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: rnakajim@soka.ac.jp

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

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(d)

0

2000

4000

6000

8000

0

1000

2000

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>335 µm

200-335 µm

100-200 µm

Bio

mas

s (m

g C

m-3

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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

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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

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0

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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

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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

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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

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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

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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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