ± 18 8 2.0 ns 14 ± 16 16 2.5
na means no appearance; n means number of samples. P values pertain to the abundance differences between day and night
(* P \ 0.05; ** P \ 0.01; ns, not significant). Copepods origin indicates whether the copepods are pelagic (P), reef associated (R), or
both (PR) based on literatures (see aJacoby and Greenwood 1988; bHeidelberg et al. 2004; cShimode and Shirayama 2004; dYoshida
unpublished)
Aquat Ecol (2009) 43:965–975 973
123
zooplankton appeared during the night. We can
roughly derive the mean weight of animal at night
and day by dividing the mean biomass by mean
density. Thus, we derived the individual biomass for
animals to be 2.18 lg C during day and 2.87 lg C at
night. In the smaller fractions, there was barely any
difference between day and night in the mean
individual weight. The weights per animal for mid
and small fractions were 0.59 lg C (day) and 0.57 lg
C (night) and 0.27 lg C (day) and 0.29 lg C (night),
respectively. The nocturnal appearance of larger
zooplankton such as amphipods, ostracods, and crab
zoea may have increased the mean weight of the large
fraction. For example, the zooplankton mean indi-
vidual weights of the large fraction in Tioman Island
were 6 lg C/amphipod, 5 lg C/ostracod, and 4 lg C/
crab zoea (Nakajima et al. unpublished). Thus, the
nocturnal increase of these larger zooplankton caused
the significant increase in zooplankton biomass at
night.
Coral-reef zooplankton have been reported to show
their peak abundance in the early hours of night; e.g.,
zooplankton was most abundant from about 1800–
2200 h at Laurel Reef in Puerto Rico (Glynn 1973).
From the U.S. Virgin Islands, zooplankton density at
the surface water rose steeply within just 30 min after
sunset and peaked one or a few hours later (McFarland
et al. 1999). At Helix Reef in the Great Barrier Reef,
the total zooplankton catch was most abundant from
2100 to 2200 h (Carleton et al. 2001). If our zoo-
plankton show their peak early in the night, because
the time of sunset is around 1900 h in the study site,
they must peak at around 2100 h. However, unlike
previous reports, both the maximum biomass and
abundance of our total zooplankton ([100 lm)
occurred much later in the night (0300 h). The
nocturnal increase in the total biomass was highly
associated with a corresponding increase in the large
fraction of which was mostly pelagic in origin. These
pelagic zooplankters undergo diel migration offshore
and may have been advected inshore with the current
or tide because of their migration to the surface water
in the nearby offshore water at night. Indeed, our
study site is a fringing reef where offshore influence is
large. Therefore, the increase during the late night
(0300 h) could be associated with the entrance of
offshore water. On the other hand, reef-associated
zooplankters (i.e., large amphipods, crab zoea, poly-
chaeta, and Pseudodiaptomus spp.) showed an early
night peak in this study (2100 h). Yahel et al. (2005a)
also reported that the zooplankton which showed
intense increase early in the night in the Gulf of Aqaba
was largely of the reef-associated origin. The reef-
associated zooplankton is likely to show its peak
abundance early in the night; this zooplankton lives
in or on the benthic substrate during daytime and
apparently needs to migrate upward into the water
column at early hours of night, i.e., before the
benthic zooplanktivores such as corals become
active and fully expand their tentacles. Accordingly,
the coral reefs, where the zooplankton show abrupt
increase early in the night, will be dominated by
reef-associated zooplankton. Also, coral reefs where
the zooplankton show a peak later in the night may
be dominated by pelagic species, similar to what we
observed in our study site. It is very likely that
alternating peaks of the reef-associated and pelagic
species overlap each other at night to produce
constant increase in abundances throughout the night
with no clear-cut peaks.
Conclusions
Our study on the diel variations in coral-reef
zooplankton from 3-h intervals reveals that nocturnal
peak in the later hours of night (0300 h) is due to the
large-sized zooplankton. These zooplankters mostly
consist of pelagic species that undergo diel migration
offshore, and these pelagic species determine the
peak later in the night. However, the 48-h sampling
period includes only two nights in the present study,
and investigations in other seasons are also needed
to explain more clearly the temporal variation of
coral-reef zooplankton.
Acknowledgments The research project ‘‘Studies of coral
reef ecosystem biodiversity in the Malaysian waters’’ was
supported by the Japan Society for the Promotion of Science
(JSPS) and Vice Chancellor’s Council (VCC) in Malaysia. We
thank Dr. M. Terazaki, Sanyo Techno Marine Inc., for his
assistance and financial support. We are grateful to F. L. Alice
Ho, M. Y. Ng, and S. P. Kok for help in field sampling and
W. Kinjyo, A. Takamoto, and A. Nakayama for help in
microscopic analysis and providing maps of the study area. Our
thanks are also due to Dr. S. Shimode, Ocean Research
Institute, The University of Tokyo for valuable suggestions and
F. L. Wee, R. M. Yana, and members of Marine Park Section,
Department of Fisheries, Malaysia. We also would like to
express our appreciation to Dr. R. D. Gulati, Netherland
Institute of Ecology for polishing the manuscript. This research
974 Aquat Ecol (2009) 43:965–975
123
was partially funded by JSPS and Universiti Kebangsaan
Malaysia Research Grant UKM-GUP-ASPL-08-04-231.
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