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Breathing air in water and in air: The air-breathing fishes
Abstract
Introduction air breathing is an auxiliary respiratory mode utilized by some fishes when environmental factors such as exposure to hypoxic water or emergence impede aquatic respiration. All of the 28, 000 living fish species use gills to exchange o2 and co2 with their aqueous environment. However, nearly 400 species, distributed among 50 families and spanning 17 orders of bony fishes (Osteichthyes), are known to be capable of breathing air. Air breathing enables these fishes to survive in and occupy habitats in which aquatic respiration cannot be used to sustain aerobic metabolism. Among all air-breathing fishes, the principal causal factor associated with this specialization is exposure, at some point during their life history, to either chronic or periodic environmental hypoxia. A chapter on air breathing in fishes is essential for a book about vertebrate adaptation to hypoxia, because fishes are the basal vertebrates and were also the first vertebrates to breathe air (Graham, 1997). The recent literature contains substantive accounts of the adaptations for air breathing (Graham, 1997; Graham, 1999; Graham, 2006) and emersion from water (Sayer, 2005) in fishes. Using three cases studies, this chapter shows how both hypoxia and aerial o access have shaped the behavior, physiology, and natural history of different fish groups. Oxygen and water with the increasing overlap in disciplines such as comparative physiology, field ecology, and environmental biology, there is a need for precise quantitative terminology describing the properties of water affecting respiration.
... Many teleost fish resort to air-breathing in hypoxic and warm tropical waters and this ability has evolved independently more than 80 times [1]. These multiple appearances have resulted in a variety of air-breathing organs (ABOs), which have typically evolved as modifications or extensions of existing organs [2][3][4]. The dependence on air-breathing in fish falls along a spectrum ranging from obligate air-breathers that will drown without access to air in normoxic water to facultative air-breathers that may only access the air-phase when water hypoxia is deep enough to prevent sufficient aquatic oxygen uptake [5]. ...
... It is generally agreed that irrespective of how an air-breathing fish takes up oxygen it will excrete most of the produced CO 2 to the water-phase as a consequence of the much higher CO 2 solubility than O 2 solubility in water [2,[8][9][10][11][12][13][14]. Thus, it has been argued repeatedly that with the undivided fish heart and associated circulation, airbreathing fish must suffer branchial loss of aerially sourced oxygen when residing in sufficiently hypoxic water [2,3,[15][16][17]. However, it has also been argued that there must be strong selective pressure to reduce this loss because of the importance of oxygen in ATP production [2,18]. ...
In hypoxia, air-breathing fish obtain O2 from the air but continue to excrete CO2 into the water. Consequently, it is believed that some O2 obtained by air-breathing is lost at the gills in hypoxic water. Pangasionodon hypophthalmus is an air-breathing catfish with very large gills from the Mekong River basin where it is cultured in hypoxic ponds. To understand how P. hypophthalmus can maintain high growth in hypoxia with the presumed O2 loss, we quantified respiratory gas exchange in air and water. In severe hypoxia (PO2: ≈ 1.5 mmHg), it lost a mere 4.9% of its aerial O2 uptake, while maintaining aquatic CO2 excretion at 91% of the total. Further, even small elevations in water PO2 rapidly reduced this minor loss. Charting the cardiovascular bauplan across the branchial basket showed four ventral aortas leaving the bulbus arteriosus, with the first and second gill arches draining into the dorsal aorta while the third and fourth gill arches drain into the coeliacomesenteric artery supplying the gut and the highly trabeculated respiratory swim-bladder. Substantial flow changes across these two arterial systems from normoxic to hypoxic water were not found. We conclude that the proposed branchial oxygen loss in air-breathing fish is likely only a minor inefficiency.
... Most of the fishes in the Gillichthys clade inhabit shallow coastal to estuarine environments. Gillichthys mirabilis is well known for its facultative air-breathing (Graham & Wegner, 2010;Todd & Ebeling, 1966), and species of Quietula may also possess this ability (Todd & Ebeling, 1966). Typhlogobius is a blind goby living secretively under rocks, in holes in rocks, and in kelp beds in shallow water (Froese & Pauly, 2023). ...
Otoliths are common and diverse in the Neogene of tropical America. Following previous studies of Neogene tropical
American otoliths of the lanternfishes (Myctophidae), marine catfishes (Ariidae), croakers (Sciaenidae), and cuskeels
(Ophidiiformes), we describe here the otoliths of the gobies (Gobiidae). The Gobiidae represent the richest
marine fish family, with more than 2000 species worldwide and about 250 in America. In the fossil record too they
are the species richest family in the Neogene of tropical America. We have investigated otoliths sampled from Ecuador,
Pacific and Atlantic Panama, Atlantic Costa Rica, Dominican Republic, Venezuela, and Trinidad, ranging in age
from late Early Miocene (late Burdigalian) to late Early Pleistocene (Calabrian). Most of the studied material originates
from the collection expeditions of the Panama Paleontology Project (PPP). Our study represents the first comprehensive
record of fossil gobies from America, and we recognize 107 species, of which 51 are new to science, 35 are
in open nomenclature, and 19 represent species that also live in the region today. Previously, only two fossil otolithbased
goby species have been described from the Neogene of tropical America. The dominant gobies in the fossil
record of the region are from the Gobiosomatini, particularly of genera living over soft bottoms or in deeper water
such as Bollmannia, Microgobius, Antilligobius, and Palatogobius. Another purpose of our study is to provide a first
comprehensive account of otoliths of the extant Gobiidae of America, which we consider necessary for an adequate
identification and interpretation of the Neogene otoliths. We studied otoliths of 130 extant American gobiid species
and figured 106 of them for comparison. We also present a morphological analysis and characterization of the extant
otoliths as a basis for the identification of fossil otoliths. Problems that commonly arise with the identification of fossil
otoliths and specifically of fossil goby otoliths are addressed and discussed. A comparison of the history of the Gobiidae
in tropical America reveals a high percentage of shared species between the Pacific and the Atlantic basins
during the Late Miocene (Tortonian and Messinian) from at least 11 to 6 Ma. A recording gap on the Pacific side
across the Pliocene allows a comparison again only in the late Early Pleistocene (Calabrian, 1.8 to 0.78 Ma), which
shows a complete lack of shared species. These observations support the effective closure of the former Central
American Seaway and emersion of the Isthmus of Panama in the intervening time. Groups that today only exist
in the East Pacific were also identified in the Miocene and Pliocene of the West Atlantic, and there is also at least one
instance of a genus now restricted to the West Atlantic having occurred in the East Pacific as late as the Pleistocene.
The evolution of gobies in tropical America and the implications thereof are extensively discussed. Furthermore,
observations of fossil gobies in the region are discussed in respect to paleoenvironmental indications and paleobiogeographic
aspects.
... For air-breathing fish, we preferred regressions based on bimodal respiration (i.e. aquatic + aerial) when available, as this is their normal behaviour in nature (Graham & Wegner, 2010). We excluded regressions measured in fish larvae only, given that this life stage exhibits different metabolic influences from those on non-larval stages (Glazier, 2005), related to exponential growth and high surface-area of respiratory organs (Post & Lee, 1996). ...
Metabolism underpins all life‐sustaining processes and varies profoundly with body size, temperature and locomotor activity. A current theory explains some of the size‐dependence of metabolic rate (its mass exponent, b) through changes in metabolic level (L). We propose two predictive advances that: (a) combine the above theory with the evolved avoidance of oxygen limitation in water‐breathers experiencing warming, and (b) quantify the overall magnitude of combined temperatures and degrees of locomotion on metabolic scaling across air‐ and water‐breathers. We use intraspecific metabolic scaling responses to temperature (523 regressions) and activity (281 regressions) in diverse ectothermic vertebrates (fish, reptiles and amphibians) to show that b decreases with temperature‐increased L in water‐breathers, supporting surface area‐related avoidance of oxygen limitation, whereas b increases with activity‐increased L in air‐breathers, following volume‐related influences. This new theoretical integration quantitatively incorporates different influences (warming, locomotion) and respiration modes (aquatic, terrestrial) on animal energetics.
... While Hughes' chapter contains only a relatively short summary of this work, the diversity of such fish air-breathing organs adds to the rich tapestry of morphological and physiological specialization that excites researchers in the field of comparative physiology. Indeed, Hughes's works not only inspired my career trajectory, but also that of my previously mentioned graduate advisor, Jeffrey Graham, who became one of the world's authorities on the respiratory physiology of air-breathing fishes (Graham, 1997(Graham, , 2006Graham and Wegner, 2010). ...
... This respiratory behavior may be a response to reduce the cost of gill ventilation under stressful hypoxic conditions (Da Cruz et al., 2013). Under extremely low O 2 levels, airbreathing fishes typically increase their reliance on air-breathing and minimize aquatic ventilation as mechanisms to minimize transbranchial O 2 loss (Bicudo & Johansen, 1979;Graham & Wegner, 2010;Johansen, 1970). In water-breathing fishes, osmoregulation and ionoregulation are important functions of the gills that typically suffer under hypoxic conditions, but this problem might be minimized in airbreathing fishes because of a combination of smaller functional gill surface areas and only slight increases in fv (Burleson et al., 1998). ...
Air‐breathing in fish is believed to have arisen as an adaptation to aquatic hypoxia. Although air‐breathing has been widely studied in numerous fish species, little is known about the obligate air‐breathing African bonytongue, Heterotis niloticus. We evaluated if abiotic factors and physical activity affect air‐breathing patterns in fingerlings. The air‐breathing frequency (fAB) and behavioral responses of H. niloticus fingerlings were assessed in response to environmental oxygen, temperature, and exhaustion and activity in a series of experiments. The air‐breathing behavior of H. niloticus fingerlings under optimum water conditions was characterized by swift excursions lasting less than 1 s to the air–water interface to gulp air. The intervals between air‐breaths were highly variable, ranging from 3 to 259 s. Body size only slightly affected fAB, while hypoxia, hyperthermia, and exercise stress significantly increased fAB. Progressive hypoxia from 17.69 to 2.17 kPa caused a ~2.5‐fold increase in fAB. Increasing temperatures to 27 and 32°C, from a baseline temperature of 22°C, significantly increased fAB from 0.4 ± 0.2 to 1.3 ± 0.5 and 1.6 ± 0.4 breaths min⁻¹, respectively. Lastly, following exhaustive exercise, fAB increased up to 3‐fold. These observations suggest that H. niloticus fingerlings are very reliant on aerial oxygen, and their air‐breathing behavior is sensitive to environmental changes and activity levels.
... air-breathers). For air-breathing fish, we preferred regressions based on bimodal respiration (i.e., aquatic + aerial) when available, as this is their normal behaviour in nature (Graham & Wegner 2010). We excluded regressions measured in fish larvae only, given that this life stage exhibits different metabolic influences from those on non-larval stages (Glazier 2005), related to exponential growth and high surface-area of respiratory organs (Post & Lee 1996). ...
Metabolism underpins all life-sustaining processes and varies profoundly with body size, temperature, and locomotor activity. Explaining variation in metabolic rates is crucial in ecology. Current theory explains the variation in body mass-scaling exponent (b) through changes in metabolic level (L), depending on whether these changes mainly affect volume (V)-or surface-area (SA)-related processes. Another theory predicts that evolved avoidance of oxygen limitation in water-breathers experiencing warming will diminish the increased respiration at large sizes. We test these predictions using intraspecific metabolic scaling responses to temperature (523 regressions) and activity (281 regressions) in diverse ectothermic vertebrates (fish, reptiles and amphibians). We show that b decreases with temperature-increased L only in water-breathers, supporting SA-related avoidance of oxygen limitation, whereas b increases with activity-increased L only in air-breathers, following V-related influences. This new quantitative theoretical integration extends explanatory power to incorporate different influences (warming, locomotion) and respiration modes (aquatic, terrestrial) on animal energetics.
... It has been suggested (140, 1035) that stable or even reduced rates of gill ventilation during aquatic hypoxia serve to minimize the loss of O 2 (gained by air-breathing) to the water. Indeed, unaltered or reduced gill ventilation during hypoxia has been reported for several air-breathing species (140,244,447,448,450,686,687,1035,1158). ...
The ectothermic vertebrates are a diverse group that includes the Fishes (Agnatha, Chondrichthyes, and Osteichthyes), and the stem Tetrapods (Amphibians and Reptiles). From an evolutionary perspective, it is within this group that we see the origin of air-breathing and the transition from the use of water to air as a respiratory medium. This is accompanied by a switch from gills to lungs as the major respiratory organ and from oxygen to carbon dioxide as the primary respiratory stimulant. This transition first required the evolution of bimodal breathing (gas exchange with both water and air), the differential regulation of O2 and CO2 at multiple sites, periodic or intermittent ventilation, and unsteady states with wide oscillations in arterial blood gases. It also required changes in respiratory pump muscles (from buccopharyngeal muscles innervated by cranial nerves to axial muscles innervated by spinal nerves). The question of the extent to which common mechanisms of respiratory control accompany this progression is an intriguing one. While the ventilatory control systems seen in all extant vertebrates have been derived from common ancestors, the trends seen in respiratory control in the living members of each vertebrate class reflect both shared-derived features (ancestral traits) as well as unique specializations. In this overview article, we provide a comprehensive survey of the diversity that is seen in the afferent inputs (chemo and mechanoreceptor), the central respiratory rhythm generators, and the efferent outputs (drive to the respiratory pumps and valves) in this group. © 2022 American Physiological Society. Compr Physiol 12: 1-120, 2022.
... The gas bladder of a few osteoglossiforms is adapted to aerial respiration as well as buoyancy regulation, sound production and reception (Graham, 1997). The ability of breathing air is seen in representatives of each family (Graham, 1997;Graham and Wegner, 2010;Moritz and Linsenmair, 2007). To breathe, A. gigas and H. niloticus use a voluminous alveolate gas bladder, whereas G. niloticus possesses a highly developed, lunglike gas bladder ( Figure 4) (Graham, 1997;Liem, 1989). ...
Osteoglossomorpha is a significant taxon for studies of evolution and various aspects of fish biology as an evolutionarily old group of fish. The taxon exhibits anatomical, morphological and physiological diversity and various adaptations such as air breathing or electroreception as well as modifications visible in sight and olfactory organs. A peculiarity of this group is the presence of four types of spermatozoa, namely complex introsperm and uni-, bi-, and aflagellate aquasperm. Given the unique morphology and large dimensions of some species, osteoglossomorphs are popular in aquaristics as ornamental fish, and in fisheries because they are an important source of food in many countries. The aim of this paper is to focus on some aspects of the biology and unique features as well as the importance for humans of this unusual group of fish.
The gas exchange function of the avian respiratory system is explained. The following important structural—and functional aspects are presented: the mechanisms of airflow through the airway (bronchial) system and the air sacs; the four-phase respiratory modus operandi of the avian respiratory system and the inspiratory and the expiratory aerodynamic valving mechanisms by which air is shunted across the airways; the physiological adaptations of coping with hypoxia and hypocapnia, especially during high altitude residence and flight; the functional significance of the physical strength of the avian lung, the air and the blood capillaries and the blood-gas barrier; the gas exchange designs, namely, the countercurrent, the crosscurrent, and the multicapillary serial arterialization systems of the avian lung and; the morphometric specializations of phylogenetically different species of birds and those that lead various lifestyles. The exceptional functional efficiency of the avian respiratory system is highlighted.
Background. Periophthalmus chrysospilos and Favonigobius reichei are most abundant gobies species (Family: Gobiidae) inhabiting estuaries in the west coast of Peninsular Malaysia. Thirty-six goby species are amphibious: the rest remain in water, like other teleosts. However, information on the fine structure of gills and skins of these gobies species that may help to understand their functions in air breathing is still lacking. This study was aimed at describing fine structure of the gills and skins of these two co-existing species of gobies living in the terrestrial and aquatic environment. Materials and Methods. Fifty-six specimens of amphibious (Periophthalmus chrysospilos) and 67 specimens of non-amphibious gobies (Favonigobius reichei) were collected from estuary. Gills and skins were dissected out and samples were treated following the standard electron microscopy sample preparation. Samples were affixed onto specimen stubs with silver paint and then coated with a thin layer of gold using a BIO-RAD-SC500 ion sputter. All samples were viewed using SEM Series XL 30, Philips. Results. P. chrysospilos possesses short, thick, bent and twisted gill filaments whereas the F. reichei has long, thin, and straight filaments. There were differences in shapes and numbers of the secondary lamellae attached to the filaments in P. chrysospilos and F. reichei. The skin of F. reichei also has a significant difference in architectural build-up compared to P. chrysospilos. The functional adaptation on the use of gills and skins in P. chrysospilos and F. reichei in natural environment are discussed. Conclusions. The gills of P. chrysospilos show some unique features (i.e. low density of secondary lamellae and smaller gill rakers) that can be used to explain the animal.s ability to successfully live out of water in comparison to F. reichei that are more adapted to aquatic life like other teleosts. Special architectural plan of gills and skins of both goby species may have contributed to their existence in the estuary area.
The chapter examines the features of the habitat that may have led to the evolution of air-breathing among amphibious intertidal fishes, and then describes the behavior and physiology of the transition from water to air in air-breathing intertidal fishes. The emergence of many species of rocky intertidal fishes into air during low tide, including adults guarding nests of eggs, must be considered an appropriate and natural behavior rather than an error or an occasional atypical excursion. Many intertidal fishes of temperate coasts can breathe air, although in the past far more attention has been paid to the most terrestrially active amphibious marine fishes, the mudskippers and rockskippers. Intertidal fishes that breathe air on occasion share certain morphological and behavioral characteristics with the more actively amphibious mudskippers and rockskippers. Remarkably, marine air-breathing fishes generally have no air-breathing organs, unlike their freshwater counterparts. Therefore, respiratory gas exchange must take place across the same surfaces in air as it does in water: the gills, the skin, and perhaps the linings of the opercular and buccal cavities.
Laboratory observations of three genera of Eleotridae (Hypseleotris-two species, Philypnodon-two species, Gobiomorphus) and 11 genera of Gobiidae (Redigobius, Pandaka, Gobiopterus, Parkraemeria, Favonigobius-two species, Pseudogobius, Arenigobius-two species, Cryptocentroides, Mugilogobius-three species, Bathygobius, Chlamydogobius) revealed four distinctive ways for survival in hypoxia. Each involved aquatic surface respiration (ASR) in which >50% of fish ventilated their gills with surface water when O2 fell below 2.1 ppm. Control of buoyancy was an important element in three of these strategies. Firstly, midwater eleotrids and gobies used ASR while swimming slowly at the surface maintaining near neutral buoyancy. Secondly, 11 species of benthic, negatively buoyant gobies performed ASR in the shallows resting on the substrate propped up on the pelvic fins with the head arched upwards to the water surface. Nine of these species held a bubble in the buccal chamber which was frequently exchanged. Thirdly, four of the above bubble-gulping species frequently took a buccal bubble of sufficient size to attain a vertical position at the surface while performing ASR. In both positions the bubble was held only when fish were using ASR and it appeared to function in providing lift to the head or body, facilitating ASR, and in addition, adding O2 to buccal water prior gill ventilation. In one benthic goby, the percentage of fish using a buccal bubble increased with an increase in salinity. Fourthly, one benthic goby used anaerobic respiration for several hours prior to using ASR.
The catfish Pangasius hypophthalmus from South-Eastern Asia uses the airbladder as an accessory respiratory organ. The airbladder is situated at the dorsal part of the body cavity and is connected with the esophagus by a short pneumatic duct lined with mucus cells. The histological and ultrastructural study reveals that the wall of the airbladder is composed of three layers: the outer layer of serosa membrane, the middle one of connective tissue with many collagen fibres, and the inner layer - the simple respiratory epithelium. The medium and inner layers form numerous septa protruding into the lumen of the airbladder. The central septum divides the airbladder longitudinally into two chambers. The respiratory epithelium consists of a single type of flat cells covering a dense capillary network. Ciliated and mucus cells are absent. Epithelial cells possess long and thin microvilli on their surface. Their cytoplasm contains a large nucleus, the Golgi apparatus, rough endoplasmic reticulum, mitochondria, and a few electron-dense and lamellar bodies accumulating surfactant. The air-blood barrier is composed of epithelium, connective tissue, and endothelium with a thickness ranging from 0.2 to 2.4 μm.
Buccal movements at the air-water interface causing surface water and air bubble inhalation ("surface breathing") and the resultant effects on blood O₂ transport have been quantified as a function of inspired water Po₂ in the goldfish, Carassius auratus. At 26 C, surface breathing occurred below a Po₂ of about 70 mmHg and increased to a peak of 180 surface breathing periods/h at Po₂ 20 mmHg. At this severe level of hypoxia, surface breathing resulted in a significant elevation of arterial Po₂ by 1.2 mmHg above that in control goldfish, which were not surface breathing. This very small rise in arterial Po₂ caused a sharp rise in arterial blood O₂ saturation from 16% to 33%, because of the high oxygen affinity () and steep slope of the blood O₂ equilibrium curve. The net effect of surface breathing at the air-water interface during severe aquatic hypoxia is a 2.5 times increase in the arterial-venous O₂ saturation difference compared with strictly aquatic ventilation. Surface breathing with a nitrogen rather than air atmosphere significantly increased surface-breathing frequency and significantly decreased arterial blood oxygenation at a constant water Po₂. Surface breathing, which includes both "air gulping" and irrigation of the gills with the surface water layer, is thus demonstrated to have a significant respiratory function in the goldfish.