Breaking wind to survive: fishes that breathe air with their gut

Abstract

Several taxonomically disparate groups of fishes have evolved the ability to extract oxygen from the air with elements of their gut. Despite perceived difficulties with balancing digestive and respiratory function, gut air breathing (GAB) has evolved multiple times in fishes and several GAB families are among the most successful fish families in terms of species numbers. When gut segments evolve into an air-breathing organ (ABO), there is generally a specialized region for exchange of gases where the gut wall has diminished, vascularization has increased, capillaries have penetrated into the luminal epithelium and surfactant is produced. This specialized region is generally separated from digestive portions of the gut by sphincters. GAB fishes tend to be facultative air breathers that use air breathing to supplement aquatic respiration in hypoxic waters. Some hindgut breathers may be continuous, but not obligate air breathers (obligate air breathers drown if denied access to air). Gut ABOs are generally used only for oxygen uptake; CO₂ elimination seems to occur via the gills and skin in all GAB fishes studied. Aerial ventilation in GAB fishes is driven primarily by oxygen partial pressure of the water (PO₂) and possibly also by metabolic demand. The effect of aerial ventilation on branchial ventilation and the cardiovascular system is complex and generalizations across taxa or ABO type are not currently possible. Blood from GAB fishes generally has a low blood oxygen partial pressure that half saturates haemoglobin (p50) with a very low erythrocytic nucleoside triphosphate concentration [NTP]. GAB behaviour in nature depends on the social and ecological context of the animal as well as on physiological factors.

Oxygen consumption rate v. rate of energy utilization of fishes: a comparison and brief history of the two measurements

“…Certainly one major assumption of indirect calorimetry, that of net aerobiosis, does not apply to the gut microbiome of many fishes. Nelson (), however, mentions the untested idea that the gut microbial community of fishes that breathe air with their digestive tract would have to be aerobic or at least microaerophiles. Considering the inevitable proliferation of oxygen consumption studies following the advent of optodes, it may be time to start considering O 2 as its own measurement and not a surrogate for metabolic rate.…”

Cytotoxic Effect of MTH1 Gene Silencing in Gemcitabine Resistant Breast Cancer Cells

“…Some accessory air-breathing organs are located in the digestive tract, such as the esophagus, stomach and gut (Podkowa and Goniakowska-Witalinska, 2002). Gut air-breathing as an accessory respiratory approach are mainly subordinate to Cobitidae and Callichthyidae (Nelson, 2014). Studies of the gut airbreathing of fish such as Misgurnus anguillicaudatus (Goncalves et al, 2007), Lepidocephalichthys guntea (Moitra et al, 1989), Hoplosternum thoracatum (Huebner et al, 1978), Corydoras aeneus (Podkowa et al, 2002) have been reported.…”

Air‐breathing fishes

“…Nelson () offers a wide‐ranging review of the physiology of the taxonomically disparate groups of teleosts that obtain oxygen from air through portions of their gut. Although such adaptations might be expected to engender serious trade‐offs with digestive function, this method of air breathing has evolved multiple times and several gut air‐breathing families are very speciose.…”

“…Among the reviews, two focus on particular groups of air-breathing species, four focus on particular aspects of the physiology of air-breathing in general, and the final review considers the increasing importance of air-breathing fishes in global aquaculture. Nelson (2014) offers a wide-ranging review of the physiology of the taxonomically disparate groups of teleosts that obtain oxygen from air through portions of their gut. Although such adaptations might be expected to engender serious trade-offs with digestive function, this method of air breathing has evolved multiple times and several gut air-breathing families are very speciose.…”

“…Physiological adaptations for air breathing have evolved multiple times in bony fishes and have fascinated researchers for well over a century (Poey, ; Dobson, ; Wilder, ; Day, ; Das, ; Carter & Beadle, ). Currently around 450 species are known to have some capacity to obtain oxygen from atmospheric air, although many of these belong to poorly described families, such as the neotropical loricarids (Nelson, ); so this number is certainly an underestimate of the true total.…”