Wetlands Ecology and Management 13: 55–67, 2005.
# Springer 2005
Spatiotemporal variation in benthic polychaetes (Annelida) and relationships with environmental variables in a tropical estuary Santosh Kumar Sarkar1,*, Asokkumar Bhattacharya1, Sankar Giri3, Badal Bhattacharya3, Dipak Sarkar4, Dulal Chandra Nayak4 and Asish Kumar Chattopadhaya2 1
Department of Marine Science; 2Department of Statistics, University of Calcutta, 35 B.C. Road, Kolkata, India; 3Department of Metallurgical Engineering, Jadavpur University, Kolkata, India; 4National Bureau of Soil Survey and Land Use Planning (ICAR), Regional Center, Block DK, Sector II, Salt Lake, Kolkata, India; *Author for correspondence (e-mail:
[email protected]; phone: +91 33 2889 0822; fax : +91 33 2476 4419)
Received 23 December 2002; accepted in revised form 5 July 2003
Key words: Ecology, Heavy metals, Mangrove forest, Pollution, Polychaetous annelids, Sundarban Biosphere Reserve
Abstract Annelida constitute a dominant functional component in soft-bottom macrobenthic communities and reveal a wide range of adaptability to different marine and coastal habitats. Analyses in different polychaete assemblages and their responses to habitat conditions reflect the biological effects of marine pollution and habitat disturbance. The present study is designed to study colonization and community structure of polychaetes in two ecologically distinct locations of the Sundarban Biosphere Reserve on the northeast coast of India. Polychaete assemblages are characteristically different at the two sites in the extreme northern (Ghusighata) and southern (Gangasagar) portions of the Biosphere Reserve. Levels of heavy metals in polychaete body tissues also reveal interspecific and regional variations. The predominant polychaete fauna exhibited a distinct and unique assemblage of two types: (i) Mastobranchus indicus – Dendronereides heteropoda in the sewage-fed substratum at Ghusighata and (ii) Lumbrinereis notocirrata – Ganganereis sootai – Glycera tesselata at Gangasagar at the mouth of the Hugli estuary where chronic anthropogenic stress and contamination with agricultural and industrial effluents occur. The faunistic composition of polychaetes and their potential for the accumulation of heavy metals from the ambient medium are distinctly different. The study demonstrates that textural composition of the sediments, together with hydrodynamic and geotechnical properties, seem to have the greatest control to quantify the differences of the polychaete community in the two study stations. An in-depth comparative study of polychaete community structure at multiple spatial scales is strongly recommended for future environmental impact assessment in this fragile environment. Introduction Polychaetes, the dominant component of softbottom macroinvertebrate communities, are diverse, abundant, and ecologically significant functional component of coastal ecosystems, exhibiting a high stability and adaptability to different habitats (Simboura et al. 1995, 2000). These worms are pivotal parts of food webs, multiplying trophic
connections with their richness, abundance, and diverse feeding strategies (Fauchald 1977), and they serve as an important descriptor of environmental conditions (Gambi and Giangrande 1986; Inglis and Kross 2000; Samuelson 2001). Polychaetes may directly affect sediment biogeochemical processes (Rhoads 1985) and sediment
56 stability (Aller 1983) while providing a coupling between meiofaunal and macrofaunal communities (Hodson et al. 1981; Robertson and Lenanton 1984). These organisms tend to be the initial macrobenthic colonists after any physical and/or chemical disturbance, and a large number of taxa inhabit the most stressed regions of a pollution gradient (Pearson and Rosenberg 1978). Natural habitat disturbance can result in major changes in salinity, temperature, currents, and wavegenerated resuspension of sediments (Thistle 1981; Orlando et al. 1993; Bhattacharya et al. 2000). Anthropogenic sources of stress often include energy production (Gaston 1985; Gaston and Edds 1994), disposal of channel dredged material (Ingle et al. 1955), over-enrichment of nutrients (Rabalais 1992) leading to hypoxia (Harper 1977; Gaston et al. 1985), and enrichment of toxic materials (Macauley et al. 1994). The intertidal belt of the Sundarban Biosphere Reserve (SBR) supports diverse macrobenthic fauna (Mishra et al. 1983; Subba Rao et al. 1983; Chaudhury et al. 1984; Chakraborty et al. 1986) of which polychaetes constitute the most important community (Nandi and Chaudhury 1983). Little information is available on the distribution and community structure of polychaetes from this tropical coastal environment, but Sarkar et al. (1999a, b) have studied the probable role of polychaetes in monitoring pollution-induced changes in the SBR. The present work was undertaken to determine the degree of disturbance or stress inflicted on the benthic polychaete communities and to identify certain polychaete species that may be used for specifying the rate of environmental degradation on a local or regional scale in tropical coastal environments. In addition, attempts were made to understand the response of individual polychaete species to organic enrichment and obtain information necessary to evaluate the status of the coastal environment.
Methods Study site The SBR represents the largest single continuous tract of diverse mangrove forest (9630 km2) in India, and encompasses the lowest part of the vast
estuarine delta of the Ganges–Brahmaputra rivers. Situated in the Bengal Basin, the area exhibits many features that are typical of deltas in southeast Asia (Woodroffe 2002). It has the potential for being a global biodiversity ‘hotspot’ as it is a potential reservoir of very rich and diverse faunal and floral communities (Bhattacharya and Sarkar 2003). The climate is humid (up to 96%), tropical oceanic with three prominent seasons; a hot dry season from March to June with temperatures ranging from 28 to 38 C (pre-monsoon), a wet season from July to October with temperatures ranging from 20 to 37 C and heavy rainfall with an annual average of 1600 mm (monsoon), and a cool dry season from November to February with temperatures of 10–22 C and low precipitation (post-monsoon). Study stations were separated by a distance of about 220 km along a NNE–SSW transect and belong to the northern and southern extremities of the SBR with contrasting tidal environments, wave energy fluxes, distance from the sea, and differential human interference. These contrasting habitats were selected in order to find out the sensitiveness in the behavior of polychaete communities to different environmental conditions. Station 1 at Ghusighata (latitude 21 000 N– 21 530 N and longitude 88 020 E to 88 150 E) is a shallow coastal area, situated at the northern boundary of the SBR (Figure 1). The area belongs to the low–lying mesotidal (2–4 m tidal amplitude) flat of the Bidyadhari River, receiving semidiurnal tides with slight diurnal inequality. Situated at a distance of about 210 km from the sea face of the Bay of Bengal, the area is generally sheltered from direct wave action being. This tidal system is heavily contaminated by outfall from a 20 km long sewage canal from the Kolkata (former Calcutta) metropolis with a population of 14.5 million. Tannery byproducts and aquaculture wastes derived from adjoining areas also enter the system. As a result, sediment and water quality problems are increased in the absence of flushing by any perennial source of water. Station 2 at Gangasagar (latitude 21 310 N to 21 530 N and longitude 88 020 to 88 150 E) is situated on the extreme southern fringe of Sagar Island at the mouth of the Hugli estuary (Figure 1). The Hugli River embraces the island on the north and
57
Figure 1. Map showing location of sampling sites in the Sundarban Biosphere Reserve on the northeast coast of India.
northwest and the Mooriganga River on the east. Seawater from the Bay of Bengal washes the southern fringe of the island including the study area. The study site, situated in an estuarine macrotidal (>4 m amplitude) regime, is regularly flushed by semi-diurnal tides with little diurnal inequality. Wave energy is moderate, except in some sheltered areas behind the bars where patches of muddy deposits provide habitat for polychaetes. The polychaete beds often shift from one place to another during periods of seasonal cyclonic storms when wave energy becomes very high. Such shifting of positions of estuarine mud also results in mixing of sediments (Dyer 1972). In addition to the annual ‘Sagar Mela’ – a pilgrim fare of over half a million of people – the area is impacted by anthropogenic stresses arising from rapid growth of settlements, aquaculture practices, and tourism throughout the year. Habitat conditions under this environment allow for a better sustainability of polychaete species both in number and diversity.
Sampling and analysis During March 1999–February 2000, polychaete samples were collected from 25 25 15 cm areas between mean high water and mean low water lines. Three replicate random samples were pooled, sieved through 0.5 mm mesh size sieve, narcotized by magnesium sulfate solution, and preserved in 4% buffered formalin. After staining with Rose Bengal, the samples were identified to taxonomic level using a stereomicroscope, and polychaete density was expressed in number per square meter. Hydrological parameters (salinity, dissolved oxygen) were determined using standard methods (Strickland and Parsons 1968). Organic carbon content of the soil was determined following Walkey and Black (1934) rapid titration method. Mechanical analyses of substrate sediments were done by sieving in a Ro-Tap shaker (Krumbein and Pettijohn 1938), and statistical computation
58 of textural parameters was done by using the formulae of Folk and Ward (1957) and following standards of Friedman and Sanders (1978). Relative permeability of the sediment was measured by dropping a 164 g, 10 mm diameter stainless steel rod down a 1 m tube. The depth to which the rod penetrated into the sediment was measured four times at each station and the mean was taken (Bally 1983). Available phosphorous was extracted from the soil with 0.5 M NaHCO3 at pH 8.5 (Olsen et al. 1954). Available nitrogen was estimated by the alkaline KMnO4 method (Keeney and Bremner 1966). For heavy metal concentration analysis, 20 congeneric polychaete species of uniform size (Simpson 1979) were collected from each station, transported to the laboratory in acid-washed plastic containers (Moody and Lindstrom 1977), depurated properly for 4–5 days (defecation of sediments and any undigested materials), and dried to a constant weight at 80 C. Samples were pulverized and homogenized in a teflon mortar and digested using a HNO3 and H2O2 mixture in the ratio of 5 : 1 of proanalysis Merck (Dalziel and Baker 1983). Total mercury concentration was determined after reduction with 10% stannous chloride solution using cold vapor atomic absorption spectrometry (CVAAS) with a mercury hydride system equipped with an electrodeless discharge lamp and EDL system 2 generator. Other metal concentrations were determined by aspirating the sample into a flame atomic absorption spectrophotometer (Perkin Elmer 2380) with a deuterium background corrector and acetylene as fuel. All glassware used in metal analyses were precleaned with pyroneg detergent, thoroughly rinsed, and soaked in 10% nitric acid for at least one week before rinsing four times with deionized water prior to use. Accuracy and precision of the method used was established by analysis of a reference material (fish flesh homogenate MA-A-2) obtained from IAEA, Monaco. Analyses were done in triplicate, and the mean values expressed in g g1 dry wt1 Blank digests were also prepared to determine background correction in the reagents. Replicates were pooled and the total number of individuals for each species was determined. Data were used to calculate the following descriptive measures: species richness (S) (Margalef 1968), number of individuals m2, Shannon–Weaver
diversity index (H0 ) Shannon and Weaver (1963) and Pielou (1977) evenness (J) of distribution of individuals among species. The degree of similarity between the two stations in each month was determined using a coefficient of similarity (Rosenberg 1975) calculated as: (C 100)/(A + B C ) 100, where A and B are the number of species in each sample and C is the number of species occurring in both samples. The raw data, expressed as number of individuals per m2 (mean value of the replicate samples), were transformed using the transformation: Yji ¼ log(xji + 1) (Field et al. 1982), where Yji denotes values of polychaete density corresponding to the j-th polychaete and i-th time period.
Results Hydrodynamic and textural settings of the study sites Hydrology of these coastal waters presents a cyclic pattern, characterized by significant deposition and tidal interplay. A sharp contrast in salinity and dissolved oxygen values between the two stations was noticed: salinity values ranging from 0.05 to 10.08 ppt and 1.06 to 27.2 ppt at Station 1 and Station 2, respectively, with the attainment of lowest and the highest values during the late monsoon and pre-monsoon times, respectively. Dissolved oxygen values ranged from 0.27 to 2.80 ml l1 and 5.10 to 8.30 ml l1 at Station 1 and Station 2, respectively, with lowest values during the premonsoon season and highest values during the post-monsoon season. Organic carbon and textural composition of sediments differ greatly between Station 1 and Station 2. Geotechnical properties of the sediments in terms of relative permeability or penetrability also differ between the two stations. The higher energy Station 2 at Gangasagar is prone to more erosion and resuspension of sediments and thus revealed a greater penetration depth or high permeability. In contrast, the sediment bed of Station 1 is less prone to resuspensions and revealed a greater compactibility of sediments. Distinct differences were observed in the textural and geotechnical properties of the two stations, particularly in terms of grain size, grain sorting, permeability of substratum and hydrodynamic conditions, all of
59 which are considered as ‘superparameters’ for benthic organisms. At Station 1, the high organic carbon content of the sediments and low dissolved oxygen in the interstitial water (Table 1) reflect a reducing environment. Tidal current velocity is low and fluctuates within a range of 80–120 cm s1. The hydrodynamic regime is controlled by bi-directional currents: (a) longitudinal flow along the river course during neap tides and (b) transverse helical flow during the spring tidal periods. The fine to very fine sand (Mz ¼ 2.81 – 3.70 phi) and moderately well to moderately sorted (1 ¼ 0.63 – 1.01 phi) sediments together with low permeability (penetration depth ¼ 7.8–8.2 cm) have a bearing on the sustainability of two opportunistic polychaete species in this study area (Creutzberg et al. 1984). At Station 2, sediments are well to very well sorted (1 ¼ 0.18 – 0.48) fine sand (Mz ¼ 3.19– 3.95 phi) with patches of mud. The seasonal transference of the polychaete beds often promotes a mixing of grain sizes enabling a greater tolerance for the polychaetes in a wide range of sediments (Knox 1977). The relative permeability of the substratum is high, with penetration depth ranging from 9.7 to 12.5 cm. The overall hydrodynamic condition reflects a higher energy environment compared with that of the Station 1. Species composition, ecological indices, and seasonal changes of the communities A list of polychaete species together with their feeding habits for the two stations is presented in Table 2. Faunistic surveillance studies at Station 1 showed that polychaetes are the only macrozoobenthos with an impoverished community structure consisting of only two species (Mastobranchus indicus and Dendronereis heteropoda; Table 3). The capitellid worm (M. indicus) is an important determinant of polychaete community structure, and was present in a consistent pattern throughout the study period with a peak density of 186 m2 in June 1999. In comparison with Station 1, Station 2 is rich in polychaete faunal assemblages having 10 species belonging to 10 genera and 6 families, all with diverse feeding guilds (Table 2). Distribution patterns of the polychaete community over the seasons changes periodically, with an impoverished
community during May and October 1999 (Table 4). With the advent of monsoonal precipitation, the number of polychaete fauna declined drastically at Station 2 when only two species were present out of 10 species. True estuarine polychaete species might be surviving by their high osmoregulatory capacity or by some protective secretion around their body as suggested by Kinne (1964). The numerically abundant herbivorous polychaete Pereneries cultrifera that showed a peak density of 1680 m2 on February 2000 was restricted mainly during the post-monsoon period. The deposit feeder Lumbrineris notocirrata and tube-dwelling carnivore Diopatra cuprea might be considered as occasional species and are mainly present during the post-monsoon period. Unlike Station 1, few casual migrant species get access into this substrate. The results of ecological indices in terms of diversity index (H0 ) and richness (R1) indicate higher values with Station 2 in comparison with Station 1, which is indicative of a healthy benthic community as endorsed by MacArthur (1965) and Margalef (1968). The range of variations of the values of ecological indices at the two stations is presented in Table 5. Coefficients of similarity calculated for the two stations showed low and intermediate levels of affinity (0–25%). Results of analysis of variance (ANOVA) showed that community diversity values between the two stations differ significantly (F ¼ 48.66; P ¼ 0.000001), whereas the difference in total polychaete values between the two stations was not highly significant (F ¼ 3.912; P ¼ 0.06). Analyses of the correlation between environmental conditions and polychaete communities To ascertain the effects of environmental variables on total polychaete density (dependent factor), multiple regression analyses were done. The regression summary for Station 1 and Station 2 is shown in Tables 6 and 7, respectively. The results reveal that variables like organic carbon and available phosphorous for Station 1, and salinity and available nitrogen for Station 2 act as the most important factors for controlling the total number of polychaetes. However, for variations in species
a
3
28 ± 0.9 30 ± 0.4 28 ± 1 28 ± 1 21 ± 1 21 ± 1
7.4 ± 0.09 8.1 ± 0.01 7.5 ± 0.14 8 ± 0.04 7.6 ± 0.23 8.1 ± 0.08
Soil (pH)
1, pre monsoon; 2, monsoon; and 3, post monsoon.
St-1 St-2 St-1 St-2 St-1 St-2
1
2
Station
Seasona
Soil temperature ( C) 7 ± 2.0 21 ± 7.0 1 ± 0.9 8 ± 4.0 4 ± 0.7 19 ± 3.0
Salinity (ppt) 2 ± 0.2 6 ± 1.0 0.8 ± 0.3 7 ± 0.7 2 ± 0.8 6 ± 0.5
D.O. ml l1 0.89 ± 0.94 0.32 ± 0.05 0.74 ± 0.08 0.39 ± 0.04 0.88 ± 0.08 0.38 ± 0.04
Organic carbon % 44 ± 10 18 ± 11 38 ± 12 14 ± 6 38 ± 7 23 ± 3
Sand % (2–0.05 mm) 42 ± 7 53 ± 7 49 ± 12 50 ± 2 42 ± 6 50 ± 1
Silt % (0.05–0.002 mm)
14 ± 2 26 ± 4 13 ± 5 36 ± 7 20 ± 6 27 ± 3
Clay % ( Cr > Zn > Mn > Cu > Hg. This decreasing trend was somewhat different at Station 2, especially in cases of Cr and Hg. Analyses revealed small variations of mean concentration of heavy metals within the seasons. The Cr level is much higher at Station 1, rising to 164 g g1 during monsoon months. The Hg concentration at Station 2, on the other hand, is much higher with 0.57 g g1 in comparison with Station 1, where the value is as low as 0.18 g g1 during the same period.
Discussion This study reveals that sediment quality parameters have an immense effect on the spatiotemporal distribution and variation of benthic polychaetes under two different morphological and hydrodynamic conditions. Geotechnical properties of the sediments like relative permeability or penetrability also differ in the two stations, and these are controlled by variations in the amount of erosion and resuspension of sediments, rate of burrowing versus rate of consolidation, and water content in the sediment. The higher energy Station 2 at Gangasagar with more erosion and resuspension
62 Table 4. Population density of the dominant polychaetes (number m2 ± SD) at Gangasagar (Station 2) during March 1999 to February 2000. Month
M. indicus
L. notocirrata
D. cuprea
P. cultrifera
P. tenuis
G. tesseleta
G. sootai
March 1999 April May June July August September October November December January 2000 February
0.00 0.00 0.00 47 ± 12 7 ± 12 53 ± 12 7 ± 12 0 0 0 0 0
40 ± 20 80 ± 35 60 ± 20 7 ± 12 0 100 ± 20 0 0 0 93 ± 50 93 ± 46 205 ± 47
33 ± 12 0 0 0 0 0 0 0 53 ± 12 87 ± 50 33 ± 12 27 ± 12
0 0 0 0 0 0 7 ± 12 0 1673 ± 64 213 ± 81 0 1680 ± 1187
0 567 ± 61 0 0 53 ± 50 60 ± 20 26 ± 30 0 0 0 0 0
67 ± 12 80 ± 20 7 ± 12 26 ± 12 0 13 ± 142 20 ± 35 47 ± 42 40 ± 20 0 0 20 ± 20
200 ± 53 13 ± 23 0 73 ± 15 53 ± 61 0 0 0 1505 ± 218 693 ± 186 193 ± 42 140 ± 89
Table 5. Range of ecological indices at Station 1 (Ghushighata) and Station 2 (Gangasagar). Ecological indices
Station 1
Station 2
Community diversity 0.000 < H < 0.693 0.649 < H < 1.777 Richness 0.000 < R1 < 0.888 0.685 < R1 < 2.183 Evenness 0.858 < E1 < 1.701 0.938 < E1 < 0.996
of sediments has thus revealed a greater penetration depth or high permeability of sediments. At this station, burrowing organisms in the mud increases the water content in the sediments and decreases near surface sediment compaction (Bokuniwicz et al. 1975). As a result, along with other physicochemical conditions, this substrate favors the settlement of a greater variety and number of burrowing polychaetes. Rare or opportunistic species like Eteone barantollae, Namalycastes fauveli, and Ceratonereis burmensis were present during the low saline monsoon period probably due to their unique potential to utilize the unstable substratum. Differences in the superparameters at the two stations, namely grain size, sorting, and hydrodynamic conditions including water movements (Lardicci et al. 1993), also control the distinctive distribution of polychaetes. The results of multiple regression analyses indicate that sediment quality parameters played significant roles on total polychaete density as well as species diversity. This observation corroborates the findings of Rodriguez-Villanueva et al. (2000) from the Baja California coast, Mexico. Species diversity is favored mainly by textural composition of the sediments, which is also endorsed by other workers
(Gaston et al. 1998; Simboura et al. 2000). Nichols (1970) also observed the role of clay content in the sediment to control the change in species composition of benthic polychaetes from Port Madison, Washington. Hypoxic conditions (
