Harmful algal bloom by the dinoflagellate Noctiluca scintillans (Macartney) Kofoid &amp; Swezy severely impacts coral reef fishes in the Gulf of Mannar, Southeast coast of India

doi:10.21203/rs.3.rs-1882617/v1

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Harmful algal bloom by the dinoflagellate Noctiluca scintillans (Macartney) Kofoid & Swezy severely impacts coral reef fishes in the Gulf of Mannar, Southeast coast of India

https://doi.org/10.21203/rs.3.rs-1882617/v1

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Marine fisheries and biodiversity in the Gulf of Mannar, Tamil Nadu, were severely impacted by the blooms of dinoflagellate Noctiluca scintillans, on 10th October 2021. The bloom affected the marine biodiversity in a 15 km² area between Keelarai to Mudal in the Gulf of Mannar, Tamil Nadu, India. Post bloom observations showed mass mortality of a variety of finfish, ornamental fish, bivalves, shellfish, sea anemones, sea slugs, sea cucumbers, sea horses, polychaete worms, and seaweed that washed ashore. Two damselfish species Dascyllus reticulatus and D. trimaculatus were deleteriously affected. The intense N. scintillans bloom killed 0.83 tons of damselfish, equivalent to approximately 9 million fish, and 1.67 tons of commercially important fish valued at US$ 11.5 M.

HABs

Noctiluca scintillans

Chlorophyll-a

Fishes

Gulf of Mannar

In marine ecosystems, phytoplankton is the primary producer of the oceans and supplies the partial primary production worldwide. They are providing the energy for the higher trophic levels in the food chain through organic carbon (Jin Hee et al., 2021; Steinberg and Landry, 2017; Armengol et al., 2019). An abundance of a single dominant species is called an algal bloom; they frequently cause water discolorations (Garrison, 2005). Blooms are rapid events that can be initiated and end within days and spread over hundreds of square kilometers of the ocean surface. Algal blooms can be due to eutrophication, coastal upwelling, anthropogenic activity, and oceanographic changes (Simon and Shanmugam, 2012). Some blooms, so-called harmful algal blooms (HABs) can produce toxic compounds and can be responsible for fish mortality, shellfish poisoning, episodic mortalities of birds, mammals, and other animals including humans with symptoms of skin irritation, lesions, respiratory, digestive tract issues, seizures, memory loss. Severe impacts can result in coastal resources including aquatic flora and benthic fauna (Hallegraeff, 2003; Da - Zhi Wang, 2008; Sellner et al., 2003).

The large dinoflagellate of N. scintillans (Macartney) Kofoid & Swezy consumes phytoplankton, micro- mesozooplankton, and their eggs. They occur in temperate and tropical oceans (Elbrachter and Qi, 1998; Hansen et al., 2004; Harrison et al., 2011). This species is non-toxic, but during the massive occurrence of blooms they can produce phytotoxins, the reason for the mortality of fish and marine invertebrates is thought to be due (Escalera et al., 2007; Kopuz et al., 2014). The water coloration of the blooms can be red or green, red Noctiluca is heterotrophic grazing on microzooplankton while green Noctiluca contains chlorophyll from green symbionts and is mixotrophic (Murugesan et al., 2017; Piontkovski et al., 2021). The occurrence of N. scintillans blooms can be caused by hydrographic and biological factors such as temperature, salinity, chlorophyll-a, and ocean stability, with the density of blooms based on wind, ocean currents, and tidal influences (Umani et al., 2004; Miyaguchi et al., 2006; Mohamed and Mesaad, 2007).

In India, the occurrence of Noctiluca blooms was reported for August to October on the west coast of the Arabian sea. On the east coast, in the Bay of Bengal, it was reported from April to October. In Tamil Nadu, particularly the region of Palk Bay and the Gulf of manner, the blooms occurred in association with fluctuating diatoms abundance (D’Silva et al., 2012). The blooms of N. scintillans might be affecting large-scale fish mortality and other species of marine organisms, and loss of biodiversity directly or indirectly impacts the coastal people’s livelihoods. Recently, reports of harmful algal blooms by Noctiluca scintillans in Indian coastal waters and occurrences worldwide in the past two decades have been claimed to have increased due to eutrophication and climate change (Karunasagar, 2000; Eashwar et al., 2001; Nayar et al., 2001; Dharani et al., 2004; Sahayak et al., 2005; Mohanty et al., 2007; Joseph et al., 2008; Prakash et al., 2008; Sanilkumar et al., 2009; Gopakumar et al., 2009; Padmakumar et al., 2008, 2010; Anantharaman et al., 2010; Madhu et al., 2012; Gomes et al., 2014; Tholkapiyan et al., 2014; Sulochanan et al., 2014; Matondkar et al., 2004, 2012; Peter et al., 2016; Baliarsingh et al., 2016; Vijayalakshmy et al., 2018; Raj et al., 2020; Shunmugaraj et al., 2020). Recently studies have reported that Noctiluca scintillans blooms worldwide via. Southeast coast of Australia (Dela-cruz et al., 2002): Northern Adriatic Sea (Umani et al., 2004); Sagami Bay, Japan (Miyaguchi et al., 2006); Sea of Marmara, Turkey (Turkoglu, 2013); Sea of Marmara, Turkey (Yilmaz et al., 2005); Southern Brazil (Souza Cardoso, 2012); Northern south China sea (Wang et al., 2012); the Red Sea off the coasts Saudi Arabia (Mohamed and Mesaad, 2017); Hong Kong (Zhang et al., 2017); Dubai coastal waters (Murugesan et al., 2017); Matsu archipelago China (Tsai et al., 2018); East China sea (Qi et al., 2019); Seto Inland Sea, Japan (Tada et al., 2004, 2020); Yellow sea and Bohai sea, China (Xue et al., 2020).

Study area

The Gulf of Mannar region is rich in productive habitats such as coral reefs, seagrasses, mangroves, estuaries, rocky shores, and sandy beaches. The diverse nature of ecosystems in the Gulf of Mannar supports a wide variety of 181 species of seaweeds, 15 species of seagrasses, 117 species of corals, 158 species of arthropods, 856 species of mollusks, 1147 species of finfishes, 5 species of sea turtles. The biologically rich areas were recently affected by harmful algal blooms (Gopakumar et al., 2009; Diraviya Raj et al., 2020). Hence, the present study attempts to estimate the occurrence of HABs by Noctiluca scintillans and assess the habitat loss of vertebrate and invertebrate marine organisms from the Gulf of manner, Southeast coast of India, Tamil Nadu India. The incidence of harmful algal blooms occurred on 8th -10th October 2021 from the Gulf of Manner, the Bay of Bengal. During the time of blooms, the surface watercolors were dark green from Pamban to Mundal (15 km²) coastal regions. The blooms were spreading over 15 km² of the Gulf of Manner. Ten stations were occupied to collect the samples on 11th October from different coastal regions along the Gulf of Manner and Fig. 1 shows each station's name and geographical location. To assess the blooms, 1 L of water samples were collected at ≈ 1m depth in wide mouth polypropylene bottles, and with 4% formalin added to preserve the samples (APHA, 1995). Followed by the mass mortality of marine organisms we examined the area by using a 1×1 m quadrats method, with each station with 8 to 10 quadrats placed randomly in five-meter intervals, and each transect parallel to the seashore (Good, 2004; Gevertz, 1995).

The dead specimens of vertebrate and invertebrate organisms were collected in polythene bags and labeled. After that, the water samples and dead specimens were transferred to CAS in Marine Biology Laboratory, Annamalai University, Tamil Nadu, India for further analysis. For the identification of algal blooms, 1 ml of water samples was enumerated on a Sedgwick Rafter by using an Olympus light microscope at a magnification of 40 × (Olympus, Tokyo, Japan), and bloom species were identified by standard manuals (Al-Kandari et al., 2009; Santhanam et al., 1987). The collected dead fish had their length and weight measured and fish were identified based on the FAO identification sheets followed by the FISHBASE database (www.fishbase.org) described by Froese and Pauly (2011). In this study, the time-series of satellite remote sensing, chlorophyll-a concentration, and Sea Surface Temperature (SST) data products of the sea waters of the Moderate Resolution Imaging Spectroradiometer (MODIS, Level-3, 4 km spatial resolution, 2019 to 2021) were used. The Ocean Data Processing System (ODPS) generated these two products from the MODIS sensors onboard the NASA Terra and Aqua platforms acquired from the NASA Ocean Color Web (http://oceancolor.gsfc.nasa.gov) that have been aggregated/projected onto a well-defined spatial grid with mapping data. The tools that were used in this study were a set of computers equipped with image processing software, namely Seadas 7.0 (Windows) and Microsoft Excel. For the visualization of chlorophyll-a distribution, the tool was Ocean Data View software (ODV) 4.0. A one-way analysis of variance (one-way ANOVA) test was performed to assess the abundance of species washed ashore at every station.

This study assessed the impact of N. scintillans HABs and evaluated the biodiversity losses from the ten stations at the Gulf of Mannar (GoM), the Southeast coast of India. The results of surface water temperature (SST) (Fig. 2), Chlorophyll, and wind velocity of the study showed that chlorophyll a' (17.5mg/m^− 3 in 2021) (Fig. 3) and temperature (29.22C°) values were high during the N. scintillans bloom whereas the variation of wind velocity (7.79 m/sec) was low (Fig. 4).

N. scintillans were found in water temperatures of 14.2–24.2°C, and salinities of 28.0–36.5 (Table 1). The temperature increased gradually at Station 1 from an initial 16.2°C in August to a maximum of 22.5°C in February, while salinity fluctuated between 34.6 and 36.5. At Station 4, both temperature and salinity showed greater variation, fluctuating between 14.2 and 24.2°C, and between 28.0 and 36.0, respectively. The chlorophyll concentration in the surface waters at the Port Hacking offshore station, measured within 2 days of the sampling for Noctiluca, was highest in September when concentrations reached 2.9 µg L^− 1 (Table 1). Apart from this, and small increases in December and June, concentrations remained low (< 1 µg L^− 1) throughout the study period.

Table 1

List of marine invertebrates and vertebrates found during the bloom event.
S. No	Species list	S1	S2	S3	S4	S5	S6	S7	S8	S9	S10
1	Abudefduf septemfasciatus	-	+	+	+	+	+	+	+	+	+
2	Amphiprion sebae	-	+	+	+	+	+	+	+	-	-
3	Amphiprion clarkii	-	+	-	-	+	+	+	+	-	-
4	Ambassis nalua	-	+	+	+	+	+	+	-	-	-
5	Arothron caeruleopunctatus	-	+	-	+	+	+	+	-	-	-
6	Arothron hispidus	-	+	-	-	+	+	-	-	-	-
7	Chaetodon collare	-	-	+	+	+	+	-	-	-	-
8	Dascyllus reticulatus	+	+	+	+	+	+	+	+	+	+
9	Dascyllus trimaculatus	+	+	+	+	+	+	+	+	+	+
10	Decapterus russelli	-	+	-	+	+	+	-	-	-	-
11	Diodon holocanthus	+	-	-	+	+	+	-	-	-	+
12	Diodon hystrix	+	-	-	+	+	+	+	+	-	-
13	Epinephelus chlorostigma	-	-	-	-	+	+	+	-	-	+
14	Epinephelus diacanthus	-	-	-	-	+	+	-	-	-	-
15	Epinephelus coioides	-	-	-	+	+	+	-	-	+	+
16	Gazza achlamys	-	-	-	-	+	+	+	-	-	-
17	Gymnothorax favagineus	-	+	+	+	+	+	+	+	+	-
18	Gymnothorax flavimarginatus	-	+	+	+	+	+	+	+	+	-
19	Gymnothorax meleagris	+	+	-	-	+	+	+	-	-	-
20	Gymnothorax monostigma	+	+	-	-	-	+	+	+	-	-
21	Gymnothorax pictus	-	-	-	+	+	+	+	+	+	-
22	Leptoscarus vaigiensis	-	-	-	-	+	+	+	-	-	-
23	Platax orbicularis	-	-	-	-	+	+	-	-	-	-
24	Plectorhinchus schotaf	-	-	-	-	+	+	+	-	-	-
25	Pomacanthus semicirculatus	-	-	-	+	+	+	+	-	-	-
26	Pomadasys argyreus	-	-	-	-	+	+	-	-	-	-
27	Sargocentron rubrum	-	-	+	+	+	+	-	-	-	-
28	Scarus rubroviolaceus	+	+	-	-	+	+	+	-	-	-
29	Scarus russelii	+	+	+	-	+	+	-	-	-	-
30	Siganus canaliculatus	+	+	+	+	+	+	+	+	-	-
31	Siganus javus	+	+	+	+	+	+	+	+	+	-
32	Siganus vermiculatus	-	-	+	+	+	+	+	+	-	+
33	Teraporn jarbua	-	-	-	+	+	+	+	-	+	+
34	T. puta	-	-	+	+	+	+	+	-	-	-
Crustaceans
35	Atergatis integerrimus	-	-	-	-	+	+	+	-	-	-
36	Charybdis natator	-	-	-	+	+	+	+	+	-	-
37	Neocallichirus sp.	-	-	-	-	+	+	-	-	-	-
38	Scylla serrata	-	-	-	-	+	+	-	-	-	-
39	Thranita crenata	-	-	-	+	+	+	+	-	-	-
Cephalopods
40	Sepia sp.	-	-	-	-	-	+	-	-	-	-
Sea Anemone
41	Stichodactyla haddoni	-	-	-	-	+	+	-	-	-	-
Sea Hourse
42	Hippocampus kuda	-	+	+	+	+	+	+	+	-	-
43	Hippocampus kelloggi	-	+	+	+	+	+	+	+	-	-
Sea Cucumber
44	Holothuriya sp	-	-	+	+	+	+	+	+	+	-
Sea hare
45	Dolabella sp	-	-	-	-	+	+	+	-	-	-
Polychaete worms
46	Arenicola sp	-	-	+	+	+	+	-	-	-	-
47	Eurythoe sp	-	-	+	+	+	+	-	-	-	-
Molluscs (Bivalve)
48	Donax cuneatus	+	-	-	+	+	+	+	-	-	-

In Total of 48 marine vertebrates and invertebrate organisms were identified, of which 34 fish (16 families), 5 crustaceans, 2 polychaetes, single species of bivalve, cephalopod, sea anemone, sea hare, and two endangered animals of the sea horse, sea cucumber were reported from the of HABs areas (Table 1). Compared to all stations, 48 vertebrates and invertebrates were recorded at Kilakarai station, and 8 were recorded from Mundal. The fish mortality was assessed at a total of 7.2 tones, among these the lowest 0.037 tonnes was from Valinokkam and the highest 1.1 tonnes from Keelakarai were recorded.

Fish mortalities were determined by the fish weight percentage, including families such as Muraenidae (44%), Pomacentridae (12%), Serranidae (6%), Siganidae (11%), Scaridae (4%), Tetraodontidae (6%) Terapontidae (0.004%), Haemulidae (1%), Diodontidae (9%), Carangidae (2%), Ambassidae (1%), Leiognathidae (0.002%), Chaetodontidae (0.004%), Ephippidae (0.004%), Pomacanthidae (1%) and Holocentridae (0.003%) (Fig. 5). Whereas the mass mortality weight (0.83 tonnes) recorded in the Pomacentridae family was less than three folds compared to the Muraenidae family. However, the maximum number of fish mortality of Pomacentridae family fish viz damselfish species of Dascyllus reticulatus, D. trimaculatus, and other species Adudefduf septemfasciatus, were 0.83 tonnes, which is equivalent to nearly 9 million fish killed in only 3 days and the minimum number of Leiognathidae (162 kg) family fish viz Gazza achlamys occurred due to N. scintillans HABs. High fish mass mortality was recorded at the Kilakarai and Sethukarai stations (Fig. 6). The results of the analysis of variance (ANOVA) showed that there were significant variations (P > 0.5; F > 000) among the total weights estimated between the stations, indicating the severe impact of N. scintillans HABs.

The results from this study revealed mass mortality by 34 fishes at all ten stations. It was divided into commercially important 14 fish species and the remaining 20 fish were non-commercially important (Fig. 7). The maximum commercially important fish were recorded at Kilakarai (4,701 kg) followed by Sethukarai (4,027 kg) and the minimum was recorded at Valinokkam (378 kg) (Fig. 8). In particular, the fish families of Siganidae and Serranidae were affected at all the stations. In the case of non-commercially important fish, the maximum was recorded at Kilakarai (15,986 kg), followed by Sethukarai (12,612 kg), and the minimum was recorded at Mundal (2,125 Kg). The Muraenidae (31,874 kg) fish family was highly affected by N. scintillans HABs. Fishes can suffocate due to the low oxygen level in seawater (Diaz and Rosenberg, 1995). In various parts of the world, the mass mortality of fish has been recorded due to low dissolved oxygen caused by harmful algal blooms. Similarly, the present study also shows that the mass mortality of fishes and invertebrates, particularly damselfish were killed huge number.

The enriched nutrient content (ammonia and phosphate), disposal of ballast water, and short-term hypoxic conditions from the Gulf of Mannar have been suggested as key factors of HABs (Gopakumar et al., 2009; Baliarsingh et al., 2016; Diraviya et al., 2020; Shunmugaraj et al., 2020). Various environmental factors might have contributed to the high cell abundance and persistence of the N. scintillans bloom in the Gulf of Mannar, the Southeast coast of India. Similarly, meteorological factors such as rainfall, wind velocity, and wind direction are also triggering the N. scintillans bloom in coastal waters (Miyaguchi et al., 2006). According to earlier studies, N. scintillans severely impacted the variety of coral reef fishes such as rabbitfish, moray eels, goatfish, parrotfish, damselfish, clownfish, mollusks, and sea snakes from Pudumadam to Periapattinam and Manpdapam group of Islands at Gulf of Mannar region (Gopakumar et al., 2009; Shunmugaraj et al., 2020).

The N. scintillans bloom event washed nearly 14 tons of commercially important fishes at the Gulf of Mannar, the Southeast coast of India (Gopakumar et al., 2009). However quantitative analysis of family-wise mortality rate, and commercially important fish economic value data was not recorded for the Gulf of Mannar region. In the present study, the intense N. scintillans bloom killed an amount of 0.83 tonnes of damselfish, equivalent to approximately 9 million fish in only 3 days (Fig. 9), which is now considered the large mass mortality of damselfish ever caused by an N. scintillans bloom. In addition, N. scintillans bloom killed an amount of 1.67 tonnes of commercially important fish which is equivalent to US$ 11.5 M. The earlier study reported that N. scintillans bloom caused losses of nearly 100 M of shrimp Penaeus orientalis, which is valued at US$ 1M (Chen and Gu, 1993). In addition, Muhammad, (2016) found that the N. scintillans bloom event occurred in the East Bay of Ormara, Pakistan. Due to the extreme density of N. scintillans triggered the reduction of dissolved oxygen in the East Bay region causing mass mortality of commercially important finfish and shellfish i.e. mullets, Chinese pomfrets, Groupers, shrimps, and crabs.

Recently, Diraviya raj et al., (2020) observed that the intense dinoflagellate bloom of N. scintillans occurred in 2019 at GoM, Southeast Coast of India. This bloom created temporary hypoxic conditions (DO below 2 mg L^− 1) which resulted in the fast-growing coral such as Acropora, Montipora, and Pocillopora being severely affected at GoM Southeast Coast of India. Similarly, Fire et al., (2009) reported that the New England coastal waters are highly devastated by toxic producing Alexandrium bloom. The extremely high densities of Alexandrium bloom events produced Saxitoxin, causing mortality on shortnose sturgeon Acipenser brevirostrum in 2009 at Sagadahoc Bay, Maine, USA. In addition, the toxic Alexandrium bloom is considered a major threat to the health of the shortnose sturgeon fish population. The recent study also found that the Pseudo-nitzschia bloom event occurred at Chunnamber backwater of Puducherry, Southeast coast of India. During this event, 1 metric ton of mass mortality of backwater fish is killed (Mishra et al., 2021).

The Chilean coastal zone has severely affected by the Alexandrium catenella bloom in the summer of 2009 and 2016. The exceptional bloom outbreaks spread over the Chilean coast causing economic losses in the Chilean salmon farm industry of over $10 M USD (Mardones et al., 2010). The same coast has been massively impacted by Pseudochattonella cf. verruculosa and A. catenella in 2016. The high density of Pseudochattonella cf. verruculosa and A. catenella bloom event killed 27 million salmon (Salmo Oncorhynchus kisutch and Oncorhynchus mykiss) and trout fishes resulting in 39,000 tons (Montes et al., 2018). Michel et al., (2017) found that the multispecies mass mortality of marine fauna is massively impacted by toxic dinoflagellate Alexandrium tamarense bloom in Belle-Isle and Cabot, Canada. The intense algal bloom contains a mixture of Paralytic shellfish toxins (PST) and it extensively spread all over the St. Lawrence Estuary, as a consequence of this event mass mortality of multispecies such as beluga (Delphimapterus leucas) harbor porpoise (Phocoena phocoena) juvenile fin whale (Balaenoptera physalus) and Seals killed.

Similar predictive strength was found for the temperate fish species rainbow wrasse (Coris julis) off the Azores (Fontes et al., 2016). However, caution is needed when considering environment-recruitment correlations as they seldom hold when extending the original time series (Myers, 1998). Also, remote sensing data only capture the surface manifestation of the bloom and may therefore not necessarily represent a larger part of the water column. Superimposed on these stresses, climate change is already leading to temperature increases in some areas of the earth’s oceans, and warmer waters could affect the occurrence of HABs (Moore et al., 2008; Backer and Moore, 2011; Hallegraeff, 2010; Gowen et al., 2012). Specifically, changes in the frequency, intensity and geographic extent of HABs may occur, but the possible responses are likely to be highly species-specific, given the diverse toxicity, physiology, biology, and ecology of HABs organisms.

The observations of this research study warn us of possible mass mortality due to harmful algal blooms. Thus, the shallow water coral reef fishes will be expected to be affected more frequently by environmental variables such as high temperature, high chlorophyll a', low oxygen, and low wind movement caused by harmful algal blooms. Further studies are needed to understand the mechanisms of coral reef fish mortality due to the harmful algal blooms, impacts on community composition, and the potential for subsequent recovery.

Acknowledgment

The authors are grateful to the authorities of Annamalai University for providing the facilities and the authors are thankful to Dr. V. Bharathidasan for the polychaete identification.

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Harmful algal bloom by the dinoflagellate Noctiluca scintillans (Macartney) Kofoid & Swezy severely impacts coral reef fishes in the Gulf of Mannar, Southeast coast of India

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