Elsevier

Progress in Oceanography

Volume 78, Issue 2, August 2008, Pages 163-191
Progress in Oceanography

Vertical zonation and distributions of calanoid copepods through the lower oxycline of the Arabian Sea oxygen minimum zone

https://doi.org/10.1016/j.pocean.2008.03.001Get rights and content

Abstract

This paper provides the first comprehensive analysis of calanoid copepod vertical zonation and community structure at midwater depths (300–1000 m) through the lower oxygen gradient (oxycline) (0.02 to ∼0.3 ml/L) of an oxygen minimum zone (OMZ). Feeding ecology was also analyzed. Zooplankton were collected with a double 1 m2 MOCNESS plankton net in day and night vertically-stratified oblique tows from 1000 m to the surface at six stations during four seasons as part of the 1995 US Joint Global Ocean Flux Study (JGOFS) Arabian Sea project. The geographic comparison between a eutrophic more oxygenated onshore station and an offshore station with a strong OMZ served as a natural experiment to elucidate the influence of depth, oxygen concentration, season, food resources, and predators on the copepod distributions.

Copepod species and species assemblages of the Arabian Sea OMZ differed in their spatial and vertical distributions relative to environmental and ecological characteristics of the water column and region. The extent and intensity of the oxycline at the lower boundary of the OMZ, and its spatial and temporal variability over the year of sampling, was an important factor affecting distributional patterns. Calanoid copepod species showed vertical zonation through the lower OMZ oxycline. Clustering analyses defined sample groups with similar copepod assemblages and species groups with similar distributions. No apparent diel vertical migration for either calanoid or non-calanoid copepods at these midwater depths was observed, but some species had age-related differences in vertical distributions. Subzones of the OMZ, termed the OMZ Core, the Lower Oxycline, and the Sub-Oxycline, had different copepod communities and ecological interactions. Major distributional and ecological changes were associated with surprisingly small oxygen gradients at low oxygen concentrations. The calanoid copepod community was most diverse in the most oxygenated environments (oxygen >0.14 ml/L), but the rank order of abundance of species was similar in the Lower Oxycline and Sub-Oxycline. Some species were absent or much scarcer in the OMZ Core. Two copepod species common in the Lower Oxycline were primarily detritivorous but showed dietary differences suggesting feeding specialization. The copepod Spinocalanus antarcticus fed primarily on components of the vertical particulate flux and suspended material, a less versatile diet than the co-occurring copepod Lucicutia grandis. Vertical zonation of copepod species through the lower OMZ oxycline is probably a complex interplay between physiological limitation by low oxygen, potential predator control, and potential food resources. Pelagic OMZ and oxycline communities, and their ecological interactions in the water column and with the benthos, may become even more widespread and significant in the future ocean, if global warming increases the extent and intensity of OMZs as predicted.

Introduction

Oxygen minimum zones (OMZs) are widespread permanent suboxic features of the oceanic midwater, usually defined as extended depth intervals with oxygen concentrations below either 0.1 or 0.5 ml/L (4.5 or 22 μM) (Wyrtki, 1973, Kamykowski and Zentara, 1990, Morrison et al., 1999). The northern Arabian Sea, the location of the research described here, is one such area (Fig. 1). OMZs strongly affect distributions and abundances of zooplankton, nekton, and benthos, as well as metabolic and biogeochemical processes (reviewed by Childress and Seibel, 1998, Levin, 2003). Mesozooplankton biomasses and abundances within the center of strong OMZs are typically much reduced compared to more oxygenated depths above and below, although high numbers of larger animals often migrate into OMZs daily (Longhurst, 1967, Brinton, 1979, Judkins, 1980, Saltzman and Wishner, 1997a, Saltzman and Wishner, 1997b, Herring et al., 1998, Wishner et al., 1998, Morrison et al., 1999, Ashjian et al., 2002). A few taxa have abundant diapausing (resting) stages or reproductive individuals that live seasonally or temporarily in OMZs (Smith et al., 1998a, Smith et al., 1998b, Smith and Madhupratap, 2005, Seibel et al., 2005).

Upper and lower OMZ boundaries differ in character. The upper OMZ boundary, typically the thermocline, is a sharp stratification feature, sometimes within the euphotic zone. The lower boundary of prominent OMZs, however, is an extended “oxycline” region where oxygen concentrations increase markedly with depth (∼500 to >1000 m in the northern Arabian Sea OMZ). Mesozooplankton biomass often shows a secondary peak associated with the lower OMZ oxycline, especially the oxygen gradient between ∼0.05 and 0.15 ml/L (2.3–4.5 μM) (∼600–800 m in the Arabian Sea) (Wishner et al., 1998). High biological activities (high feeding rates) of zooplankton have been reported from the Eastern Tropical Pacific OMZ oxycline (Wishner et al., 1995). An indicator species from this feature in the Arabian Sea, the copepod Lucicutia grandis, had a progression with age of the various depth and oxygen levels inhabited by different life history stages; this copepod showed clear evolutionary adaptation to life in the lower OMZ oxycline (Wishner et al., 2000).

While an oxygen level of about 0.1 ml/L is usually considered the boundary triggering oceanic OMZ biological effects (such as alterations in biomass, abundances, and metabolic rates) (Longhurst, 1967, Childress, 1975, Judkins, 1980, Wishner et al., 1995, Wishner et al., 1998), zooplankton distributions obviously extend into depths with even lower oxygen concentrations. There are also examples of distinct zooplankton layers within sharp oceanic oxyclines, including diapausing Calanus pacificus in the Santa Barbara Basin (Alldredge et al., 1984) and zooplankton in the Black Sea (Vinogradov et al., 1986). Deep-sea benthos also show strong responses to oxygen gradients where OMZs or oxic–anoxic interfaces impinge on the seafloor (Wishner et al., 1990, Wishner et al., 1995). Levin (2003) reviewed occurrences of these benthic “edge effects” near upper and lower OMZ boundaries, and Arabian Sea benthic “edge effects” have also been studied (Levin et al., 2000, Woulds et al., 2007). We show in this paper that there is no precise oxygen concentration affecting all pelagic copepods at the lower OMZ edge; instead, there is strong zonation of different species through the lower oxycline. Furthermore, some of these copepod distributional changes occur at extremely low oxygen concentrations, lower than the oxygen boundaries often used to denote OMZs in the literature.

The pronounced OMZ of the Arabian Sea affects vertical distributions of total zooplankton biomass and species (Vinogradov and Voronina, 1962, Böttger-Schnack, 1996, Smith et al., 1998b, Wishner et al., 1998, Wishner et al., 2000, Madhupratap et al., 2001, Fabian et al., 2005, Koppelmann and Weikert, 2005, Smith and Madhupratap, 2005). However, although broad patterns of zooplankton distributions relative to the Arabian Sea OMZ have been documented, details of zooplankton vertical zonation associated with specific oxygen concentrations in OMZs are poorly known. This is especially true for the oxygen gradients of the lower OMZ boundary. Furthermore, previous investigators did not deal comprehensively with overall differences in zooplankton community structure related to different oxygen levels.

Potential food for zooplankton in the OMZ and lower oxycline is apparently abundant. Microbial layering, especially prominent within oxic–anoxic interfaces (Fenchel et al., 1990, Taylor et al., 2001, Lin et al., 2006), likely occurs in the Arabian Sea lower OMZ oxycline as well. Microbial biomass, processes and indicators, including denitrification, high nitrite concentrations, lipid biomarkers, and chemoautotrophy, have been reported from OMZs and strong oxyclines including the Arabian Sea (Bird and Karl, 1991, Taylor et al., 2001, Ho et al., 2004, Wakeham et al., 2002, Koppelmann et al., 2005, Devol et al., 2006). Microplankton is abundant in the Arabian Sea OMZ (Gowing et al., 2003). The copepod L. grandis in the Arabian Sea consumed food items representing five different trophic levels (bacterivore, herbivore, microbivore, detritivore, carnivore) and appeared to be intercepting and repackaging sinking particles (Gowing and Wishner, 1998, Wishner et al., 2000).

The Joint Global Ocean Flux Study (JGOFS) was an extensive international program of expeditions and research related to carbon cycling that focused on the Arabian Sea during 1994–1996 (Smith et al., 1998a). Zooplankton sampling described in this manuscript was undertaken during cruises of the US JGOFS project. The major seasonal signal of the Arabian Sea is the wind-driven monsoon cycle, with the Southwest Monsoon (strongest sustained winds annually) occurring from July to September and the Northeast Monsoon occurring from December to January (Weller et al., 1998). Primary productivity is high year round (slight peak during the Southwest Monsoon: Barber et al., 2001), but there are marked seasonal and geographic changes in phytoplankton composition and size (Campbell et al., 1998, Garrison et al., 1998, Garrison et al., 2000). A large peak in export flux of organic material to depth occurs during and following the Southwest Monsoon (Lee et al., 1998, Honjo et al., 1999).

Observations at sea of fresh zooplankton samples from vertically-stratified net tows taken during the US JGOFS Arabian Sea cruises suggested that unique zooplankton communities existed at different levels through the OMZ and its lower boundary. The sudden occurrence both day and night of many bright red deepwater shrimp, lophogastrids, and mysids along with abundant black-colored fish (especially Cyclothone spp.) imparted a distinctive “red and black” appearance to samples from the lower oxycline region (∼500–800 m). This contrasted sharply with the sparse pale beige nighttime zooplankton samples of the OMZ core just above (supplemented during day tows in the OMZ core with the occurrence of vertically migrating euphausiids and myctophids).

This paper focuses on calanoid copepod distributions and vertical zonation through the lower portion and oxycline of the Arabian Sea OMZ and defines ecological subregions of the lower OMZ. We also describe the feeding ecology of Spinocalanus antarcticus, a copepod abundant in the oxycline, in comparison to that of L. grandis, mentioned above. We use the geographic comparison between an onshore and an offshore station as a natural experiment to help elucidate the influence of depth, oxygen concentration, season, location and other environmental parameters on copepod distributions and vertical zonation. Station S2 was a coastal eutrophic station (147 km offshore), with the highest biomasses and strongest signal of monsoon-driven upwelling and production (Smith et al., 1998a, Wishner et al., 1998) (Fig. 1). Station S7, located 630 km offshore, was near the Findlater wind jet of the Southwest Monsoon, had a strong well-developed OMZ, and had high abundances of an OMZ indicator copepod species previously analyzed (Wishner et al., 2000). Oxygen levels at station S2 were usually higher than at S7, except during one of the cruises, when very low midwater oxygen extended shoreward.

Section snippets

Sampling

Zooplankton were collected with a double 1 m2 MOCNESS (two 1 m2 MOCNESS systems side-by-side), a multiple opening–closing net system with environmental sensors and control of the nets from shipboard (Wiebe et al., 1976). The nets were 153 μm mesh. Electronic data from the MOCNESS included time, volume filtered, depth, temperature (Sea-Bird SBE 3), salinity (Sea-Bird SBE 4), light transmission (SeaTech 25 cm beam transmissometer), and oxygen (Sea-Bird SBE 13). Typically, about 500–800 m3 of water

Environmental overview

Onshore station S2 and offshore station S7 illustrate two contrasting hydrographic regimes with regard to the OMZ (Fig. 2). Station S7 usually had a more pronounced and thicker OMZ than station S2. At both stations, the sharp upper boundary of the OMZ at ∼100 m was coincident with the thermocline. In the upper 300 m, salinity layers corresponding to various interleaving water masses, were apparent (Morrison et al., 1999), but below that depth, salinity and temperature steadily decreased while

Overview

This study documents midwater copepod zonation and community structure associated with the Arabian Sea OMZ. Starting with distributions of individual species, we defined statistically significant Species Groups and their vertical zonation relative to environmental parameters, especially the strong ozygen gradients at the lower oxycline of the OMZ. In the following sections, we discuss the broader context and implications of these results and develop the concept of ecological subzones of the OMZ

Conclusions

This paper provides the first comprehensive analysis of copepod zonation and community structure at midwater depths (300–1000 m) through the center and lower oxycline of a strong OMZ with extremely low oxygen concentrations (0.02 ml/L to ∼0.3 ml/L). Copepod species and species assemblages of the Arabian Sea OMZ differed in their spatial and vertical distributions relative to environmental and ecological characteristics of the water column and region. Features affecting distributions included

Acknowledgments

We thank the many people who helped at sea and in the lab during the JGOFS program (see acknowledgments in Wishner et al., 1998, Gowing and Wishner, 1998, Wishner et al., 2000), especially our zooplankton colleagues S. Smith and M. Roman and their groups. For specific assistance with the plankton samples reported in this paper, we thank J. Saltzman and C. Venn. Assistance and verifications for some species identifications were provided by F. Ferrari (US National Museum), S. Smith and P. Lane

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