Hypoxia tolerance of the mummichog: the role of access to the water surface

Abstract

Low dissolved oxygen (DO) had a significant effect on specific growth rate (GS), length increment (IL) and haematocrit (Hct) of the mummichog Fundulus heteroclitus. Regardless of access to the water surface, F. heteroclitus maintained high growth rates (GS and IL) at DO concentrations as low as 3 mg O2 l−1. With access to the water surface, both GS and IL of F. heteroclitus decreased by c. 60% at 1·0 mg O2 l−1 compared to all higher DO treatments. When denied access to the water surface, a further decrease in GS (c. 90%) and IL (c. 75%) was observed at 1 mg O2 l−1. There was no effect of diel‐cycling DO (1–11 mg O2 l−1) with or without surface access on GS, IL or Hct of F. heteroclitus. Similar trends between GS and faecal production across DO treatments suggest that decreased feeding contributed significantly to the observed decrease in growth rate. Haematocrit was significantly elevated at 1 mg O2 l−1 for fish with and without access to the water surface. Increased Hct, however, was not sufficient to maintain high GS or IL at severely low DO. When permitted to respire in the surface layer, however, F. heteroclitus was capable of maintaining moderate growth rates at DO concentrations of 1 mg O2 l−1 (c. 15% saturation). Although aquatic surface respiration (ASR) was not quantified in this study, F. heteroclitus routinely swam in contact with the water surface and performed ASR at DO concentrations ≤3 mg O2 l−1. No hypoxia‐related mortality was observed in any DO or surface access treatment for as long as 9 days. This study demonstrates that surface access, and thus potential for ASR, plays an important role in providing F. heteroclitus substantial independence of growth rate over a wide range of low DO conditions commonly encountered in shallow estuarine environments.

Distinct physiological strategies are used to cope with constant hypoxia and intermittent hypoxia in killifish (Fundulus heteroclitus)

“…This is starkly contrasted by the extensive literature on intermittent hypoxia in mammals, which has uncovered widespread physiological, developmental and genomic consequences that are distinct from continuous hypoxia exposure (Neubauer, 2001;Douglas et al, 2007;Farahani et al, 2008). There is evidence that exposure to repeated bouts of hypoxia compromises growth in some fish species (Atlantic salmon, Salmo salar, and southern catfish, Silurus meridionalis) but not others (spot, Leiostomus xanthurus, and killifish, Fundulus heteroclitus) (Stierhoff et al, 2003;McNatt and Rice, 2004;Burt et al, 2013;Yang et al, 2013). Exposure to daily oxygen cycles has been observed to increase hypoxia tolerance and aerobic swimming performance in hypoxia in southern catfish (Yang et al, 2013), to increase resting metabolism measured in normoxia in summer flounder (Paralichthys dentatus) (Taylor and Miller, 2001), and to reduce red blood cell GTP concentration and increase plasma bicarbonate concentration in carp (Cyprinus carpio) (Lykkeboe and Weber, 1978).…”

“…We examined the killifish F. heteroclitus, an estuarine species that copes with both seasonal and daily fluctuations in dissolved oxygen content in its native habitat (Stierhoff et al, 2003;Burnett et al, 2007;Tyler et al, 2009). These fluctuations can be sudden, severe, and are mediated by factors such as the daily interplay between photosynthesis and cellular respiration, tidal movements, temperature, and wind patterns (Tyler et al, 2009).…”

Diel hypoxia in marsh creeks impairs the reproductive capacity of estuarine fish populations

“…Overall energy expenditure may be suppressed or specific portions of the energy budget may be reduced, particularly growth and reproduction. In the laboratory, constant and cyclic hypoxia suppress juvenile and adult growth of estuarine fishes (Stierhoff et al 2003, McNatt & Rice 2004, Stierhoff et al 2006, Landry et al 2007). In wild fish, intermittent estuarine hypoxia reduces juvenile growth of the Atlantic croaker Micropogonias undulatus and the summer flounder Paralichthys dentatus (Eby et al 2005, Stierhoff et al 2006.…”

Regulation of pyruvate dehydrogenase in the common killifish,Fundulus heteroclitus, during hypoxia exposure.

“…Diel fluctuations in oxygen are caused by plant and animal respiration at night when no photosynthesis occurs to replenish dissolved oxygen. As a result of the environmental fluctuations in dissolved oxygen, killifish have evolved an amazing suite of adaptations to enhance hypoxia survival including modifications to behavior (48) and biochemical and molecular responses (25,37). In F. grandis, long-term hypoxia exposure led to tissue-specific phenotypes in metabolic capacity with an upregulation in glycolytic capacity (i.e., increases in enzyme activities) in liver and decreases in muscle (29).…”