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Influence of nutrient input on the trophic state of a tropical brackish water

D Ganguly1,3,∗, Sivaji Patra1, Pradipta R Muduli2, K Vishnu Vardhan1, Abhilash K R1,3, R S Robin1,3 and B R Subramanian3 1ICMAM Project Directorate, Ministry of Earth Sciences, NIOT Campus, Chennai 600 100, India. 2Wetland Research and Training Centre, Chilika Development Authority, Odisha 752 030, India. 3National Centre for Sustainable , MOEF, Chennai 600 025, India. ∗Corresponding author. e-mail: [email protected]

Ecosystem level changes in and biotic communities in coastal have been associated with intensification of anthropogenic pressures. In light of incipient changes in Asia’s largest brackish water lagoon (Chilika, India), an examination of different dissolved nutrients distribution and phy- toplankton , was conducted through seasonal water quality monitoring in the year 2011. The lagoon showed both spatial and temporal variation in nutrient concentration, mostly altered by fresh- water input, regulated the distribution as well. Dissolved inorganic N:P ratio in the lagoon showed nitrogen limitation in May and December, 2011. Chlorophyll in the lagoon varied between 3.38 and 17.66 mg m−3. Spatially, northern part of the lagoon showed higher values of DIN and chlorophyll during most part of the year, except in May, when highest DIN was recorded in the southern part. Sta- tistical analysis revealed that dissolved NH+–N and urea could combinedly explain 43% of Chlorophyll-a 4 − − (Chl-a) variability which was relatively higher than that explained by NO3 –N and NO2 –N (12.4%) in lagoon water. calculated for different sectors of the lagoon confirmed the inter- sectoral and inter-seasonal shift from mesotrophic to eutrophic conditions largely depending on nutrient rich freshwater input.

1. Introduction aquatic water bodies. Changes in nutrient concen- tration can shift the competitive advantage bet- During the last few decades, several research works ween different . Also, it can have been carried out on the nutrient dynamics change the chlorophyll specific carbon uptake rate of , and fresh waters. These nutri- by the individual species (Ganguly et al. 2013). ents are present in natural waters both in organic These modifications at the primary producer level and inorganic forms. Inorganic nitrogen occurs in can have significant impact on the net the form of nitrate, nitrite and ammonia which can metabolism as well as its . Apart from be readily consumed by the phytoplankton with DIN, dissolved organic nitrogen (DON) is also rec- different degree of preference. Elevated concentra- ognized to be a dynamic component of the nitrogen tion of dissolved inorganic nitrogen (DIN) results in pool in aquatic systems (Seitzinger et al. 2002; increased phytoplankton production and biomass, Berman and Bronk 2003) and has also been which may in turn be followed by increased popula- suggested to accumulate seasonally in coastal tion of consumer animals. At the same time exces- waters (Miyazaki et al. 2010; Violaki et al. 2010). sive nutrient enrichment can be detrimental to the Among DON, urea alone accounts for 11–65% of

Keywords. Chilika lagoon; dissolved inorganic nitrogen; urea; chlorophyll; trophic state.

J. Earth Syst. Sci. 124, No. 5, July 2015, pp. 1005–1017 c Indian Academy of Sciences 1005 1006 D Ganguly et al. water-soluble organic nitrogen (Mace et al. 2003). to quantitatively assess the present trophic status Indeed, urea has a range of natural and anthro- of the lagoon ecosystem along with its important pogenic sources; it is the most widely applied nitro- regulating parameters, trophic state index (TSI) gen fertilizer in many parts of the world (Glibert could be very useful (Carlson 1977, 1991; Lee et al. et al. 2005). However, its use has increased exponen- 2010). These types of studies defining the trophic tially such that urea presently accounts for 50% of status are very few in Indian waters. The objec- current global nitrogen (N) fertilizer applications tive of the present study was to evaluate the sig- (Glibert et al. 2006). In the present day, urea nificance of nutrient concentrations available at a appears to be a reliable tracer of the diffusion of varying degree at different seasons and sectors of wastewaters in the coastal marine environment, the tropical lagoon, to support the phytoplankton more specific and sensitive than other nutrients, . Special emphasis was given to with a behaviour that also reflects the technol- find the abundance and role of dissolved urea in ogy of the treatment plants (Cozzi et al. 2014). phytoplankton biomass distribution in the lagoon In addition, a large number of studies have shown water. Trophic state of the entire lagoon was also that urea is an important source of N for a great determined for the first time by using seasonally variety of marine phytoplankton, ranking often in observed data. importance as much as, or greater than, nitrate (Kudela and Cochlan 2000). Coastal waters can be supplied with urea through terrestrial and atmos- pheric inputs (Middelburg and Nieuwenhuize 2000; 2. Study area Glibert et al. 2001) and transfer from sediments (Rysgaard et al. 1998). Urea uptake by phytoplank- Chilika (19◦28′–19◦54′N; 85◦06′–85◦35′E), the lar- ton communities as a percentage of total nitrogen gest brackish water lagoon in Asia, has been desig- uptake can contribute upto 50% of the total nitro- nated as a on the gen taken up in coastal and estuarine regions (e.g., of in 1981. The shallow water body (aver- Chesapeake Bay, Glibert et al. 1991; Gulf of Both- age depth 2 m) is about 65 km in length, spreading nia, Sweden, Cochlan and Wikner 1993, etc.). With from northeast to southwest parallel to the - concentrations that often exceed 1 µM-N, urea can line with a variable breadth reaching 20.1 km. The be a significant nitrogen source for phytoplankton. lagoon is spread over an area of 950 km2 during Besides this, knowledge on urea uptake can give summer, which swells up to 1165 km2 during mon- precised estimation of f ratio (ratio of new to total soon (Siddiqui and Rao 1995). The lagoon is production) which is often used to examine the connected to the near Satapara biological efficiency of that ecosystem (Allen et al. (Sipakuda) by means of an artificial opening made 2002). Despite its significant influence, records in September 2000. High evaporation from the on dissolved urea distribution along the Indian shallow water body during the summer and large coastal waters and its impact on the ecosystem inflow of through various rivers and have not been studied much. A coastal water rivulets at the northern end of the lagoon during body like Chilika which regularly receives a large the monsoon and post-monsoon seasons contribute amount of fresh water (through 19 rivers/rivulets) significantly to the water spread area. The catch- carrying significantly high amount of inorganic ment area of the lagoon is 4406 km2,inwhich68% and organic load, could easily be affected by is constituted by western catchment and 32% by any change in agricultural practices in the catch- the Mahanadi delta, with an average rainfall of ment area. Since 1980–2009, the increase in total 1238 mm (southwest or summer monsoon); nearly nitrogen fertilizer used in Orissa state was repor- 75% of it occurs during the southwest monsoon. ted to be ∼600% (http://www.agriorissa.org/pdf/ 19 rivers/rivulets (R1–R19; figure 19) drain enor- FertilizerConsumptioninOrissa.pdf). This could mous fresh water into the lagoon together with sig- significantly influence the aquatic bodies (at its nificant loads of nutrients and suspended matter ecosystem level) situated in and along the state. resulting in appreciable changes in hydrological On the basis of its physicochemical properties, the conditions both seasonally as well as annually. trophic state of the lagoon like Chilika can be clas- While the northeast rivers (e.g., Makara (R15), sified as one of the four general classes, i.e., (1) oligo- Daya (R16), Nuna (R17), Bhargavi (R18)) repre- trophic (meaning low nutrient level and high clarity), senting the Mahanadi system contributes 68–85% (2) mesotrohic (a moderate elevation in nutrient of total freshwater discharge, the western rivers concentrations resulting in lower clarity and a re- (e.g., Janjira (R4), Kansari (R5), Kusumi (R7), duced desirable biological ), (3) eutrophic, Tarimi (R10), etc.) account for the rest (figure 1). (the enriched state), and (4) hyper-eutrophic (the During pre-monsoon, there is practically no dis- most enriched environment which can result in sub- charge from northwest rivers (R8–R14). Flow from stantial loss of environmental qualities). In order all the rivers reached a maximum during monsoon Trophic state of a tropical brackish water lagoon 1007

Figure 1. Location of the Chilika Lagoon and the sampling stations (R1–R19 are the 19 rivers draining into the lagoon). followed by significant reduction in post- and pre- and chlorophyll concentrations derived from the monsoon. Ecologically, the shallow lagoon repre- present study also supported the previous grouping sents a combined character of marine, brackish and of all the stations into identical sectors (Muduli freshwater (Muduli et al. 2012) with et al. 2013). The air temperature and wind velocity very low stratification. were also recorded using automatic probes (DAVIS 7440). Surface water samples (∼0.2 m) were col- lected during the daytime of each sampling month 3. Material and method (each seasonal sampling lasted for five consecutive days) assuming steady state conditions during the 3.1 Sampling and analysis sampling period as the tidal amplitude inside the lake is negligible (Gupta et al. 2008). Earlier stud- For sampling in pre-monsoon, monsoon and ies revealed the well mixed nature of the water post-monsoon, three representative months (May, column and very low vertical stratification in the August and December, 2011) were selected. Three lagoon (Mahapatro et al. 2013). At the inlet front independent observations were carried out seasonally (lagoon mouth), the tide was little more prominent during the representative months corresponding to than the rest of the lagoon and it was mostly semi- each season, viz., pre-monsoon (May), monsoon diurnal in nature with a maximum tidal range of (August) and post-monsoon (December) for the 1.2 m in spring time. However, in the main body of year 2011, covering a spread of 36 hydrologically the lagoon, the effect of tidal variation was found differing stations representing the south (1–14), comparatively less with order of 5–20 cm. central (15–17, 19–21, 23), north (22, 24–33) sec- Nutrient samples were collected in acid-cleaned tors and the outer channel (18, 34–36) (figure 1). buckets and Niskin-type bottles. The water was Sectorwise zonation of the selected stations was filtered through combusted GF/F filters (47 mm done by following the earlier research works carried Whatman) and stored frozen in HDPE bottles out in the same stations (Gupta et al. 2008; Muduli (cleaned with a phosphate-free soap solution). et al. 2012). Seasonal group average clustering Analysis was completed on the same day of from Euclidean distances by using salinity, nutrient collection (except urea). DIP (dissolved inorganic 1008 D Ganguly et al. phosphate) and DIN (dissolved inorganic nitrogen during the day. The light availability during day as the addition of nitrate, nitrite and ammonium time at the incubation depth was always main- concentrations) (Grasshoff et al. 1999) were ana- tained above the light saturation level (calculated lyzed using spectrophotometer (Model-1650 Shi- from the laboratory experiment for the major madzu). In order to estimate urea concentration, phytoplankton species available in Chilika waters; the direct chemical method introduced by Revilla unpublished data) using an underwater spectral et al. (2005) was followed. Each sample (4 ml) was radiometer (Satlantic Model Hyper OCRII). The treated with the colour developing reagent which Nalgene bottles were tightly capped and attached consisted 1 part of reagent A (3.4 g of diacetyl- to a rope hanging from a buoy and suspended monoxime in 100 ml of doubled distilled water at the same sampling depths. On retrieval, sam- (DDW)) and 3.2 parts of reagent B (300 ml of ples were immediately passed through Whatman concentrated sulfuric acid diluted to 535 ml with GF/F filter paper under gentle suction. The filters, DDW together with 0.5 ml of a ferric chloride after exposing to concentrated hydrochloric acid solution [0.15 g of ferric chloride in 10 ml of DDW]). fumes for a minute, were preserved in scintillation After 72 hr of incubation at room temperature, vials until analysis. Later, these filters were treated urea concentration of each sample was calculated with 5 ml scintillation cocktail in dioxane and the spectrophotometrically by measuring the absor- radioactivity was measured using a liquid scintil- bance at 520 nm. Total dissolved phosphorus (TDP) lation counter (Wallac 1409 DSA, Perkin Elmer, and total dissolved nitrogen (TDN) in the seawater USA). NPP rates were calculated based on a 12 hr were determined by alkaline persulphate oxidation photo-period and expressed as mg C m−3 d−1. (filtered water)following digestion with a buffer mix- ture (potassium peroxo disulphate, boric acid and sodium hydroxide) and by the spectrophotometric 3.2 Statistical analysis method (Grasshoff et al. 1999). Dissolve organic nitrogen (DON) and dissolve organic phospho- One way ANOVA test was performed to determine rous (DOP) were calculated as the difference spatio-temporal variation between various param- between TDN/TDP and DIN/DIP, respectively. eters (salinity, primary , etc.) in the Suspended matter (SPM) was collected by lagoon. Stepwise multiple regression analysis was filtering one litre of each sample through 0.45 µm carried out to determine the relative importance cellulose acetate membrane (Millipore) filters of various biologically active water quality parame- followed by drying the filters at about 75◦Cto ters (independent variable) in regulating the water constant weight. SPM was expressed as the dif- column Chl-a concentration (dependent variable) ference between the final and the initial weight in the lagoon. of the filter paper. Particulate organic nitrogen Trophic state indices (TSI) of the reservoir were was measured by the method given by Labry calculated using the four equations (Secchi disk, et al. (2002)whereas particulate organic phosphorous TSISD; total nitrogen, TSITN; chlorophyll pigments, was measured by the method given by Valderrama TSICHL; and total phosphorus, TSITP) described by (1981); Pujo-Pay and Raimbault (1994). Total nitro- Carlson (1977) and Kratzer and Brezonik (1981). gen (TN) was computed from the sum of TDN and The equations are as follows: particulate organic nitrogen (PON). Similarly, total phosphorus (TP) was calculated as the summa- − . tion of TDP and POP. The transparency of the TSISD =60 14 42 ln (SD) water was measured using a Secchi disk (SD) to TSITN =54.45 + 14.43 ln (TN) define the euphotic layer. The water samples were TSITP =14.42 ln (TP) + 4.15 filtered through GF/F Whatman filter paper for TSICHL =9.81 ln (Chl) + 30.6 the analysis of chlorophyll-a (Chl-a). Measurement of the acetone extract was done by means of a UV-visible spectrophotometer. where SD was in meters, TP and Chl-a were in mg Net primary production (NPP) was measured at m−3 and TN was in mg l−1. The waters with TSI 11 selected stations (St. no. 3, 6, 13, 18, 19, 20, <40 are grouped into oligotrophic state, and the 23, 26, 29, 33, 35) by in situ 14C assimilation waters with TSI ranging from 40 to 50 are distin- method (UNESCO 1994). Surface waters (water guished into mesotrophic state. If the TSI values samples filtered to remove grazers) in perfectly range from 50 to 70, the waters belong to eutrophic transparent Nalgene bottles (two light and one state. The value of TSI higher than 70, suggests 14 dark) were inoculated with labeled NaH CO3 hypertrophic state (Kratzer and Brezonik 1981). (activity 5 µCi ml−1; BARC, Mumbai) and incu- All mathematical and statistical computations bated at in situ conditions (at ∼0.4 m depth at were made using Excel 2007 (Microsoft Office) and high tide condition) for 12 hr (06:00–18:00 hr) Minitab 16. Trophic state of a tropical brackish water lagoon 1009

4. Results and discussion watersheds as well as seawater exchange through the outer channel. Small tidal amplitude in the 4.1 Lagoon hydrography and nutrients lagoon indicated its lesser influence over the hydro- The hydrography of the Chilika lagoon is largely logical characters, whereas, the wind induced driven by fresh water, supplied from the upstream churning of bottom sediment indicates the possible

40 8

30 6

20 4 -N (µM) Salinity 4 10 2 NH

0 0 9.0 30

8.6 20 8.2 pH -N (µM) -N (µM) 3 10 7.8 NO

7.4 0 300 0.8

275 0.6 M) M) µ µ 250 0.4 -N ( 2 DO (

225 NO 0.2

200 0.0 100 2.4

) 1.8 -1 75 M) M) µ 50 µ 1.2

0.6 SPM (mg l (mg SPM 25 Urea-N ( Urea-N

0 0.0 1.8 25 20 1.4 15 1.0 -P (µM) -P

4 10 DIN/DIP

PO 0.6 5

0.2 0 120 30 100 25 May August December ) 80 -3 20 M) µ 60 15 -Si ( 4 40 10 Chl-a (mg m SiO 20 5

0 0 South Central North Outer South Central North Outer Figure 2. Sectoral mean of water quality parameters at the Chilika lagoon during May, August and December, 2011. 1010 D Ganguly et al. influence of the suspended particles in the water lagoon remains significantly different from one ano- chemistry and other in situ metabolic activities. ther with respect to depth, transparency, salinity, The three sectors and the outer channel of the DO, nitrite-N, nitrate-N, ammonia-N, phosphate-P,

Pre-monsoon Monsoon Post-monsoon

Salinity

DO ( M)

Chl-a (mg m-3)

NH4-N ( M)

NO3-N ( M)

Urea-N ( M)

Figure 3. Spatio-temporal distribution of (a) ammonia-nitrogen, (b) nitrate-nitrogen, (c) urea-nitrogen, (d) salinity, (e)DO, (f)Chl-a in the Chilika lagoon. Trophic state of a tropical brackish water lagoon 1011

TN, TP and chlorophyll-a concentration. A well- sampling months at different sectors, are expressed + defined spatio-temporal heterogeneity in the dis- in table 1. The relative increase in NH4 –N fraction tribution of various water quality parameters was from monsoon to post-monsoon months could be observed in the lagoon. Mean lagoon salinity associated with several biogeochemical processes reached the maximum value during pre-monsoon dominated by dissimilatory nitrate reduction to when the fresh water discharge was the minimum ammonium (DNRA; Dunn et al. 2012) and in situ and water exchange through the outer chan- mineralization of dissolved and particulate organic nel was the most dominant. The highly dynamic matter in this shallow tropical lagoon. Except in character of the is highlighted by the fact the monsoon months, the DIN:DIP ratio in the that all the sites experienced almost the entire lagoon remained well below the Redfield ratio. range of salinities. Previous studies showed that the major sources of inorganic nutrients were through 4.2 Distribution of dissolved organic nitrogen the river discharge as evident from their maximum and phosphorous concentrations during monsoon season. The results of the present study showed almost the similar Dissolved organic nitrogen (DON) in the lagoon spatio-temporal pattern of the lagoon hydrogra- showed significant spatio-temporal variation with phy and nutrient distribution as those reported in mean seasonal values of 42.9 ± 7.65, 35.51 ± 5.32 some of the previous studies (Nayak 2004; Gupta and 39.93 ± 5.01 µM during May, August and et al. 2008; Panigrahi et al. 2009; Muduli et al. December, respectively. In May 2011, exception- 2012; Kanuri et al. 2013 and others). Seasonal vari- ally high DON concentration was observed in the ation of different water quality parameters (salin- northern sector (64.31 ± 12.23 µM), which coin- ity, pH, DO, spm, nutrients and chlorophyll-a) cided with relatively higher Chl-a concentration during this present study, at four different sec- compared to the other sectors. A substantial dilu- tors of the lagoon are given in figure 2. The tion of DON concentration in the northern sector spatio-temporal distributions of the water quality was recorded during August with the introduction parameters, was presented in the surface plot (fig- of riverine fresh water in to the lagoon. Among var- ure 3), which shows a clear pattern in the dis- ious forms of DON available in the lagoon, urea tribution of those water quality parameters in a concentration ranged between 0.02 and 4.16 µM spatial gradient over the whole lagoon, during the which was higher than the values reported in study. The salinity (p<0.05 and p =0.006) Florida Bay (Glibert et al. 2004) but considerably and DIN concentration (p =0.003, p<0.001) less than different parts of Chesapeake Bay, Mary- in the Chilika lagoon showed significant variation land (Glibert et al. 2005). Mean lagoon concen- between the seasons and the sectors. The relative trations of urea-N in May, August and December, contribution of the inorganic N species in total 2011, were found to be 0.72 ± 0.35, 1.28 ± 0.73 and − + − DIN (NO3 –N + NH4 –N + NO2 –N) during three 0.89 ± 0.31 µM, respectively. Highest and lowest

Table 1. Comparison of relative percentage contribution of urea-N concentration with + − − those of dissolved inorganic-N (DIN = NH4 + NO3 + NO2 ) during May, August and December, 2011.

Season Sector DIN (µM) %NH4 %NO3 %NO2 %Urea PRM South 3.99 ± 1.61 48 50 2 10 Central 10.59 ± 3.49 57 37 5 7 North 7.91 ± 1.73 38 59 3 13 Outer 2.85 ± 0.09 36 62 2 14 Mean 45 52 3 11

MN South 6.77 ± 1.57 35 64 1 12 Central 15.77 ± 7.45 20 78 1 9 North 24.37 ± 13.98 11 88 1 7 Outer 11.24 ± 6.89 35 63 2 4 Mean 25 73 1 8

PM South 8.14 ± 2.28 58 42 1 12 Central 10.27 ± 3.23 43 57 0 8 North 17.92 ± 9.50 31 68 1 6 Outer 6.17 ± 0.97 42 57 1 7 Mean 43 56 1 9

% urea = (urea concentration ×100)/DIN concentration. 1012 D Ganguly et al. urea-N concentration was recorded at the north- pre-monsoon but the concentrations were not sig- ern sector and the outer channel, respectively, dur- nificantly varying (p>0.05) from the adjacent ing all the sampling months. The relative contri- northern sector. During the post-monsoon, the bution of urea (being a member of DON family) contributions of both these components (inorganic was expressed as percentage of total DIN (urea% = + organic) were almost comparable in the lagoon [Urea concentration ×100]/DIN concentration). waters even though there existed a predominance Although there were dilutions in DON from pre- of the organic form for the rest of the year. Scat- monsoon to monsoon, higher mean urea-N concen- terplot between DON and Chl-a, during May when tration was recorded in the later season with the freshwater flow to the lagoon was very low, revealed highest value recorded at station 27 in the north- a strong positive association, where 58% of vari- ern sector during August (4.16 µM). Urea showed a ability of Chl-a concentration was explained by significant negative relation with the lagoon salin- DON (r2 =0.58, n = 34, p = 0.003) (figure 4). No ity (r2 =0.47, p =0.01), which indicated its terres- such significant relation was observed (p>0.05) trial origin and gradual dilution towards the higher in the other two sampling months. These results salinity waters. Table 2 represents the range of indicated the preference of the primary produc- concentrations of urea (µM-N) from some coastal ers present in the lagoon to utilize the regener- and estuarine sites including the present study. ated DON (in May) as a nutrient over the anthro- The contribution of urea to the total DON ranged pogenically derived DON (August and December). between 1.1 (December) and 8.37% (August). The Similar observations were made from the Chesa- higher contribution of urea in DON in the northern peake Bay by Bronk and Glibert (1993), where sector was attributed to the monsoonal increase in a higher degree of regenerated DON uptake by its supply and a decrease in DON in the lagoon the phytoplankton was recorded in summer than water. The relative contribution of urea-N with in spring. Mean lagoon DOP was maximum in respect to inorganic-N concentrations in lagoon August (1.95 µM) followed by May (1.71 µM) and waters was maximum during May although high- December (0.79 µM). Among the sectors, northern est urea concentrations were observed during mon- and central sectors showed higher DOP values com- soon. Sectorwise, urea-N showed its maximum con- pared to rest of the lagoon throughout the year. tribution with respect to DIN concentration at the 25 outer channel during pre-monsoon. Formation of )

-3 y = 0.2414x - 1.4953 intermediates like urea during DON mineraliza- 20 R² = 0.5841 tion at a higher salinity (Berman and Bronk 2003) could explain its relatively higher contribution dur- m (mg 15 ing this part of the year. During May, when the a riverine contribution was very small, percentage 10 of inorganic nitrogen in the lagoon waters was the minimum and the major form of nitrogen was 5 organic. In shallow coastal ecosystems like Chilika, Chlorophyll- remineralization of organic matter in the sediment/ 0 0 20406080 suspended could often be a major source DON (µM) of dissolved inorganic as well as organic nutri- ents in the water column. The relative contri- − Figure 4. Scatter plot between DON (independent variable) butions of NO3 –N and urea were higher in the and Chl-a (dependent variable) during May 2011 at Chilika outer channel than other parts of the lagoon, in lagoon.

Table 2. Range of concentrations (µM-N) of urea from some coastal and estuarine sites. Range of Location concentration Reference

Great South Bay, New York 0.6–9.4 Kaufman et al. (1983) Mankyung and Dongjin River Estuary, Korea 0.6–4.3 Cho et al. (1996) Chesapeake Bay, Mainstem <0.01–8.16 Lomas et al. (2002) Florida Bay, Florida 0.36–1.7 Glibert et al. (2004) Chicamicomico R, Chesapeake Bay, <0.01– 24.2 Glibert et al. (2005) Maryland; Kings Creek, Chesapeake Bay, Maryland and Coastal Bays, Maryland Southwest coast of India 0.05–1.34 Gopinath et al. (2002) Chilika Lagoon, India 0.02– 4.16 Present study Trophic state of a tropical brackish water lagoon 1013

4.3 Chlorophyll (Chl-a), dissolved oxygen (DO) Table 3. Multiple regression analysis with a stepwise vari- and primary productivity (PP) able selection. r2 Low water column chlorophyll in the southern sec- Predictor (stepwise) pfn tor during most part of this study (figure 3) could be attributed to less availability of inorganic nutri- S 5.3 0.432 0.22 24 ents, favouring the growth of slow growing sea- WT 15.3 0.287 1.36 24 + grass compared to the first growing phytoplankton NH4 44.7 0.035 3.79 24 (Duarte 1995) in this region. Previously, Nayak et al. Urea 58.3 0.033 4.07 24 − (2004) reported highest Chl-a concentration as NO3 68.1 0.046 3.86 24 −3 − high as 54.04 mg m from the northern sector NO2 70.7 0.08 2.48 24 3− in May 2001, immediately after the new mouth PO4 76.5 0.041 4.33 24 opening at Satapada. No such high concentrations Dependent variables: Chl-a, independent variables: salin- were recorded in the present observation, but it − − −3 ity (S), water temperature (WT), NH4, urea, NO3 ,NO2 , was well within the range (0.37–23.40 mg m ) 3− 2 PO4 .r = coefficient of multiple determination (i.e., reported by Panigrahi et al. (2007). The observed the percentage of the response variable variation that is values of dissolved nutrients as well as chloro- explained by the linear model), p = probability level, phyll in the lagoon during 2001–2002 were higher f = critical value of the F-distribution, n =numberof (Mishra and Shaw 2003; Panigrahi et al. 2007) than observations. those observed in the present study. This could be attributed to the difference in annual rainfall bet- ween the two years. Excess rainfall in 2001–2002 The DO concentrations are often regulated by ben- resulted higher runoff from the surrounding catch- thic seagrass species in the southern sector where ment area, which contained a higher nutrient load the water column chlorophyll concentration is rel- compared to 2011, when the annual rainfall in adja- atively low (figure 2). Low DO values in the south- cent Puri and Ganjam district (consisting the major ern sector during August, could be explained by catchment area) was 44.8 and 42.2% less than the the stresses caused by the freshwater intrusion, normal annual rainfall (Annual report on natural on the halophilic seagrass species (Collier et al. calamities, 2011–2012). The significance of Chl-a 2014). Positive apparent oxygen utilization (AOU) distribution in the lagoon was tested by stepwise values (less than saturation DO) were found at multiple regression analysis.The dependent variable lower Chl-a abundance (in August) and low to was Chl-a concentration and the independent vari- moderately negative AOU values (DO supersatu- ables were salinity (S), water temperature (WT), + − 3− ration)atrelativelyhigherChl-a (in pre- and post- NH4 –N, urea, NO3 –N and PO4 –P. Statistical anal- monsoon months). Although, Chl-a concentration ysis revealed a significant correlation between Chl-a reached the maximum during December followed and independent variables tested with 76.5% (table by May and August, AOU values were more nega- 3) explained variability (equation 1). The explained tive in May compared to December. Muduli et al. variability of Chl-a distribution found 5.3% for + (2012) recently reported a gradual decrease of bac- salinity, 10% for temperature, 29.4% for NH4 –N, − − terial respiration from monsoon (August) to pre- 13.6% for urea, 9.8 for NO3 –N, 2.6 for NO2 –N and 3− monsoon (May) accompanied with an increase in 5.8% for PO4 –P . The results clearly indicated + air–water CO2 efflux (increase in biological utiliza- that NH4 –N and urea in the lagoon water play a tion of oxygen) for two successive years (2009 and predominant role (43%) on the variation of Chl-a 2010) in the same lagoon. Heavy precipitation in concentration over other biochemical parameters. the monsoon months, characterized by low salin- These results were in association with the in situ ity and high turbidity led to a significant decrease observation made by Fertig et al. (2013) depict- in PP in the lagoon (ANOVA, p < 0.01) com- ing the greatest uptake preference of ammonium, pared to non-monsoon months. Among the sec- followed by urea, and nitrate by phytoplankton in tors, central sector showed highest NPP followed Chincoteague Bay, Maryland, USA. by northern, southern and outer channels both in August and December (figure 5). In all the three − − +− seasons, i.e., pre-monsoon (r2 = 0.54, p = 0.01), Chl-a =41.1 0.029 S 1.11 WT + 0.66 NH4 N 2 − monsoon (r = 0.49, p = 0.016) and post-monsoon − 2 +4.27 Urea + 0.241 NO3 N (r = 0.66, p < 0.003), Chl-a showed significant − − +8.7NO − N+3.70 PO3 − P(1)positive correlation with NPP (11 stations data) 2 4 at varying degree of significance. This observation supported the use of Chl-a as one of the best proxy Day-time DO concentration in the lagoon of phytoplankton biomass for studies of primary remained high with a high degree of saturation. productivity (Huot et al. 2007). 1014 D Ganguly et al.

300 Premonsoon Pre-monsoon Monsoon TSI-SD ) 250

1 TSI-Chl - Postmonsoon d 90 TSI-TP -3 200 TSI-TN 150

100 TSI

NPP (mgC m NPP (mgC 60 50

0 South Central North Outer

Figure 5. Spatio-temporal variation of NPP in the Chilika 30 lagoon, 2011. South Central North Outer

Monsoon 4.4 Trophic status index (TSI) of the lagoon TSI-SD 90 TSI-Chl Trophic state index deviations (Carlson 1977, 1991; TSI-TP Kratzer and Brezonik 1981) are known to be impor- TSI-TN tant for assessing historical trends in nutrient lim- itation in cases where spatio-temporal monitoring TSI data on total nutrient concentrations are available. 60 In the derivations of original TSI, Carlson (1977) intended to build equations that would produce the same TSI value for a particular lagoon, irre- spective of whether Chl-a, phosphorus, or trans- 30 parency was used to calculate the index of trophic South Central North Outer state. The accuracy of the index values based on Chl-a, phosphorus, and transparency depends on Post-monsoon the assumption that phosphorus was the main algal TSI-SD ( ) eutrophic to hyper-eutrophic biomass-limiting factor, and that underwater light TSI-Chl 90 ( ) mesotrophic to eutrophic climate was dominated by phytoplankton rather TSI-TP ( ) oligotrophic to mesotrophic than non-algal turbidity. In reality, these assump- TSI-TN tions are not easy to be demonstrated in many water bodies, and there are often obvious differ- TSI ences in the calculated trophic state (Matthews 60 et al. 2002; An and Park 2003; Lee et al. 2010). In this case, Carlson (1991) suggested giving priority to biological parameters such as Chl-a that rep- resents visible symptoms of , when classifying a lagoon’s trophic status. Several work- 30 ers supported Carlson’s idea that the trophic state South Central North Outer index determined with Chl-a would provide a bet- ter indication of lagoon trophic state than the one Sector determined with total phosphorus concentrations or transparency (e.g., Matthews et al. 2002; An and Figure 6. Seasonal variation in trophic state indices cal- culated from Secchi disk transparency (TSI-SD), Chl- Park 2003; Lee et al. 2010). a (TSI-Chl), total phosphorus and total nitrogen (TSI- In the present study, TSISD in all the four sectors TN). Dotted line represents transition from oligotrophic to ranged between 57.01 and 78.48 with the highest mesotrophic (····), dashed line (- - -) represents transition values observed in the northern sector irrespective from mesotrophic to eutrophic condition and solid line (—) of the seasons. TSI values calculated from SD, TN, represents transition from eutrophic to hypereutrophic condition. TP and Chl-a at different sectors in three different seasons were given in figure 6. The mean annual TSISD for the whole lagoon was calculated to be substantially lower values than TSISD all over the 63.7 which indicated the clear eutrophic nature in lagoon throughout the study period. These lower terms of Secchi disk transparency. TSICHL showed values of TSICHL than TSISD, clearly indicated that Trophic state of a tropical brackish water lagoon 1015 something other than algae, perhaps colour, sedi- 5. Conclusion ment particle or non-algal seston, was contributing to the light attenuation. Similarly, near the outer The present study revealed that primary produc- channel, the TSISD was mostly recorded very close tivity at Chilika lagoon was largely influenced + to 60, although the chlorophyll was relatively less. by dissolved NH4 –N and urea-N concentration Being the mouth region, the suspended particle and the lagoon remained eutrophic during Decem- could be less dominated by the algal particle com- ber, with concentrations of Chl-a regularly exceed- pared to the inorganic suspension caused by regu- ing 10 µgL−1 over the period. During the dry lar tidal activities. TSICHL showed greater spatio- season, DON could explain 58% variability of temporal variability than that of TSISD.TSICHL Chl-a concentration in the lagoon, which showed also revealed that mesotrophic nature prevailed at the relative importance of regenerated DON over the southern sector and outer channel during both anthropogenic DON to the primary producer when May and August, whereas northern and central DIN:DIP was <16. Our present understanding of sector remained marginally eutrophic during these the linkages between nitrate, ammonium and urea periods. In contrast, during December, the lagoon was fertilization and their transport to downstream in relatively enriched trophic state irrespective of the aquatic systems is limited (Silva et al. 2005; Di sectors with highest intensity at the northern part. and Cameron 2008). The influence of in situ bio- When TSICHL is equal to or greater than TSITP, geochemical processes like DNRA, denitrification, phosphorus generally is limiting to algal growth. mineralization, etc. and extent of sediment–water When TSICHL is substantially lower than TSITTP, coupling could be of equal importance compared this indicates that there is less algal material to the transport processes in regulating the nutri- present than expected, based on total phospho- ent status of the shallow lagoon and corresponding rus, and that some other factors may be limit- productivity. Further research to quantify the rel- ing. In the same manner, the deviation between ative importance of these various processes will be TSICHL and TSITN can be used to infer whether useful to protect coastal waters like Chilika from or not nitrogen limitation occurs. Those relation- rapid eutrophication incidences. This present study ships have been extensively used by most related revealed dynamic inter-sectoral and inter-seasonal studies (e.g., Matthews et al. 2002; An and Park changes in the trophic status of the Chilika lagoon, 2003; Lee et al. 2010). For instance, Matthews influenced by huge river runoff associated with the et al. (2002) employed the concept of TSI dif- southwest monsoon. From the present study, it can ferences to assess the trophic state and nutrient be concluded that the trophic state of the lagoon limitation of Lake Whatcom (WA, USA). All the was primarily controlled by the combined effect of values for TSITP remained between eutrophic to turbidity and nitrogen availability during May and hyper-eutrophic classes with mean annual value of December, while the state was directly influenced 67 in the lagoon. Significant higher TSITP than by non-algal light attenuation during intense mon- TSICHL indicated that there was less algal material soon (August). Slightest perturbation in the lagoon present than expected based on total phosphorus, water quality, due to the alteration in precipita- and that some additional factors other than phos- tion, wind, pollution source, etc., can modify these phorous may be limiting for the algal growth in the trophic states of different sectors between any two lagoon. Mean lagoon TSITN during May, August consecutive months, seasons or years. The TSI can and December, 2011 was found to be 49–50, be a valuable tool for monitoring lagoon eutroph- respectively. The monsoonal input of riverine nutri- ication and also as a simple but effective scien- ents shifted the tragic condition from mesotrophic tific technique for investigations where an objec- to eutrophic nature of the lagoon in terms of TSITN tive standard of trophic state is necessary, but a values. The trophic state index determined with more complete picture of the lagoon trophic state Chl-a presented lower value (in all the sectors) than can be achieved only by applying several indica- those determined with total nitrogen, total phos- tors (including physical, chemical, and biological) phorus, and transparency during monsoon, indicat- simultaneously. ing that non-algal turbidity rather than nitrogen and phosphorus limited phytoplankton growth in the lagoon. On the contrary, during pre-monsoon Acknowledgements (May) and post-monsoon (December), the trophic state index determined with Chl-a was found lower The authors are grateful to the Secretary, than TSITP and TSISD, but relatively higher than MoES, Government of India, and Project-Director, TSITN. 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MS received 30 July 2014; revised 14 January 2015; accepted 26 January 2015