• Coral reef;
  • production;
  • trophic structure;
  • zooplankton


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References

Quantitative research on composition, biomass and production rates of zooplankton community is crucial to understand the trophic structure in coral reef pelagic ecosystems. In the present study, micro- (35–100 μm) and net- (>100 μm) metazooplankton were investigated in a fringing coral reef at Tioman Island of Malaysia. Sampling was done during the day and night in August and October 2004, and February and June 2005. The mean biomass of total metazooplankton (i.e. micro + net) was 3.42 ± 0.64 mg C·m−3, ranging from 2.32 ± 0.75 mg C·m−3 in October to 3.26 ± 1.77 mg C·m−3 in August. The net-zooplankton biomass exhibited a nocturnal increase from daytime at 131–264% due to the addition of both pelagic and reef-associated zooplankton into the water column. The estimated daily production rates of the total metazooplankton community were on average 1.80 ± 0.57 mg C·m−3·day−1, but this increased to 2.51 ± 1.06 mg C·m−3·day−1 if house production of larvaceans was taken into account. Of the total production rate, the secondary and tertiary production rates were 2.20 ± 1.03 and 0.30 ± 0.06 mg C·m−3·day−1, respectively. We estimated the food requirements of zooplankton in order to examine the trophic structure of the pelagic ecosystem. The secondary production may not be satisfied by phytoplankton alone in the study area and the shortfall may be supplied by other organic sources such as detritus.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References

Although coral reefs account for only 0.1% of the world's ocean, their fish production supports c. 10% of the world's fish stock (Pauly et al. 2002). Coral reef fisheries are an important protein source for people in many developing countries, as globally 75% of coral reefs occur in developing countries where the human population is still increasing rapidly (Pauly et al. 2002). Since larvae and juvenile of many species of reef fishes grow by feeding on zooplankton (e.g. Sampey et al. 2007), it is important to determine the biomass and production of zooplankton as this is fundamental information for sustainable fishery management (Huo et al. 2012). In addition to fish, zooplankton are an important energy source for many reef benthic animals including scleractinian corals, hydroids, zantharians, bryozoans and ascidians (reviewed by Sorokin 1995). Therefore, zooplankton production is of major interest to determine the ecological dynamics of reef ecosystems.

Understanding ecological dynamics requires the investigation of material or energy flow from lower to higher trophic levels. For this, it is crucial to estimate the production rates of populations at different trophic levels and the transfer efficiency between adjacent trophic levels (Uye et al. 1987). Most investigations on production rate of either zooplankton or copepod community have been conducted in temperate regions (e.g. Allan et al. 1976; Joh & Uno 1983; Koga 1986; Uye et al. 1987, 1996, 2000; Uye & Shimazu 1997; Uye & Liang 1998; Shinada et al. 2001; Ara & Hiromi 2007, 2009; Huo et al. 2012). Relatively fewer studies have been done in tropical and subtropical regions (e.g. Newbury & Bartholomew 1976; Le Borgne 1982; Chisholm & Roff 1990a; Webber & Roff 1995; Goswami & Padmavati 1996; Hopcroft et al. 1998a; Lugomela et al. 2001; McKinnon & Duggan 2003; Ara 2004). Although coral reefs are one of the most productive ecosystems in the world, production estimates of zooplankton community are still comparatively sparse, making it difficult to understand the ecological dynamics of this ecosystem.

To date, the community productions of reef zooplankton or of copepods have been estimated in lagoons of the Great Barrier Reef (GBR) (McKinnon et al. 2005; Sorokin & Sorokin 2010), French Polynesia (Le Borgne et al. 1989, 1997; Sakka et al. 2002), Lakshadweep (Goswami 1983) and Okinawa (Go et al. 1997; Hayashibara et al. 2002), but studies in Southeast Asia are lacking. Southeast Asia possesses the most biologically diverse coral reefs in the world (Burke et al. 2002) and it is recognized as a major coral reef region on the planet. In the past, much biological research has been done on fish, plankton and benthos in various coral reefs in Southeast Asia (reviewed by Nishida et al. 2011) but no attempts have been made to estimate zooplankton production. Currently, over 80% of coral reefs in Southeast Asia are threatened by continued overexploitation of living marine resources and coastal pollution, causing a critical decline in fish resources in this area (Hoegh-Gulderg et al. 2009). Coral reef loss in Southeast Asia may lead to an 80% decline in food production, imperilling 100 million people (Hoegh-Gulderg et al. 2009). Understanding the biomass and production of zooplankton in Southeast Asia will facilitate more informed ecosystem-level management on fish resources in these areas.

Coral reefs are often characterized by oligotrophic environments due to low input of new nutrients and active nutrient recycling, and this is also true for the adjacent oceanic waters (Hatcher & Frith 1985). Because of a low concentration of inorganic nutrients, primary production of phytoplankton in these ecosystems is generally low, and the phytoplankton assemblage is dominated by pico-sized cells (<2–3 μm) (Sakka et al. 2002). For instance, in many lagoons of the GBR, Okinawa, French Polynesia and in Malaysia, picophytoplankton account for >50% of the chlorophyll standing stock and primary production (e.g. Furnas et al. 1990; Ayukai 1992; Tada et al. 2003; Nakajima et al. 2011). These tiny phytoplankton cells may not be readily utilized by many of net-zooplankton because they are too small to be captured (Roman et al. 1990). Yet coral reefs possess a great abundance of zooplankton compared with adjacent oceanic waters (Russell 1934; Motoda 1938; Gerber & Marshall 1974; Carleton & Doherty 1998). Roman et al. (1990) reported in Davies Reef, GBR, that the low availability of phytoplankton stocks did not meet the respiratory demands of the net-zooplankton community and suggested that the contribution of other organic available particles (detritus) was important. Likewise Le Borgne et al. (1997) and Sakka et al. (2002) acknowledged in French Polynesia that detritus is an important carbon source for zooplankton that compensates for the low availability of phytoplankton stock. Is the same true for coral reefs in Southeast Asia?

In the present study, we estimated the production rate of zooplankton community at a coral reef in Malaysia, focusing on the following questions:

  1. How great is the zooplankton production in Malaysian coral reef waters?
  2. Is the production rate high or low, compared with other reef ecosystems?
  3. Can the biomass and production of zooplankton community be sustained by the low phytoplankton biomass in coral reef ecosystems?

Study Area

  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References

This study was carried out at a fringing coral reef at Tioman Island (2°50′00″ N, 104°10′00″ E), off the east coast of Peninsular Malaysia. The mean depth of the reef was 3.3 m with a maximum depth of 8.9 m. The bottom comprised fine sand from the shore towards the open water, followed by rocky bottom and then sandy bottom. The reef flat spreads beyond the sandy bottom region, ending in a gradual sandy slope. There is no distinct reef crest separating the open sea and back reef zones, allowing water from the open sea freely to enter the nearshore area. There are neither seagrass beds nor mangroves near to the reef. The coral community of the reef had a live coverage of 35% with a dominance of Acropora spp. (Toda et al. 2007). Sampling was done during four study periods; 22–24 August 2004, 1–3 October 2004, 25–27 February, and 2–4 June 2005 at a jetty in the reef (depth: 8.3–8.9 m). Although there is little coral directly under the jetty, coral cover in the immediate surroundings is high and thus the sampling site is representative of coral reef ecosystems, assuming the water is well homogenized in the reef. During the study periods, the sea conditions at the sampling site were calm with no strong wind or rainfall, except on the night of 3 October, when heavy rain and strong winds were observed. The water temperature (average ± SD) ranged from 27.5 ± 0.3 °C in August to 29.0 ± 0.4 °C in June (overall average = 28.6 ± 0.7 °C); salinity ranged from 33.4 ± 0.6 in October to 35.3 ± 0.3 in June (overall average = 34.0 ± 0.8). The annual mean of daily integrated surface radiation in the study site was 355.7 ± 73.0 cal·cm−2·day−1. The particulate organic carbon (POC) concentration in the water column ranged from 166.9 ± 36.6 mg C·m−3 in August to 275.6 ± 43.3 mg C·m−3 in June (overall mean = 188.9 ± 65.7 mg C·m−3; Nakajima et al. 2011).


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References


We collected net-zooplankton during the day (09.00, 12.00, 15.00, and 18.00 h) and night (21.00, 00.00, 03.00, and 06.00 h) for two consecutive days and nights in each study period. Therefore, 16 samples (n) were obtained in each sampling period. The timing of sunrise and sunset was 07.00 h and 19.12 h in August, 06.50 h and 18.55 h in October, 07.14 h and 19.18 h in February, and 06.53 h and 19.10 h in June, respectively. The zooplankton was sampled each time by pooling five vertical tows of a plankton net (mesh size, 100 μm; diameter, 30 cm; length, 100 cm) equipped with a flowmeter (Rigo) from 1 m above the sea bottom to the surface. The pooled samples were brought back to the laboratory within 5 min, and fixed with buffered formalin to a final concentration of 5% for subsequent microscopic observation.

Prior to the net-zooplankton collection, seawater was sampled by a 10-l Niskin bottle at 1 m depth below the surface and 1 m above the sea bottom for the collection of micro-zooplankton that pass through the 100-μm plankton net, and for the measurement of chlorophyll-a (Chl-a) concentration. The water from the two depths were pre-filtered through a 100-μm-mesh screen to remove net-zooplankton and later combined. The combined water sample (20 l) was brought back to the laboratory along with the net sample. A subsample (18 l) of the pre-filtered water was filtered through a 35-μm-mesh screen, and the micro-zooplankton retained on the mesh screen (i.e. 35–100 μm in size) was fixed with buffered formalin to a final concentration of 2% and stored at 5 °C until observation. A subsample (2 l) for Chl-a analysis was filtered onto a GF/F filter (Whatman), then immersed in N, N-dimethylformamide (DMF) and stored at –20 °C until analysis (Suzuki & Ishimaru 1990). Chl-a concentrations were determined using a fluorometer (Turner Designs 10-AU) according to Holm-Hansen et al. (1965).

Zooplankton biomass estimates

Zooplankton was identified to the lowest taxonomic levels possible and counted under a stereomicroscope. For net-collected samples (>100 μm), large zooplankton and rare species (e.g. mysids and larval decapods) were first counted and sorted out, and the remaining then split (1/1–1/32) and all zooplankton characterized and enumerated. At least 300 zooplankton were enumerated in each sample. Copepods were identified to genus level whenever possible. For the micro-zooplankton (35–100 μm), the samples were split (1/4) and all zooplankton characterized and enumerated. Because we used mesh screens to obtain specimens of micro-zooplankton which may have caused serious damage to relatively soft-bodied protozoans, coupled with a potential loss of their individual numbers due to formalin fixation (Dale & Burkill 1982), we did not include protozooplankton (i.e. naked ciliates, tintinnids and dinoflagellates) in the analysis of micro-zooplankton. Copepods in the 35–100-μm fraction were categorized into nauplii or copepodites, with copepodites being identified to family or genus level.

The length of an appropriate body portion, e.g. prosome length for copepods, trunk length for larvaceans, was measured using either an eyepiece micrometer or a digital micrometer following Uye (1982) and Hirota (1986). The length measurements were converted to carbon weight of zooplankton individuals (CW, mg C) using previously reported length–weight regression equations (Table 1). The biomass (B, mg C·m−3) of a given taxonomic group was estimated based on its abundance (A, ind. m−3) and individual carbon weight (CW, mg C): B = A × CW. Reported length–weight regressions of many species that occur at the sampling site are not available, but we used regressions according to similarity in genus or shape. Regressions for copepods of the same genus were employed whenever possible. Regressions established in tropical seas were also employed as much as possible. For regressions that estimate copepod dry weight (DW) on the basis of body length (i.e. Chisholm & Roff 1990b; Webber & Roff 1995), the carbon content was assumed to be 47% of DW (Hirota 1981). For regressions that estimate copepod ash-free dry weight (AFDW) (Hopcroft et al. 1998a), the results were converted to DW assuming AFDW to be 89% of DW (Båmstedt 1986), and then converted to C weight. Likewise, the C content of veligers and larvaceans were assumed to be 17.7 and 44.2% of their DW, respectively (Hirota 1986).

Table 1. Length–weight regression equations used for biomass calculation of different zooplankton taxa. Log, common logarithm (log10); ln, natural logarithm (loge); n, the number of specimens used for building regression; r2, coefficient of determination for regression; NA, not available
taxonomic groupequationnr2source
  1. CW = carbon weight (μg) DW = dry weight (μg); AFDW = ash free dry weight (μg); BL = full body length; D = body diameter; PL = prosome length; SL = shell length; TL = trunk length.

 polychaetesln CW = 1.46 × ln BL (mm) + 1.03150.73Heidelberg et al. (2010)
 amphipods (Hyperids)ln CW = 1.46 × ln BL (mm) + 1.03160.73Heidelberg et al. (2010)
 cirriped naupliilog CW = 2.65 × log BL (μm) − 6.9025NA0.93Hirota (1986)
 cirriped cyprislog CW = 3.0 × log BL (μm) − 8.6439NANAJapan Fisheries Agency (1987)
Acartialn DW = 3.09 × ln PL (μm) − 19.19220.92Chisholm & Roff (1990b)
Calanopialn DW = 2.67 × ln PL (μm) − 15.47200.98Chisholm & Roff (1990b)
Undinulaln DW = 3.65 × ln PL (μm) − 22.89300.96Chisholm & Roff (1990b)
Candacialn DW = 3.38 × ln PL (μm) − 20.48660.82Webber & Roff (1995)
Centropagesln CW = 3.82 × ln PL (μm) − 24.581720.87Satapoomin (1999)
Paracalanusln DW = 3.25 × ln PL (μm) − 19.65270.96Chisholm & Roff (1990b)
Clausocalanusln DW = 3.25 × ln PL (μm) − 19.65270.94Chisholm & Roff (1990b)
Temoraln DW = 3.34 × ln PL (μm) − 19.59Chisholm & Roff (1990b)
Acrocalanusln CW = 2.26 × ln PL (μm) − 13.851140.76Satapoomin (1999)
other calanoidsln DW = 2.74 × ln PL (μm) − 16.411750.88Chisholm & Roff (1990b)
Oithona simplexlog AFDW = 3.47 × log PL (μm) − 8.76~150NAHopcroft et al. (1998a)
other Oithonidaelog AFDW = 3.16 × log PL (μm) − 8.18~150NAHopcroft et al. (1998a)
Macrosetellaln CW = 1.59 × ln BL (μm) − 10.92550.51Satapoomin (1999)
Microsetellaln CW = 1.15 × ln BL (μm) − 7.791110.26Satapoomin (1999)
other harpacticoidsln CW = 1.15 × ln BL (μm) − 7.79Satapoomin (1999)
Corycaeidaelog AFDW = 2.80 × log PL (μm) − 7.17~150NAHopcroft et al. (1998a)
Oncaealn DW = 2.10 × ln PL (μm) − 11.63420.79Webber & Roff (1995)
other poecilostomatoidsln DW = 1.96 × ln PL (μm) − 11.64600.85Chisholm & Roff (1990b)
nauplii (all species)log CW = 2.94 × log BL (μm) − 7.82NANAUye et al. (1996)
cumaceansln CW = 1.46 × ln BL (mm) + 1.03130.73Heidelberg et al. (2010)
luciferln CW = 1.46 × ln BL (mm) + 1.03Heidelberg et al. (2010)
decapod larvaeln CW = 1.46 × ln BL (mm) + 1.03340.73Heidelberg et al. (2010)
isopods (Flabellifera)ln CW = 1.46 × ln BL (mm) + 1.03330.73Heidelberg et al. (2010)
mysidsln CW = 1.46 × ln BL (mm) + 1.03190.73Heidelberg et al. (2010)
ostracodsln CW = 1.46 × ln BL (mm) + 1.0340.73Heidelberg et al. (2010)
chaetognathslog CW = 2.79 × log BL (mm) − 0.93NA0.98Hirota (1986)
larvaceanslog DW = 2.47 × log TL (μm) − 6.10280.97Hopcroft et al. (1998b)
cnidarianslog CW = 2.75 × log D (μm) − 8.71NA0.99Hirota (1986)
bivalve/gastropod larvaeDW = 6.27 × 10−7 × SL (μm)2.60NANASprung (1984)

Since the carbon content of each individual is estimated based on its size, variations due to shrinkage of specimens with formalin preservation may make biomass estimates subject to some underestimation (Steedman 1976). The relatively soft-bodied organisms are likely to shrink considerably upon preservation, although this does not significantly affect the body length of copepods including their nauplii (Durbin & Durbin 1978; Kuhlmann et al. 1982; Põllupũũ 2007), presumably due to the relatively rigid body structure (Clark et al. 2001), and this may be true for other crustaceans. We therefore considered the reported values of shrinkage for the soft-bodied organisms; i.e. 5% length shrinkage in chaetognaths (Szyper 1976), 13% trunk length shrinkage in larvaceans (Scheinberg et al. 2005), 20% body length shrinkage in cnidarians (Wang et al. 1995) and 30% shrinkage in polychaete larvae (White & Roman 1992).

The difference between day and night density and biomass of zooplankton for each size-fraction was determined using Student's t-test. A difference of P < 0.05 was considered significant.

Zooplankton production estimates

The production rate (P, mg C·m−3·day−1) of a given taxonomic group was estimated based on its biomass (B, mg C·m−3) and specific growth rate (G, day−1): P = B × G. The specific growth rates (G, day−1) of copepods, other crustaceans, chaetognaths, cnidarians, larvaceans and polychaete larvae were estimated from regression equations proposed by Hirst & Lampit (1998) and Hirst et al. (2003) (Table 2). For the remaining taxa (e.g. bivalve larvae), the production rate (P, mg C·m−3·day−1) was estimated by the equation given by Ikeda & Motoda (1978): P = R × As/(As – Gr), where R is respiration rate (μl O2 ind.−1·h−1), and As (assimilation efficiency) and Gr (gross growth efficiency) were assumed to be 0.7 and 0.3, respectively (Ikeda & Motoda 1978). R was estimated using the multiple regression model proposed by Ikeda (1985): ln R = 0.5254 + 0.8354 ln CW + 0.0601T, where T and CW are temperature (°C) and carbon weight (mg C) of individual, respectively. Respired oxygen was converted to carbon using a respiratory quotient of 0.97 for marine zooplankton (Gnaiger 1983), and then to daily rates (24-h) assuming constant respiration rates.

Table 2. Regression equations for estimating instantaneous growth rate. Log, common logarithm (log10); ln, natural logarithm (loge); n, number of data used for establishing equation; r2, coefficient of determination for regression; NA, not available
  1. G = specific growth rate (day−1); T = temperature (°C); CW = body carbon weight (μg).

  2. a

    Copepods which shed eggs freely, i.e. calanoids observed in the present study except for Clausocalanus and Pseudodiaptoms.

  3. b

    Copepods which carry their eggs externally on the body, i.e. Clausocalanus, Pseudodiaptoms, all cyclopoids, all harpaticoids and all poecilostomatoids observed in the present study.

  4. c

    Applied the equation of copepod juveniles for broadcast and sac-spawners combined.

polychaeteslog G = −0.630 + 0.409 log CW120.514Hirst et al. (2003)
adultlog G = 0.0232 T − 0.285 log CW − 1.1961,4760.22Hirst et al. (2003)
copepoditeslog G = 0.0352 T − 0.233 log CW − 1.2301800.7Hirst et al. (2003)
adultlog G = 0.0223T + 0.177 log CW − 1.6444010.179Hirst et al. (2003)
copepoditeslog G = −1.545 + 0.0408 T790.549Hirst et al. (2003)
naupliiclog G = 0.0370T − 0.0795 log CW − 1.3840NA0.347Hirst & Lampit (1998)
other crustaceanslog G = 0.0263T − 0.327 log CW − 0.9192390.447Hirst et al. (2003)
chaetognathslog G = −1.851 + 0.0367 T840.323Hirst et al. (2003)
cnidarianslog G = −0.423 − 0.219 log CW730.38Hirst et al. (2003)
larvaceanslog G = −0.495 + 0.0285 T910.566Hirst et al. (2003)

The equation for production rate of larvaceans that we used in this study (Hirst et al. 2003) does not take into consideration the production of their houses, which are discarded and re-secreted frequently (Alldredge 1976; Uye & Ichino 1995; Tomita et al. 1999). Production rate estimates would increase considerably if we account for the production of houses (Hopcroft & Roff 1998). The carbon content of newly secreted houses has been estimated as 5.3–14.1% (average 9.7%) of body carbon and the rate of house production has been estimated to 24–27 houses per day at 26–29 °C for various Oikopleuridae species (Sato et al. 2003). We therefore accounted for the production of houses assuming the carbon content of newly produced house is 9.7% of body carbon and at 27 houses per day considering the average temperature of 28.6 °C at the study site. The results were compared with those obtained without taking into account the house production.

Trophic structure

To demonstrate the food chain structure, averages of phytoplankton and zooplankton biomass and of zooplankton production rate were compared. The carbon biomass of phytoplankton was estimated from Chl-a concentration using a conversion factor of 50 (Charpy-Roubaud et al. 1989). The C:Chl-a ratio varies from about 12 to >200 in phytoplankton cultures (reviewed by Taylor et al. 1997), and the choice of these factors may affect the relative importance of phytoplankton C biomass, compared with the zooplankton. The ratios are highly regulated in response to irradiance, nutrient availability and temperature. It is minimal at high temperature (25–30 °C) and low irradiances (<20 μmol photons·m−2·s−1) under nutrient-replete conditions and increases at high irradiances, especially at low temperature and under nutrient-limiting conditions (Taylor et al. 1997). In this study, we used a C:Chl-a ratio of 50, as our coral reef experiences high irradiances in an oligotrophic environment at high temperatures. A C:Chl-a ratio of 50 has often been used for calculating phytoplankton C biomass in other coral reefs (Charpy-Roubaud et al. 1989).

Although primary production of phytoplankton was not measured in this study, it was roughly estimated from chlorophyll and light data. The primary production of phytoplankton (P, g C·m−2·day−1) was estimated using a regression proposed by Ryther & Yentsch (1957) as: P = R/k × C × 3.7, where R is relative photosynthesis for the appropriate value of surface radiation (m−3·day−1), k is the extinction coefficient (m−2), and C is phytoplankton biomass (g Chl-a·m−3).

Secondary and tertiary productions were calculated separately on the basis of the feeding habits (i.e. herbivorous, omnivorous and carnivorous) of each group based on the literature (Fulton 1982; Ohtsuka & Nishida 1997; Uye & Shimazu 1997; Turner 2004; Hansen et al. 2010; Table 3). The production by typical herbivores and carnivores was assigned to secondary and tertiary production, respectively. The production by omnivores was halved and added to each production following Uye et al. (1987). To determine the potential carbon flow from prey organisms to predators, the amount of carbon required by the consumers to support their estimated production rate was calculated using a gross growth efficiency of 0.3 for metazoan zooplankton (Ikeda & Motoda 1978). Micro-metazooplankton was assumed to be herbivorous in this study (Uye et al. 2000).

Table 3. Zooplankton taxa with different feeding habits based on the literature
Macrosetellapolychaete larvaechaetognaths
Microsetella amphipods
Clytemnestra ostracods (myodocopids)
copepod nauplii isopods
non-copepods hydrozoans
larvaceans decapods
bivalve larvae  
gastropod larvae  


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References

Primary producer

Chl-a concentration in the water column varied from 0.20 ± 0.06 mg Chl-a·m−3 in August to 0.24 ± 0.07 mg Chl-a·m−3 in February (overall mean = 0.22 ± 0.017 mg Chl-a·m−3). The Chl-a concentrations were significantly higher during the day than during the night except in February (Table 4). The estimated phytoplankton C biomass ranged from 10.1 ± 2.8 to 12.2 ± 3.4 mg C·m−3 (average = 11.1 ± 0.9 mg C·m−3).

Table 4. Average Chl-a concentrations (average ± SD) during the day and night at Tioman Island. P values pertain to the concentration differences between day and night
 daynightoverallP value
August 20040.24 ± 0.060.17 ± 0.020.20 ± 0.060.007
October 20040.26 ± 0.070.15 ± 0.030.21 ± 0.080.002
February 20050.23 ± 0.040.24 ± 0.060.23 ± 0.050.771
June 20050.28 ± 0.070.21 ± 0.040.24 ± 0.070.049
overall mean0.25 ± 0.020.19 ± 0.030.22 ± 0.020.035

Abundance and biomass of net-zooplankton (>100 μm)

Mean (average ± SD) net-zooplankton abundance was 7285 ± 2837 ind. m−3 in August, 7475 ± 2084 ind. m−3 in October, 5922 ± 2435 ind. m−3 in February, and 8363 ± 4073 ind. m−3 in June (overall mean = 7261 ± 874 ind. m−3; Fig. 1a–d), while the biomass was 3.26 ± 1.77 mg C·m−3 in August, 2.32 ± 0.75 mg C·m−3 in October, 2.37 ± 1.11 mg C·m−3 in February, and 2.72 ± 1.43 mg C·m−3 in June (overall mean = 2.67 ± 0.37 mg C·m−3; Fig. 1e–h). Copepods were the most dominant group, constituting 66.9–85.8% of the net-zooplankton abundance and 54.7–79.7% of the net-zooplankton biomass, following by larvaceans which constituted 5.2–21.0% and 5.7–17.2% of total abundance and biomass, respectively. The abundance of copepods in the net-samples was 5017 ± 2035 ind. m−3 in August, 5003 ± 1428 ind. m−3 in October, 4686 ± 1883 ind. m−3 in February, and 7178 ± 4014 ind. m−3 in June (overall mean = 5471 ± 994 ind. m−3; Fig. 2a–d), while the biomass was 1.96 ± 1.23 mg C·m−3 in August, 1.43 ± 0.50 mg C·m−3 in October, 1.89 ± 0.92 mg C·m−3 in February, and 1.49 ± 0.94 mg C·m−3 in June (overall mean = 1.69 ± 0.24 mg C·m−3; Fig. 2e–h). Moreover, small-sized copepods were dominant; nauplii, Oithona and Paracalanidae (Paracalanus, Acrocalanus and Bestiolina combined) comprised 28.8–42.7%, 16.9–28.2% and 13.6–19.3% of the net-copepod abundance and 7.4–30.0%, 16.6–32.4% and 14.1–15.2% of the net-copepod biomass, respectively. Chaetognath abundances were minor (0.4–0.9%) but they contributed 3.9–15.9% of the total net-zooplankton biomass. In October and February, bivalve larvae were one of the important groups, comprising 24.0 and 9.2% of the net-zooplankton abundance, and 17.7 and 5.0% of the total net-zooplankton biomass, respectively (Fig. 1b,c,f and g). In June, the contributions of polychaete larvae and decapods to the total abundance were minor (4.7 and 1.2%), but in terms of biomass they constituted 18.4 and 9.0%, respectively (Fig. 1d and h). Among the net-zooplankton biomass, the biomass of herbivores and carnivores was 1.28–1.91 mg C·m−3 (average = 1.54 ± 0.23 mg C·m−3) and 0.9–1.35 mg C·m−3 (average = 1.12 ± 0.16 mg C·m−3), respectively.


Figure 1. Temporal variations in abundance (a–d) and biomass (e–h) of net-zooplankton (>100 μm) and their composition in August and October 2004, and February and June 2005 at Tioman Island. Black bars indicate hours of night.

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Figure 2. Temporal variations in abundance (a–d) and biomass (e–h) of net-copepods (>100 μm) and their composition in August and October 2004, and February and June 2005 at Tioman Island. Black bars indicate hours of night.

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Net-zooplankton abundance and biomass increased during the night and decreased during the day during each study period except October (Figs 1 and 2). Nocturnal zooplankton abundance increase relative to daytime was 187, 143 and 133% in August, February and June, respectively, but 95% in October (Fig. 1a–d). In terms of biomass, the nocturnal increase from daytime was 264, 182 and 195% in August, February and June, respectively, and 131% in October (Fig. 1e–h). In August, the abundance of net-zooplankton in the water column was significantly higher (P = 0.0004) during the night (9485 ± 2155 ind. m−3) than day (5084 ± 1331 ind. m−3; Fig. 1a). The biomass at night (4.72 ± 1.03 mg C·m−3) was also significantly higher (2.6-fold, P < 0.0001) than during the daytime (1.79 ± 0.71 mg C·m−3; Fig. 1e). In October, there was neither a significant difference between day and night in the net-zooplankton abundance (7648 ± 1812 ind. m−3 at day; 7302 ± 2311 ind. m−3 at night; P = 0.76) or in the net-zooplankton biomass (2.00 ± 0.62 mg C·m−3 at day; 2.63 ± 0.69 mg C·m−3 at night, P = 0.095; Fig. 1b and f). In February, the abundance at night (6968 ± 1617 ind. m−3) was higher than during the daytime (4877 ± 2656 ind. m−3), but the difference was not statistically significant (P = 0.097) because of an increase during the day at 18.00 h on the first day due to the addition of bivalve larvae (Fig. 1c). However, the biomass at night (3.06 ± 0.62 mg C·m−3) was significantly higher (P = 0.0076) than during the daytime (1.68 ± 1.00 mg C·m−3; Fig. 1g). In June, the abundance at night (9561 ± 3487 ind. m−3) was also higher (1.3-fold) than during the daytime (7165 ± 4260 ind. m−3) but the difference was not statistically significant (P = 0.33). A difference between day and night was not significantly likely because of higher abundances during the day at 09.00 h due to the addition of copepod nauplii as well as higher abundance at 15.00 h and 18.00 h on the first day due to the addition of copepod nauplii, Oithona and Paracalanida (Figs 1d and 2d). However, the biomass was significantly (P = 0.0082) higher during the night (3.60 ± 1.24 mg C·m−3) compared with the daytime (1.84 ± 0.87 mg C·m−3; Fig. 1h).

The zooplankton taxa that contributed most to the nocturnal increase in biomass (i.e. those that constituted >3% of the net-zooplankton nocturnal biomass and increased at more than twofold of day levels) were copepods (63.8%, 3.3-fold), chaetognaths (11.8%, 2.1-fold) and decapods (3.7%, 48.2-fold) in August (Fig. 1e); chaetognaths (7.0%, 2.8-fold) and decapods (6.3%, 9.0-fold) in October (Fig. 1f); copepods (86.0%, 2.3-fold) in February (Fig. 1g); and copepods (55.2%, 2.0-fold) and decapods (13.2%, 40.8-fold) in June (Fig. 1h). The decapods mainly comprised crab zoea (23.5–87.7%) and anomuran zoea (14.2–43.7%). The copepod taxa that contributed most to the nocturnal increase in copepod biomass in each study period were as follows (Fig. 2e–h): Acartia (5.5%, 4.5-fold), Centropages (11.2%, 18.2-fold), Subeucalanus (4.1%, 11.9-fold), Paracalanidae (13.1%, 2.7-fold), Calanopia (10.8%, 43.6-fold), Temora (3.5%, 4.5-fold) and Oithona (22.6%, 3.3-fold) in August (Fig. 2e); Acartia (5.4%, 3.9-fold), Centropages (4.0%, 8.5-fold), Pseudodiaptomus (6.0%, emergence only at night) and Tortanus (5.3%, 15.5-fold) in October (Fig. 2f); Acartia (3.6%, 26.2-fold), Calanopia (31.2%, 103.8-fold) and Oithona (18.4%, 3.2-fold) in February (Fig. 2g); and Centropages (5.0%, 77.9-fold), Paracalanidae (20.5%, 4.6-fold), Pseudodiaptomus (4.4%, 94.6-fold), Euterpina (12.7%, 4.2-fold) and benthic harpacticoids (5.4%, 15.2-fold) in June (Fig. 2h).

Abundance and biomass of micro-metazooplankton (35–100 μm)

Mean micro-metazooplankton abundance (average ± SD) in each study period was 58,458 ± 14,853 ind. m−3 in August, 17,639 ± 4911 ind. m−3 in October, 17,708 ± 5865 ind. m−3 in February, and 30,417 ± 12,594 ind. m−3 in June (overall mean = 31,056 ± 16,654 ind. m−3; Fig. 3a–d). Mean biomass was 1.14 ± 0.30 mg C·m−3 in August, 0.52 ± 0.16 mg C·m−3 in October, 0.49 ± 0.23 mg C·m−3 in February, and 0.87 ± 0.56 mg C·m−3 in June (overall mean = 0.76 ± 0.27 mg C·m−3; Fig. 3e–h). The overall mean of micro-metazooplankton biomass was 3.52 times lower than that of net-zooplankton. The micro-metazooplankton was occupied by copepod nauplii constituting 78.1–87.9% of abundance and 37.3–58.6% of biomass, whereas the contribution of copepodites was 7.1–11.9% of abundance and 30.0–42.0% of biomass. Larvaceans, the second most important taxa in the net-samples, constituted 0.9–3.4% and 2.1–7.7% of the micro-metazooplankton abundance and biomass, respectively. No obvious hourly temporal variation for micro-metazooplankton abundance and biomass was observed during the study periods (Fig. 3a–h).


Figure 3. Temporal variations in abundance (a–d) and biomass (e–h) of micro-metazooplakton (35–100 μm) and their composition in August and October 2004, and February and June 2005 at Tioman Island. Black bars indicate hours of night.

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The biomass of micro-metazooplankton comprised 17.3–26.0% of total metazooplankton biomass (i.e. net- + micro-metazooplankton, >35 μm), which ranged from 2.84 ± 0.78 mg C·m−3 in October to 4.40 ± 1.85 mg C·m−3 in August (overall mean = 3.42 ± 0.64 mg C·m−3). Of the total metazooplankton biomass, copepod and larvaceans comprised 58.3–81.7% (average = 68.5%) and 4.7–14.3% (average = 7.6%), respectively. The total biomass of copepod community (net + micro) varied from 1.85 ± 0.57 mg C·m−3 to 2.97 ± 1.31 mg C·m−3 (overall mean = 2.32 ± 0.41 mg C·m−3), while those of larvaceans ranged from 0.12 ± 0.09 mg C·m−3 to 0.60 ± 030. mg C·m−3 (overall mean = 0.27 ± 0.20 mg C·m−3).

Estimated zooplankton production rates

The estimated production rate (average ± SD) of the net-zooplankton community (>100 μm) varied from 0.93 ± 0.26 mg C·m−3·day−1 in October to 1.83 ± 0.84 mg C·m−3·day−1 in August (overall mean = 1.27 ± 0.43 mg C·m−3·day−1) (Fig. 4a). The copepod production rate varied from 0.46± 0.15 mg C·m−3·day−1 in October to 0.63 ± 0.35 mg C·m−3·day−1 in August (overall mean = 0.57 ± 0.08 mg C·m−3·day−1), while that of larvaceans ranged from 0.20 ± 0.18 mg C·m−3·day−1 in October to 1.01 ± 0.53 mg C·m−3·day−1 in August (overall mean = 0.46 ± 0.32 mg C·m−3·day−1). Copepods and larvaceans were the most important groups, contributing 34.6–59.8% and 25.9–54.3% to the net-zooplankton production, respectively. However, if house production of larvaceans is taken into account, this would be equivalent to an additional 0.24–1.36 mg C·m−3·day−1. This yields a net-zooplankton production estimate of 1.17 ± 0.42 to 3.19 ± 1.52 mg C·m−3·day−1 (overall mean = 1.86 ± 0.81 mg C·m−3·day−1), which is 125.8–174.3% that of the previously estimated net-zooplankton production (Fig. 4b). As a result, the contribution of copepods to the net-zooplankton production becomes 21.8–47.3%, and that of larvaceans is 32.5–71.8%. Among the net-zooplankton production rate, the secondary production ranged from 0.96 ± 0.43 mg C·m−3·day−1 to 2.89 ± 1.39 mg C·m−3·day−1 (overall mean = 1.60 ± 0.78 mg C·m−3·day−1), whereas the tertiary production rate varied from 0.21 ± 0.08 to 0.31 ± 0.43 mg C·m−3·day−1 (overall mean = 0.26 ± 0.04 mg C·m−3·day−1).


Figure 4. Estimated production rates of net-zooplankton community without (a) and with (b) house production by larvacean, and of micro-metazooplankton without (c) and with (d) larvacean house production.

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The estimated production rate of micro-metazooplankton (35–100 μm) ranged from 0.29 ± 0.12 mg C·m−3·day−1 in February to 0.76 ± 0.22 mg C·m−3·day−1 in June with an overall mean of 0.53 ± 0.21 mg C·m−3·day−1 (Fig. 4c). However this would be 0.65 ± 0.28 mg C·m−3·day−1 if larvacean house production is taken into account; an additional 0.05–0.38 mg C·m−3·day−1 (Fig. 4d). Of the total micro-metazooplankton production (0.65 mg C·m−3·day−1), copepod nauplii contributed 28.6–45.8%, following by larvaceans (13.5–33.5%) and copepodites (17.0–31.4%). Bivalve larvae were episodically important in October and February (5.2 and 8.9%, respectively).

The production rate of the whole metazoan zooplankton community (net- + micro-metazooplankton, >35 μm) ranged from 1.23 ± 0.48 mg C·m−3·day−1 in February to 2.59 ± 0.91 mg C·m−3·day−1 in August with an overall mean of 1.80 ± 0.57 mg C·m−3·day−1. Copepods and larvaceans comprised 48.2–66.9% (average = 55.6%) and 18.9–43.2% (average = 27.3%) of the total production rate, respectively. The total production of copepod community (net + micro, >35 μm) varied from 0.71 ± 0.21 to 1.19 ± 0.39 mg C·m−3·day−1 (overall mean = 0.96 ± 0.21 mg C·m−3·day−1), whereas those of larvacean ranged from 0.26 ± 0.19 mg C·m−3·day−1 to 1.17 ± 0.58 mg C·m−3·day−1 (overall mean = 0.55 ± 0.37 mg C·m−3·day−1). However, the total production of larvaceans shifted to 0.57–2.75 mg C·m−3·day−1 (overall mean = 1.26 ± 0.88 mg C·m−3·day−1) when we considered their house production. This yields a total production estimate of 1.57 ± 0.64 to 4.17 ± 1.66 mg C·m−3·day−1 (overall mean = 2.51 ± 1.06 mg C·m−3·day−1), which is 124.4–161.0% that of the previously estimated total zooplankton production. As a result, the contribution of copepods to the total production changed to 31.4–53.0% (average = 42.9%) and that of larvaceans to 32.2–63.0% (average = 43.7%).

Of the total production rate (with larvacean house production), the secondary production ranged from 1.32 ± 0.54 to 3.85 ± 1.55 mg C·m−3·day−1 (overall mean = 2.20 ± 1.03 mg C·m−3·day−1), and the tertiary production rate varied from 0.24 ± 0.04 to 0.40 ± 0.45 mg C·m−3·day−1 (overall mean = 0.30 ± 0.06 mg C·m−3·day−1).

Trophic structure

The relative carbon biomass of primary, secondary and tertiary producers and their trophic relationship are shown in Fig. 5a. In August, if secondary producers depended entirely on phytoplankton for food, their daily carbon requirement (12.85 ± 5.17 mg C·m−3·day−1) was 126.7% of the phytoplankton biomass. The daily carbon requirement by tertiary producers (1.05 ± 0.69 mg C·m−3·day−1) corresponded to 34.3% of the secondary producer biomass. The transfer efficiency from the secondary to tertiary production was 8.1%. In October, the daily carbon requirement of the secondary producers (4.48 ± 1.62 mg C·m−3·day−1) was equivalent to 42.9% of the phytoplankton standing stock. The tertiary producers required 42.0% of their prey biomass per day. The transfer efficiency from the secondary to tertiary production was 18.2%. In February, the secondary producers required 4.41 ± 1.81 mg C·m−3·day−1 or 37.8% of phytoplankton biomass per day. The daily food requirement of the tertiary producers was 47.4% of the secondary producer biomass. The transfer efficiency from the secondary to tertiary production was 19.0%. In June, the daily carbon requirement of the secondary producers (7.66 ± 3.40 mg C·m−3·day−1) was equivalent to 62.6% of the phytoplankton biomass. The tertiary producers required 55.1% of their prey biomass per day. The transfer efficiency from the secondary to tertiary production was 17.6%.


Figure 5. Schematic daily carbon flow diagram of the plankton community in (a) August and October 2004, and February and June 2005 and (b) overall mean at Tioman Island. Values in boxes of phytoplankton denote their biomass (mg C·m−3) and values in boxes of MZ, HNZ and CNZ the production rate (mg C·m−3·day−1)/biomass (mg C·m−3). Biomass is shown in bold. Values with arrows are daily carbon requirements (mg C·m−3·day−1) of the components above them. CNZ: carnivorous net-zooplankton (carnivores + 1/2 omnivores); HNZ, herbivorous net-zooplankton (herbivores + 1/2 omnivores); MZ, micro-metazooplankton.

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The food chain structure of the overall mean is shown in Fig. 5b. The relative biomass of the primary, secondary and tertiary producers was 76.5%, 15.8% and 7.7%, respectively. The daily carbon requirement of the secondary producers (7.35 ± 3.97 mg C·m−3·day−1) approximated to 66.1% of phytoplankton carbon biomass. The daily carbon requirement of tertiary producers corresponded to 43.9% of secondary producers. The transfer efficiency from the secondary to tertiary production was 13.8%.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References

In our sampling regime, we towed the plankton net vertically through from 1 m above the bottom to the surface. Therefore, zooplankters deeper than 1 m above the bottom in the benthopelagic layer were not collected, which may have resulted in an underestimation of biomass, though recent studies on vertical distribution of zooplankton in coral reef waters showed higher abundance in the surface water than the bottom during the night (Yahel et al. 2005; Alldredge & King 2009; Heidelberg et al. 2010). We also used a 100 μm plankton net with a relatively small mouth diameter (30 cm) in the present study which may miss large and fast-moving zooplankton species such as Undinula and Nannocalanus, both rare species in the net samples in this study, due to their net avoidance (Fleminger & Clutter 1965). This may cause further underestimation of our total net-plankton standing stock in the water column. The net-zooplankton biomass and production may be higher if larger sized mesh net (e.g. 200–330 μm) and/or large net mouth diameter was employed together with the 100 μm net.

Nocturnal increase in zooplankton concentration

Similar to other coral reefs (e.g. McFarland 1999; Heidelberg et al. 2004; Yahel et al. 2005; Nakajima et al. 2008), zooplankton abundance and biomass were higher at night compared to daytime. The nocturnal increase in biomass was 180–260% of the daytime level (except October), and it is comparable to 210% increase of our previous study at Tioman reef (Nakajima et al. 2009a). A nocturnal increase of similar magnitude was also reported from Eilat (Gulf of Aqaba) at 188% (Yahel et al. 2005), and Redang Island (Malaysia) at 320% (Nakajima et al. 2008).

The nocturnal increase in zooplankton concentration in reef water generally depends on two factors: (i) transport of pelagic species by horizontal currents and (ii) vertical migrations of demersal (or reef-associated) zooplankton (Heidelberg et al. 2004; Yahel et al. 2005). In the present study, the nocturnal increase was mainly due to the addition of chaetognaths, decapods and copepods such as Acartia, Centropages, Calanopia and Pseudodiaptomus. Since we did not conduct depth-discrete sampling, sampling at outer reef or emergent trap sampling, we do not know whether our zooplankton is of pelagic or reef origin. However, previous studies extrapolated the origin of reef-zooplankton from the literature (see Heidelberg et al. 2004 and Nakajima et al. 2009a). Accordingly, chaetognaths are pelagic, whereas decapods (mainly crab zoea) are both pelagic and demersal in origin (Heidelberg et al. 2004). Among the copepods that contributed to the nocturnal increase, Acartia, Centropages, Temora, Subeucalanus, Calanopia, Tortanus and Euterpina are pelagic, whereas Pseudodiaptomus and benthic harpacticoids are demersal (Nakajima et al. 2009a). Oithona is categorized into both pelagic and demersal type. Demersal zooplankton on reefs mainly comprise swarmers and epibenthic forms (Heidelberg et al. 2004). The swarmers, active aggregations of individuals, maintain a position near the bottom or around coral formations without settling on the substratum during the day and disperse at night (Hamner & Carleton 1979), whereas epibenthic species reside on and/or within the bottom substrate or coral formations during the day with some migrating into the water column at night (Jacoby & Greenwood 1988; Mees & Jones 1997). Among the pelagic copepods, Acartia and Centropages are also known as swarmers (Hamner & Carleton 1979; Omori & Hamner 1982; Ueda et al. 1983). Some Oithona species are also known to be swarmers at various coral reefs (e.g. Heidelberg et al. 2004), but we do not know whether the Oithona in the present study are swarmers since we did not identify them to the species level; thus pelagic species originating from offshore might be included. In summary, both the pelagic and demersal zooplankton may have contributed to the higher abundance and biomass during the night in the present study.

Zooplankton production

We estimated zooplankton production rates using the multiple regression models based on temperature and body mass for various planktonic zooplankton (Ikeda 1985; Hirst & Lampit 1998; Hirst et al. 2003). Although the production rate estimated by the regression models may be crude compared with the in situ measurements of zooplankton species-specific growth rate, which require a large amount of time and effort, the use of regression models allows rapid estimates of production and the results obtained based on the models can still provide an understanding of the zooplankton production (Huo et al. 2012). The average production rate of our metazoan zooplankton community (>35 μm) was 1.80 mg C·m−3·day−1, but climbed to 2.51 mg C·m−3·day−1 if the production of larvacean houses was considered. It is difficult to strictly compare the values of production rates obtained in the present study with those of other studies because of differences in sample collection methods (e.g. mesh size of net, mouth size of net and sampling time) and estimation approaches of production rates. Still, if comparisons are to be made, they are as follows (Table 5). Since none of the previous studies took larvacean house production into consideration, our comparison with these studies excluded house production. The production rate of our net-zooplankton community (1.27 mg C·m−3·day−1, >100 μm) was c. 4 times lower than at Kavaratti atoll, Lakshadweep, even though they used a coarser mesh net (333 μm) (Goswami 1983). The community production rate of our entire metazoan zooplankton (1.80 mg C·m−3·day−1, >35 μm) was also three to six times lower than those of Uvea atoll in New Caledonia, and Tikehau and Takapoto atolls in French Polynesia (Le Borgne et al. 1989, 1997; Charpy & Charpy-Roubaud 1990). Moreover our net-zooplankton production was 12 times lower than in a deep lagoon in GBR (Sorokin & Sorokin 2010). However, our net-zooplankton production was comparable to Sesoko Island, Okinawa, Japan (Go et al. 1997). To date, few studies have been done on the community production of copepods in coral reef waters (Hayashibara et al. 2002; McKinnon et al. 2005), although specific production rates of certain copepod species populations have been estimated in some coral reefs (e.g. Kimmerer 1983; Le Borgne et al. 1989; McKinnon & Thorrold 1993). The production rate of our net-copepod community (0.57 mg C·m−3·day−1, >100 μm) was c. two times higher than in GBR, where a finer mesh net (73 μm) was used (McKinnon et al. 2005), but close to the average value in Shiraho reef, Ishigaki Island, Japan (Hayashibara et al. 2002).

Table 5. Summary of community production of zooplankton and copepods in various coral reef waters NA, not available
sitedepth mmesh μmsampling time hcopepod biomass mg C·m−3production mg C·m−3·day−1zooplankton biomass mg C·m−3production mg C·m−3·day−1source
  1. a

    Calculated from areal value by depth (m).

  2. b

    Values are for planktonic crustaceans.

  3. c

    Assuming dry weight = 0.135 wet weight (Postel et al. 2000).

  4. d

    Assuming carbon weight = 0.47 dry weight (Hirota 1981).

  5. e

    Calculated from Fig. 3 and 4 of Hayashibara et al. (2002).

  6. f

    Values are not include larvacean's house production.

Kavaratti atoll, Lakshadweep2>330?NANA16.3a5.3aGoswami (1983)
Uvea atoll, New Caledonia<40>35Day/nightNANA910Le Borgne et al. (1997)
Tikehau atoll, French Polynesia25>35Day/nightNANA45Charpy & Charpy-Roubaud (1990)
Takapoto atoll, French Polynesia25>35MorningNANA8.76a10.9aSakka et al. (2002)
barrier reef
GBR, Australia15>120Day/nightNANA266a21aSorokin & Sorokin (2010)
GBR, Australia≤20>73Day/nightNA0.3aNANAMcKinnon et al. (2005)
fringing reef
Sesoko Is., Japan<20>94?NANA2.3bcd1.40bGo et al. (1997)
Ishigaki Is., Japan<2>100Night0.67de0.72eNANAHayashibara et al. (2002)
Tioman Is., Malaysia3.3>35Day/night2.32 ± 0.410.96 ± 0.21f3.42 ± 0.641.80 ± 0.57fThis study
>100Day/night1.69 ± 0.240.57 ± 0.08f2.67 ± 0.371.27 ± 0.43fThis study

To estimate zooplankton production rate, the previous studies (Table 5) obtained specific growth rates of each zooplankton by various approaches, such as employing egg production or excretion rates based on culture experiments (Charpy & Charpy-Roubaud 1990; Le Borgne et al. 1997; McKinnon et al. 2005), through physiological models based on temperature and/or body mass (Goswami 1983; Go et al. 1997; Hayashibara et al. 2002; This study), and by means of reported turnover times (production/biomass) (Sakka et al. 2002; Sorokin & Sorokin 2010). When using turnover rates for production estimation, it is crucial to apply appropriate values. The turnover time (P/B) used for estimation of zooplankton production in GBR (0.08 day−1, Sorokin & Sorokin 2010) is low compared with other studies (0.3–1.3 day−1). Sorokin & Sorokin (2010) used a 120-μm plankton net, so the samples must contain larvae of plankton, which indicates that the turnover rate is likely to be low. Nevertheless, the production rate of zooplankton in GBR is the greatest among the coral reefs (Table 5), and it is considered to hold by far the highest biomass. Sorokin & Sorokin (2010) used a recently developed plankton net (according to them standard plankton nets undercatch the mesozooplankton between 2 and 10-fold), which they claim allowed them to obtain higher (or more accurate) zooplankton biomass. However they also acknowledge that if a normal standard plankton net was applied in GBR, the mesozooplankton biomass and production would be 10–20 mg C·m−3 and 2–4 mg C·m−3·day−1, respectively (Sorokin & Sorokin 2010), which are comparable to our results.

If we assume the zooplankton production rate in GBR is 2–4 mg C·m−3·day−1, as mentioned above, this falls below the reported range of values for atolls (Table 5). As a result, zooplankton community production is likely to be high in atolls than in other reef types (i.e. barrier reef and fringing reef). In the case of atolls in French Polynesia, a higher zooplankton turnover time (>1 day−1) may be one of the reasons for the higher zooplankton production (Le Borgne et al. 1989, 1997). Generally, short turnover times result from the presence of large amounts of organic particles, which form part of the zooplankton diet, as well as from high temperatures (Le Borgne et al. 1997). Compared with atoll lagoons in Takapoto and Tikehau, the present study site had a lower P/B (0.5) but showed similar particulate organic carbon (POC) concentrations. For instance, the POC concentration in the present study site was 189 mg C·m−3 (<100 μm size-class; Nakajima et al. 2011), whereas in Tikehau and Takapoto it was 185 mg C·m−3 (<200 μm; Blanchot et al. 1989) and 197 mg C·m−3 (<200 μm; Sakka et al. 2002), respectively. The POC concentration in Uvea atoll was even lower (<114 mg C·m−3 for <35 μm size-class; Le Borgne et al. 1997). The high temperature (>28 °C) recorded in this study was also similar to those in the atolls (29.5 °C) (Le Borgne et al. 1989). Specific and larval composition of zooplankton may also contribute to high turnover rates. For example, larvaceans and earlier copepod stages have higher growth rates (Hopcroft & Roff 1998; Hopcroft et al. 1998a) and a higher proportion of these animals in the community may lead to a higher zooplankton turnover time. In the present study, the relative number of larvaceans ranged from 4.1 to 21.4% of the total net-zooplankton abundance, whereas it was 0.3% in Takapoto (Sakka et al. 2002), but the zooplankton turnover rate was still higher in the atoll lagoons. Another possible explanation could be that primary production rate is relatively higher in atoll lagoons (Charpy-Roubaud et al. 1989; Sakka et al. 2002), which may be due to the upward convection of nutrient-rich deep-ocean water through the coral basement of the atoll by endo-upwelling (Rougerie & Wauthy 1986; Le Borgne et al. 1989). The existence of readily available alternative food particles such as detritus (Le Borgne et al. 1997), as well as higher residence times of water in atolls (Delesalle & Sournia 1992), could also lead to a high zooplankton productivity. However, only nine sets of data are available for production rate of reef zooplankton community, and further work should be conducted to confirm whether zooplankton production is always high in atoll systems.

Studies in which the biomass and production of copepods and larvaceans are estimated concurrently are rare in subtropical and tropical waters (Hopcroft & Roff 1998). In this study, copepod biomass and production were on average 2.32 and 0.96 mg C·m−3·day−1, respectively, whereas those of larvaceans were 0.27 mg C·m−3 and 0.55 or 1.26 mg C·m−3·day−1 if house production was taken into account, respectively. Thus, the biomass of larvaceans is only 12% of the copepod community biomass, but due to their higher growth rates (Hirst et al. 2003), the production of larvaceans was 57% that of the copepods, or 131% considering the house production. Hopcroft & Roff (1998) previously estimated larvacean production, taking house production into account, to be 53–71% that of the copepods in Jamaica. As the contribution of larvaceans to community production is very large in tropical water (Hopcroft & Roff 1998), it is important to take the house production into account when evaluating material recycling or carbon flow in coral reef ecosystems.

Trophic structure

The food web structures were simplified into a food chain in this study. The transfer efficiency from secondary to tertiary production was estimated at 14%. The food requirements of secondary producers were equivalent to 38–127% (average = 66%) of phytoplankton standing stock, and it is likely to be high, as it generally ranges between 1 and 28% in temperate coastal waters (Hayashi & Uye 2008). Although primary production of phytoplankton was not measured in this study, it was roughly estimated from chlorophyll and light data (Ryther & Yentsch 1957). Taking into account the average phytoplankton biomass (0.22 mg Chl-a·m−3), the daily integrated surface radiation (355.7 cal·cm−2·day−1) and the extinction coefficient (k) of the study site (0.194 m−1; Kuwahara et al. 2010), the daily primary production of phytoplankton would be 0.031 g C·m−2·day−1, or 9.4 mg C·m−3·day−1 considering the average depth of the study site (3.3 m). Therefore, the transfer efficiency from the primary to secondary production would be 23.4%. The carbon requirement of secondary producers (7.35 mg C·m−3·day−1) would be equal to 78.1% of the primary production. In this case, the remaining primary production (21.9%) is probably barely adequate to support bacterial production, which generally averages 20–60% of the primary production (Cole et al. 1988; Uye et al. 1996). This would be enhanced if we consider the food requirement of protozoan microzooplankton such as ciliates. Although we did not examine protozoan microzooplankton in the present study, the daily carbon requirement of protozoan microzooplankton (>35 μm) has been reported to be 3.12 mg C·m−3·day−1 at Takapoto atoll, French Polynesia (Sakka et al. 2002). If we assume that the food requirement of the protozoans is comparable to that of our study site, the carbon requirement of secondary producers would be 10.5 mg C·m−3·day−1, which corresponds to 111% of the estimated primary production. Phytoplankton alone may not be sufficient to sustain the secondary production and the shortage may be supplied by other organic sources, as observed in other coral reef environments (Gerber & Gerber 1979; Gottfried & Roman 1983; Le Borgne et al. 1997; Sakka et al. 2002). Nakajima et al. (2011) reported that the major portion of POC was occupied by detritus (89%) at the study site, suggesting that the diet of particle- or suspension feeding zooplankton would chiefly consist of detritus.

Determining the ingestion rates on detritus of secondary producers will assist in evaluating whether detritus fulfills the estimated zooplankton carbon requirement. A filtration rate on organic particles without phytoplankton has been estimated as 2 l·mg C−1·h−1 for natural net-zooplankton assemblage in Davies Reef, GBR (Roman et al. 1990). The carbon requirements of the net-secondary producer (i.e. herbivores + 1/2 omnivores net-zooplankton) in the present study was estimated as 5.19 mg C·m−3·day−1 considering a net-secondary production of 1.56 mg C·m−3·day−1 and a gross growth efficiency of 0.3 (Ikeda & Motoda 1978). The detritus mass during the study periods was previously estimated as 168.5 mg C·m−3 (Nakajima et al. 2011). By multiplying the filtration rate (2 l·mg C−1·h−1) with the average detritus mass (168.5 mg C·m−3) and the net-secondary producer biomass (1.54 mg C·m−3), it was estimated that the ingestion rate on detritus was 0.52 mg C·m−3·h−1 for the net-secondary producers. The results of laboratory experiments show that the assimilation efficiency of herbivorous marine copepods averaged c. 80% (Conover 1968), and if it can be assumed that all the net-secondary producers assimilate 80% of their ingested carbon in this study, the zooplankton assimilate an average of 15.6 mg C·m−3·day−1, which is much higher than their estimated carbon demand (5.19 mg C·m−3·day−1). Obviously, not all the detritus is available to the net-secondary producers (Roman et al. 1990), but even if only one-third of the detritus particles were captured by the net-zooplankton, the ingestion of detrital carbon would be fulfill their metabolic demands. Consequently, detrital carbon can be considered to be one of the important carbon sources in the study site as in other coral reef environments.

Although the origin of the detritus is beyond the scope of this study, the C/N ratio of particulate organic matter (POM) may give some insights. The C/N ratios of some potential sources of POM have been reported: 4.8–5.9 for coral mucus (Coffroth 1990), 6–8 for phytoplankton (Parsons et al. 1961), 20 for benthic marine plants (Atkinson & Smith 1983) and >30 for terrestrial vascular plants (Alexander 1977). Nakajima et al. (2009b) previously reported the C/N ratio of 4.48 for POM in the study site, which is similar to that of coral mucus. Moreover, the C/N ratio of mucus directly collected from Acropora corals at Tioman Island was 4.87 (Nakajima et al. 2009b). Hence the majority of the detritus may mainly originate from mucus produced by corals. Corals release copious mucus into the water column and the particulate fraction of this have been considered to dominate detritus (Coles & Strathmann 1973). The ingestion of isotopically labeled coral mucus by two zooplankton taxa (Mysids and Acartia copepods) was reported previously (Richman et al. 1975; Gottfried & Roman 1983). Coral mucus detritus may be one of the carbon sources of the zooplankton community that compensates for the low available phytoplankton stock (Roman et al. 1990).


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References

This study describes the production rates of the zooplankton community in a coral reef water of Malaysia. The estimated production rates of the total zooplankton community (including micro- and net-metazooplankton) were on average 1.80 ± 0.57 mg C·m−3·day−1. However this would increase to 2.51 ± 1.06 mg C·m−3·day−1 if house production of larvaceans were taken into account. Our production rates were relatively low compared with that in other reef ecosystems. Of the total production rates, the secondary and tertiary productions were 2.20 ± 1.03 mg C·m−3·day−1 and 0.30 ± 0.06 mg C·m−3·day−1, respectively. The secondary production may not be satisfied by phytoplankton alone in the study area and the shortfall may be supplied by other organic sources such as detritus. A detailed study on the composition and origin of the detritus is needed to obtain a better understanding the coral reef pelagic ecosystems.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References

The authors thank Prof. S. Taguchi (Soka University) for his helpful and critical comments on the original manuscript. We also thank F. L. Alice Ho, M. Y. Ng, S. P. Kok and K. H. Ang for their field assistance; A. A. Manap, A. G. Lim, F. L. Wee (Department of Marine Park, Malaysia) for their kind support in conducting the research at Tioman Island; and the anonymous reviewers for their comments that improved the manuscript. We also thank Dr. K. Ara (Nihon University) who provided helpful comments for the equations of copepod production. This study was partially funded by the Asian CORE Program of Japan Society for the Promotion of Science (JSPS), by the UKM Dana Impak Perdana Research Grant DIP-2012-020 and UKM Grant GUP-2012-051, by JSPS KAKENHI Grant (No. 24710013), and by the Environment Research and Technology Development Fund (S9) of the Ministry of the Environment, Japan.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Study Area
  5. Methods
  6. Results
  7. Discussion
  8. Summary
  9. Acknowledgements
  10. References
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