The rising swarms of jellyfish in Indian waters: the environmental drivers, ecological, and socio-economic impacts

Jellyfish are gelatinous organisms that form large aggregations in the ocean in response to hydrographical changes (Purcell 2005; Boero et al. 2008). Jellyfish blooms are divided into ‘true’ or demographic blooms and ‘apparent’ or non-demographic blooms. True blooms occur due to the metagenic life cycle of alteration of generation between sexual and asexual phases. However, apparent blooms are a local increase in abundance, often related to temporary phenomena like fronts and local advection (Graham et al. 2001). Aggregation is an assemblage of interacting medusae without any change in their population size or mortality (Hamner & Dawson 2009). Unlike other marine invertebrates, most jellyfish, by their wide environmental tolerance and a benthic–pelagic alternative mode of life, can cope with eclectic fluctuations in temperature and salinity and even programme their reproduction with seasonal changes in these background variables (Miglietta et al. 2008). Schnedler-Meyer et al. (2018) delineated advective loss to be an important driver of interannual fluctuations in the jellyfish population. They proposed that jellyfish showing a metagenic lifecycle (alteration between benthic polyp stage and pelagic medusa stage) were favoured in comparison to holoplanktic jellyfish. Moreover, Goldstein & Steiner (2020) regarded food availability to be an important ecological driver of jellyfish aggregation along with eutrophication and climate change.

Global warming affects coastal ecosystems by causing an increase in sea water temperature, a rise in sea level, and an increase in the acidity of water (Nazarnia et al. 2020). With a rise in anthropogenic activities in the coastal areas, the coastal ecosystems are getting deteriorated. Water pollution from the discharge of untreated industrial effluents, agricultural wastes, and domestic sewage deteriorates the water quality that affects the marine life and the coastal population. In contrast, jellyfish with high tolerance to environmental vicissitudes can take advantage of such ecological imbalance and proliferate into swarms in warm high saline, turbid, and eutrophicated waters (Purcell 2012). Jellyfish species show synanthropy and are favoured by anthropogenic activities (Richardson et al. 2009). Robinson & Graham (2013) reported higher jellyfish abundance when winter was warmer and wetter, spring sea surface temperature (SST) was lower, and summer SST higher than usual. Climate change leading to increased sea temperature and westward up-current movement were regarded to be the causative agents for the phenological shift in the swarming behaviour of Rhopilema nomadica from the summer to the winter season in the eastern Mediterranean Sea (Edelist et al. 2020). Thus, unusual seasonal changes in temperature or climate change-induced ocean warming accelerate the reproduction rate in jellyfish and help them form swarms. Moreover, ichthyofaunal abundance and diversity are greatly impacted by the introduction of invasive species and constant anthropogenic pressure (Ć osić-Flajsig et al. 2020). Twelve major estuaries worldwide have suffered more than a 30% reduction in fish stock and a 10% decline in the invertebrate stock and even underwent species extinction due to dense jellyfish swarms (Lotze et al. 2006).

The increase in jellyfish abundance has been depicted as a consequence of anthropogenic factors and the hydrodynamics of oceans (Purcell et al. 2007; Baliarsingh et al. 2015). This perception is mostly based on field research and case studies, but according to Condon et al. (2013), there has been no significant indication of an increase in jellyfish globally. Moreover, Pitt et al. (2018) also state that anthropogenic stressors leading to jellyfish swarms have been amplified beyond the evidence provided by the data. To examine whether there has been an actual increase in jellyfish abundance in Indian waters this research was undertaken.

As the United Nations has declared 2021–2030 as the Decade of Ocean Science aimed at restoring degraded ecosystems and sustainably harvesting ocean resources by protecting the life under the water (SDG-14), there is an urgent need to document the causes and processes (physical, chemical, meteorological, and biological) that challenge the healthy functioning of the marine ecosystem. The current review aims at discussing the autecology of swarm-forming jellyfish, highlighting the role of hydrographical, and anthropogenic factors promoting jellyfish swarm; the influence of these swarms on marine ecosystem functioning, human health, and the economy of the nation (through its impact on fisheries, tourism, industries, and other sectors) from Indian waters.

A literature review from authentic search engines like Scopus, Web of Science, Google Scholar, and ScienceDirect was conducted to obtain jellyfish swarm data from Indian waters. The important search terms included ‘jellyfish swarm’, ‘jellyfish bloom’, ‘jellyfish aggregation’, ‘gelatinous zooplankton swarm’, ‘gelatinous zooplankton bloom’, ‘gelatinous zooplankton aggregation’, ‘jellyfish beach stranding’, ‘stinging jellyfish’, and ‘economic impact of jellyfish bloom’. Ocean Data View (ODV) software (version 4) was used to plot jellyfish aggregations and beach stranding locations along the coastal waters of India.

Since the 1980s, the abundance and sightings of jellyfish swarms have gradually increased. It was reported that jellyfish outbreaks in Jakhau, Gujarat increased three times the previous year (CMFRI 2010b). These swarms have impacted marine ecosystems, human health, and the economy of India.

Scyphozoans have a short generation time of two to seventeen months (Pitt & Lucas 2014). Some scyphozoans like Cyanea nozakii prefer high temperature (23–26.8 °C) and high salinity (Lu et al. 2003), while species such as Pelagia noctiluca (8–22 °C) tolerate a wide range of temperature (Morand et al. 1992). Similarly, Crambionella stuhlmanni shows euryhaline nature, by tolerating a high range of salinity (Perissinotto et al. 2013). High temperature and high salinity led P. noctiluca to bloom in the Gulf of Mannar (Ramesh et al. 2021). Recently, Acromitus flagellatus was reported to swarm in the estuarine waters of Sundarbans, Bay of Bengal (Siddique et al. 2022). A. flagellatus was found to swarm in winters but when the water temperature was comparatively higher (about 25 °C) and when salinity ranged between 24 and 29. Thus, the rise in sea water temperature, accompanied by an increase in salinity in recent years, has facilitated an increase in the incidence of swarming jellyfish in Indian waters.

The general feeding ecology of jellyfish suggests that their most common prey is a copepod. Their feeding rate increases with body size and prey density, and their digestion time is influenced by temperature (Purcell 1997). For Chrysaora quinquecirrha, warm waters increase the swimming and digestion rates (Purcell 2009). Nudibranchs, shelled snails, and loggerhead turtles feed on Porpita sp. (Sahu et al. 2020). Larvae of P. noctiluca were investigated to predate on tuna eggs and get predated mostly by Olive Ridley, Leatherback turtles, and fish (Ramesh et al. 2021). Diverse prey preference is shown by scyphozoan species belonging to the family Catostylidae (feeding mostly on mesozooplankton; Pitt et al. 2008), Cyanea sp. (on organisms across different trophic levels including the scyphozoan Aurelia aurita; Hansson 1997. Thus, swarms of Aurelia aurita can usher Cyanea sp. into the system and contribute to their growth and proliferation), Porpita sp. (on phytoplankton, carnivorous calanoid copepods, crab megalopa, and fish; Sahu et al. 2020). Phytoplankton blooms and the introduction of invasive jellyfish species also cause jellyfish to form aggregates thereby impacting trophic interactions and altering plankton community dynamics spatially.

From an environmental point of view, hydrographical, meteorological, and hydrodynamic changes in the ocean facilitate the swarming of jellyfish. Besides, increased anthropogenic activities in recent years have significantly contributed to jellyfish swarms through habitat modification and coastal pollution (Richardson et al. 2009).

Ekman pumping, cold-core eddies, coastal upwelling, and mixed layer entrainment during the Indian Ocean Dipole (IOD) induce phytoplankton blooms (Thushara & Vinayachandran 2020), and since nutrients and biological productivity regulate jellyfish proliferation, the bottom-up process may aid in the development of jellyfish swarms. In the summer months, warmer sea temperatures facilitate jellyfish reproduction and growth, causing an increase in jellyfish aggregations (Baliarsingh et al. 2020). In contrast to this seasonal trend, the scyphozoan, C. stuhlmanni, reaches high abundance during the retreating monsoon (Kumar et al. 2017). Crambionella orsini abundance had shown rhythmicity with the lunar cycle (Nair 1954). Thus, monitoring of swarms, with the creation of a continuous database that accounts the abundance of jellyfish and hydrographical parameters needs to be undertaken to understand the role of hydrography on jellyfish population.

There was only one scientific report from Indian waters on jellyfish aggregation before 1980, between 1980 and 1990, and between 1991 and 2000. The reports increased to four during 2001–2010. There was a soar in jellyfish swarms, accounting for 22 reports between 2010 and 2020. Most jellyfish aggregations have been reported from the Indian coastal states of Kerala and Odisha. The recent years have witnessed a substantial increase in the geospatial spread and frequency of jellyfish swarms. Two jellyfish species (C. stulhmanni and C. quinquecirrha) forming aggregates, were reported during 1981–1990. In the second decade (1991–2000), Chiropsoides buitendijki was also reported to form aggregations. Lobonema smithii and P. porpita were recorded for swarming and beach stranding between 2001 and 2010. The diversity of jellyfish species increased to nine by 2011–2020; among which eight new species recorded blooms, swarms, aggregations, and beach stranding (Table 2). Our study is consistent with the results of Baliarsingh et al. (2020) which state that jellyfish aggregations and beach strandings have become a recurring phenomenon in the coastal waters of India and also revealed environmental factors like winds, tidal fronts, surface currents, dissolved oxygen, water temperature, salinity, and turbidity along with anthropogenic factors like deteriorated water quality, overfishing, habitat change and introduction of exotic species to play a vital role in triggering jellyfish aggregations. Hence, by the increased number of scientific reports, it is evident that jellyfish swarms have increased in recent years. Although, the frequency of jellyfish aggregations has increased in present times, the causative drivers for jellyfish swarms need to be explored further with robust evidence.

Jellyfish swarms can be detrimental to the marine ecosystem, human health, and economy of a country in different ways.

Irrespective of their adverse impacts on the marine ecosystem, jellyfish perform several crucial ecological functions, like facilitating the mixing of oceans (Leshansky & Pismen 2010), and also as a food source for several fish species, sea birds, turtles, and parasitic amphipods (Pauly et al. 2008). During the regression of swarms, the dead jellyfish that sink to the sea bed support several benthic life forms and contribute to benthic nutrient regeneration (Sweetman & Chapman 2011). Amphipods show parasitic association while crabs show commensalism and mutualism with jellyfish (Towanda & Thuesen 2006). Therefore, they are intricately linked to other marine phyla in the complex marine food web. Jellyfish swarms also act as an indicator of monsoons and earthquakes (Mackie 2002). The red tide causing dinoflagellate, Noctiluca scintillans, benefits from jellyfish swarm since jellyfish prey upon the predators of N. scintillans. Thus, jellyfish swarming might promote harmful algal blooms (HABs) in coastal waters, as reported off Gopalpur, on the east coast of India (Baliarsingh et al. 2016).

Jellyfish are opportunistic feeders and predate on all zooplankters, leading to a collapse of the mesozooplankton population and alteration of pelagic trophodynamics (Niermann 2004). Jellyfish affect zooplankton, the primary production (Kideys et al. 2008), and microbial food-web dynamics (Condon et al. 2011). By consuming the herbivorous zooplankton, gelatinous carnivores indirectly benefit the phytoplankton community. They convert an enormous amount of carbon (C), fixed through primary and secondary production, into gelatinous biomass, limiting the transfer of C to higher trophic levels since most consumers do not feed on jellyfish. They release colloidal and jelly-based C-rich-labile dissolved organic matter (DOM), which is rapidly metabolized by heterotrophic bacteria. However, since bacteria use this DOM primarily for respiration rather than biomass build-up, there could be a decrease in bacterial growth by 10–15% (Condon et al. 2011). Thus, jellyfish swarms may change the pathways of nutrients and carbon flow in the food web, affecting biogeochemical cycles, primary production, and pelagic food-web functioning.

Incidents of jellyfish swarms causing considerable economic loss to the fisheries sector, coastal industries, and tourism, have been reported from the coastal waters of India.

Jellyfish adversely affects the fish population of an area by predation (on fish larvae) and competition (by preying on zooplankton). Jellyfish aggregations cause physical damages to the fishing gears by clogging the nets and even capsizing boats, thereby decreasing the number of fishing days (Biju Kumar et al. 2017). India has sprawling aquaculture activity along its vast coastline (7,500 km). Around 152,600 ha (encompassing nine Indian coastal states) are dedicated to shrimp culture yield ∼680,000 metric tonnes of shrimp annually (MPEDA 2020). Aquaculture constructions provide a suitable substratum for the attachment of polyp stages of jellyfish. Jellyfish wreak havoc in aquaculture by fouling the cages, causing fish death by toxic stinging, and creating metabolic stress (Purcell et al. 2013). Jellyfish aggregations that occur seasonally (November–December and April–May) are the leading cause of clogging gillnets in the coastal waters of Jakhau (CMFRI 2010b).

Jellyfish clogs the water intake of the cooling system of nuclear power plants, seabed mining facilities, power and desalination plants, ships, aquaria, and naval facilities, causing a temporary shutdown of the systems (Purcell et al. 2007). Blocking of the cooling system by jellyfish caused a temporary shutdown of Madras Atomic Power Station (MAPS) located at Kalpakkam, southeast coast of India. The shutdown caused a massive loss in revenue of >75,000 US$ per day (Masilamoni et al. 2000). Jellyfish outbreak in the coastal waters of Kalpakkam near MAPS was related to the coastal water currents during southwest and northeast monsoons (Masilamoni et al. 2000).

Jellyfish swarms have been reported to disturb marine research expeditions by interfering with sampling, obtaining fish bycatch, and acoustic data acquisition. Since jellyfish compete with fish for zooplankton and predate on fish egg and larvae, biological data collection during jellyfish swarms might yield inaccurate data regarding an area's productivity potential and plankton dynamics. Jellyfish may also cause painful stings while collecting biological samples (Aznar et al. 2017).

Coastal tourism through recreational activities provides significant revenues to a country. However, incidents of jellyfish aggregations jeopardizing coastal tourism have increased in recent times. The most common jellyfish species associated with stinging are C. nozakii and P. noctiluca (Dong et al. 2010; Baliarsingh et al. 2015). Physalia physalis have been documented from Goa, Mumbai, and Andaman waters, though their aggregations are not yet known (Ramesh et al. 2021). Jellyfish toxins have been known to cause skin erythema, dermal inflammation with blisters, and burning sensation. Sometimes, the stings can trigger necrosis of the skin along with cardiovascular and neurotoxic effects (Mariottini et al. 2008). Every year, jellyfish stings have been reported during post monsoon season in Mumbai coast threatening tourism (Purushottama et al. 2013). Beach stranding of jellyfish are regularly noticed along famous tourist beaches of Puri, Gopalpur, Kochi, Chennai, Rameswaram, Goa and Mumbai (Sahu & Panigrahy 2013; Baliarsingh et al. 2020) which is impacting the tourism sector in the country, severely.

Aside from all the fatal effects of jellyfish swarms on the economy, it has been positively utilized by Indian fishermen who have now started harvesting edible jellyfish (up to 800 tonnes per season) due to their huge demands from China and Southeast Asian markets (CMFRI 2010b). Edible jellyfish like Crambionella annandalei, Catostylus mosaicus, Cephea cephea, C. orsini, Rhopilema esculentum, and Stomolophus meleagris are being harvested and exported to Southeast Asian countries and China to earn foreign exchange (Behera et al. 2020; Ramesh et al. 2021; Sreeram et al. 2021).

This study markedly advances our knowledge about the autecology of swarm forming jellyfish, and discusses the factors that promote jellyfish swarm such as hydrographical, hydrodynamic and meteorological changes in the ocean along with increased anthropogenic activities. The present review emphasizes the impact of jellyfish swarm on the aquatic community, human health, and economy of India. The four-decade data on jellyfish aggregation from Indian waters confirmed that there has been a rise in jellyfish swarming in Indian coastal and estuarine waters. There are prominent evidences for the geospatial spread of swarm incidence along with an increase in the number of swarm events along the coastal waters of India. The diversity of swarm-forming jellyfish has also surged in the recent decade. Moreover, our research points out that oceanographic conditions during the summer monsoon, fall, and early winter create a conducive environment facilitating jellyfish to swarm in Indian waters.

Variability in hydrographical features influences marine organisms in an interconnected way. Jellyfish can be an excellent indicator of climate change and eutrophication-related detrimental impacts on the marine ecosystem (Hay 2006). Furthermore, marine organisms are a useful source of biologically active substances (BAS) that show antimicrobial, antioxidative, mitogenic, and membrane protective activities. Pathogenetic therapy of some disease require high biological activity. BAS can be used for the preparation of liposomal structures for drug delivery for the treatment of cancer, infectious diseases, diabetes, skin lesions, and also in cosmetology industries (Chzhu et al. 2020). BAS extract studies from jellyfish are very meagre from Indian waters and they should be assessed in the future for their pharmacological roles.

From the literature study, it is comprehensible that vast areas of coastal India are still unexplored with respect to jellyfish diversity and ecology. Limited information is available on jellyfish distribution and abundance from the Indian waters, mainly attributable to constraints faced during sampling and preserving delicate gelatinous organisms. The impact of mesoscale processes and environmental shifts on the life history, growth, and reproduction of jellyfish from Indian waters is lacking. Therefore, future work on the impact of hydrography and meteorology on the swarming of jellyfish should be carried out. Attention should given to the identification of swarm forming jellyfish, their impact on the economy, and studies related to jellyfish toxicology. A coastal database on the distribution and systematics of jellyfish from India should be constructed to understand the geospatial spread of jellyfish species. Targeted monitoring programmes should be launched to record the hydrographical and biological changes in regions that showed jellyfish swarms earlier. It will also be pertinent to formulate effective management strategies to deal with devastating swarms.

Aznar et al. (2017) proposed using UAVs (unmanned aerial vehicles) or swarm robotics to detect the swarming of jellyfish. Jellyfish swarms have been monitored through the field, aerial surveys, acoustics, and video profiling across the world's oceans (Nickell et al. 2010; Kim et al. 2015), but such methods have not been deployed effectively in Indian waters. Predictive models can be developed and tested from remote sensing data and provide warnings to humans and coastal industries of the approaching swarm. It will also facilitate site selection for the setting up of new industries and farms. Real-time observation of swarming behaviour will be helpful for the smooth running of power plants. Moreover, investment in public information systems should be carried out to protect the marine environment and periodic evaluation of economic losses caused due to such biological impacts.

The authors (A.S., J.P. and C.R.) are grateful to the Director, Zoological Survey of India, and the Department of Science and Technology-Science and Engineering Research Board (Project: CRG/2020/005212) to provide facilities to carry out this work and to Council of Scientific and Industrial Research for providing Senior Research Fellowship to AS [sanction letter number 09/1181(0003)/2017-EMR-I]. RM gratefully acknowledges the financial and logistics support from the Environment and Life Sciences Research Centre, Kuwait Institute for Scientific Research (KISR), Kuwait.

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.