1389-1394The paper attempts to understand the interrelationship between recurring blooms of dinoflagellate, Noctiluca scintillans as well as increasing jellyfish swarms along the coastal waters of eastern Arabian Sea. The grazing of N. scintillans on diatoms in the productive waters with reduced competition pressure due to the opportunistic feeding of jellyfishes on zooplankton are described here. With the development of N. scintillans in the favourable environmental conditions, jellyfishes utilize this dinoflagellate as their food source and thrive in the coastal waters. Hence, trophic interaction between Noctiluca and jellyfishes leading to their proliferation in the coastal waters are delineated

Nandan, S B

Padmakumar, K B

Thomas, L C

NOPR

  Indian Journal of Geo Marine Sciences Vol. 49 (08), August 2020, pp. 1389-1394       Understanding the dietary relationship between extensive Noctiluca bloom outbreaks and Jellyfish swarms along the eastern Arabian Sea  (West coast of India) L C Thomas, S B Nandan & K B Padmakumar* Department of Marine Biology, Microbiology and Biochemistry, School of Marine Sciences, Cochin University of Science and Technology (CUSAT), Kochi-16, Kerala, India *[E-mail: kbpadmakumar@gmail.com] Received 12 November 2018; revised 21 December 2018 The paper attempts to understand the interrelationship between recurring blooms of dinoflagellate, Noctiluca scintillans as well as increasing jellyfish swarms along the coastal waters of eastern Arabian Sea. The grazing of N. scintillans on diatoms in the productive waters with reduced competition pressure due to the opportunistic feeding of jellyfishes on zooplankton are described here. With the development of N. scintillans in the favourable environmental conditions, jellyfishes utilize this dinoflagellate as their food source and thrive in the coastal waters. Hence, trophic interaction between Noctiluca and jellyfishes leading to their proliferation in the coastal waters are delineated.  Introduction Marine ecosystems are experiencing serious threats that affect the diversity, sustainability and services they render to human beings. Eutrophication, expansion of hypoxia, increased ocean acidification, dwindling fisheries, algal blooms and increasing gelatinous zooplankton or jellyfish swarms are some among them. Harmful algal blooms (HABs) along the productive eastern Arabian Sea are increasing in the last few decades1,2. The bloom of Noctiluca scintillans that results in red tide during summer monsoon mainly along the southeastern Arabian Sea and green tide along the northeastern Arabian Sea during winter monsoon is a recurrent phenomenon3-9. These are opportunistic dinoflagellates exhibiting high growth and reproduction rate within a particular season10.  Noctiluca is a heterotrophic dinoflagellate that feeds on small diatoms, dinoflagellates, eggs of copepods and microzooplankton10,11. They are a significant competitor for mesozooplankton that prey upon mixed diatom blooms during summer monsoon associated upwelling7,12,13. The bloom of Noctiluca generally appears in red causing a red tide. Green Noctiluca harbours green photosynthetic prasinophyte endosymbiont Pedinomonas noctilucae which is absent in red Noctiluca and provides nutrition to the dinoflagellate and imparts a green colour to its bloom14,15. However, green Noctiluca is also observed to depend on phagotrophy which is evident from the food vacuoles with diatoms inside these dinoflagellates from the northern Arabian Sea winter blooms16. Owing to its large size and high ammonia concentration N. scintillans are often avoided by smaller zooplankton and fishes, while the  major predators of N. scintillans include gelatinous zooplankton and certain large fishes16,17.  Gelatinous zooplankton mainly jellyfishes are characterised by broad diet spectrum, high reproduction as well as growth rates and experience less predation pressure18. Underpinned with these benefits they can form huge swarms in the pelagic water column under favourable environmental conditions. Climate change, alteration in aquatic habitats, eutrophication and unsustainable fisheries are the primary external factors contributing to their population outburst19,20 and are referred to as synanthropic, benefitting from the environmental alterations caused by anthropogenic influences21,22.  Materials and Methods Frequent blooms of N. scintillans were observed and reported from the eastern Arabian Sea as a part of regular monitoring programs for harmful algal blooms and associated microalgal studies. Samples were collected on the incidence of bloom events along the west coast of India. Taking into account on these studies conducted as well as from various published reports on the blooms caused by N. scintillans1,2,3-9 the INDIAN J GEO-MAR SCI, VOL 49, NO 08, AUGUST 2020   1390 frequency of bloom events were tabulated for a period of seven years (2010-2016). An increase in the pelagic population of gelatinous zooplankton is identified along the west coast of India and a pooled data on the reports of mainly salps and jellyfish outbursts were obtained through various sources for the study period (2010-2016). Monitoring of coastal waters for such outbreaks was done along with various coastal biodiversity initiatives, algae monitoring programmes etc. Information was also gathered from local fisher folks as well as from newspapers and media. A feeding experiment was carried out using jellyfishes with live Noctiluca  cells to identify the preference of this gelatinous zooplankton towards Noctiluca cells. For this, starved jellyfishes and salps were fed with a known number of N. scintillans cells collected from the bloom area in well aerated experimental tanks on-board research vessel. Those jellyfishes, as well as salps devoid  of Noctiluca cells, were identified and selected through morphological examination were used for the feeding experiments.  Results and Discussion In recent decades, there appears an increase in the pelagic populations of jellyfishes as well as their swarm outbreaks across the globe23. This macrozooplankton, with the lack of complex body structures, is adaptable to variations in the habitat and can thrive in a changing environment. The global increase in the gelatinous zooplankton community mainly jellyfishes have reflected in the productive Arabian Sea ecosystem also. The increase in the frequency and intensity of jellyfish swarms along the eastern Arabian Sea at times causes stink to beachgoers. The present study attempts to delineate the interrelationship between the jellyfish swarms and frequent N. scintillans blooms along the eastern Arabian Sea ecosystem. Recently observation on red tides caused by N. scintillans shows a yearly increase along the south-eastern Arabian Sea mainly during the mid-late phase of summer monsoon season (Fig. 1a). Interestingly, moderate to intense swarms of jellyfishes occurs in this region along with or following red tides. Similarly, along the northeastern Arabian Sea, huge swarms of gelatinous zooplankton including salps and jellyfishes are observed along with or following green tide caused by N. scintillans (Fig. 1b). In both cases, a preponderance of N. scintillans abundance was observed before or during the initial stages of jellyfish swarms. This lead to a detailed analysis of Noctiluca blooms as well as jellyfish blooms in the eastern Arabian Sea along with their feeding habits. The red tide caused by heterotrophic dinoflagellate, N. scintillans is commonly observed in the coastal waters of southeastern Arabian Sea, in the form of blooms usually during relaxation periods of upwelling. The frequency of red tide formation by Noctiluca scintillans were tabulated based on the present survey as well as from previously published reports1,2,3-9 and the analysis showed an increasing trend in the frequency of occurrence in the last decade along the southeastern Arabian Sea (Fig. 2). The major hotspots of N. scintillans blooms along the   Fig. 1 — (a) Red tides by Noctiluca scintillans along the southeastern Arabian sea (Inset- microphotograph of red Noctiluca with diatom cells inside the food vacuoles, x 40)  (b) Green tide by N. scintillans along the northeastern Arabian Sea (Inset- microphotograph of green Noctiluca with endosymbiont Pedinomonas noctilucae, x 40) THOMAS et al.: DIETARY RELATIONSHIP OF NOCTILUCA BLOOMS AND JELLYFISH SWARMS   1391 eastern Arabian Sea are shown in Figure 3. Along the Northern Arabian Sea, the blooms of green Noctiluca are also observed to be increasing during the later phases of winter monsoon season16. Attempts were also made to quantify the increasing gelatinous zooplankton blooms along the eastern Arabian Sea. An interpretation of these results clearly showed an increasing trend in the gelatinous zooplankton population as well as the frequency of swarms along the west coast of India (Fig. 2). Along the eastern Arabian Sea regular swarms of gelatinous zooplankton mainly salps and jellyfishes were observed as a part of routine monitoring programmes (Fig. 4). From the analysis, it is clear that both the blooms of N. scintillans and jellyfishes are increasing   Fig. 2 — The frequency of bloom events of N. scintillans and gelatinous zooplankton along eastern Arabian Sea during the period 2010 to 2017   Fig. 4 — Various events of jellyfish swarms and beach stinks along the eastern Arabian Sea: (a) Thiruvananthapuram, (b) Juhu beach Mumbai, (c) Kappil beach Kollam, and (d) Blue bottle jellyfish washed ashore along various beaches of Mumbai. (Photo courtesy-(a) The Hindu daily, (b) Times of India, (c) The Hindu daily, and (d) Indian express)   Fig. 3 — The major hot spots of red and green tides of  N. scintillans and gelatinous zooplankton along the eastern Arabian Sea during the period of 2010 to 2017 INDIAN J GEO-MAR SCI, VOL 49, NO 08, AUGUST 2020   1392 concomitantly (Fig. 2) showing some distinct interrelationships. Moreover, the major areas of both red tides of Noctiluca and jellyfish swarms are observed to be overlapping (Fig. 3). In a classic production pattern and trophic transfer along the west coast of India during the summer monsoon, the upwelling process and nutrient pulses trigger the mixed diatom bloom (MDB) along the southeastern Arabian sea24. The winter mixing along the north eastern Arabian sea also initiates diatom blooms. These mixed diatom blooms (MDB) are fed by mesozooplankton, the secondary producers. The jellyfishes prey upon mesozooplankton thereby reducing their grazing pressure on diatoms which in turn favours N. scintillans that devours on these diatoms as a source of their nutrition25. With the increased abundance of diatoms, N. scintillans multiply and with favourable environmental conditions, mainly relaxation phase of upwelling they develop as blooms. The preponderance of diatom blooms before N. scintillans blooms was  previously reported from eastern Arabian Sea7. Hence, indirectly jellyfishes supported the blooming of N. scintillans by reducing the competitive pressure with mesozooplankton.  A feeding experiment carried out using jellyfishes with live Noctiluca cells showed the preference of this gelatinous zooplankton towards Noctiluca cells. The gelatinous zooplankton were observed to ingest Noctiluca cells and there was a considerable decrease in the number of Noctiluca cells in the experimental tank (Fig. 5). Feeding experiments carried out previously along the northeastern Arabian Sea also observed significant grazing of salps on N. scintillans16. The schematic representation of this relationship is shown in Figure 6. The illustration shows on one side (right) a healthy and sustainable tropical coastal marine ecosystem presenting classical marine food chain in which the nutrient input through monsoonal mixing is used up by the primary producers dominated by diatoms which in turn are consumed by primary consumers mainly zooplankton and passing the energy to higher trophic levels. The other side of the schematic representation (left) shows a disrupted food chain characterising an unsustainable and less diverse ecosystem. Both the jellyfishes as well as  N. scintillans play an important role here.  The increasing jellyfish population feeds on mesozooplankton and provides favourable conditions for N. scintillans to develop into blooms by  feeding on diatoms with less competition. With the plentiful availability of N. scintillans cells, these jellyfishes utilize them as a food source and  flourish that leading to jellyfish swarming. This can   Fig. 5 — (a) Swarming of Salps along the eastern Arabian Sea, (b) Salp colony, and (c) Salps with ingested N. scintillans during feeding experiment THOMAS et al.: DIETARY RELATIONSHIP OF NOCTILUCA BLOOMS AND JELLYFISH SWARMS   1393 also lead to shortening and disruptions of the food chain in these marine ecosystems.  The increasing N. scintillans blooms thus give a decisive stroke towards the population outburst of gelatinous zooplankton in the Arabian Sea. On the other hand, their grazing on other mesozooplankton reduces the competitive pressure to the dinoflagellate N. scintillans for their major prey, diatoms. Hence, it can be assumed that there exists an interrelationship between the swarms of jellyfish and blooms of  N. scintillans both supporting each other in their bloom formation and existence. However, this relation cannot be considered solely responsible for the out burst of jellyfish swarms and Noctiluca blooms but can be one among the robust features favouring these two events along the eastern Arabians Sea. Further studies attempting to understand the biology and ecology, trophic status and swarming behaviour of the jellyfishes as well as in-situ and laboratory-based grazing experiments by both Noctiluca as well jellyfishes can bring more insight into this interrelationship. Such findings can help in managing the threat of increasing red and green tides of Noctiluca as well as jellyfish swarms along the eastern Arabian Sea.  Acknowledgements The first author is thankful to the University Grants Commission (UGC), New Delhi, India for providing Post-Doctoral Fellowship for Women (UGC-PDF-W). This investigation was carried out as a part of the UGC-BSR-Startup-Grant programme.   Conflict of Interest The authors declare that they have no conflict of interest.  Author Contributions  LCT wrote the manuscript with input from KBP. LCT and KBP conducted the field study. LCT conducted taxonomic identifications. KBP and SBN supervised this study and provided research materials.  References 1 D’Silva M S, Anil A C, Naik R K & D’Costa P M,  Algal blooms: a perspective from the coast of India,  Nat Hazards, 63 (2012) 1225–1253.  2 Padmakumar K B, Menon N R & Sanjeevan V N,  Is occurrence of Harmful algal blooms in the EEZ  of India on the rise? Int J Oceanogr, 2012 (2012) 1-7. http://dx.doi.org/10.1155/2012/263946. 3 Naqvi S W A, George M D, Narvekar P V, Jayakumar D A, Shailaja M S, et al., Severe fish mortality associated with 'red tide' observed in the sea off Cochin, Curr Sci, 75 (1998) 543–544. 4 Sahayak S, Jyothibabu R, Jayalakshmi K J, Habeebrehman H, Sabu P, et al., Red tide of Noctiluca miliaris off south of Thiruvananthapuram subsequent to the ‘stench event’ at the southern Kerala coast, Curr Sci, 89 (9) (2005) 1472–1473.   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Understanding the dietary relationship between extensive Noctiluca bloom outbreaks and Jellyfish swarms along the eastern Arabian Sea  (West coast of India)

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Understanding the dietary relationship between extensive Noctiluca bloom outbreaks and Jellyfish swarms along the eastern Arabian Sea (West coast of India)

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