Gill surface area and metabolic enzyme activities of demersal fishes associated with the oxygen minimum zone off California

Abstract

Metabolic enzyme activities and gill surface areas were measured across 10 species of demersal fishes from Monterey Canyon, California, which features a prominent oxygen minimum zone (OMZ). Comparisons were made between species living both within and outside of the OMZ. Enzyme activities showed no significant trend toward aerobic suppression or heightened reliance on anaerobic metabolism in response to the OMZ. While flatfish species living both within and outside of the OMZ had similarly low enzyme activities, the OMZ-dwelling Microstomus pacificus had 1.8-3 times larger gill surface area than comparably sized flatfishes from higher-oxygen waters, suggesting a morphological adaptation to low oxygen. In scorpaeniform fishes, high aerobic metabolism was accompanied by large gill surface areas in two routine-swimming OMZ-dwelling species (Anoplopoma fimbria and Careproctus melanurus). Low aerobic activities and small gills were found in two Sebastolobus species, suggesting a low oxygen demand resulting from a more sedentary behavior compared to other Scorpaeniformes. In gadiform fishes, no differences were measured in enzyme activity levels, but larger gill surface areas were measured in OMZdwelling Nezumia liolepis. These results indicate adaptation to low oxygen in a variety of ways that balance oxygen demand with supply, with no indication that these species rely on enhanced anaerobic metabolism. With both flatfishes and rattails, adaptation to OMZs is demonstrated through increased gill surface area.Oxygen minimum zones (OMZs) are midwater regions (200-1000 m) where dissolved oxygen levels are reduced by an order of magnitude relative to waters above and below the OMZ core, defined by a concentration of . 0.5 mL O 2 L 21 seawater (Levin 2003). While anoxic and hypoxic conditions exist temporarily in coastal margins, OMZs differ because they are temporally stable and impinge onto the continental shelf and slope.Recent data have indicated an ongoing expansion in several OMZs. Tropical OMZs have been simultaneously shoaling and deepening tens of meters over the past four decades (Stramma et al. 2010). Alaskan Gyre hypoxic waters (60 mmol L 21 ) have shoaled from 400 m to 300 m within the last five decades (Whitney et al. 2007). Additionally, California Current system dissolved oxygen levels have dropped, with the hypoxic boundary shifting 90 m vertically in the last three decades (Bograd et al. 2008).Given these recent expansions, there is a heightened importance in understanding how species living both within and nearby OMZs are adapted to low oxygen. Some benthic and midwater taxa associated with OMZ cores have been studied and exhibit adaptations to aerobically meet requirements for routine metabolism in low oxygen (Childress and Seibel 1998). However, little information is available to characterize how demersal fish species may react to changes in ambient oxygen concentrations.Fishes can cope with persistently low oxygen through two theoretical mechanisms that are not mutually exclusive: increased oxy...

Occurrence of demersal fishes in relation to near‐bottom oxygen levels within the California Current large marine ecosystem

“…Friedman et al . () noted that fishes cope with low oxygen through two mechanisms that are not mutually exclusive: increased oxygen extraction from the environment (continued normal behavior) and reduced oxygen demand (i.e., either reduced activity levels or elevated anaerobic metabolism; Childress and Seibel, ). The first method involves enhanced extraction of DO via increased gill surface areas, increased efficiency of hemoglobin and increased hemoglobin concentration.…”

“…The increased ventilator surface area has repeatedly been reported for fishes living in OMZs (Yang et al ., ; Childress and Seibel, ; Friedman et al ., ), whereas anaerobic metabolism is considered unlikely, based on documented aerobic enzyme activities (Yang et al ., ; Childress and Seibel, ; Seibel, ; Friedman et al ., ). Species able to regulate oxygen consumption down to very low concentrations include black hagfish (Drazen et al ., ), shortspine thornyhead (Yang et al ., ) and Dover sole (Friedman et al ., ), all OMZ inhabitants. The OMZ‐dwelling Dover sole had a two to three times larger gill surface area than comparably‐sized flatfishes from higher‐oxygen waters, suggesting a morphological adaptation to low oxygen (Friedman et al ., ).…”

“…Species able to regulate oxygen consumption down to very low concentrations include black hagfish (Drazen et al ., ), shortspine thornyhead (Yang et al ., ) and Dover sole (Friedman et al ., ), all OMZ inhabitants. The OMZ‐dwelling Dover sole had a two to three times larger gill surface area than comparably‐sized flatfishes from higher‐oxygen waters, suggesting a morphological adaptation to low oxygen (Friedman et al ., ).…”

“…Unlike flatfishes, Friedman et al . () found low aerobic activities and small gills in two thornyhead species ( Sebastolobus ), suggesting a low oxygen demand commensurate with a more sedentary behavior compared to other fishes. Although very few rockfishes from the genus Sebastes have been examined for response to low oxygen, Friedman et al .…”

Respiratory toxicity of cyanobacterial aphantoxins from Aphanizomenon flos-aquae DC-1 in the zebrafish gill

“…Gills are supplied by a large blood flow and can serve as an uptake site for toxic chemicals. Therefore, direct pollutants or toxicant-induced abnormalities are often encountered in the gills (Friedman et al, 2012;Jindal and Kaur, 2014). Since the toxic effects of harmful algal blooms can threaten human health and environment safety, there is a need for continued research on this matter.…”