Bacterial Growth Efficiency in a Tropical Estuary: Seasonal Variability Subsidized

Bacterial growth efficiency (BGE) is a key factor in understanding bacterial influence on carbon flow in aquatic ecosystems. We report intra annual variability in BGE, and bacteria mediated carbon flow in the tropical Mandovi and Zuari estuaries (southwest India) and the adjoining coastal waters (Arabian Sea). BGE ranged from 3 to 61% and showed clear temporal variability with significantly (ANOVA, p < 0.01) higher values in the estuaries (mean, 28 ± 14%) than coastal waters (mean 12 ± 6%). The greater variability of BGE in the estuaries than coastal waters suggest some systematic response to nutrient composition and the variability of dissolved organic matter pools, as BGE was governed by bacterial secondary production (BP). Monsoonal rains and its accompanied changes brought significant variability in BGE and bacterial productivity to primary productivity (BP/PP) ratio when compared to non-monsoon seasons in the estuaries and coastal waters. High BP/PP ratio (> 1) together with high carbon flux through bacteria (> 100% of primary productivity) in the estuarine and coastal waters suggests that bacterioplankton consumed dissolved organic carbon in excess of the amount produced in situ by phytoplankton of this region, which led to the mismatch between primary production of carbon and amount of carbon consumed by bacteria. Despite the two systems being subsidized by allochthonous inputs, the low BGE in the coastal waters may be due to the nature and time interval in the supply of allochthonous carbon. Introduction Heterotrophic bacterioplankton are the most abundant component in any aquatic system and are the major mineralizers of organic carbon (C) and nutrients. Consumption of dissolved organic carbon (DOC) by bacteria is one of the major pathways of material and energy flow in pelagic food webs [10]. DOC supporting bacterial metabolism originates either from in situ primary production (autochthonous C) or from external terrestrial inputs (allochthonous C) [31, 44]. This DOC can either be transformed to bacterial biomass (bacterial production, BP) or respired to inorganic carbon (bacterial respiration, BR), which is unlikely to reach higher consumers. In the marine offshore waters phytoplankton photosynthesis is a major source of organic carbon to bacterioplankton and there exists a balance between phytoplankton and bacterial production in time and space [6, 12], whereas in estuaries and adjoining coastal ecosystems this balance is lost due to the flow of allochthonous inputs from riverine discharge and terrestrial runoff [19, 26]. Bacterial growth efficiency (BGE, calculated using BP and BR) is a parameter that integrates various aspects of bacterial metabolism and is, in turn, affected by a variety of resource factors, such as nutrient and organic matter availability. BGE is tightly coupled to the physiological condition of bacteria, and in this respect may be an extremely sensitive index of the response of aquatic bacteria to their environment [15]. Values of BGE in aquatic systems are highly variable, and while there are a growing number of studies that have explored the environmental regulation of this variability, many important questions regarding resource control of BGE remain unanswered. The coastal oceans, especially tidally influenced estuaries, have drawn much attention as they are the most geochemically and biologically active areas of the biosphere [21]. Estuaries being on the margin between the coast and land, by nature are dynamic regions characterized by steep gradients in temperature, salinity and nutrient concentrations [14]. They mediate the export of matter to the coastal waters. In such systems the relative importance of autochthonous versus allochthonous supporting bacterial metabolism is important to our understanding of C cycling in aquatic systems. Multiple lines of evidence suggest that Mandovi-Zuari tropical system is net heterotrophic especially in the monsoon season where respiration exceeds gross primary production, which can only occur when external subsidies of organic C support estuarine metabolism [39]. This study area forms a part of the Northern Indian Ocean (southeastern Arabian Sea) is characterized by extreme wind forcing and seasonal monsoon winds which are an annual recurring phenomenon in these estuaries [29]. So, do the seasonal differences in monsoon winds affect the annual pattern in the BGE and carbon flow or not? To test the above hypothesis, the present study was carried out in tide dominated Mandovi-Zuari tropical estuary located in Goa on the southwest coast of India and was formed by the connection of two rivers, the Mandovi and Zuari into its adjoining coastal waters (Arabian Sea). Thus, this study addresses a question of significant interest to the field, and more so in a tropical marine environment for which such studies are especially scanty. Material and Methods Study site The study stations in the Mandovi-Zuari estuarine system are (1) in the Mandovi estuary (1530’N, 73 52’E), (2) in the Zuari estuary (1525’N, 7351’E) and (3) in the coastal waters (1530’N, 7344’E) adjoining the Arabian Sea (Fig. 1). The detailed characteristics of the study stations have already been described elsewhere [39]. Sampling and Sample processing Water samples from surface and close to the bottom (1 metre above the sediments) were collected at monthly intervals at the above-mentioned stations for a period of one year (January to December 1998) using Niskin water sampler (Miami, FL, USA). The water samples were pre-filtered through 220 μm nylon mesh to remove larger organisms. Samples were kept cold and dark while transported to the laboratory for analysis. Sampling months were classified according to three distinct seasons namely, the pre-monsoon (February May), monsoon (June September) and post-monsoon (October January) respectively. Depthintegrated approach was carried out to give a more accurate picture of flow and to analyze the relationships between parameters. Because of navigational constraints, the adjacent coastal station could not be sampled during the monsoon season (June-September). Water transparency was measured using Secchi disc. Water temperature was measured by field thermometer and salinity was determined with a Guildline 8400 Autosal salinometer. Dissolved oxygen concentration (DO) was determined by Winklers method using starch endpoint titration with thiosulphate [8]. Nutrient (ammonia, nitrite, nitrate and phosphate) concentrations in water samples were determined spectrophotometrically using standard methods [35]. Organic carbon concentrations were determined by high temperature (680°C) carbon analyzer (Shimadzu TOC 5000) with postassium biphthalate standard [43]. Chlorophyll a (Chl a) concentration was estimated fluorometrically from in samples (250 ml) collected on GF/F filters (Whatman, Maidstone, England) and pigments extracted in 90% acetone overnight in the dark at 4°C