[geophysical monograph series] indian ocean biogeochemical processes and ecological variability...

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Indian Ocean Biogeochemical Processes and Ecological VariabilityGeophysical Monograph Series 185Copyright 2009 by the American Geophysical Union.10.1029/2008GM000711

1. INTRODUCTION

In the pelagic ecosystems, bacterioplankton biomass is as-certained to be a substantial fraction [Azam et al., 1994; Bid-danda and Benner 1997; Wiebinga et al., 1997]. Indeed, as Fuhrman et al. [1989] and Kirchman et al. [1995] noted, bac-terial carbon can often exceed phytoplankton carbon in many regions of low chlorophyll concentrations. Primary produc-tion (PP) and consequent availability of easy-to-assimilate

dissolved organic matter (DOM) facilitate heterotrophic bacterial (Hbac) growth and abundance [Hansell and Peltzer, 1998; Brown et al., 1999; Ducklow et al., 2001]. Since much of the PP is grazed upon by larger, herbivorous zooplankton communities, proliferation of bacteria is essential for nour-ishing a plentitude of microzoans: ciliates, tintinnids, and heterotrophic flagellates particularly in regions, and seasons, of low chlorophyll concentrations [Cole et al., 1988; Gauns et al., 1996; Ramaiah et al., 1996; Landry et al., 1998]. In that, their proliferation by assimilating DOM helps nourish-ing particulate-ingesting phagotrophic microzooplankton, mesozooplankton, and/or other fauna. Further, their role is important in the biogeochemical cycling of biologically es-sential elements [Cho and Azam, 1990].

Bacterioplankton Abundance and Production in Indian Ocean Regions

N. Ramaiah, V. Fernandes, V. V. Rodrigues, J. T. Paul, and M. Gauns

National Institute of Oceanography, Council of Scientific and Industrial Research, Dona Paula, India

Microbes mediating biological and many geochemical processes are the key components in marine ecosystems. In this chapter, we provide information on spatiotemporal variations in heterotrophic bacterial (Hbac) abundance and pro-duction in three ecologically disparate regions: Arabian Sea (AS), Bay of Bengal (BoB), and equatorial Indian Ocean (EIO). In the AS, Hbac abundances were the largest during fall intermonsoon (FIM) (0.35–1.51 × 109 L−1), moderate during southwest monsoon (SWM) (0.20–0.45 × 109 cells L−1), and least during northeast monsoon (NEM) (0.05–0.35 × 109 L−1). Bacterial production (BP), ranging from 2.86 to 22.93 mg C m−3 d−1, was the highest during spring intermonsoon (SIM) when autotrophic production was the least. In the BoB, Hbac abundance was more during FIM (0.07–1.85 × 109 L−1 in the 0- to 120-m column) and lower during SIM (0.02–0.36 × 109 L−1). Spatial and temporal variations were clearly seen in BP too, which was higher during SWM (0.18–6.75 mg C m−3 d−1) and NEM (0.35–18.56 mg C m−3 d−1), moderate during FIM (0.01–4.19 mg C m−3 d−1), and least during SIM (0.001–2.49 mg C m−3 d−1). Annual BP accounted for up to 56% of primary production (PP) in the BoB. Despite the lowest Hbac abundance and production, BP:PP ratios were high in the oligotrophic EIO. As evidenced from sizable Hbac carbon biomass and from the often high BP:PP ratios (≥1.0), Hbac-biogeochemical and trophodynamic processes are very important in some regions/seasons of low autotrophic production.

120 BACTERIOPLANKTON ABUNDANCE AND PRODUCTION

Our understanding of the Indian Ocean (IO) biology has improved substantially. Beginning from the International IO Expedition, a series of major research programs such as Joint Global Ocean Flux Study (JGOFS), Global Ocean Ecosys-tems Dynamics, Monsoon Experiment (MONEX), Bay of Bengal Process Study (BOBPS), and India’s exclusive eco-nomic zone surveys among other regular ones have helped amass data on a variety of biological productivity parameters [see Qasim, 1982; Bhattathiri et al., 1996; Madhupratap et al., 1996a, 2003; Gauns et al., 2005]. Ducklow [1986] was the first to report on total abundance and production of bacte-rioplankton from sampling transects in the central and west-ern Arabian Sea (AS). Thereafter, there are many studies from northwestern AS [Burkill et al., 1993; Ducklow, 1993; Goosen et al., 1997; Veldhuis et al., 1997; Wiebinga et al., 1997; Campbell et al., 1998; Hoppe and Ullrich, 1999; An-derson and Ducklow, 2001; Ducklow et al., 2001], central and eastern AS [Ramaiah et al., 1996, 2000; Prasannaku-mar et al., 2001; Raghukumar et al., 2001; Sarma et al., 2003], Bay of Bengal (BoB) [Dileep Kumar et al., 1998; Gauns et al., 2005; Khodse et al., 2007; Fernandes et al., 2008a], and equatorial Indian Ocean (EIO) [Fernandes et al., 2008b]. These studies highlight that both bacterioplank-ton abundance and production within different regions of the IO vary seasonally. These studies are useful to note that the bacterial abundance and production are low during north-east monsoon (NEM) (December–February), moderate dur-ing spring intermonsoon (SIM) (March–May), and higher during summer monsoon (June–September) in response to coastal upwelling in particular. The euphotic zone basin-wide remains enriched in bacterial abundance of ~3 to 5 (×108) cells L−1 throughout the year, relative to other tropical regimes, presumably in response to overall high PP and dis-solved organic carbon (DOC) levels. Apparently, the Hbac processes are very crucial in the food-web dynamics and in the operation of microbial loop [Burkill et al., 1993; Landry et al., 1998]. Insights on their relationship with chlorophyll productivity and microfaunal assemblages as well as their spatiotemporal variability in their abundance and productiv-ity are essential for elucidating pelagic food-web dynamics in different regions of the IO. In view of this, a comparative account of abundance and productivity of the Hbac between seasons, regions, and depths (upper 120 m) of the IO is pro-vided in this chapter.

2. STUDY AREA

2.1. Arabian Sea

Unlike the Atlantic or Pacific Oceans, the IO is landlocked in the north and, in general, experiences seasonally chang-

ing monsoonal circulation [Wyrtki, 1973]. Most regions of the AS are biologically highly productive. Yet, seasonal dif-ferences in PP are quite large [Sarma et al., 2003]. Semi-annual reversal of monsoonal winds [Shetye et al., 1991; Banse, 1988; Madhupratap et al., 1996a; Smith et al., 1998] upwelling including the divergence in the central regions, winter cooling [Prasannakumar et al., 2001] are the main physical forcings that bring about this variability. In the AS, regular oscillation in monsoonal atmospheric conditions drive near-surface currents, affect mixed layer development, and influence nutrient supply in this region that usually experi-ences relatively constant levels of illumination [Shetye et al., 1991; Smith et al., 1998]. From the extensive measurements available, it is well established now that as a consequence of physical settings, seasonal differences in biological produc-tion greatly influence biogeochemistry [Burkill et al., 1993; Smith et al., 1998; Hansell and Peltzer, 1998; Naqvi, 2001], sedimentation rates [Nair et al., 1989; Haake et al., 1993], as well as regeneration of bioessential compounds [Hoppe and Ullrich, 1999]. Further, an extremely well-developed oxygen minimum zone [Swallow, 1984; Warren, 1994] in the northern AS is uniquely distinct with which coincides an extensive denitrification [Naqvi, 1994; Naqvi et al., 1998] at mid-depths accounting for over a third of the global marine denitrification [Naqvi et al., 2000].

2.2. Bay of Bengal

The BoB is a unique embayment receiving large river in-flow (~1.62 × 1012 m3 a−1) from Mahanadi, Ganges, Brah-maputra, and Irawaddy in the north, and Krishna, Cauvery, and Godavari on its west [Madhupratap et al., 2003]. The precipitation (~2 m a−1) exceeding evaporation (~1 m a−1) [Han and Webster, 2002], low-saline surface waters (28–33 psu), warmer sea surface temperatures (SST) (29°–30°C), and weak winds (<7 m s−1) stratify the upper 30- to 40-m column [Prasannakumar et al., 2002]. Further, absence of marked upwelling limits nutrient injection into the euphotic layer. The 4.5-layer ecosystem model used by Vinayachan-dran et al. [2005] to study phytoplankton bloom in the bay confirms the existence of subsurface chlorophyll maximum reported by Prasannakumar et al. [2002] and Madhupratap et al. [2003]. Apart from this, high terrigenous input (~1.4 × 109 tons a−1) [Subramanian, 1993] by rivers and prolonged cloud cover cause light limitation leading to low photosyn-thetic production [Prasannakumar et al., 2002].

2.3. Equatorial Indian Ocean

The open regions of EIO south of the Indian subcontinent is quite far from coastal influences, and as Schott et al. [2002]

RAMAIAH ET AL. 121

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observe, in the absence of equatorial upwelling and poorer micronutrient concentrations, the primary productivity is ex-pectedly low due to nutrient limitation. SST variations would

be small and suspended load very low leading usually to >100 m euphotic depths. In general, the biological oceanographic studies describing the primary and bacterial productivity characteristics and pigment concentrations in EIO are sparse but for a few earlier reports [Mitzkevich, 1974; Sorokin et al., 1985]. Further, the intermonsoon phases were poorly covered during the International Indian Ocean Expedition [Krey and Babenerd, 1976]. The research under the aegis of JGOFS has brought out the temporal variability in biological productiv-ity characteristics with the lowest autotrophic production, in particular, during the intermonsoon phases in the AS [Mad-hupratap et al., 1996a; Smith et al., 1998].

3. DATA AND METHODS

To provide a comparative account of Hbac numbers and production, the data used here are from three major pro-grams. From the AS, they were obtained under the JGOFS (India) Program during 1994–1997; from the BoB under BOBPS (2001–2006), and from EIO under the cobalt crust surveys (2003–2005). The sampling locations are provided in Figure 1. While a variety of biological analyses were measured under these programs, for brevity, only relevant data from these measurements are included for drawing cer-tain inferences.

Water sampling was carried out onboard ORV Sagar Kanya from the AS during April–May 1994, January–February 1995,

Figure 1. Sampling locations in different regions of Indian Ocean: CAS, central Arabian Sea; EAS, eastern Arabian Sea; WB, western Bay of Bengal; CB, central Bay of Bengal; EIO, equatorial Indian Ocean.

Table 1. Ranges of Heterotrophic Bacterial (Hbac) Abundance (No × 109 L−1) in Different Depth Zones of Vari-ous Regions of the Indian Oceana

Depth ZoneArabian Sea Bay of Bengal Equatorial

Central Eastern Western Central EIO

Southwest monsoon0–40 0.20–0.40 (4) 0.20–0.70 (7) 0.03–0.88 (14) 0.11–1.27 (19) 0.01–0.18 (24)60–80 0.40–0.52 (3) 0.28–0.35 (3) 0.10–0.29 (3) 0.02–1.45 (10) 0.02–0.19 (12)100–120 0.25–0.25 (1) 0.40–3.00 (2) 0.13–0.74 (8) 0.24–0.76 (9) 0.02–0.17 (11)

Fall intermonsoon0–40 ND 0.40–1.40 (4) 0.14–1.85 (16) 0.04–1.00 (20) ND60–80 ND 0.40–1.50 (2) 0.21–1.29 (10) 0.05–0.32 (10) ND100–120 ND 0.35–0.40 (2) 0.07–0.85 (10) 0.05–0.50 (10) ND

Northeast monsoon0–40 0.05–0.09 (6) 0.03–0.35 (3) 0.09–0.91 (16) 0.03–1.82 (19) 0.01–0.11 (28)60–80 0.05–0.08 (4) 0.10–0.10 (1) 0.10–0.54 (8) 0.09–0.31 (10) 0.02–0.22 (14)100–120 0.05–0.06 (3) 0.10–0.10 (1) 0.07–0.24 (4) 0.11–0.46 (10) 0.02–0.22 (6)

Spring intermonsoon0–40 0.25–0.95 (15) 0.55–0.75 (7) 0.04–0.25 (16) 0.02–0.36 (20) 0.01–0.06 (16)60–80 0.20–0.80 (8) 0.25–0.53 (4) 0.03–0.15 (8) 0.02–0.10 (10) 0.04–0.15 (8)100–120 0.20–0.70 (8) 0.40–0.53 (3) 0.02–0.06 (8) 0.02–0.17 (10) 0.01–0.07 (8)

aThe numbers of samples examined from each depth zone are in parentheses. ND indicates no data.


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and August–Septemeber 1996. Sampling from the BoB was during July–August 2001, September–October 2002, April–May 2003, and November 2005 to January 2006. From the EIO, sampling was carried out onboard A. A. Sidorenko during January–February and July–August 2003, and onboard A. Boris Petrov during February–March 2005.

For measuring bacterial abundance and production, sub-samples were collected from 10 or 30 L Go-Flo (General Oceanics, Florida, USA) bottles. These bottles were fixed onto the rosette equipped with conductivity-temperature-depth (Sea-Bird electronics, USA) console. Although eu-photic depth varied widely in these locations, from as shallow as ~25 m in the bay to as deep as 150 m in the EIO, to be consistant with the JGOFS protocols followed widely, eight discrete depths (viz surface, 10, 20, 40, 60, 80, 100, and 120 m) were sampled in the upper 120 m for measurements including Hbac abundance, production, chl a and primary productivity.

For estimating bacterioplankton abundance, acridine or-ange direct counts (AODC) were made following Parsons et al. [1984]. Since we estimated AODC during all the pro-grams, comparison of data from different regions is possi-ble. From all stations, 50 mL water samples from all depths were fixed with 0.22 µm prefiltered formaldehyde (2% fi-nal concentration) and stored at 4°C in the dark until slide preparation, usually within 4 weeks of sample collection. Subsample volumes of 2–3 mL were stained with acridine orange (final concentration 0.01 %) for 3 min, filtered (0.22 µm black Nucleopore filters) and mounted on glass slides using immersion oil (Botzoil, Germany) and observed im-mediately under 100X objective on an epifluorescence mi-croscope set up with 450–490 nm (blue exitation), 510 nm beam splitter, and a 520-nm emission filter on Olympus BH2 (Japan). Bacterial cells in at least 25 microscopic fields were counted, and the mean cell number per field was calculated and used for estimating total abundance by using the relation-ship detailed by Parsons et al. [1984]. Bacterial abundances were used for calculating the bacterial carbon biomass us-ing a conversion factor of 11 fg C cell−1 [Garrison et al., 2000].

Bacterial production (BP) rates were estimated from the measurements of methyl-3H-thymidine (specific activity 18 Ci mmol−1, Bhabha Atomic Research Centre, Mumbai, India) incorporation rates (tritiated thymidine incorporated (TdR)) by the water column bacteria. The protocol described by Ducklow [1993] was followed. Briefly, three 20-mL sub-samples from each depth pipetted into 50 mL polycarbonate tubes were ammended with 100 µL 59 nmol working solu-tion of 3H-thymidine and incubated in the dark at 22°–24°C for 1.5 h. The thymidine uptake was stopped by the addition

Figure 2. Heterotrophic bacterial (Hbac) carbon standing stocks calculated using 11 fg C per bacterial cell. Data from discrete sam-pling depths averaged from different stations in CAS, central Ara-bian Sea; EAS, eastern Arabian Sea; WB, western Bay of Bengal; CB, central Bay of Bengal; EIO, equatorial Indian Ocean shown in Figure 1. Annual averages derived using the mean seasonal values.

of 300 µL, 0.22 µm prefiltered formaldehyde. The zero-time blanks were run for the samples in order to obtain correc-tion for abiotic/filter adsorption. The samples were filtered through 0.22 µm cellulose acetate filters (25-mm diameter, Millipore India, Bangalore, India) and rinsed thrice sequen-tially with cold trichloroacetic acid (10% w/v) and ethanol

RAMAIAH ET AL. 123

(96%, v/v; final rinse). The filters were placed in 8-mL scin-tillation vials in moisture-free condition and 5 mL scintil-lation fluid (Cocktail-W, SRL, Mumbai, India) was added a day prior to radioassaying in a PerkinElmer Wallac 1409 DSA liquid Scintillation Counter (Waltham, Massachusetts, USA). TdR (picomole L–1 h–1) was calculated using the formula

TdR = (DPMs – DPMb) / (SV × T × SA × 2.22),

where DPMs is disintegrations per minute of the sample on the filter, DPMb is disintegrations per minute of the blank on the filter; SV is sample volume in litres; T is incubation time in hours, and SA is specific activity (m Ci m mol−1). To correct for the differences in in situ and onboard incuba-tion temperature, the Q10 value reported by Fernandes et al. [2008] was used.

The BP was estimated using a mean oceanic conversion factor of 2.17 × 1018 cells mol−1 thymidine incorporated [Ducklow, 1993]. This conversion factor appears to hold good for IO region. Our laboratory-based derivations of em-pirical factor indicated slightly higher at 3.76 × 1018 cells mol−1. To be consistent, Ducklow’s [1993] factor is used here for comparison with data available in literature.

For chl a measurements, 1 L water samples collected at predawn from all eight above-listed discrete depths were filtered through 47 mm GF/F filters. Chl a was extracted in

10 mL 90% acetone in the dark for 24 h in a refrigerator and its concentration determined using a fluorometer (Turner Designs, USA). PP was also measured from all these depths following JGOFS protocols [UNESCO, 1994]. Four (three light, one dark) 300-mL polycarbonate (Nalgene, Ger-many) bottles were filled with water samples from each depth and one ampoule each of NaH14CO3 (specific activ-ity of 185 kBq; Board of Radiation and Isotope Technol-ogy, Mumbai, India) was added into them. Following this, all bottles were tied onto a mooring system before dawn and incubated in situ at their respective depths for 12 h. Upon retrieval of the bottles by half hour past sunset, 100 mL volumes from each bottle were filtered through GF/F filters (25 mm diameter, 0.7 mm pore size; Whatman, USA). The filters were transferred into scintillation vials and exposed to 0.5 N HCl fumes overnight in a closed container. Five- milliliter liquid scintillation cocktail (Sisco Research Labo-ratory, Mumbai, India) was added to each vial, and uptake of 14C measured in a scintillation counter (Wallac 1409 DSA, PerkinElmer). The PP rate was calculated and ex-pressed as mg C m−3 d−1.

4. RESULTS

In general, the mixed layer depth in the sampling region was mostly ~40 m, and the subsurface chlorophyll maxima were in the depth zone of 40–80 m. Abundance of Hbac in

Table 2. Range of Heterotrophic Bacterial (Hbac) Production Rates (mg C m−3 d−1) in Different Depth Zones of Vari-ous Regions of the Indian Oceana

Depth ZoneArabian Sea Bay of Bengal Equatorial

Central Eastern Western Central EIOSouthwest monsoon

0–40 0.57–1.15 (4) 0.57–9.74 (8) 0.75–3.81(16) 1.92–6.75 (20) 0.004–1.78 (12)60–80 1.72 (2) 2.58–9.17 (3) 0.34–4.75 (8) 0.24–3.30 (10) 0.12–1.79 (6)100–120 2.29 (1) 2.72–4.00 (4) 0.18–0.93 (8) 0.20–1.03 (9) 0.12–0.70 (4)

Fall intermonsoon0–40 ND 2.40–4.60 (4) 0.27–3.73 (16) 0.19–4.19 (20) ND60–80 ND 1.50–2.30 (2) 0.23–0.89 (8) 0.17–1.18 (10) ND100–120 ND 0.30–0.60 (2) 0.07–0.51 (8) 0.01–0.30 (10) ND

Northeast monsoon0–40 0.05–0.19 (6) ND 2.06–18.56 (12) 0.65–3.28 (20) 0.01–1.89 (11)60–80 0.06–0.22 (4) ND 0.77–3.64 (8) 0.78–2.61 (10) 0.15–1.56 (6)100–120 0.02–0.15 (3) ND 0.35–1.31 (8) 0.42–1.22 (9) 0.20–0.47 (3)

Spring intermonsoon0–40 3.44–22.92 (12) 4.01–28.64 (6) 0.30–1.60 (16) 0.15–2.49 (20) ND60–80 3.44–7.16 (8) 2.29–22.92 (4) 0.24–0.77 (8) 0.01–0.66 (10) ND100–120 2.86–4.58 (8) 2.86–25.78 (3) 0.13–0.75 (8) 0.001–0.50 (9) ND

aThe numbers of samples examined from each depth zone are in parentheses. ND indicates no data.


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different regions in the IO suggests wide spatial and depth-wise differences (Table 1). Details of Hbac abundance in the central AS and eastern AS during different sampling periods are published previously [Ramaiah et al., 1996, 2000, 2005; Raghukumar et al., 2001]. Overall, the annual variability in Hbac abundance in the AS surface waters is of two orders (Table 1). The Hbac abundance was maximum during FIM (October 1993) ranging from 1.51 × 109 L−1 (surface wa-ters) to 0.35 × 109 L−1 (in the deeper layers). During SIM (April–May 1994) also, their abundance in the upper 120 m was quite high ranging from 0.20 to 0.95 × 109 L−1 and from 0.04 to 0.65 × 109 L−1 below 200 m. During NEM (February 1995), the Hbac abundance was the lowest (0.05–0.35 × 109 L−1) in the 0- to 120-m column. Below 200 m, their abun-dance ranged from 0.05 to 0.08 × 109 L−1. During southwest monsoon (SWM) (August 1996), Hbac abundance in the top 120 m ranged from 0.2 to 3.00 × 109 L−1.

In the BoB, the Hbac abundance was higher mostly in the central region during SWM (July–August 2001), compared to the other seasons. Thus, spatial and temporal differences in Hbac abundance are quite pronounced. Their abundance in the 0- to 120-m column was more during SWM (0.02–1.45 × 109 L−1 in the 0- to 120-m column) in the central bay and during FIM (0.07–1.85 × 109 L−1) in the western bay. During NEM, the Hbac abundance was moderate (WB: 0.07–0.91 × 109 L−1; CB: 0.03–1.82 × 109 L−1) and least during SIM (WB: 0.02–0.25 × 109 L−1; CB: 0.02–0.36 × 109 L−1). In the overall, Hbac abundance in the bay is higher than those recorded either from the AS or from the EIO.

In the EIO, the Hbac abundance ranged between 0.01 and 0.22 (× 109 cells L−1; overall seasonal average: 0.05 ± 0.03 × 109 cells L−1) during NEM. In the surface samples, Hbac showed an increasing trend from 1°N (0.05 × 109 cells L−1) to 1°S (0.08 × 109 cells L−1) and decreased thereafter (0.03 × 109 cells L−1 at 5° S). The Hbac abundance in the surface at equator was high during SWM and decreased southward. Their numbers in the surface ranged from 0.03 to 0.17 (× 109

cells L−1). The abundance during this season in the top 120 m ranged from 0.01 to 0.18 (× 109 cells L−1) with an average of 0.06 ± 0.03 × 109 cells L−1. Usually coinciding with sub-surface chlorophyll maxima, the Hbac subsurface maxima were around 80 m.

The Hbac carbon biomass calculated using 11 fg C cell−1 is shown in Figure 2. Season-wise, there is a wide difference in Hbac carbon biomass in the AS in particular. In the BoB, the standing stocks of bacterial carbon were higher during SWM in the central bay and during FIM in the western bay. They are of moderate quantity during NEM and the lowest during SIM. In the western bay, the annual bacterial carbon averaged 0.332 g C m−2 and in the central bay 0.335 g C m−2 in the 0- to 120-m column. The oligotrophic EIO had

Figure 3. Hbac productivity rates in different regions of the Indian Ocean. Data from discrete sampling depths averaged from differ-ent stations in CAS, central Arabian Sea; EAS, eastern Arabian Sea; WB, western Bay of Bengal; CB, central Bay of Bengal; EIO, equatorial Indian Ocean shown in Figure 1. Annual averages de-rived using the mean seasonal values. Seasonal averages of BP:PP ratios shown on the histograms. Unusually high BP:PP ratios obtained in particular during the SIM in the Arabian Sea excluded when PP rates were inexplicably low. Aberrantly high BP:PP ratios from other regions are also excluded.

RAMAIAH ET AL. 125

the lowest carbon biomass throughout the year showing no seasonal differences. Annual averages of calculated carbon standing stocks imply that bacterial carbon biomass is more in the eastern AS followed by that in the central bay and western bay.

The bacterial productivity in the IO region was similar in its pattern to that of the abundance (Table 2). The highest 0- to 120-m column integrated bacterial productivity was observed in the AS mostly during the SIM (Figure 3). While spatial and temporal variations are clearly seen in BoB, the productivity was usually higher during SWM and NEM and, the least during SIM. Annual BP averaged 0.134 g C m−2 d−1 in the western bay and 0.150 g C m−2 d−1 in the central bay, respectively, accounting for 43% and 56% carbon produced through PP. Though measurements from the EIO were made only during SWM and NEM, it is discernible from the data that bacterial productivity is more or less similar throughout the year. At many locations, the BP:PP ratios were unusually high. We have excluded the data of very high BP (>20 mg C m−3 d−1), in particular, from central and eastern AS. The BP:PP ratios after such exclusion are indicated on the histo-

grams in Figure 3. Often, these ratios were >1.0 signifying the importance of BP in regions of, and/or during times of, low autotrophic production.

During all the seasons, the chl a and bacterial abundance correlated poorly in most regions of the IO (Table 3). Thus, it is implicit that these two parameters are decoupled during most times of the year. The regression relationships between BP and PP from different regions are depicted in Figure 4. While the correlation between them was not that significant in the AS, western BoB, or the EIO, it was quite strong in the central Bay of Bengal. Bacterial growth rates (BGR) cal-culated using the production and abundance data for each region are the fastest during SIM and the slowest during the FIM in the AS (Table 4).

5. DISCUSSION

Hbac support microheterotrophic phagotrophs and influ-ence the atmospheric CO2 plus the water column chemis-try right from surface microlayer unto the deepest depths. Biological measurements in the AS by several investiga-

Table 3. Regression Relationships of Chlorophyll a (Chl a) Versus Hbac-C and BP Versus PP During Different Seasons in the Samples Collected From Different Regions in the Indian Oceana

Chl a Versus Hbac-C BP Versus PPCentral Arabian Sea

SIM y = 2.94x + 2.29; R2 = 0.0191 y = 0.85x − 2.49; R2 = 0.2249 SWM y = −32.20x + 24.43; R2 = 0.1017 y = −31.32x + 63.46; R2 = 0.6865NEM y = 105.88x + 2.16; R2 = 0.0424 ND

Eastern Arabian SeaSIM y = −0.87x + 3.76; R2 = 0.0014 y = 2.67x + 0.27; R2 = 0.6312SWM y = −3.35x + 10.73; R2 = 0.2240 y = 0.08x + 3.17; R2 = 0.0694NEM y = 169.57x − 1.48; R2 = 0.0815 ND

Central Bay of BengalSIM y = 0.82x + 5.79; R2 = 0.0002 y = 1.60x + 0.97; R2 = 0.2926FIM y = −7.78x + 8.52; R2 = 0.0521 y = 4.06x + 0.21; R2 = 0.6992SWM y = −1.30x + 5.48; R2 = 0.0185 y = 0.57x + 0.16; R2 = 0.3064NEM y = 0.44x + 7.46; R2 = 0.0008 y = 2.53x − 0.63; R2 = 0.5336

Western Bay of BengalSIM y = 55.09x + 3.62; R2 = 0.1357 y = 6.29x − 0.79; R2 = 0.4108FIM y = 3.37x + 5.17; R2 = 0.0239 y = 1.35x + 3.17; R2 = 0.0161SWM y = −3.39x + 6.64; R2 = 0.0268 y = 1.56x + 1.06; R2 = 0.144NEM y = 20.15x + 3.28; R2 = 0.3258 y = 0.80x + 0.46; R2 = 0.1243

Equatorial Indian OceanSIM y = 117.07x + 2.48; R2 = 0.3269 NDFIM y = −11.46x + 6.44; R2 = 0.0095 NDSWM y = 57.94x + 3.79; R2 = 0.1594 y = 0.07x + 0.19; R2 = 0.0195NEM ND y = −0.96x + 0.50; R2 = 0.0791

aChl a is given in mg C m−3, Hbac-C is given mg C m−3, BP is given in mg C m−3 d−1; and PP is given in mg C m−3 d−1. Abbreviations are SIM, spring intermonsoon; SWM, southwest monsoon; NEM, northeast monsoon; and FIM, fall intermonsoon. ND indicates no data


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Figure 4. Regression relationships between bacterial production (BP, mg C m−3) and primary production (PP, mg C m−3) during different seasons in the samples collected from different regions in the Indian Ocean. Regression equations provided in Table 3.

tors are helpful to suggest that phytoplankton experience seasonal and regional heterogeneity in their chemical ecol-ogy. Apparently, variability of Hbac abundance and their production is independent of the large, basin-wide seasonal variations in chl a and PP. It is inferable from the studies of Menzel [1964] (960 to 1440 mg m−3), Kumar et al. [1990] (from 1600 mg m−3 in the surface layers to >3600 mg m−3 at 3000 m), and Hansell and Peltzer [1998] (580 to >960 mg m−3) that the TOC concentrations in the region are quite high. Further, the particulate carbon from the excreta and mucous of the diverse fauna including myctophids could be sizable. Assuming even the lowest assimilation efficiency of 15% [Anderson and Turley, 2003] by bacteria, their car-

bon demand is well within 100 mg C m−3 d−1 in the surface waters of the AS.

This comparative account of Hbac abundance and pro-duction is helpful to suggest that there are spatiotemporal differences within the AS recognized among the biologi-cally highly productive ones. Campbell et al. [1998] have provided a detailed account of the spatiotemporal variabil-ity of Hbac abundance in the northwestern AS. In general, the Hbac abundance in the top 120 m (average: 0.53 × 108 cells L−1) in central and eastern AS locations are lower than those reported from northwestern AS (1.6 × 109 cells L−1) [Wiebinga et al., 1997]. Both Hbac abundance and their production at a common station N7 of the US JGOFS and

RAMAIAH ET AL. 127

17°N 64°E are quite comparable during the SIM. Further, both US JGOFS and our data sets from N7 show lower Hbac abundance during NEM when compared either with SIM or SWM suggesting a noticeable Hbac seasonal cycle in the central AS. The abundance of Hbac in the surface we recorded during the SWM is lower than those reported by Hoppe and Ullrich [1999]. Other than this, the seasonal trends of Hbac stocks in the central AS compare quite well with data from the AS [Wiebinga et al., 1997; Campbell et al., 1998; Pomroy and Joint, 1998]. In terms of C-biomass, Hbac account for over 50 % of the total heterotroph carbon at least during SIM and FIM [Ramaiah et al., 2005]. As also observed during the 1994–1995 US JGOFS experiments in

the northwestern AS [Campbell et al., 1998], the seasonal trends in depth-integrated abundance of bacteria differed quite substantially within the AS. The maximum abundance was much higher during the SIM and late SWM. From their abundance and faster growth rates, it is clear that the Hbac bring about rapid recycling of organic matter in the shal-lower euphotic zones of the AS [Madhupratap et al., 1996a; Campbell et al., 1998; Ducklow et al., 2001].

In the mostly net heterotrophic AS [Garrison et al., 2000; Prasannakumar et al., 2001], there is decoupling between PP and bacterial abundance. With very strong seasonal variability in PP (lowest during SIM), Hbac nourish microzooplankton and mesozooplankton during such times of low chloro-phyll production. Further, by being at the base of microbial loop, Hbac are significant players in sustaining the reported stable/invariant mesozooplankton biomass [Madhupratap and Haridas, 1992; Madhupratap et al., 1996b; Baars et al., 1994] in the mixed layer. Naqvi [2001] and Codispoti et al. [2001] recognize that over a third of the global-marine deni-trification happens in a small area ~1.2 million km2 in the AS. Further, the dentrification in the mid-depths is predomi-nantly Hbac mediated [Zehr and Ward, 2002; Jayakumar et al., 2004; Ramaiah, 2004]. Up to 75% of over 7000 isolates from the 200- to 1200-m zone reduce nitrate beyond nitrite [Ramaiah, 2004]. It is thus apparent that the Hbac assem-blages are adapted to oxygen minimum zones and facilitate rapid organic matter degradation through their ability to elaborate nitrate reductase, among a host of other hydrolytic enzymes, leading to nitrous oxide production. Probably, they also play a role contributing to atmospheric CO2. In that, in spite of the lowest PP during SIM, the estimated CO2 efflux to the atmosphere is about the same as that effluxed during SWM [Sarma et al., 2003].

In the BoB, at times, Hbac biomass is much more than that observed from the more productive AS. Yet, Hbac pro-duction rates are slower, only occasionally measuring up to a third of daily PP. Despite such spurts of higher growth rates, their biomass and production seem to be controlled by grazers particularly in the central bay. Fernandes et al. [2008a] observed high Hbac abundance but quite contrast-ingly poorer BP in the northern and westernmost locations. One suggestion was such a discrepancy might be because river discharges bring in organic particulates including lim-netic bacteria, large fractions of which may become inac-tive/dormant in the marine zones of salinities ³28 psu. This could also be substantiated by the fact that the metabolically active fractions, the direct viable counts of Hbac were lower in the western bay than those in the southern locations.

Although the daily primary productivity is known to meet up to 70% nutrients of microzooplankton and mesozooplank-ton [Landry et al., 1998], sizable Hbac biomass in the bay

Table 4. Hbac Growth Rates in Different Regions of the Indian Ocean Derived Using Hbac C and Production Rates Measured During Different Seasons

Sampling Season

Hbac C (mg C m−3)

HbacP (mg C m−3d−1)

BGR (d−1)

Doubling Time (h)

Central Arabian SeaSpring

intermonsoon0.51 5.62 10.97 2.2

Summer Monsoon

0.35 1.13 3.22 7.4

Eastern Arabian SeaSpring

intermonsoon0.52 11.54 22.11 1.1

Fall intermonsoon

1.04 2.31 2.22 10.8

Summer Monsoon

0.63 3.33 5.28 4.5

Central Bay of BengalSpring

intermonsoon0.09 0.66 7.48 3.2

Fall intermonsoon

0.19 0.83 4.33 5.5

Summer monsoon

0.53 2.33 4.40 5.5

Winter monsoon 0.28 1.52 5.39 4.4

Western Bay of BengalSpring

intermonsoon0.07 0.64 8.96 2.7

Fall intermonsoon

0.54 0.80 1.47 16.3

Summer monsoon

0.31 1.36 4.40 5.5

Winter monsoon 0.24 2.69 11.11 2.2Equatorial Indian Ocean

Summer monsoon

0.06 0.30 5.24 4.6

Winter monsoon 0.05 0.41 8.92 2.7


might be far more relevant in this region of low autotrophic production [Prasannakumar et al., 2002; Madhupratap et al., 2003). Microzooplankton biomass in the bay is much lower than that reported from the AS [Gauns et al., 1996; Jyothibabu et al., 2003]. Mainly consisting of tintinnids, dinoflagellates, ciliates, and HNF, the 0- to 150-m column integrated micro-zooplankton numbers averaged 13.4, 6.2, and 7.8 (×106 m−2), respectively, during SIM, FIM, and SWM. However, the mesozooplankton biomass in the top layers in the bay [Ra-khesh et al., 2006; Fernandes, 2008] is almost close to that reported from the AS [Madhupratap et al., 1996b; Madhu, 2004]. Thus, both allochthonous and autochthonous Hbac and particulates appear important as feed for mesozooplankton. Together with moderate populations of microphytoplankton consisting mostly of diatoms [Paul, 2007; Paul et al., 2007], abundant Hbac appear to be of primary significance in the direct nourishment of mesozooplankton, which are an impor-tant food component of nekton.

Hbac abundance and production rates in the equatorial region from 1oN to 5oS along 83oE do not show seasonal differences and are poorer than in the above two regions. However, Hbac abundance, coinciding with the subsurface chlorophyll maxima, was comparable to the results of Mitz-kevich and Kriss [1975] from the southern IO. In the appar-ently ultraoligotrophic EIO, spatiotemporal variations in chl a concentrations and PP were also not pronounced [Fern-andes et al., 2008b]. However, with quite high BP:PP ratios, the BP rate is substantial. Ducklow [1999] and Ducklow et al. [2002] suggest that the BP in the open, oligotrophic wa-ters may not exceed 25% of the PP.

Similar to bacterial abundance, the BP (0.003–4.7 mg C m−3 d−1) was also lower than that observed in the AS or BoB. It was approximately two factors lower than that in the east-ern AS. Nagata and Kirchman [1992] observed that Hbac in oligotrophic regions are efficient in the turnover of organic matter derived primarily from phytoplankton. Despite low

Table 5. Seasonal Ranges of Hbac Abundance Reported From Different Oceans From Various Programsa

Depth Zones (m)Sampling Season Surface–50 50–100 100–150 150–200

United States data sets (www1.whoi.edu)Atlantic Ocean (North Atlantic Bloom Experiment, 1989)

Mar–May 0.05–16 0.05–5.0 0.05–5.00 0.03–4.00Pacific Ocean (JGOFS, 1992; 140°W; 12°N–12°S)

Feb–Mar 0.05–0.07 0.03–0.06 0.02–0.05 0.02–0.10Mar–Apr 0.50–0.70 0.40–0.50 0.20–0.40 0.10–0.20Aug–Sep 0.04–0.10 0.02–0.08 0.01–0.08 NDSep–Oct 0.60–1.10 0.50–0.90 0.20–0.60 0.20–0.30

Indian Ocean (US-JGOFS, 1995; N and NW Arabian Sea)Jan–Feb (NEM) 0.07–0.15 0.05–0.10 0.03–0.07 0.02–0.04Mar–Apr (SIM) 0.70–2.50 0.50–1.50 0.30–0.70 0.09–0.10Jun–Jul (SWM) 0.30–1.70 0.10–1.70 0.10–0.40 0.01–0.05Sep–Oct (FIM) 0.50–1.70 0.30–0.80 0.20–0.60 0.02–0.05

JGOFS-India Arabian Sea data sets, along 64°E; west coast of India1994 Apr–May (SIM) 0.30–1.00 0.20–0.90 0.10–0.60 0.10–0.401995 Jan–Feb (NEM) 0.05–0.10 0.03–0.09 0.03–0.07 0.02–0.071996 Jul–Aug (SWM) 0.20–0.90 0.10–0.60 0.09–0.30 0.08–0.10

Bay of Bengal Process Study-India data sets; along 88°E; east coast of India2001 Jul–Aug (SWM) 0.03–1.27 0.02–1.45 0.13–0.76 0.04–1.002002 Sep–Oct (FIM) 0.04–1.85 0.05–1.29 0.05–0.85 0.01–0.022003 Apr–May (SIM) 0.02–0.36 0.02–0.15 0.02–0.17 0.03–0.042005 Dec–2006 Jan (NEM) 0.03–1.82 0.09–0.54 0.07–0.46 ND

Cobalt-crust surveys-India; along 83°E; 1°N-5°S2003 Feb (NEM) 0.01–0.11 0.02–0.22 0.02–0.07 ND2003 Jul–Aug (SWM) 0.01–0.18 0.02–0.19 0.02–0.17 0.03–0.082005 Feb–March (SIM) 0.01–0.06 0.04–0.15 0.01–0.07 ND

aNumber multiplied by 109 L−1. Abbreviations are NEM, northeast monsoon; SIM, spring intermonsoon; SWM, southwest monsoon; FIM, fall intermonsoon. ND indicates no data.

RAMAIAH ET AL. 129

rates of DOM formation, Hbac appear to efficiently utilize the available organic matter in the higher temperature re-gimes prevalent perennially in the surface layers [Kirchman et al., 1995]. As Cole et al. [1988] suggested, by serving as food, Hbac sustain most of the possible biomass of both microzooplankton and mesozooplankton in the EIO. The lat-ter’s reported biomass is in the range of 0.1–20 mL: averag-ing 10 mL 100 m−3 (displacement volume) [Rao, 1973; Krey and Babenerd, 1976]. In this regard, the observed high BP in excess of PP in the EIO calls for more sampling in such areas and modification of methods of measuring both PP and BP. In any case, assuming similar consumption rates of over 70% of the daily PP by microzooplankton and mesozoo-plankton, their food needs might far exceed the autotrophic production rates. Thus, Hbac with rapid growth rates appear important as food for microzooplankton and mesozooplank-ton in such ultraoligotrophic regions.

Wide regional and seasonal differences in Hbac abundance (Table 5) and 3H-thymidine incorporation rates (Table 6) are discernible from different oceanic regions. It is evident that the Hbac carbon biomass is substantial in different regions

of the IO. Also, the surface to 200 m integrated Hbac carbon production rates in mg m−2 d−1 are 448 during FIM (calcu-lated using data available in the work of Ducklow [1993]), 275–373 during NEM, 827–1347 during SIM, and from 275 to 478 mg m−2 d−1 during SWM. Except for SIM, our meas-urements compare well with those reported from offshore regions in Somali Basin (148–223 mg C m−2 d−1, with an exceptional high of 849 mg C m−2 d−1 during SWM, 129–139 mg C m−2 d−1 during NEM in 0–300 m column) [Wiebinga et al., 1997] and along 65°E (~373–515 mg C m−2 d−1 in 0–800 m column; derived from Hoppe and Ullrich [1999]). Dur-ing some seasons, many logistic difficulties and/or inclement weather conditions did not allow for uniform sampling from all the stations mentioned. Due to the paucity of data from some locations, we are unable to describe the north-south gradient either in Hbac abundance or in production rates. Hbac and BP rates varied spatially as well as temporally in the BoB too. Such differences were quite minor in the EIO.

Many values of calculated BP:PP ratios are unusually very high (indicated in Figure 3). The probable reason is, being light-controlled/dependent, the PP rate is the highest in the

Table 6. Seasonal Ranges of 3H-Thymidine Incorporation Rates by Hbac Reported From Different Oceans During Various Programsa

Depth Zones (m)Sampling Season Surface–50 50–100 100–150 150–20

United States data sets (www1.whoi.edu)Atlantic Ocean (North Atlantic Bloom Experiment, 1989)

Mar–May 1.00–8.00 0.50–1.50 0.50–0.60 0.10–0.40Pacific Ocean (JGOFS, 1992; 140°W; 12°N–12 °S)

Feb–Mar 0.80–1.50 0.10–1.50 0.06–0.40 0.03–0.10Aug–Sep 0.30–2.50 0.05–2.50 0.10–0.90 0.10–1.00Sep–Oct 1.80–3.00 0.10–2.00 0.10–0.50 0.07–0.10

Indian Ocean (US-JGOFS, 1995; N and NW Arabian Sea)Jan–Feb (NEM) 1.00–11.00 0.30–8.00 0.30–7.00 0.20–5.00Mar–Apr (SIM) 2.50–101.00 0.50–55.00 0.30–100.00 0.90–3.00Jun–Jul (SWM) 2.30–17.00 0.40–3.00 0.40–2.00 0.50–2.00Sep–Oct (FIM) 0.5–12.00 0.20–8.00 0.01–3.00 0.01–3.00

JGOFS-India Arabian Sea data sets, along 64°E; west coast of India1994 Apr–May (SIM) 25.00–50.00 14.00–29.00 13.00–16.00 1.00–4.001995 Jan–Feb (NEM) 0.50–1.90 0.30–0.90 0.30–0.70 ND1996 Jul–Aug (SWM) 0.90–3.00 0.20–3.00 0.10–0.30 0.06–0.10

Bay of Bengal Process Study -India data sets; along 88°E; east coast of India2001 Jul–Aug (SWM) 16.00–37.00 17.00–25.00 0.50–5.00 0.40–6.002002 Sep–Oct (FIM) 5.00–12.00 7.00–10.00 5.00–7.00 0.40–4.002003 Apr–May (SIM) 8.00–11.00 4.00–11.00 0.90–11.00 0.30–2.002005 Dec–2006 Jan (NEM) 1.13–32.4 1.34–6.34 0.61–2.28 ND

Cobalt-crust surveys-India; along 83°E; 1°N-5°S2003 Feb (NEM) 0.06–1.00 0.09–3.12 ND ND 2003 Jul–Aug (SWM) 0.07–3.11 0.10–0.52 0.80–3.00 0.80–1.80

aThe 3H-thymidine incorporation rates are given in pM L−1 h−1. Abbreviations are NEM, northeast monsoon; SIM, spring intermonsoon; SWM, southwest monsoon; and FIM, fall intermonsoon. ND indicates no data.


0- to 30-m column. Below 30 or 40 m, its rate decreases rapidly in all the regions we sampled. In our experiments, the dark respiration was often close to gross PP in bottles in-cubated below 80 or 100 m. On the other hand, BP tended to be uniform throughout the 0- to 120-m column or fluctuated without any trend. Thus, “depth-independent” BP, when di-vided by light-dependent PP in the euphotic depths that tend to be very low in the deeper column, some BP:PP ratios de-rived using the integrated values appear very high.

The autotrophic carbon fixation by phytoplankton begins a whole gamut of biochemical reactions of profound impor-tance on the whole for marine organismic assemblages, geo-chemistry, and global climate. The heterotrophs (bacteria, microzooplankton and mesozooplankton, nekton, and other top-order predators) are pivotal in supplying essential nu-trients for photosynthetic activities in the euphotic layers. Hbac, for instance, are primary agents involved in decompo-sition of innumerable complex organic molecules that ulti-mately are broken down to inorganic nutrients essential for phytoplankton. The ubiquitous, highly diverse and nutrition-ally versatile Hbac communities equipped with the unique ability of assimilating dissolved organic matter are far more relevant in biogeochemistry than their small size would suggest. As suggested by Morita [1982], they are patient, stay dormant, in the absence of their nourishment, but very fast to respond and usurp as soon as any degradable organic molecule is within their reach. Together with other micro-heterotrophs, these ubiquitous and self-regulating bacterial communities are pivotal for marine ecological dynamics. Thus, information on their abundance, distribution, produc-tion, and their involvement in nutrient cycling is essential for realizing their importance in altering the atmospheric CO2 and marine biogeochemistry.

Acknowledgments. We thank S. R. Shetye, Director, NIO, for fa-cilities and encouragement. This work was supported by the grants from the Ministry of Earth Sciences, New Delhi under JGOFS (India), BOBPS, and surveys for cobalt crust programs. We also thank the late M. Madhupratap for his leadership and guidance. We gratefully thank Raleigh Hood and the anonymous reviewers for their numerous suggestions for improving this article. This is NIO contribution number 4560.

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