Oxygen minimum zone copepods in the Arabian Sea and the Bay of Bengal: Their adaptations and status

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Highlights

  • Presents the copepods in the OMZs of the Arabian Sea (AS) and the Bay of Bengal (BoB).

  • Summarises the oceanography of a thicker OMZ in the AS than in the BoB.

  • Lucicutia grandis is an indicator of the lower boundary of OMZ in the AS.

  • Calanoides carinatus is a diapausing species of OMZ in the AS.

  • A severe lack of information exists on OMZ copepods in the BoB.

Abstract

The Arabian Sea and the Bay of Bengal are cul-de-sacs of the northern Indian Ocean, and they contain more than half of the world's Oxygen Minimum Zones (OMZs). The current study reviews the vast and advancing literature on the oceanographic settings that lead to distinct OMZs in the Arabian Sea and the Bay of Bengal and links them with the copepods thriving there, their status, and likely adaptations. The Arabian Sea has a thicker perennial subsurface OMZ (∼1000 m) than the Bay of Bengal (∼500 m), which is linked to high plankton production via upwelling and winter convection in the former and river influx and mesoscale eddies in the latter. Studies world over show that OMZs adversely affect the zooplankton community as their core always sustains reduced zooplankton biomass. Exclusive studies on copepods in the perennial OMZ in the northern Indian Ocean have been limited to the Arabian Sea so far, which showed that the calanoid copepod Lucicutia grandis is an indicator species of the OMZ lower boundary, whereas Calanoides natalis is a diapausing species in the OMZ. Studies also evidenced that many calanoids (Pleuromamma indica, Lucicutia longicornis, Rhincalanus nasutus, Paracalanus aculeatus, Eucalanus attenuatus, Euchaeta rimana, Subeucalanus subcrassus), cyclopoids (Oithona nana, Oncaea conifera, Oncaea subtilis, Saphirina), Harpacticoids (Microsetella sp., Aegisthus mucronatus) and Mormonilloids (Mormonilla minor) living in the perennial OMZ are either vertical migrators or having a patchy distribution between the epipelagic to the deeper OMZ stratum. These OMZ copepods are believed to have distinctive growth and reproductive traits that allow them to exist in the OMZs. Their high enzyme activity allows them to carry out vertical migration, their high lipid reserves allow them to stay alive in starving conditions, and their slow lifestyle reduces their energy consumption in deeper OMZs. Unlike the perennial OMZs in the Arabian Sea, copepods in the seasonal OMZs in the coastal upwelling zones are almost unexplored, except for a recent attempt that demonstrated that cyclopoids have better survival strategies there. The Arabian Sea and the Bay of Bengal around India have a strong seasonal exchange of their water masses, but how they influence and shape the copepod communities in these regions and the OMZs they harbour is completely unknown.

Introduction

Although the Arabian Sea and the Bay of Bengal are located at the same latitudes, they respond differently to similar climatic forcings and exhibit markedly distinct patterns of phytoplankton biomass and production (Jyothibabu et al., 2008, Jyothibabu et al., 2008, Jyothibabu et al., 2010, Jyothibabu et al., 2015, Jyothibabu et al., 2021a, Jyothibabu et al., 2018a, Jyothibabu et al., 2018b, Jyothibabu et al., 2021b). The Arabian Sea, in general, is a more productive basin, primarily due to the active upwelling during the Southwest Monsoon (June to September) and convective mixing during the Northeast Monsoon (November to February), and both of them eventually contribute to the formation of a thick Oxygen Minimum Zone (OMZ) in the intermediate depths (Naqvi, 1991, Jyothibabu et al., 2010). Closer to the Indian subcontinent, the Northeastern Arabian Sea has a lot more phytoplankton biomass than the Southeastern Arabian Sea. This biomass lasts for nearly 8 months in the Northeastern Arabian Sea, compared to just 4 months in the Southeastern Arabian Sea (Jyothibabu et al., 2010, Shankar et al., 2019). On the other hand, upwelling and winter convection, which promote phytoplankton biomass in the Arabian Sea, are either very weak or absent in the Bay of Bengal due to the prolonged and intense surface layer stratification caused by the significant freshwater influx (Jyothibabu et al., 2008). The nutrient loading via river discharge, which was thought to enhance nutrient levels, is inadequate to increase phytoplankton stock beyond the shelf waters of the Bay of Bengal (Jyothibabu et al., 2008, Jyothibabu et al., 2021a, Jyothibabu et al., 2018a, Jyothibabu et al., 2018b, Jyothibabu et al., 2021b). As a result, except for the very narrow shelf, phytoplankton biomass is low in the Bay of Bengal throughout the year, which is primarily governed by mesoscale eddies. In addition to oxygenating the subsurface, the dominant warm-core eddies in the Bay of Bengal also causes low basin-scale phytoplankton biomass, reducing the vertical extent of the OMZ (Sarma et al., 2018, Jyothibabu et al., 2021a).

Dissolved oxygen is widely acknowledged as an essential environmental variable in the ocean that regulates underwater life and influences biogeochemical cycles (Wishner et al., 1990, Wishner et al., 1998, Wishner et al., 2000, Padmavati et al., 1998, Stramma et al., 2008, Jyothibabu et al., 2021b). It typically remains saturated in the surface waters but gets rapidly depleted at intermediate depths due to intensive bacterial respiration associated with organic matter breakdown (Madhupratap et al., 2001, Stramma et al., 2008). In certain regions in the ocean, dissolved oxygen levels decrease significantly (hypoxic or anoxic levels) in the subsurface due to the high decomposition of organic matter and lack of ventilation, and thus OMZs are being formed (Wyrtki, 1962, Nair et al., 1989, Naqvi, 1987, Madhupratap et al., 2001). Among the many OMZs of the world ocean, the major three are in the Eastern Tropical North Pacific, the Eastern Subtropical North Pacific, and the Arabian Sea (Fig. 1) (Kamykowski and Zentara, 1990, Diaz and Rosenberg, 1995, Diaz and Rosenberg, 2008, Levin, 2003, Stramma et al., 2008). The Arabian Sea in the western part of the northern Indian Ocean has a thicker OMZ layer (∼1000 m) between 150 and 1250 m depth than the Bay of Bengal in the eastern part (∼500 m), which is located between 200 and 700 m (Fig. 2; Madhupratap et al., 2001, Banse et al., 2013, Acharya and Panigrahi, 2016, Sarma et al., 2018).

The expanding OMZs and their impact on aquatic life is an important research topic the world over (Stramma et al., 2008, Breitburg et al., 2018). A recent study described dissolved oxygen as the ocean's ‘universal currency of life’ as it is the most indispensable variable for the sustenance of sensitive ocean life such as corals (Nelson and Altieri., 2019). Studies have shown that dissolved oxygen deficiency adversely affects the zooplankton community, as evidenced by lower zooplankton biomass in the core of OMZs (Fig. 3; Vinogradov and Voronina, 1961, Wishner et al., 1990, Böttger-Schnack, 1996, Saltzman and Wishner, 1997, Childress and Seibel, 1998, Padmavati et al., 1998). It was noted in the Arabian Sea that while the epipelagic zone (0–100 m) contains around 80% of total plankton, the mesopelagic zone (100–1050 m) with OMZ contains only 14% (Madhupratap and Haridas, 1990, Böttger-Schnack, 1996, Padmavati et al., 1998, Madhupratap et al., 2001). Thus, the zooplankton biomass in a region sustaining OMZ exhibits strong vertical gradients relative to other areas where OMZ is absent (Koppelmann and Weikert, 1997). It is also well marked that there is a secondary peak of zooplankton biomass at the lower boundary of the OMZ, which is usually absent at similar depths where the OMZ is weak or absent (Vinogradov and Voronina, 1961, Madhupratap and Haridas, 1990, Wishner et al., 1998). This secondary peak of zooplankton biomass is attributed to the availability of more oxygenated water near the OMZ's lower boundary (Madhupratap and Haridas, 1990, Wishner et al., 1998). Interestingly, there could be some unconsumed organic particles reaching the bottom layers of the OMZ that would serve as the primary food source for the fauna living below the OMZs (Vinogradov and Voronina, 1961).

Copepods are the most prevalent taxonomic group in the marine metazoan zooplankton, and their contribution to the total community abundance usually rises with depth (Madhupratap and Haridas, 1990). They are the most abundant metazoans in the ocean, commonly referred to as the ‘insects of the sea’ due to their richness, accounting for around 80% of total zooplankton abundance (Humes, 1994, Madhupratap et al., 1996a, Madhupratap et al., 1996b, Kiørboe, 2011, Jagadeesan et al., 2013). Copepods have 10 taxonomic orders with the following relative abundance and diversity in the perennial OMZ of the Arabian Sea; Calanoida > Cyclopoida > Harpacticoida > Siphonostomatoida > Mormonilloida (Madhupratap and Haridas, 1990, Huys and Boxshall, 1991, Padmavati et al., 1998, Madhupratap et al., 2001, Jyothibabu et al., 2021a, Jyothibabu et al., 2021b). Copepods are known as live nutrition capsules because of their high protein, amino acid, and unsaturated fatty acid content (Santhanam and Perumal, 2012, Santhanam et al., 2019, Jayalakshmi and Santhanam, 2019). They serve as a major link in the food chain between primary producers and fishes (Madhupratap et al., 2001, Jagadeesan et al., 2013). Their faecal pellets, which are packages of organic carbon produced in the ocean's surface layers, sink faster to the ocean depths and allow for more energy transport into the deep aphotic zone (Schminke, 2007).

Earlier studies on copepods from the study domain mostly dealt with the distribution and taxonomy, and hence very little is known about their behaviour and eco-physiological adaptations in the OMZs (Fig. 4, Fig. 5). Studies have shown that calanoid copepods are more dominant (60–80%) within the perennial OMZs than outside of them (50–70%) (Madhupratap and Haridas, 1990, Padmavati et al., 1998, Madhupratap et al., 2001, Koppelmann et al., 2003). Calanoids Lucicutia grandis is considered as an indicator of OMZ where it actively feeds and reproduces without any resting stages (Gowing and Wishner, 1998, Wishner et al., 2000). Others that survive in the OMZ are the non-calanoid copepods, euphausiids, gelatinous plankton and mesopelagic fishes such as Cyclothone (Levin et al., 2009, Ekau et al., 2010). Many of them are diurnal vertical migrators, while others are diapausing and continue to stay in the OMZ as a survival strategy (Vinogradov and Voronina, 1961, Saltzman and Wishner, 1997, Childress and Seibel, 1998, Seibel, 2011). A recent study showed that euphausiids could move across significant gradients of temperature, salinity, and oxygen during diel vertical migration, implying that these species must exhibit a high degree of ecophysiological flexibility (Tremblay et al., 2020).

Over the last several decades, there has been a significant amount of progressive literature available on the oceanographic settings behind the contrasting OMZ in the Arabian Sea and the Bay of Bengal (Table 1). Similarly, there are numerous studies on copepods from the Arabian Sea and the Bay of Bengal, though exclusive studies from the OMZ especially in the latter region, are highly limited (Table 2; Vinogradov and Voronina, 1961, Padmavati et al., 1998, Madhupratap and Haridas, 1990; Böttger-Schnack, 1996; Gowing and Wishner, 1998). However, there has been a general lack of updated information in recent decades from the numerous OMZ studies in the Arabian Sea and Bay of Bengal concerning the copepods thriving in these regions. This review is initiated to collate and summarise all the information on the oceanographic settings and biophysical linkages of the contrasting OMZs in the Arabian Sea and the Bay of Bengal and link them with (a) the composition and distribution of copepods in the OMZs, (b) possible adaptation strategies of copepods in OMZs and their phylogeny, and (c) research gaps of OMZ copepods in the Arabian Sea and the Bay of Bengal.

Section snippets

Methods

This review study is based on a detailed and systematic search of the literature to reduce selection bias. The publications that are authoritative as well as sourced from standard journals were selected. The information was collated and summarised under different sections to suit the objectives. Schematic figures have been prepared and presented for a comprehensive understanding of the facts and concepts. Many summary figures were adapted and redrawn by combining information from multiple

Perennial oceanic OMZ

The Arabian Sea, one of the most productive regions in the world ocean, is bordered on three sides by the landmasses of Asia and Africa (Ryther et al., 1966, Madhupratap et al., 1996a, Madhupratap et al., 1996b, Madhupratap et al., 2001. Table 1 presents a historical overview of the OMZ hydrography studies in the Arabian Sea, as well as their key findings. The surface circulation in the Arabian Sea undergoes a biannual reversal caused by the southwest and northeast monsoon winds, leading to

OMZ in the Bay of Bengal

The Bay of Bengal is characterized by warmer SST (>28⁰C), lower salinity (28–32) as compared to the Arabian Sea, resulting in strong surface layer stratification (Prasanna Kumar et al., 2004, Fernandes, 2008, Jagadeesan et al., 2019, Sarma et al., 2013). Table 2 provides a chronological summary of the OMZ hydrography investigations conducted in the Bay of Bengal. The Bay of Bengal has a mid-depth OMZ, which is, however, weaker than in the Arabian Sea. The strong stratification prevents the

Copepods of perennial OMZ in the Arabian Sea

The John Murray Expedition (1933–1934) and the International Indian Ocean Expedition (1960–1965) gave baseline data on the distribution and abundance of zooplankton in the Arabian Sea (Kasturirangan et al., 1973, Fleminger and Hulsemann, 1973, Stephen et al., 1992, Gopalakrishnan and Balachandran, 1992). However, these expeditions sampled only the upper 200 m of the ocean using a 330 µm mesh net, and hence, do not represent the smaller forms and also the copepods inhabiting the deep ocean (

Copepods of seasonal coastal OMZ in the Arabian Sea

Naqvi (2019) showed that the world’s largest naturally-formed shallow hypoxic zone associated with the coastal upwelling along India’s west coast has been more intense in recent times as compared to the 1970 s. Even though the coastal upwelling systems are well known for their exceptional plankton and fishery yield (Mann, 1993), they have not been studied for the physiological condition of the biota living in the subsurface oxygen-deficient waters (Elliot et al., 2013). Worldwide research has

Copepods in the Bay of Bengal

Although the presence of OMZ in the Bay of Bengal has been known for decades, the impact of OMZ on the distribution of the zooplankton community, especially copepods, has yet to be studied. Earlier studies on mesozooplankton in the Bay of Bengal were mostly on the seasonal distribution of biomass, abundance, and taxonomic groups in the epi- and mesopelagic zones (Fernandes and Ramaiah, 2009, Fernandes and Ramaiah, 2013, Fernandes and Ramaiah, 2019, Jagadeesan et al., 2019). Hence, compared to

Eco-physiological adaptations

Even though scientific investigations of the biomass, abundance and distributional ranges of calanoid copepods in the OMZ waters of the Indian Ocean were documented under JGOFS, there is a lack of information on the possible survival strategies of copepods in such hostile conditions. Considering this information gap in the AS and the Bay of Bengal, and also the fact that many OMZ copepods that have already been studied have closely related species living in the OMZ in many parts of the world, an

Molecular studies on OMZ copepods

The molecular basis of copepod adaptations to oxygen deprivation in tidal pools has yielded some fascinating discoveries, but a systematic examination into the molecular basis of copepod adaptations to oxygen deficiency in perennial ocean mid-depth OMZs has yet to be conducted. The primary cellular oxygen sensing in metazoans is believed to be mediated by induction of the Hypoxia Inducible Factors (HIF) pathway, and the genes in this pathway are considered to be the master regulators of oxygen

Research gaps

Although the northern Indian Ocean is home to one of the world's most important OMZs, biological research focused on OMZs is uncommon in comparison to those dealing with their physical and chemical properties (Table 3, Table 4). This might be due to the practical difficulties of sampling the OMZ areas with standard plankton nets; ideally, a multiple plankton sampler (MPN) is required to satisfy the scientific goal. Although some data on the composition and quantity of copepods in permanent OMZs

Conclusion

Copepods are the most abundant metazoan in the ocean and so in the OMZs. This review collected and summarised the observations of the progressive literature on the distinct OMZs in the Arabian Sea and the Bay of Bengal and connected them with the copepods thriving there, their status and potential adaptations. The OMZ in the perennial mid-ocean depths in the Arabian Sea shows high percentage contributions of Calanoids in the copepod community. Based on the available literature, OMZ copepods may

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors thank the Director of the CSIR-National Institute of Oceanography for the facility and encouragement. This study is part of the SWQM-MEDAS programme of the Ministry of Earth Sciences, India. The authors thank the Directors of the Centre for Marine Living Resources and Ecology & National Centre for Coastal Research, Chennai for supporting this work. The first author is thankful to the University Grants Commission, India for the award of Junior Research Fellowship. This is CSIR-NIO

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