The deep sea is one of the world's most biologically diverse ecosystems. The deep sea starts from about 2,000 m and extends to the Challenger Deep, the deepest ocean trench (10,927 m) in the world. The variations in depth and associated altered environments are a primary factor for the diversity of life. Moreover, this biodiversity has been less explored, and perhaps most of the undiscovered species may still be covered from the oceans (Costello et al., 2012). The continental margin is a geophysical layer covered by the thick continental crust and a thin oceanic crust that extends from the coastal to the deep sea and is comprised of the shelf (0–200 m), slope (200–3,000 m), and rise (3,000–4,000 m). Its surface area covers about 11% of the oceans' total Earth area (Menot et al., 2010). In the past few decades, a variety of habitat scale levels has been identified based on their characteristic such as geomorphological, hydrographical, geochemical and biological along the continental margin (Levin and Sibuet, 2012). Collectively, these features create unique ecological settings such as coral reefs, methane seeps, canyons, oxygen minimum zones (OMZs), seamounts, and hydrothermal vents. These hotspots and the habitat heterogeneity along the continental margin create an environment to host surprisingly high rates of population (Etter et al., 2005), biomass, physiological adaptation, species endemicity (Menot et al., 2010), and some of the most diverse array of benthic life forms on the planet (Grassle and Maciolek, 1992).

Benthic meiofauna represents a group of small-sized animals (between 31 and 500 μm) with a high turnover rate (Zeppilli et al., 2018). They are used as a food source for higher trophic levels, such as several fishes, shrimps, and shellfishes (Danovaro et al., 2007). Apart from their contribution to the food chain, meiofauna also plays a crucial role in sediment energetics and bio-indicators to assess environmental health (Heip et al., 1984; Danovaro et al., 2002; Zeppilli et al., 2015). Meiofauna act as vertical conveyors between the sediments, known as the bioturbation process (Coull, 1999). Further, they contribute to modifying the sediment hydrodynamics and biogeochemical fluxes (Aller and Aller, 1992; Schratzberger and Ingels, 2018). The understanding of the meiofaunal community along the continental margin and the abyssal plain is comparatively lower than that of shallow waters. The quantitative research of the benthic meiofaunal community below the shelf and the continental slope and abyssal depths began in the 1970s (Wigley and McIntyre, 1964; Thiel, 1966). Although, since then, the exploration of meiofauna along the continental margin has increased across all the oceans, this research is relatively limited in the Indian Ocean (Soltwedel, 2000). In the 1970s to the 1990s, the meiofaunal research along the continental margin spread to the marginal slope of East Africa in the northwestern Indian Ocean (Thiel, 1966, 1979; Romano and Dinet, 1981; Duineveld et al., 1997) and western India in the eastern Arabian Sea (Ansari et al., 1980).

The present study demonstrates the meiofaunal community along the Western Indian continental margin (WICM) is impinged upon by the OMZ. The OMZ is one of the most prominent features found in the Arabian Sea, the North Indian Ocean, which hosts about 40% of the global denitrification (Al Azhar et al., 2017). The Arabian Sea is characterized by a very pronounced midwater oxygen minimum zone (OMZ), between 150 and 1,250 m, where, the dissolved oxygen levels were observed below 0.05 mL.L⁻¹ (Reichart et al., 1998) and were frequently changing the OMZ in space and time (Schulz et al., 1996; Lachkar et al., 2018). The western half of the Arabian Sea evidenced cyclonic and anticyclonic quasi-geostrophic mesoscale eddies and fronts with their associated meandering currents (Flagg and Kim, 1998; Shankar et al., 2002; Artamonov, 2006; Resplandy et al., 2011). The highest primary production was observed about 380 g C m⁻² year⁻¹ in the eastern part of the Arabian Sea, which was mainly driven by transition phases between SW and NE monsoon (Ivanova et al., 2003). Similarly, high primary productivity was observed off Trivandrum (Malik et al., 2015). The high organic carbon content were mainly associated with a depth of 200–1,200 m (Schulz et al., 1996). A vertical supply of nutrients is driven by eddies (Resplandy et al., 2011) with active nitrate reduction and denitrification (Morrison et al., 1999). Thus, the Arabian Sea is a very dynamic ecosystem—one of many OMZs in the world.

The benthic biodiversity along the WICM, including OMZs and abyssal plain, are poorly understood. Few studies discussed benthic macrofaunal community structure along the WICM (Ingole et al., 2010; Levin et al., 2013), while understanding meiofauna along the continental margin depths below 200 m and extended abyssal plain in the Arabian Sea is sparse. Ansari et al. (1980) studied the meiofaunal community at depths between 20 and 840 m along the continental slope in a 15°N transect. Further, Ansari et al. (2017) showed the meiofaunal community along the depths ranged 500–1,956 m off Ratnagiri region. These studies did not generate any meiofaunal data from the abyssal plain in the Arabian Sea. Further, there is a lack of continuous study from the shelf (non-OMZ), slope (including OMZ) and abyssal plain in the Arabian Sea. Therefore, the present study aims to understand the benthic meiofaunal community structure with their surrounding environment along the WICM (depths between 111 and 2,054 m), including the OMZ and abyssal plain (3,918 m).

Over the past few decades, research and reviews have shown that the abundance of benthic meiofauna generally decreases as the depth increases (Soltwedel, 2000). It has also been observed that the diversity and evenness of meiofauna are highly localized and associated with small-scale geochemical changes (Levin and Mendoza, 2007; Thurber et al., 2010; Van Gaever et al., 2010; Vanreusel et al., 2010). Generally, nematodes are the dominant groups among all meiofaunal communities and tend to be most tolerant than any other groups including polychaetes, to the lower concentration of dissolved oxygen concentration (Levin et al., 1991). Therefore, we are hypothesizing based on the previous studies that (1) the benthic meiofaunal density, biomass, and group diversity will vary due to depth gradients and changes in the concentration of DO; (2) the population will decrease with the increasing depths; and (3) rare taxon groups will be at a minimum in lower DO conditions.

The circulation of dissolved oxygen in the world oceans differs spatially with zones of the low oxygen water centered around the tropics (Stramma et al., 2008). The Arabian Sea, including the WICM, was among the near anoxic condition concentrations at its transitional depths in the oceans. Generally, the West Indian shelf and slope is influenced by the West Indian underwater current flow, which leads to slightly above anoxic condition. However, off Goa region was found anoxic and very static throughout the year (Naqvi et al., 2009). The Arabian Sea OMZ extends between longitudinal 60° and 75° E and latitudinal between 10 and 25° N (Naqvi and Noronha, 1991) and vertically between 150 and 1,200 m depths. In the present study, the OMZ was extended from a depth of 202 to 764 m, where 485 m was considered as the core of OMZ due to the least bottom water DO concentration.

Sediment TOC were significantly higher within the OMZ area than those at the non-OMZ-D, which were oxygenated. The strong inverse correlations between TOC and DO was observed, which was evidenced by earlier studies around the globe, such as Peru (Neira et al., 2001a), Central Chile (Neira et al., 2001b), off Costa Rica (Neira et al., 2018), and the western Indian continental margin (Ingole et al., 2010). The CPE was correlated strongly (r = 0.87), with TOC showing similar depth gradient observations. Therefore, the relationship of TOC, DO, and CPE suggest that the flux of sinking CPE on to the benthic sediment was greater in the oxygen-deficient water columns than in oxygenated waters. Correspondingly, the attenuation coefficient for sinking OM has been reported to be weak beneath OMZs off Peru (Martin et al., 1987), in the Arabian Sea (Haake et al., 1993), and off Mexico (Devol and Hartnett, 2001). This reduced attenuation of sinking OM may be attributed to reduced low oxygen conditions and microbial activity (Fenchel and Finlay, 1995). The high levels of dissolved phosphate in pore water at the OMZ site enhance phosphorite deposition by preserving organic sediments at low oxygen concentrations (Frank et al., 1975). The Chl a/Phaeo ratio was observed similar in OMZ sites (202, 485, and 764 m) with 0.32, which were lower than those of non-OMZ-D and higher than of non-OMZ-S. The higher values of Chl a/Phaeo ratio at two depths of non-OMZ deeper sites (1,204–2,054 m) suggest that the organic matter deposited was relatively fresh. The high TN values at 202 m and non-OMZ-S sites could indicate preferential use of nitrogen during the remineralization of organic matter of phytoplanktonic origin (Sánchez and Carriquiry, 2007).

The role of DO in structuring the benthic meiofauna, especially nematodes from the continental margins, as evidenced earlier in few studies (Cook et al., 2000; Neira et al., 2001a, 2018; Singh and Ingole, 2016). The environmental parameters including DO and meiofaunal taxa other than nematodes and meiofaunal biomass considered in the present study demonstrated new addition to the studies of meiofaunal community patterns along the WICM and abyssal plain in the Arabian Sea. The present study reports the remarkable changes in the meiofaunal taxa's diversity, density, and biomass along the depth gradient. The density was observed to be lower in the present study than OMZ off Chile (Veit-Köhler et al., 2009). The depth gradient as well as OMZ influenced overall density and biomass. Meiofaunal density and biomass usually decreases with increasing water depths (Rex and Etter, 2010). Differing diversity indices were also observed between OMZ v/s non-OMZ sites, where oxygen is the main limiting factor (Sellanes et al., 2010). In the OMZ site, the nematode density was at its maximum while crustacean density and diversity decreased (Table 2; Figure 5), which was also recorded by earlier studies from off Ratnagiri, eastern Arabian Sea (Ansari et al., 2017). Taxa diversity was reduced at 485 and 202 m. In contrast, it was found higher with a gradual increase in oxygen levels at 764 and 1,204 m depths. Similar results were represented by earlier studies (Gooday et al., 2009a; Levin et al., 2009). This resulted from favorable oxygen concentration and abundant food availability, described as the “edge effect” by earlier studies from the Pakistan margin (Levin, 2003; Gooday et al., 2010). Similarly, influence of DO on benthic community structure was reported from off Chile and Peru (Thiel, 1978), Mexico (Levin et al., 1991), and the Black Sea (Rhoads and Morse, 1971).

In the present study, the average density of nematode (114.66–425.39 ind. 10 cm⁻²) was recorded higher than the previous study (62.9–176.6 ind. 10 cm⁻²) carried out at 14°N (Singh and Ingole, 2016). The lower density of nematode encountered at 14°N may be variation in sampling gears where spade box corer (50 × 50 × 50 cm) was used for 14°N and multicore has been used in the present study. However, the reported nematode density of Oman margin ranged from 494 to 2495 ind. 10 cm⁻² was higher than the present study (Cook et al., 2000). The higher density on Oman margin could be related to the DO ranges (0.13–2.99 mL.L⁻¹), while in present study DO was reported lower (0.04–2.71 mL.L⁻¹) than Oman margin. The reported nematode density of the core OMZ in the present study was comparable to the core OMZ (upper and lower summit of Volcano 7) of the eastern Pacific Ocean (Levin et al., 1991). The relative percentage composition of nematodes was negatively impacted by bottom water oxygen concentration (Supplementary Figure 3). The nematode relative percentage composition at 202 and 485 m was strongly enhanced due to the effect of low oxygen concentration, which led to decrease in the density of other meiofaunal taxa. The absence of harpacticoid copepods, nauplii, and kinorhynchs shows inability to tolerate low oxygen concentrations (Murrell and Fleeger, 1989) at 202 m, and their consistent increase with the increasing DO in non-OMZ-D suggest that oxygen limitations directly control meiofaunal composition at higher taxonomic levels. Similar results were observed from off Peru and Costa Rica (Neira et al., 2018), and the Arabian Sea (Ansari et al., 2017).

The mean meiofaunal biomass was highest in non-OMZ-D (2,054 m) followed by 111 m (non-OMZ-S) and was lowest at the core OMZ (485 m), which was affected by the low DO. These findings may have attributed to a process, where low oxygen concentrations may influence the body size of individuals across the whole community related changes or within specific taxa (Rex and Etter, 2010). The effect on body size at the deficient oxygen levels was documented by earlier studies in the Arabian Sea (Levin et al., 1991; Gooday et al., 2009b; Rohal et al., 2014). The biomass of copepods was more dominant at non-OMZ-D than any other taxa from metazoan meiofauna. The experimental studies have shown that crustaceans were the most susceptible to changes in oxygen levels. The LC₅₀ (in mg O₂ L⁻¹) of crustaceans were higher than for other organisms studied (Vaquer-Sunyer and Duarte, 2008). The predictions were made that the fishes should be the first to be affected among benthic fauna, followed by crustaceans, worms, echinoderms, and molluscs as oxygen lowers (Vaquer-Sunyer and Duarte, 2008). A similar effect was also documented through experimental studies, where crustaceans such as shore crabs Carcinus maenas (L.) and shrimp Crangon crangon (L.) in the Danish fjords (Jørgensen and Jorgensen, 1980) and amphipod Monoporeia affinis, harpacticoids Microarthridion littorale, and Pseudobradya sp. in the Baltic Sea (Modig and Ólafsson, 1998) were wiped out due to low oxygen levels.

Results showed marked variations in the assemblages of rare taxa between OMZ and non-OMZ sites. The masking of the relative importance and the distribution of rare taxa in different habitats was caused by the dominance of nematodes and copepods (Bianchelli et al., 2010). Moreover, some taxa were exclusively observed in specific depths and their associated habitat. The isopods and tanaidaceans were found below 764 m at non-OMZ-D depths. However, cumaceans were recorded at 111 and 1,204 m, which were subjected to lower food quality and freshness (Cartes and Sorbe, 1996). Therefore, it seems like oxygen was the limiting factor for distribution of isopods, tanaidaceans and cumaceans, was supported by study in the OMZ off Chile (Veit-Köhler et al., 2009). However, tardigrades, gastrotrichs, turbellarians, and kinorhynchs were utterly absent in OMZ sites. Gastrotrichs and kinorhynchs were also absent in the low oxygen concentration sites Ant-7104 and Con-7161 off Chile (Veit-Köhler et al., 2009).

The sediment vertical distribution of meiofaunal density and biomass at WICM ranged similar to OMZ off Costa Rica (Neira et al., 2018), due to the approx. homologous environmental conditions and geographical location (latitude) among both regions. The maximum fauna was found in the upper 4 cm of the sediment depth, where the OM flux is low (Lambshead and Hodda, 1994). The community size structure was smaller, evidenced by the decrease in biomass wherever nematodes were dominant at the OMZ site. The annelids and their function (bioturbation) were reported in a few studies from OMZ and mainly contributed via tolerant annelids to hypoxic conditions (Levin et al., 2000; Smith et al., 2000). This may enhance the sediment layers' reworking and induce mixing downward (Levin et al., 1991), which supports nematode survival rates in the subsurface and deeper sediments (Braeckman et al., 2010). The enhanced relative proportion of copepods at non-OMZ-D sites influences the total meiofaunal biomass because of their comparably high average individual body weight (Jensen, 1988).

The meiofaunal density and biomass were known to influence by several aspects, for example, habitat heterogeneity (Gooday et al., 2010), bathymetric patterns (Gambi et al., 2010), food availability (Cook et al., 2000), and oxygen concentration (Levin, 2003; Neira et al., 2018). In the present study, the RDA plot signifies the role of dissolved oxygen (Figure 9), where a positive correlation of meiofaunal density, biomass and a number of crustacean's taxa was shown. The meiofaunal taxon richness (S and d), diversity (H′) and taxonomic evenness (J′) was found to be distinctly lower at 202 and 485 m of OMZ stations (Supplementary Figure 1), while depth also showed significant positive relation (Figure 9C). Furthermore, the meiofaunal density and biomass were observed to be positively related to food input and quality. A strong positive relation of TOC and its signifiers Chl a, phaeophytin, CPE, at OMZ (Figure 9) affect meiofaunal density, diversity and biomass which is represented by BIOENV results (Supplementary Tables 3–5). The influence of organic matter perturbation in the sediment on meiofaunal biomass has been recorded in earlier studies (Soltwedel, 2000).

OM quality and bioavailability generally decrease with depth due to degradation in the water column process. Due to this, an increase in meiofaunal density was observed at the shelf area due to OM's freshness and bioavailable OM quality (Figure 3). Nematodes and polychaetes density and biomass showed a positive relationship with OM's freshness and quality, which were illustrated in RDA plot (Figure 9). Therefore, meiofaunal density and biomass decrease with increasing depths. The CPE values were comparatively high, and meiofaunal density and abundance were found to be low at the core OMZ. Similar results were recorded at NW African margin (Soltwedel, 1997), and it has been suggested that phytodetritus deposits in that area had been transported over long distances and, therefore, were more degraded. Several investigations in OMZs from other parts of the world have noted a correlation between food quality and the lack of oxygen (Danovaro et al., 2000; Neira et al., 2001a). Therefore, food availability is a regulating factor along with the vertical sediment profile (Ingels et al., 2009). The importance of food quantity and availability on nematode abundance and diversity has been emphasized by Cook et al. (2000) from the Arabian Sea.

The present study reveals several characteristics of benthic meiofaunal communities and their response to changing depths and associated environmental factors primarily DO along the WICM. The study area was classified and summarized below with corresponding meiofaunal community characteristics based on the geophysical and hydrographic characters. The depth ranges and their related changes in environmental characteristics recorded along the WICM. The continental margin was observed with different DO concentrations, including intense OMZ with higher TOC and CPE. The density and biomass of the meiofaunal community were low within the OMZ region, where phytodetritus (CPE), TOC, and pore water nutrient were accumulated in higher amounts. The meiofaunal density showed a higher value in non-OMZ-S, while the lowest recorded at the intense OMZ (485 m) region. The diversity was observed moderate at non-OMZ-S and D, while the highest recorded at lower OMZ (764 m). The rare taxon showed the minimum richness at the lowest DO concentration along the OMZ while increasing in developing DO values. However, the result of the present study did not support our third hypothesis, as the population density did not show a trend of decreasing with increasing depths along the WICM, which could be due to several factors like OMZ and different geophysical structure in the study area. OMZs represent a principal barrier for benthic species between abyssal plain (food limitation) and continental shelf (plenty of food). These ecosystems may hold an answer to unaddressed questions such as diversified genetic speciation through evolutionary adaptations to ever reducing oxygenation of the world ocean due to global warming and eutrophication. Moreover, this study suggests that more exploration of the meiofaunal community will allow us to understand how the community patterns influence the ecosystem functioning along the heterogenous WICM and abyssal floor in the Arabian Sea.

The original contributions presented in the study are included in the article/Supplementary Material; further inquiries can be directed to the corresponding author/s.

SS designed this study. SS and SG carried out the field sampling. SK, SA, AC, and SC analyzed the meiofauna. UP, BS, SG, and SC estimated environmental variables. SS, SG, and SK performed statistical analysis, plotted map, figures, and wrote the manuscript. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.