Meiofauna of the western continental shelf of India, Arabian Sea

Estuarine, Coastal and Shelf Science 86 (2010) 665–674

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Meiofauna of the western continental shelf of India, Arabian Sea S. Sajan 1, T.V. Joydas*, R. Damodaran Department of Marine Biology, Microbiology and Biochemistry, School of Marine Sciences, Cochin University of Science and Technology, Cochin 16, Kerala, India

a r t i c l e i n f o

a b s t r a c t

Article history: Received 19 July 2009 Accepted 26 November 2009 Available online 2 December 2009

Meiofaunal standing stock and nematode community structure were investigated in the western continental shelf of India by collecting samples from every degree square of the shelf during two cruises of the FORV (Fishery and Oceanographic Research Vessel) Sagar Sampada, conducted in 1998 and 2001. Samples were collected from 30, 50, 100 and 200 m depths using a Smith Mc Intyre grab. Meiofaunal density ranged from 8 Ind. 10 cm2 to 1208 Ind. 10 cm2 and biomass from 0.07 mg 10 cm2 to 6.11 mg 10 cm2. Nematodes were the dominant meiofaunal group, contributing 88% of the density and 44% of the biomass. Harpacticoid copepods were the second important taxa, contributing 8% of both biomass and density. Altogether, 154 species of nematodes belonging to 28 families were recorded from the study area. Numerically, Desmodora spp., Dorylaimopsis sp., Tricoma spp., Theristus spp. and Halalaimus spp. were the dominant species. In general, there was a decrease in biomass and density of meiofauna and species diversity of nematodes with increase in depth. There was a 67% drop in species number from 51 to 100 m (106 species) to the shelf edge (35 species). Species richness and diversity indices showed consistent decrease with depth. The species dominance index was higher below 150 m depth. ANOSIM (from PRIMER) showed a significant difference between the nematodes of the near shore and shelf edge. Latitudinal variation was observed only in the number of nematode species. Biomass and abundance of nematodes were found to increase from coarse to fine sediment, while copepods showed an opposite trend. Multivariate analyses of nematode communities did not reveal any latitudinal or substratum differences. Variables such as depth, latitude, organic matter (OM) and amount of clay were the most relevant parameters influencing the biomass and density of meiofauna, while depth and temperature were the important parameters explaining the distribution of the nematode communities along the western Indian shelf. Ó 2009 Elsevier Ltd. All rights reserved.

Regional index terms: Arabian Sea West coast India Keywords: Meiofauna free-living marine nematodes community structure depth variation

1. Introduction Meiofauna is the major metazoan component of benthic ecosystem and its production is equal or higher than macrofauna in shallow waters to deep sea (Gerlach, 1971; Platt and Warwick, 1980; Heip et al., 1985; Coull, 1999). Meiofauna facilitates biomineralization of organic matter (OM) and enhances nutrient regeneration (McIntyre, 1969; Feller and Warwick, 1988; Montagna et al., 1995). They serve as food for a variety of higher trophic levels and exhibit high sensitivity to anthropogenic inputs making them excellent environmental indicators (Boyd et al., 2000; Gheskiere et al., 2004; Schratzberger et al., 2006). Numerically, nematodes are the dominant taxa among meiofauna. Distribution and abundance of

* Corresponding author. Center for Environment and Water, King Fahd University of Petroleum and Minerals, P.B. No. 1995, Dhahran-31261, Kingdom of Saudi Arabia. E-mail address: [email protected] (T.V. Joydas). 1 Present address: Unicomarine Limited, 7 Diamond Centre, Works Road, Letchworth, Herts, SG6 1LW, United Kingdom. 0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.11.034

meiofauna are mainly controlled by sediment characteristics and food availability (Vincx et al., 1990; Coull, 1999; Liu et al., 2005). To date there have been many benthic studies undertaken in and around Indian waters. However, most them have been on macrobenthos and information on the meiofaunal communities of the Indian shelf sediment is relatively insufficient. Most meiofaunal studies reported from the seas around the Indian subcontinent are regional works conducted in shallow coastal and estuarine waters and mangroves. Preliminary investigations on nematodes were carried out by Timm (1961, 1967a,b) from the Bay of Bengal region and Gerlach (1962) from the Maldives Islands. Rao and Ganapati (1968) studied the interstitial fauna of the beach sands of the east coast of India. Their study gave the first records of nematodes from the Indian coast. Initial meiofaunal studies reported from the west coast of India were from the Cochin estuary (Kurien, 1972) and the mud bank region of Kerala (Damodaran, 1973). Since then, a few more qualitative and quantitative studies on meiofauna have been made off both the east and west coasts of India (Ansari et al., 1980; Harkantra et al., 1980; Ansari and Gauns, 1996; Sultan Ali et al., 1998; Nanajkar and Ingole, 2007). Parulekar et al. (1982) studied

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the standing crop of meiofauna up to a depth of 75 m in the west coast of India, which was the only study reported with larger area coverage. So far, no concerted effort has been made to unravel the community composition of meiofauna and to identify links to the key environmental factors for the entire western continental shelf of India. The present study is the first major investigation into the nature of the meiofauna within a study area extending from off Cape Comorin to off Dwarka, with sampling between depths of 30 m and 200 m. For the study, samples were collected from each degree square of the western continental shelf. The focus of the study was limited to meiofauna retained on a 63 mm sieve. The objectives of the study are to (1) estimate the density and biomass of the meiofauna from the entire western continental shelf of India and compare with similar studies conducted elsewhere, (2) understand the community structure of major meiofaunal group – nematodes, (3) test whether any depth or substratum variations exist for meiofaunal organisms in the study area and (4) identify the key environmental variables controlling meiofaunal standing stock and nematode communities in the shelf sediments. Earlier studies reported a variation in macrobenthic standing stock between southwest (higher biomass) and northwest (lower biomass) coasts of India (Neyman, 1969; Harkantra et al., 1980). However, such variation was not found in more recent studies, while a lower standing stock was observed in the central region when study area was divided into southwest, central and northwest coasts (Joydas and Damodaran, 2009). The present study aimed to understand whether similar latitudinal variation exists in the meiofaunal communities of the west coast. The western continental shelf of India is a part of the Arabian Sea, covers an area of about 310,000 km2 and stretches between 7 N and 24 N latitude (Rao and Wagle, 1997). From Mumbai to Ratnagiri, the shelf width is about 280 km. Further south, between Ratnagiri and Mangalore, the average width lowers to 80 km. The Arabian Sea is influenced by the Somali current in the north and by the southwest monsoon and upwelling in the south. There is marked variation in bottom temperature, salinity and dissolved oxygen with depth, occurrence of thermocline, salinity maxima and oxygen minimum zones in this area (Wyrtki, 1971; Babu et al., 1980; Sen Gupta et al., 1980; Qasim, 1982). During the southwest monsoon, sporadic upwelling occurs on the southwest coast of India (Wyrtki, 1971; Madhupratap et al., 2001). Previous reports indicated that there are three different types of sediments on the shelf (Hashimi and Nair, 1981). The first of these is the near shore sand zone, extending from the shore to a water depth of 5–10 m. Offshore from the sand is the mud (silt and clay), which extends to a depth of 50–60 m (inner shelf). The shelf beyond 50–60 m (outer shelf) is covered by coarse calcareous sand. Generally, fine substrata of clay and silt retain higher organic matter content, whereas sandy substrata hold low organic matter content. 2. Materials and methods 2.1. Sampling strategy Meiofaunal samples for the present study were collected onboard the FORV (Fishery and Oceanographic Research Vessel) ‘Sagar Sampada’, owned by the Department of Ocean Development, Government of India. Two cruises (Cruise No. 162 and Cruise No. 192A) were conducted along the shelf regions of the west coast of India, for the study. The first cruise was carried out from 16-02-1998 to 06-03-1998 and the second from 20-02-2001 to 28-02-2001. Cruise No.162 covered 62 stations from 13 transects (T), while Cruise No. 192A covered 13 stations from 3 transects (T5, 9 and 13). The second cruise was conducted with a view to fill gaps in data from the first cruise.

Seventy-four stations representing various depths, distributed along 17 transects were covered; they extended from 08.03.96 N to 77.21.96E to 21.56.99 N and 67.57.69E (Fig. 1 and Online Appendix 1). Sampling was conducted at 30, 50, 100 and 200 m depths along each transect in order to study the change in fauna with depth. Additionally, samples from about 75 m were collected from certain transects, where the shelf width was greater (transects T3, T7, T10, T11, T12 and T14). Since the shelf was very steep beyond 100 m in T2, sampling from 200 m was not possible from this transect. In the Mumbai region, because of the restriction for the entry to the Mumbai High region, one transect (T14) was sampled north of Mumbai, and another (T15) parallel to the coast, to the north. Although this region has the widest continental shelf, sampling was restricted to waters shallower than 100 m. Two grab samples were collected using a Kahlsico No. 214 WA 250 modified Smith McIntyre grab (having a bite area of 0.1 m2) from each station. Immediately after grab hauling and after ascertaining that the sediment was undisturbed, sub-samples were taken for meiofauna by using a glass corer (with an internal diameter of 2.6 cm, and a length of 30 cm) from the middle of each grab sample. The core samples were immediately fixed in buffered formalin at a final concentration of 4%. The replicate core samples were processed separately in the laboratory and data were pooled for analyses. About 50 g of sediment was sub-sampled from each grab sample for the analysis of sediment texture and organic matter. The sediment samples were oven-dried (at 60  C) onboard and stored for further analysis. Hydrographical parameters (temperature, salinity and dissolved oxygen (DO)) of bottom waters were measured at each sampling station by Seabird CTD. 2.2. Laboratory and statistical analyses In the laboratory, core samples were washed through a set of 500 mm and 63 mm sieves. The sediment retained in the 63 mm sieve was decanted to extract meiofauna following methods described in Higgins and Thiel (1988). In order to extract the meiofaunal organisms from silt/clay sediment, the classical method of decantation by hand, using a 63 mm sieve was used as described in Somerfield and Warwick (1996). The meiofaunal organisms were stained with Rose Bengal prior to extraction and were sorted and enumerated under a stereomicroscope. Wet weight of various taxa was determined by direct weighing of several individuals (all individuals together) (Mare,1942) using a high precision electronic balance (Sartorius AG – ME215P, Germany with a precision of 0.01 mg). Wet weight of nematodes was recalculated from measurements of length and width (Wieser, 1960), assuming a specific gravity of 1.13 and compared with the direct weighing method. The biomass measures of nematodes and copepods were taken separately; all other taxa were grouped into ‘‘others’’. The numerical abundance (as individuals) and biomass (in mg) of meiofaunal organisms were expressed in 10 cm2. Identification of the dominant group (nematodes) was carried out to the species level, whereas the other groups were identified to higher taxa only. A minimum of 100 nematodes was randomly picked out from each replicate sample for identification (when there were fewer than 100, all the nematodes were identified). The nematodes were mounted onto glass slides, using the formalin-ethanol-glycerol technique described by Seinhorst (1959) and Vincx (1996), and identified to species level under the compound microscope (Nikon trinocular research microscope with 100 oil immersion objective), using standard literature (Wieser, 1953, 1954, 1956; Platt and Warwick, 1983, 1988, 1998). Grain size was estimated by combined sieving and pipette method as described by Carvar (1971). The weight percentage of sand, silt and clay was calculated and values plotted on triangular graphs according to the nomenclature suggested by Sheppard (1954). Organic carbon in the

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Fig. 1. Location of sampling stations of the western Indian shelf.

sediment was estimated by wet oxidation method (El-Wakeel and Riley, 1957), which was then converted to organic matter (Wiseman and Bennette, 1960). Univariate and multivariate community analyses were carried out using PRIMER (Plymouth Routines in Multivariate Ecological Research) (version 5), with the nematode species abundance matrix (Clarke and Warwick, 2001). Univariate measures included Margalef index (d) for species richness, Pielou’s evenness (J0 ) for evenness, Shannon-Wiener (H0 loge) for species diversity, and Simpson dominance (l0 ) for species dominance. To detect possible differences in assemblage composition between habitats, multivariate analyses were performed on square-root transformed abundance data. Bray–Curtis index and group average linkage were used for non-metric multidimensional scaling (MDS) ordination. One-way ANOSIM (Analysis of similarity) was carried out to test differences found in the communities between habitats (depth, latitudinal and substratum) and species contributing significant variation between

habitats were identified using the SIMPER (Similarity percentage) subroutine. To compare the biodiversity between the depth ranges, dominance plots were drawn by ranking the species in decreasing order of abundance. Species’ relative abundances, expressed as percentages of abundance in the sample, were plotted by increasing rank (on a log scale) along the x-axis. On the y-axis, the cumulative percentage was plotted. BVSTEP, stepwise searches of combinations of species considered to be responsible for the pattern in biotic assemblages, was also carried out. BIOENV was performed to measure the rank correlations of meiofaunal biomass and density and nematode community with environmental parameters such as depth, temperature, salinity, dissolved oxygen, percentages of sand, silt and clay and organic matter. For the convenience of analysis and interpretation, data from all the transects were pooled into specific depth ranges i.e., 30–50 m (19 stations), 51–100 m (29 stations), 101–150 m (13 stations) and >150 m (13 stations) and, to study latitudinal variation, the study

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area was divided into three, i.e. southwest, central and northwest regions. The southwest contained transects T1–T6 (24 stations); central included transects T7–T12 (27 stations) and the northwest comprised transects T13–T17 (23 stations). 3. Results 3.1. Physical characteristics The results of environmental parameters studied are summarized in Table 1. The temperature and dissolved oxygen in the bottom water showed decreasing trends with increase in depth (P < 0.001); salinity exhibited an increase with depth, though not statistically significant. The bottom water temperature range was 12.90  C (T6, 200 m) to 29.42  C (T2, 30 m). Salinity (Practical Salinity Unit-PSU) varied between 33.71 (T1, 30 m) and 37.31 (T6, 100 m) and the range of dissolved oxygen was 0.0005 ml L1 (T13, 200 m) to 3.87 ml L1 (T9, 30 m). The parameters also exhibited latitudinal variation. Temperature showed a decrease from south to north up to 100 m depth, whereas below 100 m, it decreased from north to south. Salinity exhibited an increasing trend from south to north for all the depth ranges. Near zero values of dissolved oxygen were observed along the continental shelf edge, particularly the northern shelf (0.0005–0.11 ml L1). Substrata varied considerably with the occurrence of seven sediment types: sand, silty sand, sandy silt, silt, sand–silt–clay, clayey silt, silty clay. These were combined into three: sand (more than 75% of sand, 37 stations), sand–silt/clay (mixture of sand and silt/clay and none is more than 75%, 15 stations) and silt/clay (more than 75% of silt and clay together, 23 stations). In general, substrata were silt/clay in nature in the near shore region, except for the extreme south and extreme north regions. With the increase in depth, sand seemed to replace the finer sediment. This trend was more prominent in the southwest region. Fine sediments were observed in the deeper stations of the northwest region. The percentage of organic matter ranged from 0.24% to 6.71%. Though not statistically significant, organic matter showed an increasing trend with increase in depth. Stations in the central region showed higher organic matter. Finer sediments retained more organic matter than coarser ones (silt: P < 0.01). 3.2. Meiofaunal density and biomass Nematodes were the most abundant taxon (88%), followed by harpacticoid copepods (8%) and rest of the taxa contributed about 4% only. About 44% of the biomass was contributed by nematodes, 8% by harpacticoid copepods and 48% by all other groups. Other taxa included oligochaetes, ostracods, halacarids, kinorhynchs and unidentified polychaetes in minor abundance. Total meiofaunal density ranged from 8 Ind. 10 cm2 (T1, 200 m) to 1208 Ind. 10 cm2 (T5, 30 m) whilst total biomass varied between 0.07 mg 10 cm2 (T6, 30 m) and 6.11 mg 10 cm2 (T5, 30 m).

3.3. Community composition of nematodes Altogether, 154 species of nematodes, belonging to 28 families were recorded from the samples. Species recorded were classified as ‘restricted’, ‘widespread’ or ‘ubiquitous’ depending on their depth ranges. Restricted species were those that were recorded from one station at one depth range only, widespread species were defined as occurring in at least two depth ranges, but not in all the depth ranges, and ubiquitous species were those that were recorded at all the depth ranges. Certain species that occurred at more than one station in a single depth range were included in the widespread species category. As restricted species were recorded from one station each only, they can be considered ‘rare’. In total, 33% of the species identified were restricted (51 species out of 154), 57% were widespread (88 species) and 10% were ubiquitous (15 species). Numerically (based on individual abundance per nematodes abundance), Desmodora spp. (6.8%), Dorylaimopsis sp. (5.9%), Tricoma spp., (5.4%), Theristus spp. (5.1%) and Halalaimus spp. (4.6%) were the dominant species. Apart from these, Terschellingia longicaudata in 30–50 m, Sabatieria spp. in 51–100 m to the shelf edge, Spilophorella tollenifera in 101–150 m and Promonhystera spp in >150 m were also numerically important. The determining nematode species of the study area selected by BVSTEP with their depth variation in abundance and substratum preference are presented in Online Appendix 2. Of the 28 nematode families, the dominant with respect to abundance were Desmodoridae (mean: 6.3  10.3 Ind.10 cm2), Comesomatidae (mean: 5.9  6.0 Ind. 10 cm2) and Xyalidae (mean: 4.3  4.8 Ind.10 cm2), whilst the most speciose families were Xyalidae (20 species) and Desmodoridae (16 species). Species richness, diversity and evenness were zero in two stations due to the occurrence of only one species each (T1, >150 m – Desmodora spp. and T6, >150 m – Promonhystera spp.). As expected, the dominance value was one in these stations. The maximum values for each index are as follows: Margalef richness (d) – 6.37 (T7, 50 m), Pielou’s evenness (J0 ) – 1.0 (T4, 100 m and T3, >150 m) and Shannon diversity (H0 (log 2)) – 4.76 (T7, 50 m).

3.4. Spatial and substratum variation in meiofauna and nematodes Biomass and density showed a steady decrease from the 30–50 to the 101–150 m depth range and below, biomass showed no further change, while density increased slightly at the shelf edge (Fig. 2a and b). There was a 69% decrease in biomass and an 82% decrease in density from shallow water to 101–150 m. Numbers of species in each depth range are given in Fig. 3. In general, nematode species demonstrated a reduction in numbers with increase in depth (r ¼ 0.47; P < 0.001). There was a 67% drop in species numbers from 51 to 100 m (106 species) to the shelf edge (35 species). Average species richness and diversity showed consistent decreases with depth (Fig. 2c). Recorded species evenness was within a small range (0.93–0.97) from 30 to 50 m to 101–150 m; below that depth, it reduced to 0.79 (Fig. 2c). Simpson dominance

Table 1 Summary of hydrographical and sediment characteristics for the west coast Indian shelf. Data presented as mean  SD (range). Parameter

30–50 m

51–100 m

101–150 m

>150 m

Bottom temperature ( C) Bottom Salinity (PSU) Bottom DO (ml L1) Sand (%) Silt (%) Clay (%) OM (%)

27.6  2.2 (22.64–29.42) 34.89  0.7 (33.7–36.1) 3.4  0.3 (3–3.9) 35.2  44.0 (0.2–99.7) 35.2  25.3 (0.1–72.6) 29.6  23.3 (0.2–63.7) 2.9  2 (0.2–6.7)

26.8  1.9 (22.7–29) 35.6  0.6 (33.7–36.4) 3  0.6 (1.7–3.7) 62.6  38.1 (0.1–99.7) 22.0  19.9 (0.2–63.0) 15.4  19.6 (0.1–55.5) 2.6  1.6 (0.4–5.5)

24.6  2.9 (17.4–28.2) 35.9  0.6 (34.8–37.3) 1.8  0.8 (0.2–2.9) 72.2  27.1 (8.6–98.5) 24.3  26.6 (0.8–90.6) 3.5  2.5 (0.7–7.8) 2.9  1.3 (0.9–5.1)

14.9  1.3 (12.9–17.2) 35.4  0.3 (35.1–36.1) 0.09  0.08 (0–0.2) 61.8  36.8 (0.74–97.5) 25.4  22.9 (1.7–72.9) 12.8  16.0 (0.8–50.9) 3.3  1.5 (0.8–6.2)

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a

Others

2.5

Copepods

Nematodes

Biomass (mg 10cm-2)

2.0 1.5 1.0 0.5 0.0 30-50

b

51-100 101-150 Depth range (m) Others

>150

Copepods

500

669

was also within a narrow range (0.10–0.13) up to 101–150 m; below 150 m, it increased considerably (Fig. 2c). There was no prominent latitudinal variation in biomass and density of meiofauna (Fig. 4a and b). Relatively low biomass and density were observed in the central region. A decrease in species number with increase in latitude was observed. Species numbers recorded were 117 in southwest, 100 in central and 71 in northwest region. None of the average values for indices indicate a latitudinal variation for the southwest, central and northwest regions (Fig. 4c). Total biomass did not show an obvious substratum difference, while total abundance exhibited an increase from coarse (sand) to fine (silt/clay) sediment (Fig. 5a and b). In general, average biomass and abundance of nematodes were found to increase from coarse to fine sediment, while copepods showed the opposite trend. The biomass of other groups was higher in sandy substrata. Slightly higher species numbers were recorded in sandy (125) compared to sand–silt/clay (77) and silt/clay (83) substrata. Diversity indices showed no variation with substratum (Fig. 5c).

Nematodes

Dens it y (Ind. 10cm-2)

400

a

300 200

30-50

>150

1.5 1.0 0.5 0.0

c 4

Richness

Evenness

Diversity

Dominance

Southwest

b

3

300 2 1 0 30-50

51-100 101-150 Depth range (m)

>150

Dens it y (Ind. 10cm-2)

Communit y s t r ucture indices

51-100 101-150 Depth range (m)

Biomas s (mg 10cm-2)

0

60

Widespread

13% 65%

63%

6% 58%

20 0

Ubiquitous

51%

15%

14%

29%

43%

30-50

51-100

101-150

>150

Depth range (m) Fig. 3. Depth variation in the absolute number of restricted, widespread, and ubiquitous nematode species. Percentage of species is given inside the bar of each group.

Nematodes

Southwest

c 4 Communit y s t r ucture indices

Sp ecies Number

23%

Copepods

0

Restricted

20%

Others

Northwest

100

120 100

Central Region

200

Fig. 2. Depth variation in meiofauna (a) absolute biomass, (b) absolute density and (c) community structure indices.

40

Copepods

Nematodes

2.0

100

80

Others

2.5

Central Region

Northwest

Richness

Evenness

Diversity

Dominance

3 2 1 0 Southwest

Central Region

Northwest

Fig. 4. Latitudinal variation in meiofauna (a) absolute biomass, (b) absolute density and (c) community structure indices.

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a Bioma s s (mg 10cm-2)

2.5

Stress: 0.22

Others

30-50m

Copepods

Nematodes

2.0

51-100m

1.5 1.0

101-150m

0.5 0.0 Sand

b 400

Sand-silt/clay Substratum

Fig. 6. MDS ordination of stations for nematode species abundance within different depth ranges.

Others

Copepods

Dens it y (Ind. 10cm-2)

Nematodes 300 200 100 0 Sand

Communit y s t r ucture indices

4

c

>150m

Silt/clay

Sand-silt/clay Substratum

Silt/clay

Richness

Evenness

Diversity

Dominance

3 2 1 0 Sand

Sand-silt/clay Substratum

Silt/clay

Fig. 5. Substratum variation in meiofauna (a) absolute biomass, (b) absolute density and (c) community structure indices.

3.5. Multivariate community analyses of nematodes Community composition of nematodes, examined through nMDS ordination based on the Bray–Curtis similarity did not show any grouping of stations (Fig. 6). However, one-way ANOSIM demonstrated significant differences between the nematode fauna of various depth ranges (Table 2). Higher significance was observed between 30 – 50 m and 101–150 m depth ranges and 51–100 m and >150 m depth ranges. Latitudinal (Global R ¼ 0.022; p < 0.187) and substratum (Global R ¼ 0.058; p < 0.080) differences in nematodes were not significant. SIMPER analysis was performed in order to identify the discriminating species which are responsible for dissimilarity between the shallow water and the shelf edge (30– 50 m and >150 m; 51–100 m and >150 m). The average dissimilarity was 90.55% for former and 91.51% for latter pairs. There were 13 species cumulatively contributing c. 50% of the dissimilarity between 30 and 50 m and >150 m and 14 species between 51 and 100 m and >150 m. Among these, 11 species were common:

Desmodora spp., Dorylaimopsis sp., Tricoma spp., T. longicaudata, Theristus spp., Halalaimus spp., Desmodora tenuispiculum, Sabatieria spp., Promonhystera spp., Sphairolaimus spp. and Richtersia spp. Multiple k-dominance plots (Clarke and Warwick, 2001), facilitated discrimination of nematodes according to species’ relative contribution to abundance. Up to about 43 species constituted 80% of the total nematodes at 30–50 m and 51–100 m, while it required 30 species for 101–150 m and 19 species for >150 m, proving the increase in dominance with increase in depth (Fig. 7). The dominant shelf edge nematode species were Viscosia spp. (family Oncholaimidae), Sabatteria spp. (family Comesomatidae), Richtersia spp. (family Selachinematidae), D. tenuispiculum, Desmodora spp. (family Desmodoridae), Theristus spp. and Promonhystera spp. (family Xyalidae). 3.6. Environmental correlates of fauna Correlation analysis demonstrated a negative relationship between depth and meiofauna while latitude was found to negatively influence nematode diversity only (Online Appendix 3). Among the hydrographical parameters, dissolved oxygen showed a positive correlation with biomass and density for all the meiofaunal groups and diversity of nematodes, while temperature had a positive correlation with biomass of total meiofauna and diversity. Salinity was found to negatively correlate with copepods, biomass of total meiofauna and diversity. Bulk organic matter showed a negative correlation with copepods and biomass of total meiofauna. Nematode biomass, nematode abundance and total meiofaunal abundance were negatively correlated with coarse sediment fractions (sand) while positively correlated with finer sediment (clay). Correlation of different parameters on fauna may indicate their influence in combination in the distribution of meiofauna. BIOENV analysis was performed to identify the important parameters influencing the fauna (Table 3). Results indicate that variables such as depth, latitude, organic matter and amount of clay are the most relevant parameters influencing the biomass and density of meiofauna. The two most important factors affecting nematode community structure were depth and temperature. Salinity, dissolved oxygen and silt also affected nematodes, together with depth and temperature. 4. Discussion In the western continental shelf of India, meiofauna showed an average density of 218  247 Ind.10 cm2 and an average biomass of 1.40  1.25 mg 10 cm2. The values are comparable with previous studies conducted in Indian waters. For example, the highest density reported from off Goa (Ansari et al., 1980) and the Bay of

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671

Table 2 Comparison of regions (factor-depth ranges) using one-way ANOSIM. Group

R-statistic

Significance level

Possible permutations

Actual permutations

Number observed

(Global R ¼ 0.188; p < 0.001) 30–50 m and 51–100 m 30–50 m - 101–150 m 30–50 m to >150 m 51–100 m to 101–150 m 51–100 to >150 m 101–150 m to >150 m

0.075 0.361 0.214 0.205 0.241 0.132

6.7 0.1 0.3 1.2 0.4 2.2

Too many 34,290 86,225 Too many Too many 1078

999 999 999 999 999 999

66 0 2 11 3 21

Bengal (Rodrigues et al., 1982) was <3000 Ind.10 cm2. The density of meiofauna reported from the Scotia Basin (Wigley and McIntyre, 1964), Hatteras Abyssal Plain (Tietjen, 1971), western Indian Ocean (Muthumbi et al., 2004), Chatham Rise, southwest Pacific (Grove et al., 2006) and southern Yellow Sea, China (Liu et al., 2007) are also comparable, at <2000 Ind.10 cm2. Records of meiofaunal biomass are quite few for the west coast of India. Parulekar et al. (1982) reported an average biomass of 1.42 mg 10 cm2 (dry weight) from the Arabian Sea. The biomass reported from the tropical east Atlantic (Soltwedel, 1997) was within the range of 0.06–1.64 mg 10 cm2, which is also broadly within the range of the present results. Although the fauna comprised eight taxonomic groups, nematodes and copepods accounted over 90%. This general trend of dominance of nematodes and copepods was also found in other studies from Indian waters (Ansari et al., 1980; Parulekar et al., 1982) and other parts of world (Soltwedel, 2000; Grove et al., 2006; Liu et al., 2007). In Indian waters, community studies on free-living nematodes are not available. So far, about 125 species of nematodes have been reported from various regions, including estuaries, backwaters, lagoons and mangroves on the east and west coasts of India (Timm, 1961, 1967a,b; Gerlach, 1962;Rao and Ganapati, 1968; Sultan Ali et al., 1998; Nanajkar and Ingole, 2007). The present study identified 154 species from 74 locations on the shelf. This study shows that there is large proportion of ‘restricted’ species, which contributed 34% of total nematode population to maintain high diversity and low dominance throughout the area. However, in general, the majority of the species found at any single depth range was ‘widespread’ or ‘ubiquitous’ across the study area. Below 100 m, there was a sizeable decrease in the proportion of ‘restricted’ species. At all depth ranges, the fauna was dominated by a core group of the same,

100

Cumulative Dominance%

30-50m

abundant genera (for example, Desmodora, Dorylaimopsis, Tricoma, and Halalaimus). On the whole, the nematode species/generic composition of the Arabian Sea appears to be comparable to those reported elsewhere from similar depths (Vanhove et al., 1999; Vanaverbeke et al., 2000). The generic composition of the western Indian Ocean coast (20–200 m) showed the presence of dominant genera like Terschellingia, Halalaimus, Dorylaimopsis, Sabatieria and Paramonhystera (Muthumbi et al., 2004). The distribution patterns of Sabatieria, Halalaimus and Terschellingia displayed similar trends to those discussed for various shelf sediments (Vanreusel et al., 1992; Soetaert and Heip, 1995). The occurrence of Halalaimus was relatively high in shelf and slope sediments from the western Indian Ocean (Muthumbi et al., 2004), northeast Atlantic (Soetaert and Heip, 1995) and western Atlantic (Tietjen, 1976), whereas in the Arctic and Antarctic, their relative abundance was rather low (Vanaverbeke et al., 1997). Dorylaimopsis has been reported as the dominant genus in the Southern Bight of the North Sea (Vincx et al., 1990) and the southern Yellow Sea (Liu et al., 2007). In this study, prominent spatial variation in meiofauna and nematodes was evident only with the change in depth. In general, meiofaunal biomass, abundance and nematode species diversity decreased with increased depth. Similar decreasing trends in density have been reported by Ansari et al. (1980) and Parulekar et al. (1982) for the western shelf of India, De Bovee et al. (1990) and De Leonardis et al. (2008) from the Mediterranean and by Tietjen (1992) from waters off North Carolina. There is a general tendency for the biomass and density of benthic organisms to decrease with increasing bathymetric depth (Ganesh and Raman, 2007; Joydas and Damodaran, 2009). In the present study, the two hydrographical parameters which showed significant positive correlation with biomass, meiofaunal abundance and diversity indices for nematodes were dissolved oxygen and temperature. Both parameters showed progressive decrease with depth and were very low on the shelf edge; particularly, dissolved oxygen which showed nil values for the northern shelf edge. This depletion of oxygen in the shelf edge at northern latitudes may be associated with the oxygen

80 Table 3 Results of BIOENV analyses for the meiofaunal components.

60

51-100m

Data

n

Spearman’s correlation coefficient

Variables

101-150m

Meiofaunal biomass

2 4 3 3

0.346 0.336 0.330 0.329

Depth, Depth, Depth, Depth,

Meiofaunal density

4 4 5 5

0.337 0.331 0.331 0.330

Depth, latitude, OM, clay Latitude, temperature, OM, clay Depth, latitude, temperature, OM, clay Depth, latitude, DO, OM, clay

Nematodes community

2 1 5 3

0.242 0.230 0.221 0.220

Depth, temperature Depth Depth, temperature, salinity, DO, silt Depth, temperature, DO

40

20 >150m 0 1

10

100

200

Species rank Fig. 7. k-dominance curves for nematode species abundance within different depth ranges.

clay latitude, OM, clay OM, clay latitude, clay

S. Sajan et al. / Estuarine, Coastal and Shelf Science 86 (2010) 665–674

Biomass

30

25

2.5

25

20

2.0

15

1.5

10

1.0

5

0.5

0

0.0 30-50

51-100

101-150

Temp er at ure (0C)

3.0

b

Temperature

500 450 400 350 300 250 200 150 100 50 0

20 15 10 5 0

>150

30-50

c

DO

Biomass

2.5 2.0 1.5 1.0 0.5

DO (ml L-1)

3.0

Biomas s (mg 10cm-2)

DO (ml L-1)

Depth range (m)

4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

0.0 30-50

51-100 101-150

>150

4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

d

30-50

Biomass

3.0

O M%

2.5

3.0

3.5

2.5

3.0

2.0

2.0

1.5

1.5

1.0

1.0 0.5

0.5

0.0

0.0 30-50

51-100 101-150 Depth range (m)

Density

500 450 400 350 300 250 200 150 100 50 0

51-100 101-150

>150

>150

f

OM

Density

500 450 400 350 300 250 200 150 100 50 0

2.5

OM%

OM

>150

Depth range (m)

Bio mas s (mg. 10cm-2)

e

51-100 101-150 Depth range (m)

DO

Depth range (m)

3.5

Density

Densit y (Ind. 10cm-2)

Temperature

30

Biomas s (mg 1 0cm-2)

Temp er at ure (0C)

a

proved that harpacticoid copepods are successful in the deep sea and their abundance decreases less rapidly with depth than the general decrease in macrofaunal abundance with depth. On the other hand, nematode species diversity showed a decline at the shelf edge, with an increase in the dominance of species belonging to the families Oncholaimidae, Comesomatidae, Desmodoridae and Xyalidae in low oxygen water. The high abundance and dominance of families such as Comesomatidae (genera Sabatieria), Desmodoridae (genera Desmodora) and Xyalidae (genera Theristus) have been reported on the Atacama Slope and Trench of the South Pacific Ocean by Gambi et al. (2003). The genus Sebatieria is a very common deep water form and is particularly abundant in anoxic conditions (Soetaert and Heip, 1995). Out of 41 determining species selected by BVSTEP analysis, 23 were not recorded in depths >150 m. SIMPER analysis revealed that the more abundant, ubiquitous and widespread species contribute to the observed discrepancy between shallow water and shelf edge communities. In this study area, though temperature may be acting along with other parameters on meiofauna, it is unlikely to be a major factor causing

Densit y (Ind. 10cm-2)

minimum layer (125–500 m depths in the Arabian Sea) described by Sen Gupta et al. (1976, 1980). However, this fall in dissolved oxygen and temperature at the shelf edge did not result in a corresponding decrease in biomass or density compared to the previous depth ranges (Fig. 8a–d). The results indicate that meiofaunal biomass and density are unaffected by low oxygen on the shelf edge. A simultaneous macrofaunal study conducted along with the present study showed that polychaetes were severely affected by low oxygen while macrofaunal crustaceans were found to withstand it (Joydas and Damodaran, 2009). Predation pressure from polychaetes may be less severe on the shelf edge, which may be a reason for the increase in meiofauna at this depth. Studies have reported that meiofauna in general and nematodes in particular tend to be more tolerant than macrofauna to anoxia (Murrel and Fleeger, 1989; Giere, 1993). Cook et al. (2000) reported that in the Arabian Sea, low oxygen (w0.13 ml L1) did not affect the abundance of nematodes. Among the foraminiferans, only soft-shelled taxa are rare or absent in the most oxygen-depleted (<0.2 ml L1) regions of the Arabian Sea (Gooday et al., 2000). Thistle (2001)

2.0 1.5 1.0 0.5 0.0 30-50

51-100 101-150 Depth range (m)

Dens it y (Ind. 10cm-2)

672

>150

Fig. 8. Relationship between environmental parameters and fauna (a) temperature and biomass, (b) temperature and abundance, (c) DO and biomass, (d) DO and abundance, (e) OM and biomass and (f) OM and abundance.

S. Sajan et al. / Estuarine, Coastal and Shelf Science 86 (2010) 665–674

the decline in standing stock or diversity. Salinity also may not be a controlling factor for meiofauna as the bottom salinity variation with depth is not pronounced. Latitudinal variation, unlike depth variation, was not apparent in meiofauna. In general, smaller-sized nematodes contributed higher abundance on the northwest coast and larger-sized organisms, mainly polychaetes, caused higher biomass on the southwest coast. The relatively high biomass observed on the southwest coast may be due to the high primary productivity, the substratum (coarser sediment) and physical oceanographic settings (Madhupratap et al., 2001). Sediment grain size is one of the important factors affecting the distribution of meiofauna (Wieser, 1960; Heip et al., 1985; Ansari and Parulekar, 1998). In the present study, nematodes showed an affinity towards finer sediment. Previous studies have also reported such relationships between nematodes and fine sediments, which hold organic matter in the available form as their food (Ansari, 1978; Coull, 1985). In this study, average biomass and density of nematodes were higher in silt/clay substrata than sandy and mixed sand and silt/clay substrata. In general, sediment was silt/clay in nature in the near shore region of west coast of India. Fine particles in the near shore regions may hold more labile organic matter and this may cause higher biomass and density in silt/clay substrata, along with the favourable physico-chemical conditions. On the other hand, ANOSIM result did not reveal any evidence for the occurrence of distinct nematode communities in different sediment types. The present study showed that the distribution of dominant genera such as Desmodora, Dorylaimopsis, Tricoma and Halalaimus were abundant in sandy, silt/clay and sand–silt/clay substrata. This indicates that even if many species are characteristically associated with a given sediment habitat, their distributions are rarely confined to that environment. Food supply is considered to be very important for meiofauna (Jensen, 1987; Murrel and Fleeger, 1989; Giere, 1993). High benthic biomass and density in near shore areas can be due to the rich primary production in near shore waters. The supply of food to subtidal benthic environment depends on the proximity to shore and water depth (Levinton, 1982). In the present study, average organic matter was higher in the shelf edge than near shore regions and was unable to obtain any direct positive correlation with biomass or density (Online Appendix 3; Fig. 8e and f). Organic matter reaching the sea floor at depths may have been previously attacked by a variety of decomposers and so is probably more refractory than organic matter reaching shallow bottoms adjacent to the shoreline (Trask, 1939; Levinton, 1982). It has been argued that bulk organic matter measurements may not accurately reflect the amount of organic matter that may actually be utilized by an organism (Mayer and Rice, 1992). However, BIOENV has shown the importance of organic matter, which indicates that this factor is vital in the shallow region where the labile form is adequately available to the fauna. Strong correlations between meiofauna and chloroplastic pigments have been reported, providing evidence that the standing stock of meiofauna relies on food availability (De Troch et al., 2006; Grove et al., 2006; Liu et al., 2007). 5. Conclusion This work is the first extensive study on meiofauna conducted in the western continental shelf of India and provides preliminary base-line information on the community structure of free-living marine nematodes in the area. The study showed the predominance of nematodes among the meiofauna on the shelf. A prominent depth variation in meiofauna was observed while latitudinal variation was not prominent. Meiofauna showed an affinity towards finer sediments. It appears that depth, latitude, organic matter and clay are the

673

factors which influence the distribution of meiofauna in the study area. Previous studies have clearly correlated food supply (chloroplastic pigments) with nematode communities, which could not be made in the present study due to the bulk organic matter measurement. This is a much needed prerequisite for future meiofaunal studies in Indian waters. Acknowledgements This work was supported by the Department of Ocean Development, New Delhi, India (Grant No. DOD/10-MLR 10/97/OD-II dt. 17.11.1997). We thank CMLRE, Cochin, India for providing enough ship time for successfully completing the sampling. We acknowledge our sincere thanks to Mr. V. Raveendranath and Dr. V.N. Sanjeevan, CMLRE, DOD, Cochin, India for all the help rendered to us. We thank the Captain and the crew of FORV Sagar Sampada for the help they rendered during the sampling. Thanks are also due to the Department of Marine Biology, Microbiology and Biochemistry, School of Marine Sciences, Cochin University of Science and Technology, India for the facilities offered to carry out the work. We highly appreciate the three anonymous reviewers for their comments and suggestions to improve the quality of the manuscript. Appendix A. Supplementary information Supplementary data associated with this article can be found in the online version, at doi:10.1016/j.ecss.2009.11.034. References Ansari, Z.A., 1978. Meiobenthos from the Karwar region (Central west coast of India). Mahasagar-Bulletin National Institute of Oceanography 11, 163–167. Ansari, Z.A., Gauns, M.U., 1996. A quantitative analysis of fine scale distribution of intertidal meiofauna in response to food resources. Indian Journal of Marine Sciences 25, 259–263. Ansari, Z.A., Parulekar, A.H., 1998. Community structure of meiobenthos from a tropical estuary. Indian Journal of Marine Sciences 27, 362–366. Ansari, Z.A., Parulekar, A.H., Jagtap, T.G., 1980. Distribution of sub littoral meiobenthos off Goa Coast, India. Hydrobiologia 74, 209–214. Babu, R.V., Varkey, M.J., Kesava Das, V., Gouveia, A.D., 1980. Water masses and general hydrography along the west coast of India during early March. Indian Journal of Marine Sciences 9, 82–89. Boyd, S.E., Rees, H.L., Richardson, C.A., 2000. Nematodes as sensitive indicators of change at dredged material disposal sites. Estuarine, Coastal and Shelf Science 51, 805–819. Carvar, R.E., 1971. Procedures in Sedimentary Petrology. Wiley, New York, 653 pp. Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities: an Approach to Statistical Analysis and Interpretation, second ed. PRIMER-E, Plymouth, U.K. Cook, A.A., Lambshead, P.J.D., Hawkins., Lawrence E., Mitchell, Nicola, Levin, Lisa A., 2000. Nematode abundance at the oxygen minimum zone in the Arabian sea. Deep-Sea Research II 47, 75–85. Coull, B.C., 1985. Long-term variability of estuarine meiobenthos: an 11-year study. Marine Ecology Progress Series 24, 205–218. Coull, B.C., 1999. Role of meiofauna in estuarine soft-bottom habitats. Australian Journal of Ecology 24, 327–343. Damodaran, R., 1973. Studies on the benthos of the mud banks of Kerala coast. Bulletin of Department of Marine Sciences, University of Cochin 6, 1–126. De Bovee, F., Guidi, L.D., Soyer, J., 1990. Quantitative distribution of deep sea meiobenthos in the northwestern Mediterranean (Gulf of Lions). Continental Shelf Research 10, 1123–1145. (References and further reading may be available for this article. To view references and further reading you must purchase this article). De Leonardis, C., Sandulli, R., Vanaverbeke, J., Vincx, M., De Zio, S., 2008. Meiofauna and nematode diversity in some Mediterranean subtidal areas of the Adriatic and Ionian sea. Scientia Marina 72, 5–13. De Troch, M., Van Gansbeke, D., Vincx, M., 2006. Resource availability and meiofauna in sediments of tropical seagrass beds: local versus global trends. Marine Environmental Research 61, 59–73. El-Wakeel, S.K., Riley, J.P., 1957. The determination of organic carbon in marine muds. Journal of Du Counseil International Exploration 22, 180–183. Feller, R.J., Warwick, R.M., 1988. Energetics. In: Higgins, R.P., Thiel, H. (Eds.), Introduction to the Study of Meiofauna. Smithsonian Institution Press, Washington, D.C., pp. 18–38. Gambi, C., Vanreusel, A., Danovaro, R., 2003. Biodiversity of nematode assemblages from deep-sea sediments of the Atacama slope and trench (South Pacific Ocean). Deep-Sea Research I 50, 103–117.

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