Effects of natural and human-induced hypoxia on coastal benthos

Abstract

Abstract. Coastal hypoxia (<1.42 ml L−1; 62.5 μM; 2 mg L−1, approx. 30% oxygen saturation) occurs seasonally in many estuaries, fjords, and along open coasts subject to upwelling or excessive riverine nutrient input, and permanently in some isolated seas and marine basins. Underlying causes of hypoxia include enhanced nutrient input from natural causes (upwelling) or anthropogenic origin (eutrophication) and reduction of mixing by limited circulation or enhanced stratification; combined these lead to higher surface water production, microbial respiration and eventual oxygen depletion. Advective inputs of low-oxygen waters may initiate or expand hypoxic conditions. Responses of estuarine, enclosed sea, and open shelf benthos to hypoxia depend on the duration, predictability, and intensity of oxygen depletion and on whether H2S is formed. Under suboxic conditions, large mats of filamentous sulfide oxidizing bacteria cover the seabed and consume sulfide, thereby providing a detoxified microhabitat for eukaryotic benthic communities. Calcareous foraminiferans and nematodes are particularly tolerant of low oxygen concentrations and may attain high densities and dominance, often in association with microbial mats. When oxygen is sufficient to support metazoans, small, soft-bodied invertebrates (typically annelids), often with short generation times and elaborate branchial structures, predominate. Large taxa are more sensitive than small taxa to hypoxia. Crustaceans and echinoderms are typically more sensitive to hypoxia, with lower oxygen thresholds, than annelids, sipunculans, molluscs and cnidarians. Mobile fish and shellfish will migrate away from low-oxygen areas. Within a species, early life stages may be more subject to oxygen stress than older life stages. Hypoxia alters both the structure and function of benthic communities, but effects may differ with regional hypoxia history. Human-caused hypoxia is generally linked to eutrophication, and occurs adjacent to watersheds with large populations or agricultural activities. Many occurrences are seasonal, within estuaries, fjords or enclosed seas of the North Atlantic and the NW Pacific Oceans. Benthic faunal responses, elicited at oxygen levels below 2 ml L−1, typically involve avoidance or mortality of large species and elevated abundances of enrichment opportunists, sometimes prior to population crashes. Areas of low oxygen persist seasonally or continuously beneath upwelling regions, associated with the upper parts of oxygen minimum zones (SE Pacific, W Africa, N Indian Ocean). These have a distribution largely distinct from eutrophic areas and support a resident fauna that is adapted to survive and reproduce at oxygen concentrations <0.5 ml L−1. Under both natural and eutrophication-caused hypoxia there is loss of diversity, through attrition of intolerant species and elevated dominance, as well as reductions in body size. These shifts in species composition and diversity yield altered trophic structure, energy flow pathways, and corresponding ecosystem services such as production, organic matter cycling and organic C burial. Increasingly the influences of nature and humans interact to generate or exacerbate hypoxia. A warmer ocean is more stratified, holds less oxygen, and may experience greater advection of oxygen-poor source waters, making new regions subject to hypoxia. Future understanding of benthic responses to hypoxia must be established in the context of global climate change and other human influences such as overfishing, pollution, disease, habitat loss, and species invasions.

Climate change and dead zones

“…Dead zones created by the depletion of dissolved oxygen in coastal waters are one of the most widespread and detrimental anthropogenic threats to marine ecosystems worldwide and have been doubling in occurrence each decade since the mid-1900s (Diaz, 2001;Diaz & Rosenberg, 2008;Vaquer-Sunyer & Duarte, 2008;Gooday et al, 2009;Rabalais et al, 2010). Dead zones have significant consequences for the biodiversity and functioning of marine ecosystems and the services they provide to society, including fisheries production, water column filtration, and nutrient cycling (Altieri & Witman, 2006;Breitburg et al, 2009;Conley et al, 2009;Levin et al, 2009;Diaz & Rosenberg, 2011). The exponential increase in the number, size, and severity of dead zones is linked to higher rates of nutrient inputs, making the dead zone epidemic one of the strongest arguments for controlling eutrophication (Diaz & Rosenberg, 2008;Gooday et al, 2009;Rabalais et al, 2010).…”

Coastal hypoxia and sediment biogeochemistry

“…100 µM) (Vaquer-Sunyer and Duarte, 2008;Levin et al, 2009a, b). At the most fundamental levels, a shift from normoxia to hypoxia will result in migration (away) of large, mobile invertebrates, mortality of selected taxa, emergence and a shallowing of infaunal activities within the sediment column of all but the most hypoxia-tolerant taxa (Pihl et al, 1992;Rabalais et al, 2001a, b; see also Levin et al, 2009). Hypoxia lowers the density and biomass of megafaunal-and selected macrofaunal-size organisms, leading to a smaller community body-size structure (Levin 2003;Quiroga et al, 2005).…”

“…To understand faunal diversity effects on sediment biogeochemistry therefore requires unraveling the effect of fauna on microbes via transport processes and food-web interactions (bacterial grazing), and understanding the feedback of microbes on faunal functioning. For instance, sulphate-reducing microbes generate sulphide that is toxic for many animals or that may impede their functioning (Hargraves et al, 2008), while reduced sulphur oxidizing or sulphur disproportionating bacteria detoxify the sediment so that is habitable for animals (Pearson and Rosenberg, 1978;Levin et al, 2009). Before we can understand the effect of oxygen via metazoan diversity on sediment biogeochemistry, it is necessary to elucidate the many trophic, competitive and non-competitive interactions between fauna and microbes (e.g.…”

“…Naqvi et al (2009) discuss the production and emission of radiatively active gases from hypoxic areas. Levin et al (2009) review the effect of natural and human-induced hypoxia on benthic communities and Kemp et al (2009) discuss coastal-hypoxia responses to remediation. These complementary issues will not be repeated here.…”

Biotic replacement and mass extinction of the Ediacara biota

“…R. Soc. B 282: 20151003 or small-sized organisms with reduced oxygen requirements [35,36]. Communities with high organic carbon loading also generally exhibit low evenness.…”