Abstract

The study investigates the relationship between the bottom water variables and temporal distribution of benthic foraminifera in the southern part of the Gulf of Mannar. For the study, a systematic collection of sediment and bottom water samples have been made along four traverses from off the coast of Theresapuram, Sippikulam, Mookaiyur and Valinokkam. The samples were collected from 7 stations each, along the 4 traverses and thus the total amounted to 28, ranging in depth from 0.8 to 15.0 metres. The collections were carried out once in four months starting from October 2016 to April 2017, representing the three seasons viz. October (pre-monsoon), January (post-monsoon/winter) and April (summer) and thus the collection amounted to a total of 84 samples. Faunal analysis led to the recognition of 124 foraminiferal species belonging to 59 genera, 39 families, and 21 super families of 5 suborders. The population size both as living and total (living + dead) in each of the stations during different seasons revealed that the maximum living population size was found in stations between 3 and 5 during all the collections and the living population was maximum in summer (April) and was minimum during monsoon (October). Among the 124 foraminiferal species, the following species were considered widespread and abundantly occurring viz. Ammonia beccarii, A. tepida, Asterotalia inflata, Elphidium advenum, Noninoides boueanum and Quinqueloculina seminulum. Various bottom water parameters of all the samples have been estimated and correlated with foraminiferal population. Higher temperature, salinity, pH and dissolved oxygen content noticed during April favoured higher reproduction and abundance of foraminiferal population.

1. Introduction

Benthic foraminifera are recognized as exceptional bio-indicators because of their (1) short life cycles; (2) preservation in marine sediments; (3) diversity and abundance; (4) sensitivity to rapidly changing environmental conditions and (5) easy collection with minimal impact to the environment. In addition, benthic foraminifera are ideal organisms for the studies of marine biogeography and biodiversity ¹. Due to their ability to capture both long term and short term environmental change, application of benthic foraminifera as bio indicators in tropical coral reef environments is a subject of growing interest ². Benthic foraminifers are the most diverse taxa, shelled protozoa in marine environment ^{3, 4}. The distribution pattern of foraminifera is mainly controlled by the overall effect of various environment factors ⁵. The various species of benthic foraminifera prefer various environmental conditions for higher reproduction ⁶. Foraminifera are strongly affected by changes in physical and chemical ecological parameters which may result in growth limitation and reproductive failure ⁷. The main controlling factors which determine the foraminiferal abundance and types include temperature, salinity, pH, dissolved oxygen and nature of substrate ^{8, 9, 10, 11, 12, 13}.

The study of foraminifera and its sensitiveness towards the environmental modification has been recognized as one of the important tool to identify coastal pollution and degradation levels in the coastal zone ¹⁴. The main objective of the present work is to observe the influence of bottom water variables on temporal distribution of benthic foraminifera.

2. Study Area

The study area is located in the southeast coast of India and extends from off coast of Theresapuram in the south to Valinokkam in the north, confining to the southern part of Gulf of Mannar. It is geographically situated between 78° 09' E - 78° 30' E and 8° 49' N - 9° 05' N, forming a part of Geological Survey of India Toposheets, numbering 58 K/3, 4 and 58 O/3, 4 (Figure 1). The tropical climate prevails throughout the year and the monthly average annual temperature varies from 27°C to 33°C with the maximum in April/May and minimum in January. The humidity is maximum during the month of November with an average of 80% and is minimum during the month of June with an average of 59%. This area comes under the spell of both Southwest monsoon (June to September) and Northeast monsoon (October to December). Northeast monsoon contributes about 50-60 percent of mean annual rainfall which varies from 541.8 - 825.6 mm ^{15, 16}.

3. Materials and Methods

For the present study, the bottom water and sediment samples were collected from 28 stations ranging in depths from 0.8 m to 15 m. The sediment samples were collected for three different seasons representing October 2016 (Monsoon), January 2017 (winter) and April 2017 (summer). The sediment samples were collected from 7 stations each, in all the four transects from off the coast of Theresapuram, Sippikulam, Mookaiyur and Valinokkam. Thus the collection amounted to a total of 84 samples. All the sediment samples were collected by taking necessary precautions, making use of Petersen grab. At each station, samples of water from the sediment water interface were collected using a Nansen reversible water sampler and temperature of each sample was noted using built in thermometer. Dissolved oxygen content of each sample was also observed by using portable dissolved oxygen analyser. The pH values were measured using pH meter and the salinity was detected using salino-meter after making necessary precautions in sampling and standardisation. A unit volume of 100 ml wet sediment taken from the top layer was preserved immediately in a 10 % neutralized formaldehyde solution for the study of living Foraminifera.

For identifying living foraminifera ¹⁷ staining technique with rose Bengal ¹⁸ have been used. Foraminiferal tests were then separated from the residue by floatation method using carbon tetrachloride ¹⁹. Foraminifera were recognized at the species level, following the clasification of Loeblich, A. R. Jr. and Tappan, H. ²⁰. After the identification of the species, the specimens belonging to different species were picked, counted and mounted on foraminiferal slides with help of a stereo-binocular microscope. A series of Scanning Electron Microscope photomicrographs were taken to illustrate the various views of the foraminiferal taxa.

4. Results and Discussion

The benthic foraminifera are valuable biological indicators of environmental change, particularly with respect to sea level ²¹ and water quality ^{22, 23}. The utility of benthic foraminifera as bio indicator is largely due to their high taxonomic diversity and abundance ²⁴. According to Kumar V. et al., ²⁵ the variation of foraminiferal assemblages and species distribution in an area mainly depends on spatial and temporal variation in substrate and bottom water characteristics. Alve, E.et al. ²⁶ gave a detailed review about the benthic foraminiferal response to estuarine pollution. According to Lee Y.G. et al. ²⁷ dissolution of foraminiferal tests was caused by low pH due to the decrease in salinity which was the resultant of influx of fresh water during rainy season. The Lei Yet al., ²⁸ noted that abundance of foraminiferal species and their population were positively correlated to the salinity in the intertidal zone of the Yellow sea in China.

The foraminiferal studies from the sediments collected from the present study area led to the recognition of 124 foraminiferal species belonging to 59 genera, 39 families, and 21 super families of the suborders Textulariina, Spirillina, Miliolina, Lagenina and Rotaliina (Table 1). Of all the species identified, 53 were calcareous perforate (Sub order Rotaliina) 41 were calcareous porcelaneous imperforate (Sub order Miliolina), 18 were arenaceous agglutinated (Sub order Textularina), 11 were calcareous hyaline forms (Sub order Lagenina) and 1 was calcareous imperforated hyaline (Sub order Spirillinina). Among these 124 living species, 6 species were found as abundant and wide spread in the present study area viz., Ammonia beccarii, A. tepida, Asterotalia inflata, Elphidium advenum, Noninoides boueanum and Quinqueloculina seminulum. Least represented species in the study area include Siphonina pulchera, Monalysidium politum, Quinqueloculina echinata and Quinqueloculina sulcata.

Living foraminifera were found in all the 84 samples collected from the study area. Among the 124 species, 6 were found to be abundant and found as living in all the samples collected. The distribution of abundant living foraminifera reveals that the sub order Rotaliina was best represented with 5 species (Ammonia beccarii, Ammonia tepida, Asterotalia inflata, Noninoides boueanum and Elphidium advenum) followed by Miliolina with 1 species (Quinqueloculina seminulum). Ammonia beccari was found to be the most abundant living species followed by Quinqueloculina seminulum in the present area. The temporal distribution of abundant species revealed that they have maximum living population in April and minimum in October except for Quinqueloculina seminulum which have minimum living population in January (Figure 2). Siphonina pulchera was found to be the least represented species and found only in one sampling station (station: TP3).

The living population size varied from 32 to 553 specimens per 100 ml of wet sediment. The maximum count of living population was found in Mookaiyur (station: MK 5) in April, and minimum in Valinokkam (station: VN1) in January. The observation on spatial distribution of living foraminifera in the study area revealed that the living foraminifera were found to abundant in stations 3, 4 and 5 which forms the middle segment of the traverse, while the minimum population was found at the near shore stations (stations 1 and 2). Seasonally, the maximum population was observed during summer (April) with 2335 specimens and the minimum with 1934 specimens during monsoon (October) (Figure 3).

The total (living + dead) population size ranged from 105 to1790 specimens per 100 ml of wet sediment, the maximum being at station MK5 in April and minimum at VN1 in January. The study on temporal distribution of total population in the study area revealed that minimum total population size was observed in October (24615) and maximum in April (28883). In general, during all the seasonal collections the total population size was maximum in stations (3, 4 and 5), which were intermediate in the traverse from the shore (Figure 4).

The present study revealed the relationship existing between the foraminiferal population with the bottom water parameters. Seasonal and spatial variation in the values for each parameter have been correlated with the population of foraminifera. Kumar. V, et al., ²⁹ has reported that the foraminiferal population have a positive relationship with the environmental parameters such as temperature, salinity and dissolved oxygen content of bottom water in the Palk Bay area, off Rameswaram. Sivakumar, K., ³⁰ has reported that in the Bay of Bengal, off Chennai, foraminiferal population has a positive correlation with temperature and dissolved oxygen content of bottom water. Gangaimani, T., ³¹ after studying the inner shelf sediments of Gulf of Mannar concluded that the higher temperature and dissolved oxygen content of bottom water are favourable for abundance of foraminiferal population. Alve et al. ³² observed that the spatial and temporal variations in the bottom water characteristics largely determine the variation of foraminiferal assemblages in the Norwegian Skagerrak coast (NE North Sea).

Water depth is an important factor in determining the foraminiferal distribution. The other ecological variables which determines the abundance and diversity of foraminifera are directly associated with changes in depth. According to Kumar et al., ³³ stations near to the shore with less than 1m depth in the Pak bay contain negligible living population. Kumar et al., ^{34, 35} observed that the foraminiferal population shows an increase with respect to depth. Examination of living specimens have linked depth distribution in certain foraminifera (Uvigerina peregrina) to macro fauna -influenced microhabitat such as zones containing biotic structures ^{36, 37}. Denne R. A. et al. ³⁸, from an investigation in the North-western Gulf of Mexico, demonstrated that the depth distribution of benthic foraminifera is strongly correlated with the limits of water masses. The deep sea foraminifera are adapted to limited or no supply of food materials for long periods ³⁹. The response of foraminifera to phytodetritus found to be varied with the depth at which the species were found in ocean. Thus the depth had a great influence on foraminiferal responses to food and play an important role in the changes in diversity and abundance of foraminifera observed during various seasons and in different geographical regions.

In the present study area comprising 28 stations, depth ranges from 0.80 m to 15 m. Stations TP1, SK1, MK1 and VN1 are the nearest stations with depth ranges from 0.8m - 1.2m and stations TP7, SK7, MK7 and VN7 are the farthest with depth ranges from 10.6m - 15m (Figure 5). It is observed that in all seasons the diversity and the population size (living and total) of foraminifera were found to be minimum at nearest stations, because of wave agitation and sandy substrate, and maximum at the stations (3, 4 and 5) which forms the middle segment of the traverse with a depth range from 4.2 m to 11.6 m where the other parameters are congenial for higher reproduction (Figure 5.1 - Figure 5.3).

Temperature is an important parameter that governs the growth and reproduction of foraminifera in coastal areas ^{40, 41}. Kurtarkar et al., ⁴² suggested that the foraminiferal response to temperature variation is species-specific; the shell size of several benthic foraminifera increased with decreasing temperature but a few other benthic foraminifera shows a decrease in shell size with decreasing temperature. The studies of Titelboim et al. ⁴³, about the response of some benthic foraminifera such as Pararotalia calcariformata to extremely warm temperatures (42°C) in a thermally- polluted area revealed that foraminifera can both survive and grow well in warm waters. Laboratory culture experiment on benthic foraminifera (Cymbaloporetta plana) by Kurtarkar et al. Titelboim et al., ⁴⁴ discovered that out of all the specimens fed with the same amount of food, both the growth was more rapid and the reproduction were more frequent in specimens kept in comparatively warmer waters. Based on the study in Gulf of Mannar off Tuticorin, Manivannan, V. et al., ⁴⁵ observed that, temporally, the temperature prevailed during summer season shows a higher population.

In the present study area temperature varies between 27.1°C and 33.2°C. The highest temperature (33.2°C) was observed for SK6, SK7 and MK7 stations in April and the lowest temperature (27.1°C) was recorded for MK1, MK2, MK4 and MK7 stations in October. Seasonal variation in temperature can be positively correlated with both the living and total population. The higher population observed during April (Summer) was positively correlated with the high mean temperature observed during April (Figure 6).

Foraminifers are very sensitive to change in salinity values. This change affects the foraminiferal assemblages by influencing the growth rate of foraminifera and disturbing the preservation conditions. The spatial and temporal change in salinity can influence the abundance and diversity of species. According to Kasilingam, K. et al., ⁴⁶ the general trend in modern shallow water foraminiferal assemblage is increasing spatial diversity with increasing salinity gradients and environmental stability. Kumar V. et al., ⁴⁷ from their study in Uppanar river estuary, confirmed that salinity is the important controlling environmental parameter which governs the spatial distribution of foraminiferal population and the faunal population and diversity decreases with decreasing salinity values. The higher salinities are found to be more favourable for the abundance of living population ^{48, 49, 50}.

In the present study area the average salinity varied from 30.89 ppt in the month of January to 33.08 ppt in the month of April. The salinity did not show any appreciable variation among the stations. Temporally the salinity showed positive correlation with living and total population abundance (Figure 7). The lack of evaporation and mixing of fresh water may be the reasons for low salinity values in January. Seasonally, foraminiferal population had a positive relationship with salinity values.

Dissolved Oxygen has repeatedly been shown to be a limiting factor for benthic foraminifera ⁵¹ and to have an influence on morphology in terms of shell and pore size ⁵². Oxygen minimum zones are subsurface hydrographic zones in which oxygen depletion acts as biological barrier in benthic environments ^{53, 54}. Some low oxygen benthic foraminifera have been observed to migrate to habitats with low oxygen conditions ^{55, 56, 57, 58, 59, 60}. In benthic foraminifera, species with smaller shells, larger pores and higher pore densities have been linked with low oxygen ^{61, 62, 63}. Kumar, et al., ⁶⁴ observed that the dissolved oxygen content did not show notable change between stations of a traverse but temporally, they showed variation and the population of foraminifera is positively correlated with an increase of dissolved oxygen content in the Cauvery river of Poombuhar area.

The distribution of dissolved oxygen overall ranged between 4.4 ml/l-6.4 ml/l in the study site. The observation on values of dissolved Oxygen content in the present study area revealed that they have spatially not much relevance to influence the foraminiferal population. In the present study, the lowest mean value of dissolved oxygen (4.67ml/l) was observed in the month of October and the highest mean value (6.00 ml/l) in the month of April. Temporally foraminiferal population is positively correlated with dissolved oxygen content (Figure 8).

Gangaimani, T., ⁶⁵ observed that the pH values of the bottom waters do not vary much in the different stations during any season and hence a correlation with foraminiferal population cannot be achieved. Kumar et al., ⁶⁶ observed that pH has only very little variation both spatially and temporally and hence a convincing correlation between foraminiferal population and pH values cannot be achieved. The reduced pH is generally associated with low abundance and diversity of foraminifera ⁶⁷.

Spatially the pH values of the bottom water showed a negligible variation in the study area and hence, this may not be a critical environment factor to control the population distribution. Seasonally highest mean value was observed in April (8.09) and a positive relationship with foraminiferal population and abundance was noticed (Figure 9).

5. Statistical Interpretation

In the study area, Pearson correlation (r) linear regression method was used for the statistical interpretation to compare the water parameters determined with the benthic foraminiferal population for all the three seasons such as October, January and April (Table 2 - Table 4). The results of the correlation matrix shows a significant positive correlation between the foraminiferal population with depth, temperature, salinity, pH and D/O. The correlation matrix shows that the foraminiferal population is not only controlled by depth but also due to temperature salinity, pH & D/O of the study area.

6. Summary and Conclusion

For the present study, systematic collection of sediment and bottom water samples, along four traverses, off the coast of Theresapuram, Sippikulam, Mookaiyur and Valinokkam, Gulf of Mannar have been made for three seasons. Faunal analysis led to the recognition of 124 foraminiferal species belonging to 59 genera, 38 families, and 21 super families of 5 suborders. Among the 124 foraminiferal species, the following species were considered to be widespread and abundantly occurring; Ammonia beccarii, A. tepida, Asterotalia inflata, Elphidium advenum, Noninoides boueanum and Quinqueloculina seminulum. The population size both as living and total (living + dead) in each of the stations during different seasons revealed that the maximum living population size was found in stations between 3 and 5 during all the collections and the living population was maximum in summer (April) and was minimum during monsoon (October).

The bottom water characters considered for the present study include depth, temperature, salinity, dissolved oxygen and pH. The diversity and the population size of foraminifera were found to be minimum at nearest stations and maximum at the stations which forms the middle segment of the traverse with a depth range of 4.2 m to 11.6 m. Though this segment was with intermediate depth range of the present study, the other parameters prevailed in these stations were more congenial for higher reproduction and hence the maximum population. Spatially the comparison between bottom water parameters and population was inconvincible. Higher temperature, salinity, dissolved oxygen and pH content noticed during April has favoured higher reproduction and hence abundance of foraminiferal population. Hence temporally, the values of temperature, salinity, dissolved oxygen and pH are positively correlated with foraminiferal population abundance.

The bottom water characters considered for the present study include depth, temperature, salinity, dissolved oxygen and pH. The diversity and the population size of foraminifera were found to be minimum at nearest stations and maximum at the stations which forms the middle segment of the traverse with a depth range of 4.2 m to 11.6 m. Though this segment was with intermediate depth range of the present study, the other parameters prevailed in these stations were more congenial for higher reproduction and hence the maximum population. Spatially the comparison between bottom water parameters and population was inconvincible. Higher temperature, salinity, dissolved oxygen and pH content noticed during April has favoured higher reproduction and hence abundance of foraminiferal population. Hence temporally, the values of temperature, salinity, dissolved oxygen and pH are positively correlated with foraminiferal population abundance. (repetation of last paragraph)

Acknowledgements

The authors are sincerely thankful to the Principal and the Secretary of National College (Autonomous), Tiruchirappalli for providing the lab and infrastructural facilities and their helpful cooperation. The first author is grateful to Rev. Sr. Lillirose (Administrator, B.K College, Amalagiri, Kerala), Rev. Sr. Rose Valiyaparambil (Former Principal, B.K College, Amalagiri, Kerala), Dr. Leena Mathew (Principal, B.K College, Amalagiri, Kerala ) for giving permission to pursue the research.

References