Oxygen Minimum Zone Benthos: Adaptation and Community Response to Hypoxia

Abstract

Mid-water oxygen minima (Ͻ0.5 ml l Ϫ1 dissolved O 2 ) intercept the continental margins along much of the eastern Pacific Ocean, off west Africa and in the Arabian Sea and Bay of Bengal, creating extensive stretches of sea floor exposed to permanent, severe oxygen depletion. These seafloor oxygen minimum zones (OMZs) typically occur at bathyal depths between 200 m and 1000 m, and are major sites of carbon burial along the continental margins. Despite extreme oxygen depletion, protozoan and metazoan assemblages thrive in these environments. Metazoan adaptations include small, thin bodies, enhanced respiratory surface area, blood pigments such as haemoglobin, biogenic structure formation for stability in soupy sediments, an increased number of pyruvate oxidoreductases, and the presence of sulphide-oxidising symbionts. The organic-rich sediments of these regions often support mats of large sulphideoxidising bacteria (Thioploca, Beggiatoa, Thiomargarita), and high-density, low-diversity metazoan assemblages. Densities of protistan and metazoan meiofauna are typically elevated in OMZs, probably due to high tolerance of hypoxia, an abundant food supply, and release from predation. Macrofauna and megafauna often exhibit dense aggregations at OMZ edges, but depressed densities and low diversity in the OMZ core, where oxygen concentration is lowest. Taxa most tolerant of severe oxygen depletion (Ͻ0.2 ml l Ϫ1 ) in seafloor OMZs include calcareous foraminiferans, nematodes, and annelids. Agglutinated protozoans, harpacticoid copepods, and calcified invertebrates are typically less tolerant. High dominance and relatively low species richness are exhibited by foraminiferans, metazoan meiofauna, and macrofauna within OMZs. At dissolved oxygen concentrations below 0.15 ml l Ϫ1 , bioturbation is reduced, the mixed layer is shallow, and chemosynthesis-based nutrition (via heterotrophy and symbiosis) becomes important.OMZs represent a major oceanographic boundary for many species. As they expand and contract over geological time, OMZs may influence genetic diversity and play a key role in the evolution of species at bathyal depths. These ecosystems may preview the types of adaptations, species, and processes that will prevail with increasing hypoxia over ecological and evolutionary time. However, many questions remain unanswered concerning controls on faunal standing stocks in OMZs, and the physiological, enzymatic, metabolic, reproductive and molecular adaptations that permit benthic animals to live in OMZs. As global warming and eutrophication reduce oxygenation of the world ocean, there is a pressing need to understand the functional consequences of oxygen depletion in marine ecosystems.

Adaptive strategies of sponges to deoxygenated oceans

“…The experimental chamber effect was included to address pseudo-replication. For these models, fixed-and randomeffect terms were tested using the function anova and ranova (R package lmerTest; Kuznetsova et al, 2017), respectively, whilst post hoc pairwise comparisons were computed on estimated marginal means using emmeans (R package emmeans; Lenth, 2021). The ratio of expanded papillae in P. crocea from experiment 2 and expansion ratio in S. australiensis from experiment 3 were investigated using repeated-measure univariate PERMANOVA (Anderson, 2001(Anderson, , 2014 because it did not meet the normality assumption for mixed-effects models.…”

Similar fish species composition despite larger environmental heterogeneity during severe hypoxia in a coastal ecosystem

“…The observed shifts in the relative occurrence frequency from the bottom to surface waters during hypoxia can be a result of upward movements of individuals or higher mortality in the bottom (Diaz & Rosenberg, 2008; Levin, 2003). As fish are highly mobile, they can respond sharply to the environmental changes by avoiding unfavorable conditions.…”

“…Specifically, the reduced concentration of DO in the bottom water to a critical level imposes extreme stress for demersal organisms, such as increased mortality rates (Hrycik et al, 2017; Levin, 2003). Therefore, the species‐sorting paradigm (Figure 1a) expects that species that do not possess morphological or physiological traits adapted to the hypoxic conditions are likely to be filtered out from the bottom water (Bickler & Buck, 2007; Kodama & Horiguchi, 2011; Levin, 2003), and different species composition between bottom and surface water is expected during that season. In contrast, it is also probable that the bottom hypoxia was so intense that many species suffer from it or actively avoid it to a similar extent (Eby & Crowder, 2002; Pihl et al, 1991), and species can be apparently neutral with respect to the responses to the severe hypoxia, weakening the effect of species sorting (Figure 1b).…”

Biotic Response to Rapid Environmental Changes During the Permian–Triassic Mass Extinction

“…A recent study showed that the Northeast Pacific OMZ had expanded at a rate of 3.0 ± 0.7 m/year in the last 60 years and had lost 15% of its oxygen (Ross et al, 2020). Low oxygen levels could increase the dominance of benthos tolerant to anoxic conditions (Levin, 2003). For example, one foraminifer genus Earlandia flourished as the major "disaster form" in the MU after the first PTME pulse (Figure 9A) and probably migrated from the Chibi site during the Early Triassic transgression.…”

“…6.2 log mm 3 in the end-Permian, which fell to 5.5 log mm 3 after the mass extinction (Song et al, 2011). The reduction in size and diversity of fauna with calcified skeletons have been linked to oxygen shortage in modern oceans (Byers, 1978;Levin, 2003). Laboratory experiments showed that the oxygen consumption rate increased significantly in foraminiferal specimens larger than 250 mm (Bradshaw, 1961).…”