www.elsevier.com/locate/jembe

Journal of Experimental Marine Biolog

Spatial distribution and trophic ecology of dominant copepods

associated with turbidity maximum along the salinity

gradient in a highly embayed estuarine

system in Ariake Sea, Japan

Md. Shahidul Islama,*, Hiroshi Uedab, Masaru Tanakaa

aDivision of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, JapanbCenter for Marine Environmental Studies, Ehime University, Bunkyo-cho 3, Ehime 790-8577, Japan

Received 23 September 2004; received in revised form 8 October 2004; accepted 2 November 2004

Abstract

The present study aimed to investigate into the feeding ecology of the dominant copepods along a salinity gradient in

Chikugo estuary. Copepod composition was studied from samples collected from stations positioned along the salinity

gradient of the estuary. Copepod gut pigment concentrations were measured by fluorescence technique and hydrographical

parameters such as temperature, salinity, transparency, suspended particulate matter (SPM); pigments such as chlorophyll-a

(Chl-a), phaeopigment; and particulate nutrients such as particulate organic carbon (POC) and particulate organic nitrogen

(PON) were measured. Two distinct zones in terms of nutrient and pigment concentrations as well as copepod distribution

and feeding were identified along the estuary. We identified a zone of turbidity maximum (TM) in the low saline upper

estuary which was characterized by having higher SPM, higher POC and PON but lower POC:PON ratios, higher pigment

concentrations but lower Chl-a/SPM ratios and higher copepod dry biomass. Sinocalanus sinensis was the single dominant

copepod in low saline upper estuary where significantly higher concentrations of nutrients and pigments were recorded and a

multispecies copepod assemblage dominated by common coastal copepods such as Acartia omorii, Oithona davisae and

Paracalanus parvus was observed in the lower estuary where nutrient and pigment concentrations were lower. Copepods in

the estuary are predominantly herbivorous, feeding primarily on pigment bearing plants. However, completely contrasting

trophic environments were found in the upper and the lower estuary. It was speculated from the Chl-a and phaeopigment

values that copepods in the upper estuary receive energy from a detritus-based food web while in the lower estuary an algal-

based food web supports copepod growth. Overall, the upper estuary was identified to provide a better trophic environment

for copepod and is associated with higher SPM concentrations and elevated turbidity. The study demonstrates the role of

estuarine turbidity maximum (ETM) in habitat trophic richness for copepod feeding. The study points out the role of detritus-

0022-0981/$ - s

doi:10.1016/j.jem

* Correspon

E-mail addr

y and Ecology 316 (2005) 101–115

ee front matter D 2004 Elsevier B.V. All rights reserved.

be.2004.11.001

ding author. Tel.: +81 75 753 6225; fax: +81 75 753 6229.

ess: msi@kais.kyoto-u.ac.jp (Md. S. Islam).

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115102

based food web as energy source for the endemic copepod S. sinensis in the upper estuary, which supports as nursery for

many fish species.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Copepod feeding ecology; Copepod dry biomass; Gut fluorescence; Estuarine turbidity maximum; Sinocalanus sinensis; Chikugo

estuary; Ariake Sea

1. Introduction

Estuaries are coastal regions where abrupt changes

in environment occur due to the influence of tides and

mixing of marine and freshwaters. As such, estuaries

are highly dynamic and diverse regions of high

productivity with plankton assemblages that exhibit

variable abundance and composition. Spatio-temporal

variations and habitat types are among the most

important factors that influence observed patterns of

species abundance, composition and size structure of

estuarine planktons. Therefore, it is important that

studies of the feeding ecology of estuarine copepods

include a wide spatial scale to have a comprehensive

understanding on copepod ecology in dynamic

estuarine ecosystems.

The estuarine turbidity maximum (ETM) resulting

from high turbulence is a ubiquitous feature in many

estuarine ecosystems that have substantial impacts on

the life of planktonic biota. Rothschild and Osborn

(1988) proposed the theory of plankton feeding related

to turbulence and described that planktonic predators

encounter more prey under conditions of increased

turbulence and turbidity. A similar relationship

between turbidity and larval fish abundance and

feeding was proposed by Houde and Rutherford

(1993) who introduced the concept of the ETM and

described the role of ETM in the survival of larval and

juvenile fishes. It is generally expected that high

abundance of planktonic copepods occurs in areas of

turbidity maxima and, consequently, higher numbers of

larval and juvenile fishes gather in these regions. These

relationships have been clarified and described later by

several workers, both theoretically (MacKenzie et al.,

1994) and experimentally (MacKenzie and KiO/ rboe,

2000; Visser et al., 2001). Irigoien and Castel (1997)

described the relationships between chlorophyll-a

(Chl-a) and suspended particulate matter (SPM) in

zone of estuarine turbidity maximum. In the absence of

potential primary production, they reported that Chl-a

appears to be related to SPM in the maximum turbidity

zone (MTZ) in the Gironde Estuary, SW France. They

reported that the MTZ was characterized by low Chl-a/

SPM ratios which gradually increased seaward of the

MTZ where SPM concentration was lower; this

processes resulted in highly significant relationships

between chlorophyll pigments (Chl-a and phaeopig-

ments) and SPM. Therefore, these processes are

expected to significantly influence the distribution

and feeding ecology of planktonic copepods. However,

being a recently developed concept, the processes

associated with ETM and its biological and ecological

influences in copepod trophic environment over wide

spatial scales have been poorly known.

The Ariake Sea is the home for a number of

endemic fish species that use estuaries during their

early life and settle down to the bottom of the Ariake

Sea during their adult ages. Some of these fishes are

considered as dcontinental relict speciesT because

closely related species are distributed in China and

Korean peninsula (Takita et al., 1988; Takita and

Chikamoto, 1994; Takita, 1996). Chikugo estuary is

the largest estuary of Ariake Sea with the highest tidal

differences in Japan and is characterized by high

salinity gradients and a zone of turbidity maximum

(TM) in its upper region. In one of our recent

investigations, we identified an endemic calanoid

copepod (Sinocalanus sinensis) distributed restrict-

edly in the brackishwater areas and associated with

the TM zone and some common non-endemic coastal

copepods (such as Acartia omorii, Paracalanus

parvus and Oithona davisae) distributed restrictedly

in the high saline lower part of the estuary. Many

larval and juvenile fish species utilize the estuary as

nursery ground before settlement and the copepods

occupy a key position between phytoplankton and

higher levels such as larger zooplankton and fish

larvae. We identified two spatially different regions

along the estuary in terms of copepod distribution as

well as larval fish distribution and feeding. We

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115 103

observed that the distribution and feeding of endemic

fish species were intimately associated with the

distribution of the endemic copepod S. sinensis in

the upper estuary while the non-endemic fishes make

use of a number of other common coastal copepods in

the lower estuary. We hypothesize that copepods from

the two spatially different assemblages receive energy

from different sources along the estuary. With a view

to elucidate the feeding ecology of dominant cope-

pods along the Chikugo estuary as a broader focus,

the present study was conducted with the following

objectives: (i) to investigate the food habit and the

source of energy of S. sinensis in the ETM zone of the

upper estuary as compared to that in the lower estuary

and (ii) to clarify the role of ETM in the feeding

ecology of S. sinensis. This study is expected to

contribute significantly to our understanding on the

estuarine food web in general as well as to the specific

role of ETM in copepod feeding and survival over a

wide spatial scale in a dynamic estuarine system.

2. Materials and methods

2.1. The study area and sampling

The Ariake Sea is located in Kyushu Island in the

southwestern part of Japan. The bay is a highly

embayed area with the highest tidal differences

(about 6 m) in Japan. Chikugo River is the largest

river in Kyushu that inflows into the bottom of the

bay, forming a wide estuarine area, which is the

largest and the most intensively flushed estuary of

the Ariake Sea (Fig. 1). Detailed description of the

study area can be found in Matsumiya et al. (1982).

Seven sampling stations were set up along the

estuary (Fig. 1) that were lined along the tideway

of the Chikugo River. Among them, four stations

were along the river (R4, R3, R2 and R1) and the

other three are outside the river mouth along the

estuary (E1, E2 and E3). Station R1 is located at the

river mouth and R4 is the uppermost station, 16 km

upstream from the mouth and with little seawater

influence even at spring high tide. Starting from the

river mouth, the estuarine stations are situated on the

tidal flat and E3 is the most distant station with the

highest salinity. Samples were collected for a period

of 3 months from March to May 2003.

2.2. Hydrographical parameters, particulate nutrients

and pigments

The parameters studied were temperature (8C),transparency (cm), salinity (PSU), SPM (mg l�1),

particulate organic carbon (POC) (mg l�1), parti-

culate organic nitrogen (PON) (mg l�1), Chl-a (Agl�1) and phaeopigment (Ag l�1). For each station,

temperature, salinity and dissolved oxygen (DO)

were recorded on the board by an Environmental

Monitoring System (YSI 650 MDS, YSI, USA).

Water transparency was determined by using the

secchi disc method. SPM, as a measure of turbidity

was determined after Gasparini et al. (1999). A

known volume of water was filtered onto a pre-

weighed and pre-dried (45 8C for 24 h) Whatman

GF/F filter. The filter was then oven dried at 45 8Cfor 24 h and SPM was calculated by comparing the

initial and final weights. Water samples for POC and

PON were filtered through pre-dried (120 8C for

6 h) Whatman GF/F filters. Filters were freeze-dried

and POC and PON were determined by a CHN

auto-analyzer using Antipyrine (SMA-SP-9) (70.19%

C, 14.88% N, 8.5% O and 6.43% H) as the

standard. To analyze the total pigment (Chl-

a+phaeopigment) concentration a known volume of

water was filtered through Whatman GF/F filters,

which were immediately frozen in dry ice, trans-

ported to the laboratory and frozen immediately

at �85 8C in complete darkness. In the laboratory,

Chl-a and phaeopigment were determined fluoro-

metrically before and after acidification using a

Turner design fluorometer (Turner Designs 10AU

005, Sunnyvale, CA); acetone extraction and calcu-

lation of Chl-a concentration was done according to

Clesceri et al. (1989).

2.3. Copepod sampling and gut fluorescence analysis

Copepod samples were collected by oblique tows

of a plankton net (45 cm mouth diameter and 0.1 mm

mesh size). The contents of the cod end were poured

onto a 0.25 mm sieve bag, washed with filtered

seawater and immediately frozen in dry ice and

transferred to the laboratory and subsequently deep

frozen at �85 8C. The amount of Chl-a and

phaeopigment in copepods, referred to as the gut

fluorescence was determined using the method

Fig. 1. Map of Ariake Sea and Chikugo River estuary showing the sampling stations; the scale applies only to the spatial areas used for

sampling.

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115104

described by Mackas and Bohrer (1976), used and

modified later among others by Perissinotto (1992),

Pasternak (1994), Kerambrun and Champalbert

(1995), Tirelly and Mayzaud (1999) and Besiktepe

(2001). In the laboratory, copepods of the desired

species were picked up under microscope in dim light

using micropipette capillary and jeweler’s forceps; we

minimized the illumination and picking time as much

as possible. Samples were then washed with filtered

water taken from the respective station. Twenty-five

to 250 individuals were picked per taxon, placed on

25 mm Whatman GF/F filter paper and subsequently

transferred into glass tubes containing 10 ml 90%

acetone. The filter papers containing the sample were

ground and homogenized using glass rod and kept in

refrigerator at �20 8C under complete darkness

overnight for pigment extraction. The extracts were

then centrifuged at 5000 rpm for 30 min. The

Fig. 2. Spatio-temporal variation in the hydrographical parameters

along Chikugo estuary. The letters assigned to each mean value

indicate the significance of difference; the mean values having

different letters are significantly different from each other.

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115 105

supernatant was used for fluorescence measurement in

a Turner design fluorometer (Turner Designs 10AU

005) before and after acidification with two drops of 1

N HCl. The concentrations of Chl-a and phaeopig-

ment (which was expressed as the total pigment

throughout the paper) per individual were calculated

according to Perissinotto (1992) as follows; gut

pigment is the sum of Chl-a and phaeopigment and

were calculated by the following formulae:

lg Chl� a per individual copepod½ �

¼ fc r= r � 1ð Þf g fb� fað Þ�=n ð1Þ

lg Phaeopigment per individual copepod½ �

¼ rfc rfa� fbð Þ= r � 1ð Þf gmwr½ �=n ð2Þ

Where fc=the fluorometer constant, r=the ratio of fa/

fb for pure chlorophyll, fb=fluorescence before acid-

ification, fa=fluorescence after acidification, mwr=the

molecular weight ratio of phaeophorbide to Chl-a and

n=number of copepods per sample.

A second set of copepod samples were collected in

the same way to determine the abundance and

distribution of copepods in ambient water. Samples

were immediately fixed in 10% seawater formalin and

transported to the laboratory. The plankton net was

equipped with a flow meter to determine the volume

of water filtered. Copepods were sorted from the

suspended particles and detritus under a binocular

stereomicroscope. The abundance of copepods was

determined by identifying and counting the total

number, and copepod density was expressed as

number per cubic meter of water. Copepod dry

biomass at each sampling station was determined by

drying samples at 45 8C for 24 h in a thermostat oven

and the dry weight was expressed as mg m�3.

2.4. Statistical analysis

One-way analysis of variance (ANOVA) was used

to examine the difference among the sampling

stations. ANOVA was followed by least significant

difference (LSD) test to compare the means and to

assign the level of significance. Correlations between

different parameters were assessed by calculating the

correlation coefficients. Values were considered sig-

nificant at 95% level of confidence.

3. Results

3.1. Hydrographical parameters, particulate organic

nutrients and pigments

Overall ranges of different hydrographical param-

eters were: temperature 10.9–20.1 8C, salinity 0.07–

28.8 PSU, transparency: 4.5–25.0 cm and SPM: 42.4–

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115106

524.0 mg l�1. While temperature was almost stable

over the spatial scale, salinity increased consistently

and significantly toward the sea (Fig. 2). Station R4

had the lowest salinity and station E3 had the highest

(Fig. 2). Secchi disc transparency (SDT) also

increased consistently and significantly toward the

sea; station R4 had the lowest transparency while

station E3 had the highest (Fig. 2). In contrast, SPM

concentrations decreased consistently and signifi-

cantly from stations R4 to R2 although in other

stations (stations R1–E3), SPM values were relatively

stable. The analysis of the correlation coefficient

produced a highly significant negative correlation

(r=�0.969) between SPM and SDT (Table 1).

POC ranged 1.22–20.9 mg l�1, PON ranged 0.06–

1.55 mg l�1 and POC:PON ratios ranged 7.0–26.3.

POC and PON were distributed along the estuary in

an exactly similar fashion producing a strong and

highly significant correlation (r=0.984) (Table 1). For

both the parameters, three statistically different values

were recorded (Fig. 3); the highest concentrations

recorded in station R3, followed by stations R4 and

R2 and the lowest amounts were from stations R1 to

E3 where the values were relatively stable. While

POC and PON were generally higher in the upper-

most three stations and decreased toward the sea,

POC/PON ratio showed general seaward increase

(Fig. 3). POC, as a percentage of SPM, ranged

between 1.9% and 11.8% and PON between 0.14%

Table 1

Correlation (the values of the correlation coefficient, r) between differen

along Chikugo estuary; all values are significant at 5% level

Temperature Salinity Transparency SPM POC PON

Temperature –

Salinity 0.722 –

Transparency 0.776 0.985 –

SPM �0.621 �0.975 �0.969 –

POC �0.798 �0.802 �0.789 0.735 –

PON �0.830 �0.871 �0.873 0.826 0.984 –

Total pigment �0.571 �0.969 �0.951 0.990 0.703 0.7

Chl-a 0.730 0.970 0.962 �0.954 �0.895 �0.9

Phaeopigment �0.730 �0.970 �0.962 0.954 0.895 0.9

Density 0.885 0.784 0.840 �0.693 �0.607 �0.6

Dry weight �0.625 �0.965 �0.922 0.949 0.859 0.8

Copepod C �0.625 �0.965 �0.922 0.949 0.859 0.8

Copepod N �0.625 �0.965 �0.922 0.949 0.859 0.8

and 0.92%; on average, station R4 had the lowest and

station R3 had the highest values of POC as %SPM

and decreased consistently toward the sea and a more

or less similar pattern was observed for PON also

(Fig. 4).

The ranges of Chl-a and phaeopigment were

respectively 3.76–22.97 and 0.83–32.32 Ag l�1 and

total pigment (Chl-a+phaeopigment) ranged 5.10–

49.70 Ag l�1. Chl-a was almost stable over the spatial

scale, while significantly higher values of phaeopig-

ment were recorded in stations R4 and R3 and

phaeopigment decreased consistently toward the sea

(Fig. 5). A more or less similar pattern was observed

also for total pigment, i.e., the highest amount of total

pigment was recorded in station R4 and concentra-

tions reduced consistently towards the sea (Fig. 5).

The contrasting pattern between Chl-a and phaeopig-

ment was even more apparent when they were

calculated as percentage of the total pigment (Fig.

6). Chl-a had lower contributions in upper estuary and

increased towards the sea in contrast to phaeopigment,

which contributed higher in the upper estuary and

decreased consistently towards the sea (Fig. 6).

Spatial distribution of Chl-a and phaeopigment had

highly significant negative correlation (r=�1). The

ratio of Chl-a to SPM was calculated as an indicator

of Chl-a production; when plotted in the stations

along the salinity gradient, this ratio produced two

clearly different sets of values: significantly lower

t hydrographical parameters, nutrients and pigment concentrations

Total

pigment

Chl-a Phaeopigment Copepod

density

Copepod

dry

weight

Copepod

C

91 –

44 �0.931 –

44 0.931 �1.000 –

78 �0.657 0.721 �0.721 –

99 0.947 �0.974 0.974 �0.619 –

99 0.947 �0.974 0.974 �0.619 1.000 –

99 0.947 �0.974 0.974 �0.619 1.000 1.000

Fig. 3. Spatio-temporal variations in POC and PON and the

corresponding POC/PON ratios. The letters assigned to each mean

value indicate the significance of difference; the mean values having

different letters are significantly different from each other.

Fig. 5. Spatio-temporal patterns of chlorophyll-a, phaeopigment and

total pigment (chlorophyll-a+phaeopigment), while chlorophyll-a

was almost stable over the spatial scale, phaeopigments had

significantly higher values in stations R4 and R3.

Fig. 4. Spatial variation in the POC and PON as percent of SPM,

showing a downstream reduction in the contribution of both POC

and PON to SPM.

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115 107

values were found in stations R4–R2 and the higher

values in the other stations (Fig. 7). The lowest values

of Chl-a/SPM ratios corresponded to the ETM zone.

3.2. Copepod composition, density, biomass and gut

fluorescence

Two clearly different copepod assemblages were

identified along the estuary (Fig. 8); one, the upstream

low-saline assemblage overwhelmingly dominated by

a single species S. sinensis in station R4 and R3 and,

the other, the medium-to-high saline assemblage

which is a multispecies assemblage dominated by a

number of common coastal copepods namely, A.

omorii, O. davisae, P. parvus from station R2 to E3.

Although horizontal distribution of S. sinensis extends

Fig. 6. Two completely contrasting scenarios in the spatial patterns

in contribution of chlorophyll-a and phaeopigment (%) to the total

pigment. Fig. 8. Spatial variation in copepod composition; two distinctly

different regions were identified: the two uppermost stations had a

single species composition overwhelmingly dominated by S

sinensis and the other stations in the lower estuary had a

multispecific assemblage, dominated by a number of common

coastal copepods.

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115108

down to station E1 (mean salinity 23.7 PSU), this

copepod was overwhelmingly dominant at stations of

low salinity, especially in stations R4 and R3.

Copepod density ranged from 5963 to 34,214

individuals m�3 and showed a general and steady

increase from station R4 seaward. Spatially, station

R4 had significantly lowest and stations E1–E3 the

significantly highest densities (Fig. 9). In contrast,

copepod dry biomass, which ranged from 4.89 to

122.2 mg m�3, was significantly higher in stations R4

and R3 than in the other stations (Fig. 9).

Copepod gut pigment concentrations showed very

high individual variations and ranged from 0.08 to

0.548 in S. sinensis, from 0.016 to 0.266 in A. omorii,

from 0.012 to 0.284 in O. davisae and from 0.054 to

Fig. 7. Spatio-temporal variations in Chl-a/SPM ratio: showing two

clearly defined patterns, lower ratios were observed in the zone of

turbidity maximum in the upper estuary and higher ratios in the

lower estuary.

.

0.099 Ag in P. parvus. The gut Chl-a did not vary

considerable among species and over the spatial scale;

in the upper estuary, S. sinensis had the gut Chl-a

levels of 0.053–0.075 Ag copepod�1, which was

almost similar to the gut Chl-a of 0.027–0.075 Agcopepod�1 in the other copepods in lower estuary. In

contrast, much higher values of gut phaeopigment

were recorded in S. sinensis in the upper estuary than

in the lower estuary in other copepods (0.107–0.216

Ag copepod�1 in contrast to 0.003–0.032 Agcopepod�1, respectively). The gut phaeopigment

content showed general decrease toward the sea.

Similar to the gut phaeopigment contents, much

higher values of total gut pigments were recorded in

S. sinensis in the upper estuary than in the lower

estuary in other copepods (0.181–0.277 Ag copepod�1

in contrast to 0.041–0.100 Ag copepod�1, respec-

tively). Total gut pigment concentrations of S. sinensis

declined steadily from stations R4 to R2, while, in

other species, no clear spatial pattern was observed

(Fig. 10). In general, gut pigment concentrations had

two clearly contrasting patterns (Fig. 10): the first for

S. sinensis in the upper estuary where the majority of

the gut pigments was formed by phaeopigment which

dropped consistently toward the sea and the second,

for the other species in the lower estuary where Chl-a

contributed the majority of the gut pigments; in this

Fig. 9. Spatial variation in copepod density (upper) and dry biomass

(lower); the letters assigned to each mean value indicate the

significance of difference; the mean values having different letters

are significantly different from each other. Copepod density and dry

biomass showed contrasting scenarios in that density increased

consistently towards sea with the highest values in three lowermost

stations while the highest dry biomass values were observed in the

two uppermost stations with significantly lower in the sea.

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115 109

areas, the contribution of phaeopigment decreased

consistently toward the sea.

4. Discussion

The present study identified two distinctly different

regions along the Chikugo estuary in terms of

hydrographical parameters, particulate matter and

nutrient concentrations. This spatial pattern was

reflected in copepod distribution, copepod composi-

tion, copepod dry biomass as well as gut pigment

concentrations. The low saline area in the upper

estuary (stations R4–R2) had higher nutrient concen-

trations than the medium-to-high saline lower estuary.

The low-saline area was highly turbid, having higher

SPM concentrations and, therefore, lower transpar-

ency values, clearly indicating that a zone of turbidity

maximum exists in the upper region of the estuary

which was characterized by having a lower Chl-a,

higher phaeopigment (and total pigment), lower Chl-

a/SPM ratios, higher POC and PON but lower POC/

PON ratios, higher copepod dry biomass and copepod

gut pigments.

The POC/PON ratio had spatial trends, which

were completely contrasting to the spatial patterns of

POC and PON alone. Downstream increase in POC/

PON ratios simply mean a downstream increase in

POC in relation to PON. Yamamuro (2000) reported

down-river increases in carbon and concluded that

such increases are attributable to the source of the

carbon fixed by autochthonous phytoplankton along

the estuarine salinity gradient, and not to mixing of

organic matter from the land and sea sources. A

similar relation was described also by Canuel and

Cloern (1995) which are in agreement with our

results because, in our study, the downstream stations

are less likely to receive organic loads form runoff

and drainage from the land sources and the higher

POC/PON ratio might be caused by the organic

matters from autochthonous sources such as phyto-

plankton. Nevertheless, this does not essentially

mean that downstream stations had better nutrient

conditions than the upstream stations because lower

POC/PON ratios in the upstream stations also

indicate higher PON in these areas. This might be

caused by accumulation of N-rich detritus in river as

well as benthic resuspension in the highly flushed

estuary (Dong et al., 2000; Cloern, 2001; Tappin,

2002). POC and PON as percent of SPM provided a

reliable comparison of the nutrient conditions

between the upper and the lower estuary; down-

stream decrease of these parameters indicate the

upper estuary had the better nutrient conditions than

the lower estuary.

Although considerable seasonal and regional var-

iations in the relationships between Chl-a and SPM

concentrations and, therefore, estuarine turbidity are

obvious (Irigoien and Castel 1997), Chl-a concen-

trations are generally lower in highly turbid ETM

zones than in the zones with lower turbidity as

observed in the present study. The spatial patterns in

pigment distribution found in the present study are in

close agreement with many reports in different

Fig. 10. Spatial and species-specific patterns in gut pigment concentrations; note that the scales in the primary and secondary axes are different.

While chlorophyll-a was almost constant over the spatial scale, phaeopigment as well as total pigment in the upper estuary were several orders

of magnitude higher than in the lower estuary. S. sinensis belongs to the primary axis and the other species belong to the secondary axis.

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115110

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115 111

regions. For instance, in the Bristol Channel, Joint and

Pomroy (1981) found much greater production of

Chl-a in less turbid waters. In the Chesapeake and

Delaware Bays, a chlorophyll maximum occurs

downstream of the turbidity maximum (Fisher et al.,

1988). The same observation was reported by

Pennock (1985) and Harding et al. (1986). The spatial

distribution of total pigments (Chl-a+phaeopigment)

and the distribution of Chl-a and phaeopigment

separately produced completely contrasting scenarios.

The total pigment concentrations reduced consistently

towards the sea. However, when the concentrations of

Chl-a and phaeopigment was calculated separately,

Chl-a increased consistently towards the sea while

phaeopigment showed a corresponding decrease

towards the sea with highly significant negative

correlation (r=�1) among them. This pattern of

spatial distribution clearly indicates that pigments in

the highly turbid upper estuary were more degraded

than that in the lower estuary. The mechanisms

involved in the turnover of chlorophyll pigments are

complex because a number of processes are involved

which affect the concentration of chlorophyll and

phaeopigments in the photic layer. These include

phytoplankton growth, zooplankton grazing, cell

sinking, cell senescence, photo-degradation, fecal

pellet sinking, physical mixing and advective trans-

port (Welschmeyer and Lorenzen, 1985). Unless

removed from the photic zone in large fecal pellets

or transported by vertical migration, cell sinking or

physical mixing, the phaeopigments or chlorophyll

associated with the phytoplanktonic senescing cells or

phytodetritus would undergo photo-oxidation (Soo-

Hoo and Kiefer, 1982; Welschmeyer and Lorenzen,

1985; Carpenter et al., 1986; Leavitt and Carpenter,

1990). In this way, most of the detrital chlorophyll

remaining in the photic layer would be photodegraded

(Nelson, 1993; Cuny et al., 1999). Therefore, distri-

bution pattern of Chl-a and phaeopigment in the

present study suggests that most of the pigments in the

upper highly turbid areas were associated with detrital

particles, since it has been reported that phaeopigment

forms the majority of the total pigments and this is

associated with higher detrital biomass which con-

tributes to higher turbidity in ETM zones (Poulet,

1973, 1976; Gasparini et al., 1999). Moreover, in

estuaries with higher rates of turbulence as in the

Chikugo, exposure of the detrital chlorophyll pig-

ments to the sunlight is long enough to induce their

photo-degradation. Consequently, most of the chlor-

ophyll sinking out of the photic zone is photodegraded

in the upper layer of the water column. Therefore, it

clearly appears from this study that the bulk of the

detrital chlorophylls, and probably their fluorescent

degradation products (phaeopigments), undergoes

photodegradation before sinking out of the photic

layer and this degraded pigments formed the major

portion of the total pigment concentrations in the

ETM zones of the Chikugo estuary given that Chl-a

concentrations were almost constant over the spatial

scale. Irigoien and Castel (1997) described a similar

fashion of Chl-a distribution in a comparable estuar-

ine ecosystem and opined that and important portion

of the chlorophyll in the ETM zone originates from re-

suspended microphytobenthos. Using Chl-a/SPM

ratio as an indicator of chlorophyll production along

a salinity gradient in the Gironde estuary in SW

France, they reported that lower Chl-a/SPM ratios

were associated with the ETM zone with a peak

seaward, indicating that higher turbidities are asso-

ciated with poor chlorophyll productions in the ETM

zones.

The distribution of copepods reported in the

present study is in close agreement with that reported

by Hibino et al. (1999) from the same study area;

similar assemblage was also observed in our previous

studies (Islam et al., submitted). We recorded seven

consistently identified species of copepods and

unidentified copepod nauplii. Although copepod

composition is affected by a number of factors which

are associated with the diel as well as seasonal cycle

of abundance, the number of species recorded in the

present study is close to that reported by Hibino et al.

(1999).

From the gut fluorescence analysis, it was appa-

rently clear that the copepods in Chikugo estuary are

predominantly herbivorous, feeding primarily on

chlorophyll bearing plant materials. Similar to

nutrients and environmental pigment concentrations,

two different sets were recorded also for the gut

pigment contents; S. sinensis had much higher gut

pigments in the upstream areas than the other species

in the lower estuary. We assume that the gut pigment

concentration was a function of environmental pig-

ment concentration, i.e., the difference between upper

and lower estuary was caused by the difference in

Fig. 11. Contribution of chlorophyll-a and phaeopigment in the diet of different copepod species. In the upper estuary, phaeopigment

contributed the major portion of the total pigment in S. sinensis while chlorophyll-a formed the majority of the gut pigments in the lower estuary

in other copepods.

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115112

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115 113

food supply between the two regions and was

presumed to be associated with suspended particle

concentrations, which is usually composed, in most

part, by detritus. In contrast, in the lower estuary and

in the sea A. omorii, P. parvus and O. davisae did not

show considerable variation in their gut pigments;

these species are supposed to feed on a relatively

stable source such as phytoplankton. Li et al. (2004)

commented that a positive correlation between gut

pigment and environmental pigment concentrations is

usually obtainable in areas, which are food limited for

copepods. However, our results indicated that Chi-

kugo estuary is not food limited for copepods and as

such do not support the generalization made by Li et

al. (2004). The values of SPM, POC, PON and total

environmental pigment were higher than the values

reported for other estuaries (Uncles et al., 1998; Abril

et al., 2002; Kress et al., 2002). Similarly, the gut

pigment concentrations were also higher than the

reported values (Ellis and Small, 1989; Perissinotto

and Pakhomov, 1996; Kibirige and Perissinotto,

2003), indicating that the Chikugo estuary provides

a rich environment for copepod foraging. Paffenhofer

and Strickland (1970) reported that detritus serves as

substrate for vast organic aggregates and a vast

reserve of suspended organic matters, both living

and non-living in natural environment. Detritus also

harbor numerous microalgae and is an attractive

source of energy for the zooplankton. Therefore,

higher particulate concentration in the upper river

was likely to contribute to higher gut pigment values

in this region. On the contrary, gut pigment concen-

trations in the lower estuary were likely to be

contributed largely by the microalgae in the absence

of considerable SPM concentrations. The role of SPM

and detritus in copepod feeding has been described

also by Gasparini et al. (1999). Microalgae are usually

more patchily distributed in the lower estuary than is

the upper river and this should be a potential source of

difference in the gut pigment concentrations between

the two regions.

While the gut Chl-a concentrations in the upper

areas were almost similar to that in the lower estuary

(Fig. 10), the gut phaeopigment concentrations were

several orders of magnitude higher in the upper

estuary than in the lower estuary. This trend clearly

indicates that the gut pigments in the upper estuary

were originated from a detritus-based source. This is

also evident from a consistent decrease of gut

phaeopigment toward the sea since detritus settle

down to the bottom as they are transported toward the

sea and is available at generally lower rates. While the

gut pigment concentrations in the estuarine copepods

were rather stable over the spatial scale, gut pigments

of S. sinensis decreased consistently as the distribu-

tion of the species extends downstream suggesting

that this copepod grazed predominantly on the

naturally occurring particulate matters and detritus

and their feeding rates decrease gradually due to the

fact that the particulate matters gradually settle down

to the bottom and are, therefore, available to a lesser

extent. Fig. 11 produced an even clearer picture of the

relative contribution of Chl-a and phaeopigment in

the diet of copepods. While copepod diet in the upper

estuary was mainly phaeopigment-based, contribution

of phaeopigment dropped down steadily toward the

sea where copepod diet was based largely on Chl-a.

Therefore, we speculated that two completely con-

trasting regions in terms of hydrography, particulate

nutrient concentrations and copepod trophic environ-

ment exist along Chikugo estuary; one, the detritus-

based food web in the upper estuary which is the zone

of turbidity maximum and characterized by higher

particulate nutrient concentrations and the other, the

algal-based food web in the lower estuary which is

characterized by relatively lower concentrations of

nutrients and lower turbidity.

5. Conclusion

Two contrasting regions exist in the Chikugo

estuary in terms of hydrographical parameters,

nutrients richness and pigment distribution. These

spatial variations significantly affect copepod ecology,

resulting in a completely different copepod composi-

tion and abundance in the two regions. The low-to-

medium saline zone in the upper estuary is charac-

terized by a rich trophic environment for copepod; this

area was dominated by a single copepod species. In

contrast, the highly saline lower estuary is charac-

terized by a multispecies assemblage and provides

relatively poor trophic environment for copepod. It

was speculated that these variations was caused by a

difference in SPM loadings of which detritus form the

most important part. We identified the existence of a

Md.S. Islam et al. / J. Exp. Mar. Biol. Ecol. 316 (2005) 101–115114

detritus-based food web in the upstream areas and an

algal-based food web in the lower areas of the estuary.

The study demonstrates the role of ETM in habitat

richness for copepod feeding and survival. The study

also clarifies the reason why productivity is higher in

the regions of ETM where primary production is

likely to be light-limited.

Acknowledgement

[SS]

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