Symbiont bearing foraminifera from inner shelf area of Great Nicobar Island, Andaman Sea: Coral retrieval

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1 Indian Journal of Geo Marine Sciences Vol. 47 (03), March 2018, pp Symbiont bearing foraminifera from inner shelf area of Great Nicobar Island, Andaman Sea: Coral retrieval Sachin Kumar Tripathi Marine and Coastal Survey Division, Geological Survey of India, Kolkata, , India *[ Received 24 April 2015 ; revised 13 June 2016 Present study is an attempt to use algal symbiont bearing foraminifera as tool to monitor the coral ecology. Inner shelf area of Great Nicobar Islands have maximum abundance of symbiont bearing foraminifera, mainly Amphistegina lessonii, calcarina hispida, Baculogypsinoides spinosus, Heterostegina depressa, Planoperculina heterosteginoides, Operculina ammonoides, Cycloclypeus carpenteri, Planostegina operculinoides, Discorbis sp., and Sorites sp. Dominance of these different genera in the samples depicts congenial environment for reef ecology. Present study from inner shelf area shows maximum diversity of corals and symbiont bearing foraminifera, implies faunal retrieval and congenial environment for coral reefs. [Keywords: symbiont bearing foraminifera, ecology, coral reef]. Introduction Hallock 1 suggested a mathematical model (Foraminifera Index, FI) for coral reefs worldwide, which includes study of algal symbiont foraminifers, opportunistic taxa group and other smaller benthonic foraminifers. This model is mainly based on benthic foraminiferal assemblage along with planktonic foraminifer s data to quantify the suitability of an environment for prolific growth of algal endosymbionts (zooxanthellate corals) and larger benthic foraminifera 2. These larger benthic foraminifera have endosymbionts to facilitate calcification and food production, in same way like zooxanthallae is useful for corals, 2, 3. Therefore, the abundance of symbiont bearing foraminifera is coexisting parallel to coral abundance. As their abundance and occurrences have been reported by different authors in different parts of the world i.e. western Atlantic region, specifically Florida 4, Puerto Rico and Low Isles Reef, reef environments in Australia 2,3,5,6,7, Brazil 8, Akajima, Okiawa, Japan 9. In India these assemblages are recorded from east and west coast. Ragothaman and Kumar 10 reported from east coast and Siebold & Siebold 11, Setty 12, Setty and Nigam 13 reported from Cochin and Karwar. Saraswati 14 reported the occurrence of these symbiont foraminifera from Lakshadweep. Present study consist the evidence of coral retrieval by virtue of occurrence of symbiont bearing foraminifera in the study area. Materials and Methods The Great Nicobar Island is a part of complex tectonic setting that lies along subduction zone of the Indian-Australian plate beneath the southeast Asian plate occurs all along the Sunda arc 15,16. In the East, study area is bounded by West Andaman Fault and Sumatran fault system, forming continuity of Sagaing fault system. These tectonic domains are highly active and have major threats over coral colonies in form

Causes severe damage to marine ecosystem and more than 70% of the corals were died 21 due to tilting and submergence.

2 630 INDIAN J. MAR. SCI., VOL. 47, NO. 03, MARCH 2018 of earthquakes and giant tsunami waves, as reported in historic times by Oldham 17, Oritiz and Bilham 18. Recent earthquake of 26 December 2004 considered as a plate-boundary mega-thrust type, which generated a giant tsunami waves on the coastal area of Andaman and Nicobar Islands 19, 20. Causes severe damage to marine ecosystem and more than 70% of the corals were died 21 due to tilting and submergence. A total of four samples (one spade core and three grab samples) have been collected from different geomorphic domains at water depth from 50 to 70 meters (Fig. 1) during the expedition cruise R.V. Samudra Ratnakar, as part of Geological Survey of India's annual field season programme for mapping and generation of sediment sample. During the survey, different variety of red, purple colour of branching, encrusting, spongy and massive living coral along with gastropods and crabs were recovered from the samples, which strengthen the idea to assess the ecology of coral reef through algal symbiont bearing foraminifera. The samples were prepared as detailed by Hallock et al. 6 The representative aliquots of seabed sample were naturally dried and the reference portions of samples were taken for systematic analysis. Only fresh looking specimens were taken for analysis, because these specimens would give the direct information about the present coral ecology. During microscopic study each individual foraminifer s specimens were identified to the specific level. Fig.1- Sample location map of study area, south of Great Nicobar Island, Andaman Sea (after Smith and Sandwell, 1997). Inset map of multibeam, dot line represents the track of Sub Bottom Profile line. Result and Discussion The geomorphology of the survey area is mainly gentle sloping and graban shaped structure noticed in the central part (Fig.1). Sample collected from the shallower part contain mostly coral sand. Based on coral occurrences, Andaman and Nicobar Islands have been classified into five major zones: North Andaman, Middle Andaman, South Andaman, Little Andaman and Nicobar reefs. These reefs are mainly dominated by family Acroporidae, Faviidae, Poritidae, Fungidae and Agariciidae 21. So each separate group of coral colonies comprise mainly characteristic type of ecosystem, which is also noticed in the recovered sample. These samples mainly contain red and purple coloured living massive, branching corals, generally marked by Acropora, Foliose, and Porites corals along with other forms. Moreover samples from the location G-06, G-08 and G-09, contain cobble to very coarse grained sand with different variety of massive, branching and encrusting corals. These samples have higher fragments of calcareous algae, molluscan shells and bio-eroded coral with different size of sea urchins and crabs. However sample SC-07 is relatively finer and marked by coarse grained sand with red color branching, stony coral and echinoderm shell. Besides this no other information was generated, which could easily predict the ecological setup and symbiotic relationship with other micro-organism. So, symbiont bearing foraminifera is used as an important tool to delineate the ecological setup of the survey area. Study of the coarse fraction sample (greater than +63 µm size) is dominated by symbiont bearing group of foraminifera viz. Amphistegina lessonii, Calcarina hispida, Baculogypsinoides spinosus, Heterostegina depressa, Planoperculina heterosteginoides, Operculina ammonoides, Operculina complanata, Cycloclypeus carpenteri, Planostegina operculinoides, Planostegina longisepta, Discorbis sp., Neoconorbina trequemi, Neorotalia sp., and Sorites sp., (Table-1 & Plate no. 1, 2 & 3). Presence of both immature and mature forms of Amphistegina, Baculogypsinoides, Calcarina and Heterostegina in samples shows their evolutionary growth in the same regime. However Amphistegina is represented by A. lessonii, A. bicirculata, A. radiata, A. lobifera and A. papillosa in decreasing order of abundance. Moreover it also noticed that the test of the A. lessonii is covered with the green algae and depicting symbiotic relationship with Calcarina hispida and Baculogypsinoides spinosus. Abundance of A lessonii, A. bicirculata,

3 TRIPATHI: SYMBIONT BEARING FORAMINIFERA FROM INNER SHELF AREA 631 Calcarina hispida and Baculogypsinoides spinosus at 50 to 70m water depth with other symbiont foraminifera indicates water transparency 6, 22. Although the occurrence of Operculina ammonoides and Operculina complanata at various depths near Great Nicobar also pointing towards water transparency, as reported from deeper part of Red Sea to the West Pacific and East Indian Ocean. Whereas, Cycloclypeus carpenteri is relatively deeper water species and is also getting at deeper water depth (60m), justifying by the statement of Fujita and Hallock 23. Amphistegina lessonii, Baculogypsinoides spinosus, Calcarina hispida, Calcarina mayori and Calcarina calcar are representative member of water-depth indicator in coarse sand sediments 22, as their abundance is noticed in coarse sand of Great Nicobar. Moreover Calcarina sp., is characterized by hispid test with several spines 24, 25. In present area opportunistic group taxa is less as compare to the symbiont bearing foraminifera, which is characterized by Elphidium crispum, Elphidium craticulatumm, Pararotalia sp., Brizalina sp., and Bolivina sp. The genera in the other small taxa group are Spiroloculina depressa, Quinqueloculina sp., Triloculina sp., and Miliolinella sp., as well as rare occurrences Table-1: Faunal abundance South of Great Nicobar Island. SPECIES NAME SAMPLE NUMBER SPECIES NAME SAMPLE NUMBER G-6 SC-7 G-8 G-9 G-6 SC-7 G-8 G-9 Amphistegina lessonia A A A A Sorite sp. R C R R Amphistegina radiata A A A A Discorbis sp. R R R R Amphistegina lobifera C C A A Aveolinella sp. R R R R Amphistegina bicirculata A A A A Ammonia sp. R R R R Amphistegina papillosa R R R R Lenticulina sp. R C C C Calcarian hipsida A A A A Textularia sp. R C R C Calcarian sp. A C A C Dentalina sp. R R R R Operculina ammonoides C A C C Ephidium crispum R C R R Operculina complanta R C R R Quenquiloculina sp R C C C Planoperculina heterosteginoides C C C C Siproloculina depressa R C R R Planostegina operculinoides R C R C Bryozoa C C C C Planostegina longisepta R R R R Ostrocoda C C C C Neorotalia sp. R R R R Gastropoda C C C C Neoconorbina Terquem R C R R Lamallebranchia C C C C Cycloclypeus carpenteri C A C C Planktonic foraminifera R C R R Heterostegina depressa C A A A Soft corals R C C C Baculogypsinoides spinosus A C A A A= Abundance (more than 45%) C= Common (30-15%), R= Rare(less than 15%)

Plate-2: SEM image of symbiont foraminifera observed south of Great Nicobar, Andaman Sea; 1) Calcarina hisipida;2) Heterostegina drepressa; 3) Baculogypsinoides spinosus 4) Neoconorbina trequem 5)

Plate-3: Symbiont foraminifera observed south of Great Nicobar, Andaman Sea 1) Amphistegina papillosa; (200µm) 2) Amphistegina radiata; (200µm) 3) Cycloclypeus carpenteri (500µm) 4) Planostegina

4 632 INDIAN J. MAR. SCI., VOL. 47, NO. 03, MARCH 2018 Plate-1: SEM image of symbiont foraminifera observed south of Great Nicobar, Andaman Sea, 1 and 5) Baculogypsinoides spinosus 2) Amphistegina lessonii; 3& 4) Calcarina sp. Plate-2: SEM image of symbiont foraminifera observed south of Great Nicobar, Andaman Sea; 1) Calcarina hisipida;2) Heterostegina drepressa; 3) Baculogypsinoides spinosus 4) Neoconorbina trequem 5) Operculina sp. Plate-3: Symbiont foraminifera observed south of Great Nicobar, Andaman Sea 1) Amphistegina papillosa; (200µm) 2) Amphistegina radiata; (200µm) 3) Cycloclypeus carpenteri (500µm) 4) Planostegina operculinoides (500µm) 5) Planostegina sp., (500µm). of Textularia sp., and Globigerina was noticed. Based on these taxa groups, a mathematical model is used to calculate the Foraminifera Index (FI) for all four samples, reveal FI is greater than 4, representing healthy coral ecology. The distribution pattern of these taxa group is represented in pie diagram (Fig. 2). Planktonic foraminifera are also one of the important factors in the analysis, because as their populations flourish can stress symbiont bearing foraminifera in same way like other smaller benthic taxa. As per the available literature and understanding, these symbiont bearing foraminifera is not recorded before from the present study area (southern part of the Great Nicobar Island) till now, however their occurrences were studied in details by several researchers in different parts of pacific reefs 26, Caribbean reef, Hateruma and Motobu Island, Okinawa, Japan 22,27. On examining the collected samples, it is noticed that sample is full of symbiont bearing foraminifera, having symbiotic relationship with corals, as they are found to be attached to the surface of coral body (Fig.3).

TRIPATHI: SYMBIONT BEARING FORAMINIFERA FROM INNER SHELF AREA 633 ecology is in better condition and environment is very congenial for their growth. Fig.

3- A) Baculogypsionoides adhere on the surface of montipora coral species, B) Acropora species, C) Acropora species (during sampling it was red in color), D) Symbiosis nature of coral.

, 21, he recorded that the coral cover of Great Nicobar Island was declined to 20 % due to direct impact of the giant tsunami waves, but post tsunami study by Saxena et al.

As also witnessed from the collected samples and sub bottom profiler section during present survey, physiography of the sample area is almost flat and the reefs projecting above the sea floor (Fig.4).

and foliose coral (montipora) is a major clue that supports the coral recovery, as evidenced by the present study and recalls the view of Saxena et al., 21. According to Kulkarni et al.

Based symbiont bearing foraminiferal study, it seems that the coral Fig. 4- Sub-bottom profiler image showing coral colony on a rocky sea floor at water depth of 40 m coordinates between 6 0 30.

Conclusion The present study has established a most interesting fact that wherever corals are noticed in the samples, larger foraminifera are found to be in common association indicating a symbiotic

5 TRIPATHI: SYMBIONT BEARING FORAMINIFERA FROM INNER SHELF AREA 633 ecology is in better condition and environment is very congenial for their growth. Fig. 2- Distribution of different foraminifera from each sampling sites of inner shelf area of Great Nicobar Islands. Fig. 3- A) Baculogypsionoides adhere on the surface of montipora coral species, B) Acropora species, C) Acropora species (during sampling it was red in color), D) Symbiosis nature of coral. This observation is supported by the study of Saxena et al., 21, he recorded that the coral cover of Great Nicobar Island was declined to 20 % due to direct impact of the giant tsunami waves, but post tsunami study by Saxena et al., 21 indicate that the inner shelf area of Great Nicobar was flourishing with different variety of corals. As also witnessed from the collected samples and sub bottom profiler section during present survey, physiography of the sample area is almost flat and the reefs projecting above the sea floor (Fig.4). The abundance of algal symbiont foraminifera along with Acropora sp. and foliose coral (montipora) is a major clue that supports the coral recovery, as evidenced by the present study and recalls the view of Saxena et al., 21. According to Kulkarni et al., 28 and Saxena et al., 21, Acropora sp., is an excellent indicator of environmental changes and their recovery is much faster than other relatives. Based symbiont bearing foraminiferal study, it seems that the coral Fig. 4- Sub-bottom profiler image showing coral colony on a rocky sea floor at water depth of 40 m coordinates between N, E and N, E. Conclusion The present study has established a most interesting fact that wherever corals are noticed in the samples, larger foraminifera are found to be in common association indicating a symbiotic relation, hence algal symbiont bearing foraminifera is providing a direct relationship with coral ecology. The coarse grained sediment samples are also one of the witnesses for this fact, in which A. lessonii test found to be covered with the green algae and depicting symbiotic relationship with Calcarina hispida and Baculogypsinoides spinosus. The existence of Amphistegina lessonii, Calcarina hispida, Baculogypsinoides spinosus, Neorotalia sp., Heterostegina depressa, Planoperculina heterosteginoides, Operculina ammonoides, Operculina complanta, Cycloclypeus carpenteri, Planostegina operculinoides, Planostegina longisepta, Discorbis sp., Neoconorbina trequemi and Sorites sp. in the present collection of the samples, pointed towards conjecturing the coral recovery after post tsunami, as also evidenced by earlier workers. In nutshell it may concluded that the abundance and diversity of the symbiont bearing foraminifera provides a direct clue for coral abundance. Acknowledgement The author is grateful to Deputy Director General, M&CSD, GSI, for providing all possible facilities to carry out the work. Sincere thanks to Chief scientist and all cruise participants of SR- 003 who extended their kind help during survey. My special thanks to SEM, Laboratory, GSI, Kolkata, for providing all facilities during study. Author also thankful to Dr. Amitava Lahiri, Director, M&CS, Kolkata; Prof Pamela Hallock Muller, University of South Florida and Prof.

6 634 INDIAN J. MAR. SCI., VOL. 47, NO. 03, MARCH 2018 Johann Hohenegger, University of Vienna for their valuable guidance and encouragement towards identification of the symbiotic relationship. References 1. Hallock, P., Algal symbiosis a mathematical analysis, Mar. Biol., 62 (1981): Schueth, D. J. & Frank, D. T., Reef Foraminifera as Bioindicators of Coral Reef Health: Low Isles Reef, Northern Great Barrier Reef, Australia; J. of Foraminiferal Res., 38 (2008): Hallock, P., Symbiont-bearing foraminifera: harbingers of global change: Micropaleontology, 46 (2000): Williams, D. M., Impacts of Terrestrial Run-off on the Great Barrier Reef World Heritage Area: CRC Reef Research Centre, Townsville, Australia, 2001:pp: Cockey, E. M., Hallock, P., & Lidz, B. H., Decadalscale changes in benthic foraminiferal assemblages off Key Largo, Florida: Coral Reefs, 15 (1996): Hallock, P., Lidz, B. H., Cockey-Burkhard, E. M. & Donnelly, K. B., Foraminifera as bioindicators in coral reef assessment and monitoring, the FORAM Index: Environmental Monitoring and Assessment, 81(2003): Uthicke, S. N., Vogel, J., Doyle, Schmidt, C. & Humphrey, C., Interactive effects of climate change and eutrophication on the dinoflagellate-bearing benthic foraminifer Marginopora vertebralis. Coral Reefs, 31(2012): Barbosa, S. S., Kelaher, B. P. & Byrne, M., Patterns of abundance, growth and size of the tropical intertidal chiton Acanthopleura gemmata. Mollusc. Res., 30 (2010): Saraswati, P. K., Seto, K. & Nomura, R., Oxygen and carbon isotope variation in co existing larger foraminifera from a reef flat at Akajima, Okiawa, Japan, Mar. Micropalentol, 50 (2004): Ragothaman, V. & Kumar, V., Recent foraminifera from off the coast of Rameswaram Palk Bay, Tamil Nadu, Bull. Geol. Min. Met. Soc. India, 52 (1985): Siebold, I. & Siebold, E., Offshore and lagoonal benthic foraminifera near Cochin (southwest India) distribution, transport, ecological aspects, Neues Jahrb, Geol. Palaeontol. Abh., 162 (1981): Setty, M. G. A. P., Recent marine microfauna from the continental margin, west coast of India, J. Sci. Ind. Res., 41(1982): Setty, M. G. A. P. & Nigam, R., Benthic foraminifera as pollution indices in the marine environments of west coast of India, Rev.Ital. Paleontol. Stratigr, 89 (1984): Saraswati, P. K., symbiont-bearing benthic foraminifera of Lakshadweep, Indian J. Mar. Sci. 36 (2007): Curray, J. R., The Sunda Arc: A model for oblique plate convergence, Neth. J. Sea Res., 24(1989): Kamesh Raju, K.A., Three-phase tectonic evolution of the Andaman backarc basin, Curr. Sci., 89 (2005): Oldham, R. D., Note on the earthquake of 31 December 1881, Rec. Geol. Surv. India, 17 (1884): Oritiz, M. & Bilham, R., Source area and rupture parameters of the 31 December 1881 Mw = 7.9 Car Nicobar earthquake estimated from tsunamis recorded in the Bay of Bengal, J. Geophys. Res. 108 (B4) (2003): doi: /2002jb001941, USGS website, 2005, Thakkar, M. G. & Goyal, B., Historic submergence and tsunami destruction of Nancowrie, Kamorta, Katchall and Trinket Islands of Nicobar district: Consequences of 26 December 2004 Sumatra Andaman earthquake Curr. Sci, 90 (2006): Saxena, A., Rajan, R. & Choudhury, S. S., Status of Coral Reefs in Post-Tsunami Period in Andaman & Nicobar Islands'' Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, Florida, 7-11 Session No. 18 (2008): Hohenegger, J., Large Foraminifera - Greenhouse constructions and gardeners in the oceanic microcosm. The Kagoshima University Museum, Kagoshima, Bulletin No.5, 2011:pp Fujita, K. & Hallock, P. A., Comparison of phytal substrate preferences of Archaias angulatus and Sorites orbiculus in mixed macroalgal-seagrass beds in Florida Bay, J. Foraminiferal. Res. 29 (1999): Jell, J. S., Maxwell, W. H. G. & Mckellar, R. G., The significance of the larger foraminifera in the Heron Island Reef sediments, J. Palaeo., 39 (1965): Lobegeier, M.K., Benthic foraminifera of the family Calcarinidae from Green Island Reef, Great Barrier Reef province, J. Foraminiferal Res., 32 (2002): Hohenegger, J., The importance of symbiont-bearing benthic foraminifera for West Pacific carbonate beach environments, Mar. Micropaleontol, 61(2006): Saraswati, P. K., Shimoike, K., Iwao, K. & Mitra, A., Distribution of larger foraminifera in the reef sediments of Akajima, Okinawa, Japan, J. Geol. Soc. India, 61 (2003): Kulkarni, S. & Saxena, A., The Conservation Status of Coral Reefs of Andaman & Nicobar Islands, published in Coral Reef Degradation in Indian Ocean- Status Report, 2002 by CORDIO, University of Kalmar, Sweden, 2002.

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