Abstract
Of the many anthropogenic and climate-related changes occurring in marine biota reported in oceanic ecosystems worldwide, the recent advent of green Noctiluca scintillans (herein after Noctiluca) as the dominant bloom-forming organism represents the most dramatic and extreme. Widespread and intense blooms of Noctiluca have now become a common feature in the Arabian Sea and in many other tropical coastal ecosystems that come under the influence of the Indian monsoons. Noctiluca is a mixotroph, and even among this subset of marine organisms, it is considered exceptional because of its permanent, independent, free-swimming endosymbionts that are capable of photosynthesis. Since the endosymbionts are dependent on nutrients, Noctiluca competes with other phytoplankton, and since it feeds on other phytoplankton, it competes with many secondary producers for food. Because Noctiluca is not a preferred food for zooplankton, its emergence at the base of the food chain represents a threat to many countries where coastal marine resources are of great economic and cultural significance. Here we have drawn on previously published information to establish the major ecological drivers of Noctiluca blooms. Although prior research has established a good foundation, more detailed studies are needed to establish the ecophysiological mechanisms that underpin Noctiluca’s ability to grow and persist as massive blooms for several months and at a time when conditions would be considered hostile for maintaining a classic marine phytoplankton community.
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1 Introduction
The earliest documented reports of green Noctiluca blooms date back to the 1950s (Subrahmanyan 1954; Charernphol 1958), and recent observations in many parts of the world have made it abundantly clear that these blooms are expanding rapidly in terms of their intensity and their longevity, posing serious challenges for local fisheries and coastal activities. What is particularly alarming is that Noctiluca blooms have begun to appear offshore and in deeper waters as is the case in the Arabian Sea. Along the coast of Oman, the impacts of Noctiluca are not just ecological but economic. Effects of these blooms are felt far beyond fisheries, to tourism and recreation; aquaculture, oil refineries, ship repair, and a host of other coastal industries, including desalination plants threatening the supply of freshwater to major cities of Oman.
In the offshore Arabian Sea, the emergence of Noctiluca as the dominant wintertime species in place of diatoms is a recent phenomenon. Ever since Noctiluca blooms were first detected in 2000, they have been occurring with predictable regularity and increasing intensity. In the winter of 2017, for instance, the green Noctiluca bloom was one of the most widespread and long-lasting blooms of recent years. It appeared off the coast of Oman in November of 2016, and by February 2017, it spread westward, stretching across the entire Arabian Sea into the coastal waters of Pakistan (Fig. 17.1). For the first time ever, the bloom was found as far south as ~17°N off the coast of Ratnagiri, India. At the peak of its growth, the bloom occupied an area that was roughly three times the size of the state of Texas, USA. Although the bloom disappeared over most of the Arabian Sea by end of April, it persisted along the coasts of Pakistan and Oman even after the commencement of the summer monsoon season in June, causing significant loss of water and air quality, disruption to normal coastal services, and massive losses to fishermen due to fish mortality. Although all coastal regions around the Northern Arabian Sea have been experiencing large Noctiluca blooms, the bloom of 2017 was extraordinary because of the socioeconomic losses that it left in its wake, leading to renewed international interest in the rapidly changing state of the Arabian Sea ecosystem.
Outbreaks of Noctiluca are not exclusive to the Arabian Sea. They have been frequently reported in the coastal waters of many Southeast Asian countries [Harrison et al. 2011; see also Chap. 14, Furuya et al. (2018)], most often in the Manila Bay, Philippines (Furuya et al. 2006a); the upper Gulf of Thailand (Sriwoon et al. 2008; Lirdwitayaprasit et al. 2006); Jakarta and Ambon Bays, Indonesia (Nurdjaman and Yanagi 2002; Sidharta 2013); and the coastal waters of Vietnam (Hai et al. 2010).
Here, we briefly summarize some of the distinct physiological characteristics of Noctiluca, including some common environmental characteristics associated with bloom outbreaks of this organism, in two ecosystems, i.e., the Arabian Sea and the Gulf of Thailand, both of which are monsoonally driven.
2 Physiology of Green Noctiluca: Mixotrophy
Green Noctiluca is a mixotroph (Stoecker et al. 2017). It acquires its colour from the hundreds of green, free-swimming symbionts Protoeuglena noctilucae belonging to the class Pedinophyceae (Wang et al. 2016) living within its central symbiosome (Fig. 17.2a). It can sustain itself through carbon (C) fixation by its endosymbionts and by ingestion of exogenous prey (Gomes et al. 2014; Furuya et al. 2006a, b). This dual mechanism of obtaining energy presents Noctiluca with several advantages, the most significant being that it affords it the ability to out compete both its prey and predators allowing it to grow as thick green blooms (Fig. 17.2b). This mixotrophic behaviour of green Noctiluca makes it very different from the more extensively studied red Noctiluca found in temperate coastal waters which is devoid of endosymbionts and exclusively heterotrophic (Harrison et al. 2011).
In the Arabian Sea, surface populations of Noctiluca typically contain large quantities of diatoms in their food vacuoles (Fig. 17.2c; Gomes et al. 2014). However, endosymbiont photosynthetic rates are very low because the typical wintertime incident irradiances of 1500–1800 μE m−2 s−1 are far in excess of the ~200 μE m−2 s−1 at which light becomes photo-inhibiting for the endosymbionts (Goes and Gomes 2016). In contrast, subsurface populations of Noctiluca are generally devoid of ingested diatoms, and endosymbiont photosynthetic rates are unusually high. Despite these stark differences, growth rates of surface and subsurface populations are comparable, suggesting that actively growing cells of Noctiluca have a remarkable capacity to transition to a greater dependence on heterotrophy either when conditions for photosynthesis are not favourable to its endosymbionts or when an external source of food is available to the host cells.
In controlled feeding experiments, Noctiluca exhibited preferential feeding tendencies, growing best when the external food source was a dinoflagellate, followed by single-celled diatoms (Mile et al. 2017). Growth rates of Noctiluca were much slower when the only available extraneous food was a chain-forming diatom and slowest when no food was available. Additional experiments showed that Noctiluca grew best in the presence of an extraneous source of food and when incident irradiance light conditions were optimal (~200 μmol m−2 s−1, 12L:12D) (Mile et al. 2017). Under light-limiting conditions (30 μmol m−2 s−1), even when an external source of food was available, growth of Noctiluca was almost negligible, suggesting co-dependency on heterotrophy and autotrophy for growth.
Grazing experiments with Noctiluca as the sole food source revealed that it is not a preferred food for most micro- and meso-zooplankton (Gomes et al. 2014). Instead, it was largely preyed upon by salps (Fig. 17.2d) and jellyfish, indicative of a shorter food chain. These observations are consistent with the idea that in mixotroph-dominated systems, the food chain is much shorter and the trophic structure fundamentally different from the traditional planktonic food web [Mitra et al. 2014; see also Chap. 7, Flynn et al. (2018)].
Noctiluca’s dependence on inorganic nutrients and its ability to graze on other phytoplankton implies that it competes for resources with both its prey and predators. As with most mixotrophs, the emergence of Noctiluca represents a challenge for ecosystem modelling studies because of the complexity of its behaviour [Stickney et al. 2000; Flynn and Mitra 2009; see also Chap. 7, Flynn et al. (2018)].
3 Physiology of Noctiluca: Nitrogen Sources
Despite evidence that Noctiluca blooms are expanding their spatial and temporal range, and becoming more pervasive and intense worldwide, mechanisms that trigger these blooms are still unclear. Global distribution maps of green Noctiluca (Harrison et al. 2011) afford us some potential clues and insights about conditions that promote the growth of this organism to bloom proportions. Based on these maps, it is apparent that most, if not all, countries that are being impacted by green Noctiluca blooms come under the influence of the Indian monsoon system. Furthermore, these blooms typically occur in regions that experience significant influxes of nutrients due to upward shoaling of nutrient-rich subsurface waters and/or land runoff (Hai et al. 2010; Sriwoon et al. 2008; Buranapratheprat et al. 2008, 2009; Gomes et al. 2014; Swaney et al. 2015). With the exception of Oman, all these countries experiencing Noctiluca blooms are predominantly agricultural economies and have a long history of use of synthetic fertilizers, which have been implicated as the predominant cause for the proliferation of harmful algal blooms (HABs) other than Noctiluca in the coastal waters of many countries (Glibert et al. 2006). Although there is strong evidence in support of the idea that many HABs are related to fertilizer use and excessive nitrogenous (N) nutrient loading into coastal ecosystems [see also Chaps. 4, 12, Glibert et al. (2018a, b)], linkages between green Noctiluca blooms and N nutrient loading at present seem at best tenuous, particularly because Oman, a country which presently experiences the worst outbreaks of Noctiluca blooms, has no long history of N fertilizer use, and blooms are most intense and extensive during winter, a period when land runoff is low. In the case of blooms off the coast of Oman, it seems mostly likely that the N-nutrient-rich source waters for Noctiluca blooms are from depth. In winter, cyclonic eddies that typically begin to populate the coast of Oman around the beginning of the winter monsoon season have been implicated in bringing subsurface nutrient-rich waters into the euphotic zone and growth of Noctiluca blooms (Gomes et al. 2009, 2014).
On account of the uncertainty as to the primary N-nutrient driver for Noctiluca blooms, we compared its growth rates in the presence of NO3−, NH4+, and urea under controlled experimental conditions. The results revealed that urea, a common ingredient in commercially available fertilizers, is the most preferred N source for Noctiluca (Tan et al. 2016). Cells of Noctiluca grown in seawater enriched with urea were also the largest in size (>1000 μm), had the highest content of endosymbionts, and exhibited the highest levels of photosynthetic competency as compared to other N nutrients tested. Although Noctiluca grew well in seawater enriched with NH4+, the cells were much smaller, and endosymbiont content much lower as compared to those grown with urea. Inorganic NO3− appeared to be the least preferred N source of the three N-nutrient sources, and the cells were by far the smallest and had the lowest biomass of endosymbionts (Fig. 17.3a–c).
In separate experiments, it was observed that when extraneous N nutrients were low, Noctiluca was still capable of accumulating a large quantity of N nutrients, particularly NH4+, when grown in the presence of an extraneous phytoplankton prey (Mile et al. 2017).
4 Comparative Bloom Regions
Although Noctiluca blooms occur typically in regions with significant influx of N nutrients, field data as well as onboard experiments suggest that bloom outbreaks typically occur when the upwelled waters are hypoxic, as hypoxia is especially conducive for photosynthesis by Noctiluca’s population of endosymbionts. In an earlier investigation, which was based on microscopic data on phytoplankton from a sequence of cruises, Gomes et al. (2008) were able to show that Noctiluca blooms were often preceded by diatom blooms which were invariably short-lived presumably due to rapid grazing by Noctiluca.
In the Gulf of Thailand, Noctiluca co-occurs with the dinoflagellate Ceratium furca (Lirdwitayaprasit et al. 2006; Sriwoon et al. 2008). The presence of C. furca within the food vacuoles of Noctiluca provides concrete evidence that this organism serves as a source of food and that its presence could enhance Noctiluca bloom formation. For a while, Noctiluca blooms in the upper Gulf of Thailand were looked upon favourably, because of the belief that their ability to graze on other phytoplankton, kept toxin-forming HABs in check, especially in an environment that experiences excessive anthropogenic N loading. With Noctiluca blooms becoming more intense, this perception is slowly changing, because the increased frequency of Noctiluca bloom events and their increasing intensity are posing serious threats to fisheries, tourism, and a host of other coastal industries on which these coastal communities depend.
The predictable regularity with which Noctiluca blooms occur in the Arabian Sea and the upper Gulf of Thailand and commonalities in their ocean circulation processes resulting from seasonally reversing monsoonal winds allow us to examine these blooms in the context of regional hydrographic conditions that develop seasonally at both these locations. Both the Arabian Sea and the Gulf of Thailand are semi-enclosed systems that receive considerable amounts of freshwater during the two monsoon seasons. Circulation is anticyclonic during the summer monsoon and cyclonic during the winter monsoon (Fig. 17.4a–d).
In the Arabian Sea, massive basin-wide Noctiluca blooms are a winter monsoon phenomenon, facilitated in large measure by the uplift of cold, nutrient-rich hypoxic waters from depth to the surface by large, long-lived cyclonic mesoscale eddies (Gomes et al. 2009). Noctiluca blooms have also been recorded during the summer monsoon, along the west coasts of India and Pakistan, but rather sporadically especially during periods when coastal upwelling is strong and there is significant intrusion of hypoxic waters onto the continental shelf (Devassy and Sreekumaran Nair 1987). In recent years, summertime Noctiluca blooms have become more frequent in coastal embayments along the coasts of Pakistan and Oman, both of which experience upsloping of hypoxic waters due to wind-driven upwelling (Goes et al. 2005; Munir et al. 2013). These embayments are sheltered from strong monsoonal winds and are much calmer (Al-Azri et al. 2007; Al-Hashmi et al. 2015) as compared to more wind-exposed regions along the coast and offshore, where mixing is stronger and possibly a deterrent to Noctiluca blooms. In the upper Gulf of Thailand, the data of Sriwoon et al. (2008) also suggest that Noctiluca blooms survive best in waters that are highly stratified and calm. Active mixing within the water column in all likelihood provides an explanation as to why Noctiluca blooms are not found offshore during the summer monsoon despite significant influx of nutrient-rich and hypoxic waters into the euphotic column. During winter monsoon, winds coming off the nutrient-rich Indian subcontinent (e.g., Swaney et al. 2015) are comparatively weaker and the water column more stratified which creates ideal conditions for Noctiluca to grow to bloom proportions.
The upper Gulf of Thailand is much smaller in size (100 km2) and is extremely shallow (max. depth 25 m, avg. depth ~15 m) as compared to the Arabian Sea which occupies an area of 3.86 × 106 km2 and is much deeper (max. depth ~4500 m, avg. depth ~2730 m). Four rivers empty into the upper Gulf of Thailand, and because of the disproportionate amount of freshwater that it receives relative to its size, its waters are more estuarine and more stratified than the oceanic waters of the Arabian Sea for most part of the year. This may be the reason why Noctiluca blooms occur twice a year in the upper Gulf of Thailand when there is a significant influx of N nutrients either due to land runoff or due to coastal upwelling. In all likelihood, Noctiluca blooms in the upper Gulf of Thailand are initiated during the summer upwelling season and in the western half of the Gulf, where there is up-shoaling of subsurface hypoxic nutrient-rich waters. However, because of the prevailing direction of flow of the currents, which is clockwise along the northern coastline, Noctiluca blooms accumulate downstream in the eastern half of the Gulf, where they benefit from a huge influx of N nutrients from land runoff during the rainy season (Fig. 17.4c, d). When the currents reverse their direction and become anticlockwise during the winter monsoon, Noctiluca begins to accumulate in the western half of the upper Gulf of Thailand. Growth at this time of the year is also sustained by excess nutrients and the presence of prey phytoplankton throughout the water column.
Although there is no indication of a systematic rise in anthropogenic N loading in the upper Gulf of Thailand (Wiriwutikorn 1996), the increased frequency of super-intense blooms of Noctiluca witnessed in recent years has been ascribed to excessive N-nutrient influxes from agricultural lands, urban waste water treatment plants, as well as shrimp farms located along the coast (Cheevaporn and Menasveta 2003). Although Noctiluca are nontoxic, thick blooms in the upper Gulf of Thailand often exacerbate oxygen loss and also cause massive accumulation of NH4+ in water column, both of which have been blamed for massive fish kills that follow Noctiluca blooms (Wattayakorn 2006).
5 Conclusions
The emergence of Noctiluca as the dominant player in the planktonic food web, and its portended disruptive impacts on the food web, demands a more systematic understanding of this organism’s ecology, biology, growth, and grazing vis-à-vis its reliance on photosynthesis by its endosymbionts. What lends special urgency to this situation is the fact that many of the countries being impacted by Noctiluca blooms have large coastal populations that are dependent on fisheries and several other coastal industries for their livelihoods. Although prior research has provided us with important clues as to what likely triggers the growth of this mixotrophic organism, more detailed ecological studies are urgently needed to address the recent and rapid advent of this organism at the base of the food chain and its implications for the food web and biogeochemical cycles of regions that were once dominated by autotrophs. This ecophysiological information would also be essential to build a holistic perspective of how complex phytoplankton communities evolve in response to human activities and climate-induced changes. Further international collaboration on the ecology, oceanography, and socioeconomics of HABs, as emphasized in the new global HAB Programme, GlobalHAB [see Chap. 22, Berdalet et al. (2018)], will help to advance our understanding and management of these large Noctiluca blooms.
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Acknowledgments
This work is partially supported by grants NNX13AI29A and NNX17AG66G from the National Aeronautical and Space Agency, USA, and grants from the Gordon and Betty Moore Foundation and the Sultan Qaboos Cultural Center, USA, to J.I. Goes and H.do R. Gomes. Al-Hashimi is supported by Sultan Qaboos University and the Ministry of Agriculture and Fisheries Wealth, Sultanate of Oman, and A. Buranapratheprat is supported by the National Research Council of Thailand, Thailand, and the Japan International Cooperation Agency, Japan.
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Goes, J.I., Gomes, H.d.R., Al-Hashimi, K., Buranapratheprat, A. (2018). Ecological Drivers of Green Noctiluca Blooms in Two Monsoonal-Driven Ecosystems. In: Glibert, P., Berdalet, E., Burford, M., Pitcher, G., Zhou, M. (eds) Global Ecology and Oceanography of Harmful Algal Blooms . Ecological Studies, vol 232. Springer, Cham. https://doi.org/10.1007/978-3-319-70069-4_17
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