Community structure of mesozooplankton in coastal waters of Sundarban mangrove wetland, India: A multivariate approach

Journal of Marine Systems 141 (2015) 112–121

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Journal of Marine Systems

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Community structure of mesozooplankton in coastal waters ofSundarban mangrove wetland, India: A multivariate approach

Bhaskar Deb Bhattacharya a, Jiang-Shiou Hwang b, Santosh Kumar Sarkar a,⁎, Dibyendu Rakhsit a,Murugan K c, Li-Chun Tseng b

a Department of Marine Science, University of Calcutta, 35 Ballygunge Circular Road, Calcutta 700019, Indiab Institute of Marine Biology, National Taiwan Ocean University, Keelung 20224, Taiwanc Department of Zoology, School of Life Sciences, Bharathiar University, Coimbatore 641 046, India

⁎ Corresponding author. Tel./fax: +91 33 2461 4849.E-mail address: [email protected] (S.K. Sarkar).

http://dx.doi.org/10.1016/j.jmarsys.2014.08.0180924-7963/© 2014 Elsevier B.V. All rights reserved.

a b s t r a c t

Article history:Received 9 January 2014Received in revised form 23 June 2014Accepted 26 August 2014Available online 30 August 2014

Keywords:Community structureCopepodsSpecies diversityMesozooplanktonSundarban mangrove wetland

Spatial and temporal distribution of community structure and seasonal distribution of mesozooplankton(MZ; 20–200 μm) in the context of environmental parameters were studied in the coastal waters ofIndian Sundarban wetland formed at the confluence of Hugli (Ganges) River estuary, India. The work hasbeen aimed for better understanding of its ecological characteristics in terms of the most dominantmesozooplankton group in a tropical mesomacrotidal setting. Samples were collected from four samplingsites of different hydrodynamic set up using a ring trawl net (Hydro-Bios No. 438 700, mesh size 200 μm)equipped with a calibrated flowmeter and both water and plankton samples were analyzed by standardmethods. Distribution of MZ showed bimodality with two peak periods, primary peak during April coincidingwith maximum number of copepod species (974 ind. m−3) and the secondary one during August. Copepod wasthe most dominant taxon where the calanoids formed bulk of the biomass representing 33 species of 7 genera,while cyclopoids formed the next dominant group comprising 4 species of 3 genera followed by 4 monogenericharpacticoid species. Results of correlation matrix revealed that two copepod families Acartiidae andPseudodiaptomidae maintain negative relationship with other six families indicating that they form a group bythemselves. Results of multiple regression analysis reveal that salinity, chlorophyll-a and transparency are thepotential hydrological factors in the distribution and existence of the dominant copepods and total chaetognaths.An overall high diversity index values (max. 3.21) was associated with high richness index (4.39) and high even-ness index (0.96) at the site of the mouth of the estuary. In terms of feeding guild, the herbivore copepods weredominant followed by omnivores. Cluster analysis confirmed an overall dominance of the calanoid copepodBestiolina similis as a solitary group for all the sites. The chaetognath Sagitta bedoti was perennial in distributionwhere the contribution of juvenile form (recognized as Stage I) was dominant. Among the other MZ, hydromedu-sae, ctenophore, sergestid and mysid were also encountered contributing insignificant part of the total density. Along-term decadal change in copepod community was pronounced which might be due to climate-induced envi-ronmental changes which also modulate the physicochemical characteristics of water.

© 2014 Elsevier B.V. All rights reserved.

1. Introduction

Mesozooplankton (MZ) are the major consumers of primary pro-ductivity and important contributors and modifiers of vertical flux ofmaterial to depth and play an important role in the consumption andsedimentation of new production and therewith in the modeling of thecarbon dioxide dynamics of the oceans (Morrison et al., 1999). Theirdistribution in space and time is therefore essential in understandingandmodeling community dynamics (Wishner et al., 1998), and essentialto understand physical and biological processes that structure marine

ecosystems (Hitchcock et al., 2002). They also play an important role asprey for many juvenile and adult zooplanktivorous fish (Schipp et al.,1999; Sommer et al., 2002) thus they can be termed a key factor in thecontrol of fish stock sizes (Evjemo et al., 2003; Payne and Rippingale,2001). In most subtropical and tropical parts of the world's oceanscopepods dominate the MZ community, where they comprise about75% of total abundances (Cornils et al., 2007; Deevey and Brooks,1977; Webber and Roff, 1995). Subtropical and tropical regions arealso known to be inhabited by diverse assemblages of species (Cornilset al., 2007; Deevey and Brooks, 1977; Hwang et al., 2006 2009 2010;Madhupratap and Haridas, 1986; Tseng et al., 2008). Recent informa-tion relating to distribution and community structure of the MZ inSundarban coastal regions is very scarce and about two decades old(Sarkar and Choudhury, 1988; Sarkar et al., 1985a,b, 1986a,b). An

113B.D. Bhattacharya et al. / Journal of Marine Systems 141 (2015) 112–121

estimate of the zooplankton standing stock can provide useful informa-tion on the biological production potential of the area and any changesin the water quality parameters will directly affect the communitystructure and abundances of zooplankton. Hence the present studyhas been undertaken in the Sundarban mangrove wetland, northeast-ern part of the Bay of Bengal with the following objectives: (i) to inves-tigate the spatiotemporal and seasonal variations of theMZ communitystructure; (ii) to quantify copepod composition patterns and seasonalvariations and dominance patterns; and (iii) to quantify chaetognathpopulation and their different life stages.

2. Materials and methods

2.1. Area investigated

The Indian Sundarban (21°32′ to 22°40′N and 88°85′N to 89°00′E),the largest prograding delta in the estuarine phase of the tidal Hugli(Ganges) River , has an area 9630 km2 and is situated in the low lying,humid and tropical coast of eastern India. Four sampling sites werechosen, namely, Jambu Island (S1) (21°36′10″ N–88°11′09″ E), Gosaba(S2) (22°11′02″ N–88°49′07″ E), Canning (S3) (22°12′13″ N–88°40′01″ E) and Dhamakhali (S4) (22°20′26″ N–88°53′18″ E), based on dif-ferent hydrodynamic conditions, wave energy fluxes and distancesfrom the sea (Bay of Bengal) (Fig. 1). The geographic positions of eachsite were fixed using GPS (global positioning system). These sitesbelong to a lower deltaic plain experiencing intense semidiurnal tidesand wave action with a meso-macrotidal setting (3–6 m amplitude).The average depth at the sampling locations was about 3–8 m. Threedistinct seasons are present with the following characteristics: a mild

Fig. 1.Map showing location of four sampling sites (S1 to S4) in Indian Sundarban wetland alonindicates the northern-most limits of estuarine zone affected by tidal fluctuations.

winter season between October and March, a hot humid spring seasonbetween March to June and the warm and humid southwest monsoonseason from July to October when most of the precipitation occurs(average annual rainfall ~ 1800 mm). Jambu Island (S1), a virgin Islandon the Bay of Bengal, is located in the open sea and thus faces directwave action. The sampling sites Canning (S3) and Dhamakhali (S4),are situated on the bank of the Matla River, a main tributary of HugliRiver, whereas Gosaba (S2) is situated by the Gosaba River, which isalso a tributary of Hugli River.

2.2. Collection of zooplankton samples

DuringMarch 2011 to February 2013, MZ samples were collected inthe forenoon hours during high tide on monthly basis using a RingTrawl Net (Hydro-Bios No. 438 700, Germany), mouth area 0.78 sq. m,mesh size 200 μm. The net was towed at the water surface (1 m) for10 min and the volume of water filtered was measured by a calibratedflow-meter (Hydro-Bios No. 438 110, Germany) mounted in themouth of the net. Sincemost siteswere located in shallowwaters (aver-age depth 3.53 m), zooplankton samples were collected by a horizontaltow, 1 m below the surface for each sampling (Herman and Dapolito,1985). The zooplankton were fixed with 4% buffered formaldehydesolution and taken to the laboratory for further analyses.

2.3. Zooplankton sample analyses

In the laboratory, copepod samples were sorted, preserved in 4%buffered formaldehyde for taxonomic identification with the help of abinocular microscope (LEICA BME, model no. 13395H2X). The copepod

g with the intricate river network. Dampier–Hodges as shown is an imaginary line which

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community could thus be described from both a qualitative andquantitative perspective using data expressed in terms of abundance(individual m−3). For quantitative analyses, the large size organismsother than copepods were removed manually from the sample. Theresidual sample was made up to 100 ml and a homogeneous mixtureof zooplankton was made using a stirrer. From this part, 1 ml of themixed aliquot sample was taken in a Sedgewick-Rafter counting celland examined under a binocularmicroscope. This processwas repeatedfive times for each sample and the mean value of the numerical enu-meration was calculated and expressed in ind. m−3.

Zooplankton biomass was determined by a displacement method.The displacement volume of the plankton was determined by takingthe volume difference of the whole plankton mass in measured volumeof water. The wet weight of the plankton was determined by weighingthe sampled plankton after carefully removing all the adhered waterparticles using a blotting paper, and then the dryweight of the planktonwas determined after drying the sample in an oven at 60 °C for 24 h.Finally the ashweight of planktonwas determinedbyburning the sampleat 650 °C for 6 h in a muffle furnace. All the measures were thenexpressed in gm−3. Zooplankton biomass valuewas estimated using dis-placementmethod (Margalef, 1967). Feeding habit of individual copepodhas been considered on the basis of the findings of previous workers(Islam et al., 2005; Nakamura and Turner, 1997; Stoecker and Sanders.,1985; Turner, 2004). Different maturity stages of the chaetognath Sagittabedoti were worked out on the basis of the classification by Russell(1932), later modified by Zo (1973).

2.4. Water sample collection and analyses

Simultaneously, surface water samples were collected in pre-cleaned acid-washed polythene bottles. Winkler's titrimetric method(Strickland and Parsons, 1972) was followed for the estimation of dis-solved oxygen (DO) and biological oxygen demand (BOD5: difference be-tween DO of 100% saturatedwater on day 1 and after 5 days incubation).Temperature was measured onboard using a mercury thermometer(0–100 °C) and transparency (cm) of the water was determined usinga secchi disk. pH and turbidity (nephelometric turbidity unit, NTU)were measured by a Deluxe Digital pH Meter (Labtronics, Model No.101 E) and a Turbidity meter (Electronics India, Digital TurbidityMeter 331) respectively. The dissolved micro-nutrients such as nitrate,phosphate and silicate were estimated by colorimetric methods de-scribed by Strickland and Parsons, (1972), after filtering the waterthrough 0.45 μ Millipore filter paper. Chlorophyll pigments (chloro-phylls a, b and c)were analyzed by spectrometry following the standardmethod (Parsons et al., 1984a; Strickland and Parsons, 1972). Chemicaloxygen demand (COD) was estimated by the method described byParsons et al. (1984a).

2.5. Statistical analyses

Statistical analyses were performed using statistical softwares,MINITAB 14, STATISTICA 6 and XL-STAT.While performing any statisticaltest, all the raw datawere transformed to log(n + 1) to avoid any anomaly(Turner, 1998). For comparison of the valueswith other studies in the re-gions adjacent to this study area, the following formulaewere used (Yanget al., 1999):

Yi ¼ Ni=Nð Þ � f i andR ¼ a þ b – 2cð Þ= a þ b – cð Þ � 100%;

where Yi is the dominance of species i, Ni is the number of individuals ofspecies i at all sites,N is the number of individuals of all species at all sites,and fi is the frequency of sites at which species i occurs. Species with a Yvalue of more than or equal to 0.02were defined as dominant species. Ris the seasonal replacement rate of dominant species, a and b are thenumbers of dominant species occurring in two adjoining seasons,

respectively, and c is the number of dominant species common toboth seasons (Lee et al., 2009). Canonical Correspondence Analysis(CCA) was performed with the help of XL-STAT software. The CCAmap allows to simultaneously visualize the objects (dominant copepodspecies), the sites, and the variables (water quality). Estimation of inter-specific association was based on the index of association (Southwood,1978) where, a positive association between two species is indicative ofthe similar requirement in environmental gradients, while a negativeassociation is indicative of different environmental requirements or ac-tive competition between the species involved.

3. Result and discussions

3.1. Environmental parameters

A distinct spatial and temporal heterogeneity in distribution of dif-ferent water quality parameters was observed in four sampling sites(S1 to S4) (Fig. 2). Average surface water temperature recorded duringthe study period was 25.82 ± 2.85 °C. Of all the sites, Dhamakhali (S4)showed highest mean temperature (27.68 ± 3.15 °C) and turbidity(25.33±4.03NTU) throughout the study period and the correspondinglowest values of 19.35 ± 2.38 °C and 9.5 ± 1.5 NTU respectively at thesame site.

Dissolved oxygen (DO) concentration ranged from 5.16 to6.91mg L−1. All the sites showed an averagemoderate dissolved oxygencontent (6.11 ± 0.59 mg L−1), except Dhamakhali (S4). Biochemicaloxygen demand (BOD) values are moderately low at Jambu Island (S1),Gosaba (S2) and Canning (S3) ranging from 0.86 to 1.36 mg L−1 but,in case of Dhamakhali (S4) an elevated level of BOD value was found(ranging from 1.78 to 2.41 mg L−1). Low values of dissolved oxygenand elevated BOD values coincide with the low numerical density oftotal zooplankton at this site throughout the year.

Values of pHas recorded during thepresent study ranged from7.1 to8.8. The observed variations in pH could be attributed to the relativelyhigh land drainage and terrestrial run-off at this location and to freshwater discharges from the other perennial rivers (Satpathy et al.,2009). The alkaline nature (pH N 7), with low variations in the down-stream sites, suggests that the water mass in this part of the Sundarbanremained well buffered throughout the study period and indicates thepresence of biodegradable organic matter in the water column (Sarkaret al., 2007a,b). The highest COD values (101.28–111.31 mg L−1) atJambu Island (S1) might be derived from the primary production ofthe dense mangrove forests (mainly populated with Avicennia marina,A. alba, Nypa fruticans and Excoecaria agallocha) present at this sitewhich greatly contribute to the organic matter content (Hernandez-Romero et. al., 2004). In Gautami–Godavari estuarine system, eastcoast of India, Bouillon et al., (2000) identified mangrove litter as a sig-nificant source of high dissolved organic carbon (DOC) and its effectiveconversion into microbial biomass (Benner et al., 1986; Bouillion et al.,2003) during the spring intermonsoon. Their theory of mangroveoutwelling in coastal enrichment, if proved true, would significantly in-crease the importance of microbial production (and hence that of themicrobial loop). This phenomenon can certainly alter theMZ communitystructure at this specific site (S1) of Sundarban ecosystems. The organicenrichment might be related to the presence of stenohaline detritivorecopepod species (such as Clytemnestra scutellata and Euterpina acutifrons)at S1 as these species have intense affinity towards organic load in water.High COD values in a tropical coastal wetland in Southern Mexico werealso noticed by Hernandez-Romero et al. (2004) associated withmangrove-enriched organic matter.

The nutrients in the Hugli river estuary mainly originate from thepoint sources like domestic sewage, industrial wastewater, effluentsfrom fishery and Kolkata sewage (Manna et al., 2012). In addition,non-point sources of pollution like excess fertilizers from agriculturalfield wash, street runoff during tide and flooding etc. are also the mainsources of nutrients as endorsed by Carpenter et al., 1998. During the

Fig. 2.Water quality parameters at four study sites (S1 to S4) of Sundarban. [Annual mean and standard deviation (SD)].

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south-west monsoon months (September–October), concentration ofnitrate increases considerably which is ascribed to land drainage andprecipitation (Sarkar et al., 2007b). In contrast, during the post-monsoon season (January–February), the prevalent low concentrationis linked to the biological utilization of nitrate which appears to playan important role in primary production in shallow water zones likethis estuary (MacIntyre et al., 1996). Phosphate levels were observedto be maximum (2.25 μg atom L−1) at Dhamakhali (S4) during thesouth-west monsoon period which might be derived from land-basednutrients especially from the adjacent agricultural fields. Mathewand Pillai (1990) reported that the higher concentration of phosphatein coastal waters may be attributed to enrichment by freshwaterdrainage.

3.2. Mesozooplankton displacement values

The zooplankton standing crop as determined by biomass was highduring the pre-monsoon (February–May) period, low during late mon-soon (August–September) and showed a minor secondary value duringthe post-monsoon (October–January) season (Table 1). Displacementvolumes of all the sites were high during June and August and thismay be attributed to the greater abundance of decapod larvae at thesesites. During April a peak of biomass was observed in Jambu Island (S1).

3.3. Copepod

3.3.1. Copepod composition, distribution and numerical abundanceAverage numerical abundances of total copepods, zooplankton

and the biomass values are shown in Table 1. Holoplanktons domi-nated throughout the year in all sites, ranging from 59.8 to 98.8% ofthe total MZ, whereas meroplanktons contributed 1.7–40.6% of thetotal MZ. Zooplankton abundance was higher during premonsoon(February–May) (N1000 individual (ind. m−3)) than in the SWMonsoonseason (b500 ind. m−3), which indicates a key role for salinity incontrolling the zooplankton community (Jyothibabu and Madhu,2007). Copepods were by far the most prominent in terms of speciesrichness, numerical abundance, constituting 62% to 91% of the totalzooplankton in Sundarban coastal waters. The mean abundance was(723.92 ind. m−3 ± 615.87). A total number of 41 copepod specieswas encountered, out of these, 33 calanoid species belonging to sevengenera formed the bulk of the total counts (~87.5%), followed bycyclopoids and harpacticoids each comprised four species andaccounted 10.1% 2.15% respectively. In mangrove area of northwesternTaiwan, Hsieh (2004) also reported copepods as the dominant MZgroup in different tidal periods. The higher density and relativeabundance of five calanoid copepods (Acartiella tortaniformis,Pseudodiaptomus serricaudatus, Paracalanus parvus, Bestiolina similisand Acrocalanus gracilis) at intermediate and low salinity corroborates

Table 1Detailed statistics (annual mean ± standard deviation) of the numerical density of total zooplankton and total copepod, values expressed in ind. m−3; biomass value (displacementvolume) and dry weight are expressed in ml/m3 and mg m−3 respectively.

Station Total copepod Total zooplankton Biomass Dry weight

S1 565.67 ± 90.24 972.17 ± 125.82 0.1132 ± 0.0064 0.0180 ± 0.0048S2 212.67 ± 23.26 303 ± 59.59 0.1248 ± 0.0044 0.0012 ± 0.0001S3 1394.17 ± 730.59 1458.67 ± 718.77 0.282 ± 0.0147 0.0301 ± 0.0025S4 128.67 ± 19.26 161.83 ± 32.7 0.0342 ± 0.0035 0.0011 ± 0.0001

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the opportunistic characteristics of these species and might be relatedto their high capacity to develop in eutrophicated and polluted areas(Bhattacharya et al., 2014). Species adaptability to the habitat and envi-ronmental heterogeneity at four sites of Sundarban could influencesuch discrete assemblages of MZ in Sundarban coastal regions.

Thedominant copepod species belonged to the families Paracalanidae,Acartiidae and Pontellidae that tolerate a wide range of salinity oscilla-tions (7.0–31.0 ppt) throughout the year and play major roles in termsof feeding ecology and carbon transfer in this estuarine system (Turner,2004). In contrast, Heliodiaptomus cintus, Acartia tropica, Paracalanusdubia and Mesocyclops sp. were abundant in late monsoon period(August) when the salinity drastically dropped (0.50–5 ppt) denotingtheir limnetic nature (Tiwari and Nair, 1993). The presence of Euchaetamarina, Clytemnestra scutellata and Euterpina acutifrons are exclusivelyrecorded at Jambu Island (S1) (salinity 21.0–34.5 ppt) which impliestheir stenohaline characteristics which corroborated the previousstudies by Sarkar et al. (1986 a,b) from the same coastal region.Hence it is evident that the functional diversity of copepods recordedunique features sharing ecological niches most precisely and efficientutilization of coastal resources.

3.3.2. Food and feeding habits of the copepodsHerbivorous copepods were found to be dominant over the omni-

vores and carnivores throughout the year and this specific trophiccomponent contributed 52–63% and 66–82% of the total number ofcopepodnumbers at Jambu Island (S1) andDhamakhali (S4) respectively.Most strikingly, an exclusive overall dominance of the carnivorous cope-pods at Canning (S3) was observed mainly due to the presence of thecyclopoids of the family Oithonidae (Giesecke and González, 2004;Lampitt, 1978). In contrast, the omnivores contributed the major partat the site Gosaba (S2) due to presence of species belonging to the familyAcartiidae. During the premonsoon months of high salinity, omnivorouscopepods dominated over the herbivores. Detritivores were found onlyat the site Jambu Island (S1). Two omnivore calanoid copepod species(A. spinicauda and A. tortanifromis) showed very significant positive asso-ciations (Index of association I=1) indicating similar requirement in en-vironmental gradients, whereas, a solitary representative of carnivores(O. brevicornis) and herbivores (P. parvus) showed negative significantassociations (I=−0.69)which are indicative of different environmentalrequirements or active competition between the species involved(Southwood, 1978).Most strikingly, small scale site-specific assemblagesof copepods were observed in relation to the prevailing feeding guildswhich are mainly attributed to different levels of food availability atthat particular site. Different copepod species have different feedingskills. Calanoid copepods have a complex behavior and their swimmingpatterns that affect both the way they avoid predation (Ohrnan, 1988)and the way they gather food (Tiselius and Jonsson, 1990). Accordingto Koehl (2004) calanoid copepod shifts their feeding habit by morpho-logical alteration/modifications depending on the food availability. Themain food for the copepods are the phytoplanktons (Parsons et al.,1984b), variability of which depends on environmental conditionsin oceanic region in contrast to physical accumulation of particles(suspended loads) in coastal waters brought through river dischargeimpinging photosynthetic activity, local upwelling and sinking

controlled by climatic events (e.g., prevailing wind systems), seasonalnutrient enrichment or impoverishment, differences in growth ratesof individual plankters and nutrient uptake and predation patterns offood chain etc could be held responsible (Parsons et al, 1984b).

3.3.3. Coexistence of Paracalanidae and Acartiidae familiesTwo calanoid copepod families, namely Paracalanidae and Acartiidae,

formed the bulk of the numerical abundance in majority of the sites(except at Canning, S3), contributing about 25–38% (Paracalanidae)and 23–35% (Acartiidae) of the total copepod biomass. Similar coinci-dence of dominance of the family Paracalanidae with high numericaldominance of Paracalanus aculeatus was encountered by Hsieh,(2004) in the southwestern coastal part of Taiwan. The significant roleof this calanoid family to the total copepod community from Indiancoastal waters was also established by other workers (Fernandes andRamaiah, 2009; Goswami, 1996; Padmavati and Goswami, 1996). Thecongeneric association of five and six species of the families Acartiidaeand Paracalanidae respectively was largely evident at Jambu Island(S1). However, their distribution was erratic at other three study sites,exhibiting site-specific abundance of a particular species. The calanoidsAcartiella tortaniformis, A. spinicauda as well as B. similis were ubiqui-tously present at all four sites and thus seem to be well-adapted tothe stresses of the estuarine environment. It is worthwhile to mentionthat the omnivore A. tortaniformis, found exclusively in Indian coastalwaters (Razouls et al., 2008), was the most abundant at the site Gosaba(S2) and might be considered as an index to prevailing pollution load(Gajbhiye et al., 1991). These coexisting species exhibited certain strat-egies (e.g., shifting the feeding habit) in their opportunistic behaviors, inorder to adapt to a highly variable marine environment, such as thatfound in Sundarban coastal regions (e.g., Lakkis, 1994).

3.3.4. Contribution of the small-sized copepodsAn overall dominance and diversity of the small-sized copepods

(b1 mm) belonging to the genera Paracalanus, Acrocalanus, Bestiolina,and Oithona was pronounced accounting ~48–67% of the total MZ.Thus they shaped theMZ community structure across the area, reducingthe importance of large-sized forms. The influence of copepods of small-sized fraction on estuarine zooplankton has also been reported fromother tropical (Darwin Harbor, northern Australia, Duggan et al, 2008;Sangga estuary, Malayasia, Chew and Chong, 2011; Danshuei river estu-ary, northern Taiwan, Hwang et al., 2004, 2010 ; Godavari river system,east part of India, Rakhesh et al., 2013), and temperate (Waquoit Bay,MA, Lawrence et al., 2004; Galway Bay, west coast of Ireland, McGintyet al., 2012; Gironde estuary, south-west Europe, Chaalali et al., 2013)systems.

Small copepods connect the classical and microbial food-webs andare used as prey for other pelagic carnivores. Hence they exhibit variousreproductive and feeding strategies which help tomaximize populationsize, in order to counter heavy losses due to predation (Turner, 2004).The unique contribution of the four congeneric species of the familyOithonidae (Oithona similis, O. brevicornis, O. rigida and O. aurensis)was markedly evident at Canning (S3) where they accounted for 87.2–98.3% of the total zooplankton numbers with a maximum abundanceof 2776 ind. m−3 during April, 2007. The dominance of Oithonidae

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suggests their high adaptability to trophic and hydrologic conditions.The overall stable dominance of Oithonidae at the site Canning (S3)might be attributed to continuous reproduction and reduced mortalityrates (Nielsen and Sabatini, 1996; Pages et al., 1996). In contrast, a com-plete absence of Oithona at Dhamakhali (S4) is a characteristic featurewhich cannot be fully explained. However, prevailing high turbid condi-tion (25.33± 4.03 NTU) at this sitemight be the causative physical pro-cesses for this anomalous distribution. The genus Oithona contributes asubstantial part of the total zooplankton numbers, accounting for nearly40 to 50% overall (except Canning S3), a situation also observed byAtkinson (1998) in the Yellow Sea, China. In addition, Hsieh (2004)reported an abundance of Oithona copepods of 37.66% during a hightide period in the mangrove area of the Danshuei river estuary, north ofTaiwan. He reported the abundance of copepods in small size categories(b1.0 mm and 1–2 mm) was significantly higher than large size catego-ries (N2.0 mm). Dominance of the small copepods might be related tothe following key factors: (i) efficient feeding at low food concentrationand low metabolic rate (Boto and Bunt, 1981); (ii) possess much higherper stage growth rate and high egg production rate and rapid per-stagegrowth rate (Turner, 2004); (iii) lower predation by visual predatorscompared to larger copepods (Kimmerer, 1991) and (iv) a balancebetween food concentration and predation pressure (Ueda, 1991).

3.3.5. Species diversityCopepod species richness (R1) and diversity index (H′) values exhib-

ited wide variations, reaching their maximum values at Jambu Island(S1) andminimumvalues at Dhamakhali (S4).Maximumvalues for spe-cies richness (2.12) and diversity (4.19) were recorded at Jambu Island(S1), and this might be due to the intrusion of stenohaline species (fourin number) from the Bay of Bengal. In contrast, theminimum values forspecies richness (0.24) and diversity (1.7) were recorded at the siteDhamakhali (S4), where four calanoid copepod species (B. similis,Acartiella tortaniformis, Acartia spinicauda and Pseudodiaptomusserricaudatus) were persistent and dominated throughout the year.The co-occurrence of these copepods is due to local effects which revealthat they might share advantageous life history traits that make themmore successful (Dur et. al., 2007). The lowest evenness index (J)(0.26) was found at Canning (S3), and the highest evenness (0.56)was recorded at Jambu Island (S1). Species diversity was recorded lowduring monsoon months (June to September), but it gradually in-creased during latemonsoon (August-September) and post-monsoonmonths (October to January). However, comparatively high values ofspecies diversity (average 0.86± 0.08) associatedwith species richness(average 1.62 ± 0.74) were observed at Canning (S3) where thesefactors were influenced by the absolute dominance of a solitary species,O. rigida, which suggests an asymmetric distribution of resources andrepresents a reduced stage of complexity (Trujillo and Morales, 2000).

3.4. Chaetognaths, density of maturity stages

Chaetognaths were represented by two species, S. bedoti, a tropicalestuarine species and S. enflata, an oceanic species (Ramaiah and Nair,1993). The total chaetognath population was dominated by the formerone while the latter was found in low numbers during high salinityperiods (32–27 ppt) exclusively at Jambu Island (S1). S. bedoti showedan average numerical abundance of 29.28 ± 2.97 ind. m−3, whereas,the highest number of S. enflata was 9 ind. m−3 during April–May.Stage I of S. bedoti was predominant throughout the year at all thesites (Fig. 3), exhibiting its maximum numerical abundance(55 ind. m−3) during late SW monsoon period (September–October)at Jambu Island (S1). But a definite seasonal pattern in the occurrenceof the maturity stages of S. bedotiwas not clearly observed. The contin-uous presence of the juveniles of the species was also recorded fromCochin backwaters (Nair, 1973) Mumbai coastal waters, the southernand western part of India respectively. Nair (1973) pointed out thatthe occurrence of juveniles in most of the collection is suggestive of

continuous breeding which is also prominent in Indian Sundarbancoastal waters. Higher percentage contribution of developing stages ofS. bedoti is suggestive of the fact that the species prefers an estuarine en-vironment for its development. The lowest abundance (12 ind. m−3) ofStage I was found at Dhamakhali (S4) coinciding with lowest overallzooplankton abundance (124 ind. m−3). Stage II was present only duringthe winter months (November–January). The maturity stage III was veryscarcely present exclusively at Jambu Island (S1) which is likely due totheir preference to stay in deeper layers (Alvarino, 1964; David, 1955;Mackintosh, 1937). Hsieh (2004) demonstrated the highest record ofchaetognaths was 11.05% and 15.38% of total zooplankton numbersduring high tide and low tide periods in a mangrove area respectively.This taxon is commonly identified from zooplankton samples and itsabundance ranked third.

3.5. Statistical analyses

TwowayANOVAwas performedwithin sites andmonths consideringthe studied copepod species of diverse feeding guilds taken into account(as shown in Table 2). Themajority of the copepod species showed signif-icant variations between sites except three copepod species O. rigida,A. tropica and A. dubia. However, these species did not exhibit any signif-icant variation between months except A. dubia.

The correlation coefficient between any two pairs of the copepodfamilies Paracalanidae, Pontellidae, Oithonidae and Ectinosomidae pro-vides evidence that these families combine to form a group by them-selves. The families Acartiidae, Oithonidae and Pseudodiaptomidaeshow negative correlations with other families implying formation ofanother group by themselves (as shown in Table 3).

Results of stepwise multiple regression analyses revealed that amajority of the dominant copepod species, as well as the diversityindex values, were related to water temperature at all the four sitesfollowed by dissolved oxygen and salinity (Table 4). The best regressionequationwas shown byA. gracilis and B. similis at Jambu Island (S1)withR2 values 92.52 (P = 0.108) and 91.65 (P = 0.046) respectively.B. similis, in particular, reached a maximal Y value of 0.69 associatedwith high abundance in post-monsoon, among all species throughoutthe year (Table 5) at all three seasons. Oithona brevicornis showedmod-erate Yi values as follows: premonsoon (0.33), monsoon (0.31) andpostmonsoon (0.34) as this is considered as organic pollutant-tolerantspecies (Anakubo and Murano, 1991; Uye, 1994). The large amount ofriver run-off from the upstream during southwest monsoon carriesagricultural sewage as well as mangrove litter to the downstream. Infact, the supremacy of the ten dominant species fluctuated seasonally.According to the replacement rates of the copepod community structurebetween two adjoining seasons (Southwood, 1978), values of thepremonsoon–monsoon, monsoon–postmonsoon and postmonsoon–premonsoon, interchangeswere 23.08%, 14.28% and 21.43%, respectively.The highest replacement rate during premonsoon–monsoon is mainlydue to shifting of estuarine copepod species and intrusion of freshwater copepod species (such as Cyclops sp., Mesocyclops sp., Acartiatropica, Paracalanus dubia etc.) with huge fresh water runoff fromupstreams.

The CCA map allows simultaneous visualization of the objects (domi-nant copepod species), the sites, and the variables (temperature, salinity,chemical oxygen demand (COD), nitrate, phosphate, silicate and chl aconcentration in surface water). The map, as shown in Fig. 4, shows thatfor L. euchaeta and A. spinicauda the frequency is more associated withhigh salinity, COD and chl a but low temperature, nitrate and phosphateconcentration, as both of these species are omnivore in nature, feedingmainly on phytoplankton as well as on small copepods (Wong et al.,2000). The frequency of P. parvus was more associated with high tem-perature proving itself a warm water species, which is also reportedby Stephen (1984) and Wong et al., (2000) in the Arabian Sea andZhujiang estuary, China respectively. The frequency of occurrence ofB. similis is associated with high phosphate concentration. Similarly,

Fig. 3. Canonical Correspondence Analysis (CCA) ordination diagram of planktonic taxa, samples and environmental data of four study sites (S1 to S4) in Sundarban. Only the dominantcopepod species are considered, the sites which grouped together are indicated by ellipses.

118 B.D. Bhattacharya et al. / Journal of Marine Systems 141 (2015) 112–121

the calanoid A. tortaniformis has clustered at Dhamakhali (S4) showingits affinity to phosphate concentration. The high concentration of phos-phate indicated that land-basednutrients from the adjacent agriculturalfields near this site contributed greatly. Mathew and Pillai (1990)opined that the higher concentration of phosphate in coastal watersmight be enriched by freshwater drainage (Sarkar and Bhattacharya,2008, 2010).

Table 2Result of two way ANOVA, nature of feeding guilds and the maximum numerical abundance o

Feeding guild Between stations

Paracalanus parvus, (Claus, 1863) H ⁎⁎

P. indicus, (Wolfenden, 1905) H ⁎⁎

P. dubia, (Sewell, 1912) H NSAcrocalanus gibber, (Giesbrecht, 1888) H ⁎⁎

Bestiolina similis, (Sewell, 1914) H ⁎

Acartia spinicuada, (Giesbrecht, 1889) O ⁎⁎⁎

A. tortaniformis, (Sewell, 1912) O ⁎⁎⁎

A. plumosa, (Scott, 1894) O ⁎

A .tropica, (Ueda & Hiromi, 1987) O NSPseudodiaptomus serricaudatus, (Scott, 1894) H ⁎⁎

P. annandalei, (Sewell, 1924) H ⁎

Canthocalanus pauper, (Giesbrecht, 1888) H ⁎

Eucalanus subcrassus, (Giesbrecht, 1888) H ⁎⁎

Labidocera euchaeta, (Giesbrecht, 1889) H ⁎

Temora turbinata, (Dana, 1849) H ⁎⁎

Corycaes danae, (Giesbrecht, 1891) H ⁎

Oncea venusta, (Philippi, 1843 ) H ⁎⁎

Oithona rigida, (Giesbrecht, 1896) C NSO. brevicornis, (Giesbrecht, 1891) C ⁎

O. similis, (Claus, 1866) C ⁎⁎⁎

Clytemnestra scutellata, (Dana, 1847) D ⁎

Euterpina actifrons, (Dana, 1847) D ⁎

S. bedoti, (Beraneck, 1895) C ⁎

Lucifer Hanseni, (Nobili, 1905) C ⁎

Nauplius – ⁎⁎

Zoea – ⁎⁎

NS = not significant.⁎ = significant at P = 0.000.⁎⁎= significant at P = 0.001.⁎⁎⁎ = significant at P = 0.005.H = herbivore.O = omnivore.D = detritivore.C = carnivore.

3.6. Decadal change in copepod community structure

A pronounced decadal change in zooplankton community composi-tion along with their feeding guilds was noticed while comparing theprevious data published by Sarkar et al. (1985a, b, 1986a, b) during1980–1986 and the present findings of Sundarban coastal environmentwith same instrumental and analytical setup. Herbivorous copepods

f dominant mesozooplankton group encountered in coastal regions of Sundarban.

Between months Maximum abundance

Stations Months abundance (ind/m3)

NS 1 February 34NS 2 June 44⁎⁎⁎ 1, 3 October 89NS 1 June 28NS 3 February 374NS 1 June 84NS 2, 3 April, August 174NS 1 April 39NS 1 October 28NS 1 February 64NS 1 February 7NS 1 February 21NS 1, 4 February, April 31NS 1, 4 February, April 31NS 1 February 19NS 1 February, April 64NS 1 June, August 4NS 3 December 1947NS 1, 2, 3 December, June 598NS 3 December 251NS 1 April 31NS 1 February, April 39NS 1, 3 February, April 27NS 1 April 10NS 1, 3 February, June 348NS 2 April, June 159

Table 3Correlationmatrix showing correlations betweenmajor copepod families (n = 9) (signif-icant values are shown in bold).

A B C D E F G H

B 0.53⁎⁎

C −0.35 −0.68⁎

D −0.19 0.06 −0.03E −0.12 −0.08 0.28 0.59⁎

F −0.03 0.01 −0.07 0.75⁎ 0.74⁎

G 0.14 0.14 −0.19 0.69⁎ 0.66⁎ 0.88⁎

H 0.14 0.17 −0.20 0.79⁎ 0.68⁎ 0.89⁎ 0.85⁎

I 0.62⁎⁎ 0.45 −0.21 −0.36 −0.22 −0.32 −0.17 −0.21

A=Paracalanidae, B=Acartiidae, C=Pseudodiptomidae, D=Calanidae, E=Eucalanidae,F = Pontellidae, G = Temoridae, H = Corycaedae, I = Oithonidae.⁎ Significant at b0.01.⁎⁎ Significant at b0.05.

Table 5The seasonal dominance (Y) and abundance (X, ind. m−3) of dominant species of copepodsin four sites of Sundarban mangrove waters; (#) denotes Y b 0.02. The data are consideredfor all stations (S1 to S4) in Sundarban together.

Dominant species Premonsoon Monsoon Postmonsoon

Y X Y X Y X

Paracalanus parvas # # 0.036481 40.12P. indicus 0.0416 29.25 0.029512 27.62 0.025912 28.5P. dubia # 0.482607 225.87 0.259348 142.62Bestiolina similis 0.473067 332.62 0.628964 392.5 0.693488 508.5Acartia spinicauda 0.095467 67.12 0.088736 55.37 0.105694 58.12A. tortaniformis 0.351467 247.12 0.585965 274.25 0.433004 238.12Pseudodiaptomusserricaudatus

0.032 22.5 0.104961 65.5 0.10774 79

Canthocalanus pauper 0.0304 21.37 0.037257 23.25 0.024889 18.25Eucalanus subcrassus 0.0704 37.12 0.059291 27.75 0.078645 43.25Labidocera euchaeta 0.0272 19.12 0.046672 29.12 0.050972 37.37Corycaeus danae # 0.023369 43.75 0.02523 55.5Oithona brevicornis 0.335289 353.62 0.341323 319.5 0.314581 346O. similis 0.039111 41.25 0.237431 222.25 0.041709 45.87O. rigida 0.346133 730.12 # 0.186555 410.37Number of species 11 12 14

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were found to be dominant throughout the year constituting ~66–82%of the total copepods while omnivores contributed a substantial partonly during the monsoon and post-monsoon during 1980–1985. Incontrast, herbivores and omnivores contributed 55.47–79.48% and26.20–59.30% respectively during recent times. Again, during the1980s,the copepod community was dominated by Saphirella indica, Pontellaandersoni, Pseudodiaptomus hickmani, Cladostrata brevipoda, Laophontesetosa and Centropages dorsispinatus (Sarkar et al., 1985a,b, 1986a,b)which are totally absent in recent times. These sharp changes might bedue to biological interactions like predation and competition, changesin the feeding habit of the copepod species, as well as due to climatechange. Decadal changes in increase of the water quality parameters(such as salinity, water temperature, ph and DO) at different magnitudesin the coastal regions of Sundarban were recorded by previous workers(Mitra et al, 2009; Sarkar and Bhattacharya, 2008, 2010). In addition, sig-nificant changes of climate variables (evaporation, wind speed, relativehumidity, sunshine hours etc., ) was also precisely detected by Mandalet al., 2013 over last three decades (1982–2010) in Sagar Island, thelargest island of Sundarban deltaic complex. This climate-driven multi-farious changes is reflected in distribution and diversity of the dominantcopepod species (B. similis, A. tortaniformis, P. parvus and C. pauper) inpresent observations, were either absent or numerically scarce during1980s. This suggests a shift in the functioning of the pelagic ecosystem(Molinero et al., 2008) revealing that changes in biodiversity andcommunity structure reflect adjustments of pelagic ecosystems to

Table 4Stepwise multiple regression [y = ax1 + a x2 + …………. + anxn] between dominantcopepod abundance and environmental factors as independent variables for four studysites (S1 to S4) in Sundarban wetland.

Stations Copepod species R2 P-value

S1 P. parvus 84.82 0.083A. gracilis 94.52 0.108B. similis 91.65 0.046A. spinicauda 84.15 0.092A. tortaniformis 87.53 0.080E. subcrassus 81.31 0.012C. danae 82.41 0.144C. scutellata 84.48 0.044E. acutifrons 87.30 0.006

S2 P. aculeatus 79.25 0.004A. gracilis 88.05 0.079C. pauper 83.85 0.002E. subcrassus 85.42 0.112

S3 P. indicus 88.83 0.000A. tortaniformis 89.42 0.035O. similis 84.76 0.051O. brevicornis 76.32 0.017O. rigida 63.36 0.076

S4 B. similis 73.65 0.098A. tortaniformis 68.6 0.017P. serricaudatus 68.70 0.116L. euchaeta 76.60 0.010

large-scale climate-driven modifications in water mass distributions(Beaugrand et al., 2002; Hooff and Peterson, 2006). The decadal changesin copepod community structure could be considered as biological indi-cators to climate change related stressors on biodiversity. The data indi-cate the extreme flexibility of copepods in adapting to a fluctuating andhostile environment and thus acting as causal link between climatechange and alteration in biodiversity in Sundarban.

The observed reorganization of plankton communities might alsohave dramatic socioeconomic impacts through the effects on commercialfisheries. During their larval stages, all fish consume zooplankton andsome adult fish continue to be at least planktivorous. Hence abundanceand timingof copepodsmight affectfish recruitment, although the detailsof this linkage are only just being revealed.

4. Conclusion

The study highlights short-term spatiotemporal variations of thediversity, distribution and abundance of MZ in a meso-macrotidaltropical and turbid estuarine system of Sundarban wetland. Thisseems to be strongly coupled to hydrography, especially salinity, Chl aand transparency along with physical and local factors. The discrete as-semblage of MZ, ‘site-specific’ heterogeneity of the copepods and theirfeeding guilds as well as numerical dominance and diversity of smallsize copepods are distinguished features of the present investigationwhich demand further studies. The pronounced decadal changes inMZ composition as recorded is a matter of concern and has implicationsfor the Convention of Biological Diversity and many other biodiversityconservation programmes (Gray, 1997).

As a consequence of ongoing and intensified water quality degrada-tion across the coastal regions of Sundarban, the interspecific competitionamong the presently dominant tolerant MZ and more sensitive onesmight get changed. Water quality deterioration will probably also affectfeeding conditions for zooplankton (e.g., increase in phytoplankton-detritus ratio) and finally trophic structure of the ecosystem (Muylaert,1999).

Anthropogenic activities and climate-induced forces may causereplacement of large copepods with small ones and this shift in sizestructure of the copepod community in Sundarban may have nega-tive impact for existence of other zooplankton community andzooplanktivorous fishes. Hence a long term trend analyses related tochanges in MZ diversity, abundance and production is recommendedto identify the complex biota–environment interactions. This wouldhelp for a deeper understanding of MZ variability in this vulnerablemegadelta which was largely devastated due to the severe tropicalcyclonic storm ‘Aila’ occurred on 25thMay 2009. This caused enormous

-10

0

10

20

30

40

50

60

70

J F M A M J JY A S O N D

ind

. m-3

Stage I Stage II Stage III

Fig. 4.Graph showing the annual distribution of threematurity stages of the chaetognath Sagitta bedoti in Sundarban coastal waters (pooledmean values of four study sties (S1 to S4) havebeen considered; values expressed in ind. m−3).

120 B.D. Bhattacharya et al. / Journal of Marine Systems 141 (2015) 112–121

changes in water quality and community structure of MZ documentedby Bhattacharya et al., (2014) from coastal regions of Sundarban.

Acknowledgments

The researchworkwasfinancially supported by bilateral collaborationbetween the National Science Council of Taiwan (NSC 102-2923-B-019-001-MY3) and Department of Science and Technology & Confederationof Indian Industry of India (GITA/DST/TWN/P-48/2013) for the researchproject titled “Mesozooplankton population dynamics as a response toenvironmental changes of two tropical mangrove wetlands in India andTaiwan: An approach to ecosystem indicator” under India-Taiwan Coop-eration Program in Science and Technology.

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