AIR-BREATHING FISHES | The Biology, Diversity, and Natural History of Air-Breathing Fishes: An Introduction

PHYSIOLOGICAL SPECIALIZATIONS OF DIFFERENT FISH GROUPS Air-Breathing Fishes Contents The Biology, Diversity, and Natural History of Air-Breathing Fishes: An Introduction

Respiratory Adaptations for Air-Breathing Fishes

Circulatory Adaptations for Air-Breathing Fishes

The Biology, Diversity, and Natural History of Air-Breathing Fishes: An Introduction JB Graham, University of California at San Diego, La Jolla, CA, USA ª 2011 Elsevier Inc. All rights reserved.

Introduction The Diversity of Fish Air Breathing The Types of Air-Breathing Fishes The Evolution of Air Breathing

Glossary Air-breathing organ (ABO) A structure or body surface of a fish having the specialized structural capacity for aerial gas exchange; utilized by air-breathing fishes to supplement the normal respiratory mode which is aquatic respiration using gills. Amphibious air breathing The mode of air breathing when a fish is out of water. Aquatic surface respiration (ASR) A hypoxia-driven behavior in which a fish surfaces and places its the mouth as close to the water surface as possible in order to ventilate the gills with the upper few millimeters of water that remains well oxygenated because of atmospheric diffusion. Autapomorphy A specialization unique to one group and thus not useful for establishing relationships. Bimodal respiration The capacity to exchange respiratory gases in both air and water and to do so either simultaneously or sequentially. Continuous air breathing The frequent and regular occurrence of air gulping, even when aquatic oxygen levels are sufficient to sustain aquatic respiration. This behavior often indicates the use of ABO gas for functions other than respiration such as buoyancy.

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Air Breathing and Natural History Summary Further Reading

Facultative air breathing Emergency aquatic air breathing initiated in response to a diminished capacity for aquatic respiration usually associated with aquatic hypoxia or some other stress factor. Hypoxia-inducible factor (HIF-1�) Integrated hypoxia response that activates genes whose protein products either increase O2 transfer (i.e., erythropoiesis, Hb affinity increases, angiogenesis, etc.) or upregulate metabolic adaptation by regulating anaerobiosis and O2 consumption rate. HIF-1� induction is an ancient adaptation that first appeared in eukaryotic cells and thus long preceded the origin of metazoans. Lung The principal aerial respiratory organ of all vertebrates and some primitive air-breathing fishes. An outpocketing along the vertebrate digestive tube having a vascular epitheilial surface that functions for aerial gas exchange through its connection to the body surface by a duct through which air can be inhaled and exhaled. Obligatory air breathing A high degree of physiological dependence on air breathing for the maintenance of basal oxidative processes or to prevent suffocation. This is usually associated with a reduction in gill surface area that occurs with progressive specialization for air breathing.

Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes

Physoclistous gas bladder A gas-filled structure within the body of the fish that has lost its connection to the body surface and thus cannot function for gas exchange but retains functions for buoyancy and either or both sound production and sound reception. Physostomous gas bladder A gas-filled structure within the body of a fish that is connected to the body surface by the pneumatic duct that allowing inflation or deflation. In different fishes, functions of this organ may include aerial respiration as well as buoyancy and both sound reception and production. Placoderm Armored Paleozoic fish that were the first vertebrates to have jaws.

Introduction All of the over 28 000 living fish species use gills to exchange O2 and CO2 with water (see also Gas Exchange: Respiration: An Introduction). However, some fishes are also bimodal breathers, that is, they have the capacity to respire aerially as well as aquatically. This most usually happens when the water in which a fish lives becomes hypoxic (i.e., lower than atmospheric O2 partial pressure). Because air has both a greater and less variable quantity of oxygen than water, some species have evolved the capacity to use aerial oxygen. Air breathing is an auxiliary respiratory mode that enables a fish to live in hypoxic waters or to become amphibious and to perhaps further utilize the mechanical processes integral to this adaptation in the augmentation of functions such as buoy­ ancy, sound reception or production, and reproduction. Air breathing is an ancient trait that first evolved in fishes and has played a significant role in vertebrate evolu­ tion. Not only were fishes the first vertebrates to breathe air, it was an air-breathing, lobe-finned fish that gave rise to the Tetrapodomorpha – a group that lived in shallow water, developed an amphibious capacity, invaded the land in the late Devonian period (360 million years ago, mya), and became the ancestors of all tetrapods. While air breathing is an ancient fish trait, it has also evolved in a number of derived fish groups, including the modern teleosts. The objective of this article is to develop a biological synthesis of fish air breathing that examines the evolution and diversity of this adaptation and the ways it has con­ tributed to the survival, radiation, and natural history of different species. This perspective sets the stage for sub­ sequent articles on the structure and function of fish airbreathing organs (ABOs; see also Air-Breathing Fishes: Respiratory Adaptations for Air-Breathing Fishes) and on how the blood circulation of air-breathing fishes is

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Plesimorphy A primitive trait. Pneumatic duct Tube linking the pharynx to either the lung or physostomous gas bladder which functions for the passage of air for either air breathing, volume control, or both. Synapomorphy A specialized trait shared by two or more groups, which implies that an ancestral group also possessed this trait. Tetrapodomorpha The group of vertebrates consisting of the tetrapods (four-limbed vertebrates) and their closest sarcopterygian (lobefin fish) relatives which invaded the land during the Devonian period.

modified for the transport of respiratory gases between the body tissues and both aerial and aquatic gas-exchange surfaces (see also Air-Breathing Fishes: Circulatory Adaptations for Air-Breathing Fishes, Design and Physiology of Arteries and Veins: Anatomical Pathways and Patterns, Branchial Anatomy, Circulation: Circulatory System Design: Roles and Principles, and Design and Physiology of the Heart: The Coronary Circulation).

The Diversity of Fish Air Breathing Phylogeny and Diversity An understanding of the evolutionary relationships of fishes is required to comprehend the evolution and diver­ sity of air breathing as well as the structure and function of fish ABOs. The phylogenetic relationship of the families of air-breathing fishes is shown in Figures 1(a) and 1(b). Air breathing occurs only in the bony fishes (Osteichthyes) where it is found in nearly 400 species distributed among approximately 140 genera in 50 families and spanning 18 orders. The Osteichthyes have a 400-million-year-old history and air breathing was present in many, if not all, of the earliest bony fishes and predated the Silurian (438–408 mya) separation of this group’s two subdivisions: the Sarcopterygii (lobefins) and Actinopterygii (rayfins). The broad phyletic distribution of the air-breathing fishes suggests that this adaptation is autapomorphic, meaning that it evolved independently in many groups. Assuming that the lack of an air-breathing synapomorphy (the absence of this specialization in the common ances­ tors of many of the groups that have it) indicates the independent origin of air breathing; then this adaptation has evolved independently at least 38 times in the bony fishes. Or, if it is further assumed that air breathing evolved independently among many of the species that

1852 Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes (a)

Pygidium+

Ancistrus* Clarias*+ Pangasius* Hoplosternum*+ Bunocephalus Heteropneustes* Lithoxus

Arapaima Pantodon Gymnarchus Notopterus*+ Brevimyrus? Hypopomus* Phractoleamus

Megalops* Lepidosiren

Protopterus*

Lepidogalaxias

Erythrinus*+

Gymnotus Electrophorus

Osteoglossiformes Amia Neoceratodus

Misgurnis* Piabucina+

Gonorynchiformes Characiformes Anguilla* Cypriniformes Gymnotiformes Siluriformes

Osteoglossomorpha Elopomorpha

Polypterus*+

Neochanna*+ Umbra*+

Salmoniformes

Ostariophysi Protacanthopterygii

Lepisosteus*+

Neoteleostei Euteleostei Halecomorphi Ginglymodi

Tetrapoda Cladistia

Teleostei

Halecostomi Neopterygii

Actinopterygii

Sarcopterygii

(b)

Xiphister*

Helcogramma*

Apodichthys*

Andamia*

Dialommus

Periophthalmus*

Mastacembelus*

Dormitator Odontamblyopus* Luciocephalus Anabas*+ Helostoma

Sicyases*

Kryptolebias

Fundulus*

Clincottus*

Anabantoidei Osphronemus

Gobiesociformes Cyprinodontiformes

Paracanthopterygii

Scorpaeniformes

Acanthopterygii

Betta*+

Synbranchiformes Channiformes

Monopterus*

Synbranchus*

Channa*

Neoteleostei Figure 1 Phylogenetic arrangement of the 50 air-breathing fish families within the class Osteichthyes: (a) phylogeny from the subclass Sarcopterygii to the teleost infradivision Euteleostei, (b) infradivision Neoteleostei. (Note: Family names are replaced by the name of a genus representative of that family.) Asterisk indicates the presence of more than one air-breathing species in the specified genus. Cross indicates more than one genus of air breather in the family. Question mark indicates newer and incomplete data. Colors indicate ABO type: red, lung; blue, gas bladder; black, other structure. Modified from Graham JB (1997) Air Breathing Fishes: Evolution, Diversity and Adaptation. San Diego, CA: Academic Press.

use either a lung or a gas bladder as an ABO (see also Air-Breathing Fishes: Respiratory Adaptations for AirBreathing Fishes), then this adaptation could have independently evolved as many as 70 times. Air breathing is not known to occur in any fish group other than bony fishes. It may occur in jawless fishes as several species of lampreys make occasional amphibious excursions during upstream migration and laboratory

studies with one of these, New Zealand lamprey Geotria australis show it can respire in air and endure prolonged aerial exposure. There are no known chondrichthyan (sharks and rays) air breathers, although one species, the sand tiger shark, Odontaspis taurus, does swallow and discharge air in order to adjust its buoyancy. The only suggestion of air breathing at an earlier stage of vertebrate evolution than the Osteichthyes is the report of paired

Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes

lung-like structures in fossils of the Devonian (408–360 mya) placoderm Bothriolepis canadensis. The interpretation of these structures as lungs has remained controversial for nearly 70 years and should be resolved using high-resolution X-ray computed tomogra­ phy on some of the many well-preserved Bothriolepis fossils (there are over 70 species) residing in many museum collections. Because placoderms are ancestral to the chron­ drichthyans, the report of lungs in Bothriolepis and knowledge that no air-breathing structures occur in living chondrichthyans prompted speculation that air breathing evolved in placoderms, was lost in chondricthyans, and reappeared in the osteichthyans. Support for this hypoth­ esis has never been strong; however, in view of the extent to which the independent origin of air breathing occurs among osteichthyans, the presence of this specialization in a placoderm or an early jawless fish is not unexpected. Orthacanthus (at least three known species), a large, eel-like shark that lived in freshwater swamps during the mid- to late Paleozoic (400–225 mya), would seem a likely candi­ date for air breathing. Phylogeny and the ABO The vertebrate lung originated in fishes and is present in both the sarcopterygians (e.g., lungfish) and the actinop­ terygians (Figures 1(a) and 1(b)). In nearly all instances tetrapod evolution is linked to increased lung efficacy; however, for actinopterygians the evolutionary history of the lung took a quite different course; it became gradually transformed, first into a physostomous (remotely linked to the air via a tube, the pneumatic duct, connection to the pharynx) respiratory gas bladder, then to a nonrespiratory physostomous gas bladder, and finally to a physoclistous (no duct connection) gas bladder primarily specialized for sound reception or production, buoyancy control, or sev­ eral of these (see also Air-Breathing Fishes: Respiratory Adaptations for Air-Breathing Fishes and Buoyancy, Locomotion, and Movement in Fishes: Swimbladder Function and Buoyancy Control in Fishes). The transi­ tion from lung to gas bladder closely paralleled the adaptive radiation of actinopterygians; paired lungs occur in the primitive Cladistia (bichirs, Polypterus (P. senegalus and about 13 other species) and the ropefish, Erpetoichthys calabaricus), while respiratory gas bladders occur exclusively in the other primitive groups (Ginglymodi, gars Lepisosteus occulatus, Atractosteu sp., and about seven total species; Halecostomi, Amia calva) and even in some teleosts (Figure 1(a)). Among the Euteleostei, which includes the most highly derived bony fishes, the respiratory gas bladder is limited to the most primitive superorders Ostariophysi and Protacanthopterygii (Figure 1 (a)). The ostariophysan order Siluriformes (catfishes) illustrates the manner in which the evolutionary canalization of the gas bladder

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structure and function (e.g., in some cases being embedded in bone to augment sound reception) had proceeded to the point where this organ could not be converted, through natural selection, into an ABO in cases where environmen­ tal or climate changes or a group’s ecological radiation placed it in a habitat necessitating air breathing. Only one silurid, Pangasius (P. sutchi and at least three other species) has a respiratory gas bladder featuring a lung-like vascular or pulmonoid epithelium. Pangasius is in the family Pangasiidae which, as seen in the silurid cladogram (Figure 2), is not a basal group, is one of eight siluriform families with air-breathing species, but the only one of these having a respiratory gas bladder. This indicates the apomorphy of the pulmonoid gas bladder in Pangasius as well as the other siluriform ABOs, which occur in many genera and species in these other families and range in diversity from the buccal chamber (Bunocephalus amaurus) to the stomach (Ancistrus (¼ Liposarcus) chagresi, Hypostomus plecostomus, Pygidium striatum, and Lithoxus lithoides ), the intestine (Misgurnis anguillicaudatus, Hoplosternum thoracatum, Callichthys asper, and Corydoras aeneus), and a suprabranchial chamber with gill-derived dendrites and fans (Clarias batra­ chus and several other species) having extended pharyngeal pouches (Heteropneustes fossilis) (see also Air-Breathing Fishes: Respiratory Adaptations for Air-Breathing Fishes). Thus, and commencing with the Ostariophysi, adap­ tive specialization of the gas bladder for functions discordant with bimodal respiration led to natural selec­ tion for novel ABOs in all of the higher teleosts, especially the Neoteleostei (Figure 1(b)). Correlations between phylogeny and bimodal breathing morphology extend to the patterns of blood circulation, to the mechanisms for and the control of ABO ventilation, and to morpholo­ gical specializations (body size and shape, gill structure, and fin position) favoring amphibious life (see also Air-Breathing Fishes: Respiratory Adaptations for AirBreathing Fishes and Circulatory Adaptations for AirBreathing Fishes).

The Types of Air-Breathing Fishes Initial categorizations of air-breathing fishes were based on ABO structure (see also Air-Breathing Fishes: Respiratory Adaptations for Air-Breathing Fishes) but these had limited utility because they did not account for phylogeny, were not based on the fine-scale ABO structure, and were not inclusive of the many neoteleost air breathers lacking a well-developed ABO. A categor­ ization based on the functionality of air breathing is an efficient way of incorporating these important features and circumscribing the range of physical and ecological factors likely affecting aerial and aquatic respiration.

1854 Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes Diplomystidae Cetopsidae Pseudopimelodidae Amphiliidae Nematogenyidae Trichomycteridae (S) Callichthyidae (I) Scoloplacidae (S) Astroblepidae Loricariidae (S) Amblycipitidae Akysidae Sisoridae Erethistidae Aspredinidae (B) Heptapteridae some Bagridae Cranoglanididae Ictaluridae Ariidae Mochokidae Auchenipteridae Doradidae Siluridae Auchenoglanididae Malapteruridae Chacidae Plotosidae Clariidae (SBC) Heteropneustidae (SBC) Austroglanididae Pangasiidae (PGB) Schilbidae Claroteidae some Bagridae Pimelodidae Figure 2 Phylogenetic relationships within the order Siluriformes showing the families in which air breathing occurs (blue) and their ABO type in parentheses: B, buccal chamber; I, intestine; PGB, pulmonoid gas bladder; S, stomach; SBC, suprabranchial chamber. Modified from Graham JB and Wegner NC (2010) Breathing air in water and in air: The air-breathing fishes. In: Nilsson GE (ed.) Respiratory Physiology of Vertebrates: Life With and Without Oxygen, pp. 174–220. Cambridge: Cambridge University Press.

Aquatic Air Breathers From a functional standpoint, fish air breathing is readily classified as either aquatic or amphibious. Aquatic air breathers remain in water (although some species doing this can also be amphibious air breathers) and there are two types, facultative and continuous. Facultative air breathers normally respire aquatically and use air breath­ ing only when it is required by environmental conditions, principally hypoxia. Functional hypoxia caused by intense exercise or other stress factors can also elicit facultative air breathing. Included among many faculta­ tive air breathers are the Australian lungfish Neoceratodus forsteri, nearly all of the genera of the South American suckermouthed armored catfishes (Loricariidae, e.g., Liposarcus chagresi and many other species) and other Amazon catfishes (Gymnotus carapo, Hypopomus brevirostris, and H. occidentalis), the swamp eel (Synbranchus marmora­ tus), the salmoniforms (Umbra limi and three other species and Dallia pectoralis), the estuarine goby (Gillichthys

mirabilis), and the Asian eel goby (Odontamblyopus lacepedi and other species), which switches to air breathing only when its burrow water becomes hypoxic at low tide. Some aquatic air breathers do this regularly even in normoxic water and are termed continuous air breathers. Continuous air breathing is common in species living in habitats where hypoxic water is either a chronic or fre­ quent occurrence, and in many cases continuous air breathing is not solely for respiration but also functions to maintain the volume and wall tension of the ABO in order to serve additional and potentially multiple purposes such as buoyancy and either or both sound production and reception (e.g., featherbacks Notopterus notopterus and two other species, also Papyrocranus afer and Xenomystus nigri).

Obligate Air Breathers Although most aquatic air breathers are continuous air breathers, some are also obligatory air breathers, meaning

Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes

they completely depend on and require access to aerial oxygen and, even if they are in water that is well oxyge­ nated, they will have a reduced aerobic scope or possibly even drown if prevented from air breathing. Examples of obligatory air breathers include the four African lungfish (Protopterus atheiopicus, P. amphibius, P. annectens, and P. dolloi), the South American lungfish (Lepidosiren para­ doxa), the Amazon osteoglossid (Arapaima gigas), the African butterfly fish (Pantodon bucholzi), the Atlantic tar­ pon (Megalops atlanticus), the silurid (Pangasius sutchi), some species of clariid catfishes (but results vary, C. batrachus, C. lazera, C. gariepinus, C. macrocephalus), the armored catfish H. thoracatum, the monotypic Amazon electric knifefish (Electrophorus electricus), several anabantoids including Anabas testudinus, Osphronemus goramy, Trichogaster trichop­ terus and T. pectoralis, and Colisa fasciatus), the swamp eel (Monopterus cuchia), and probably the seven other species in this genus), and probably some of the 12–14 species of snakehead (Channa), but this has not been studied. Obligatory air breathing appears to be the consequence of developing such a proficient level of air-breathing spe­ cialization that the capacity for aquatic respiration using the gills is compromised (see also Air-Breathing Fishes: Circulatory Adaptations for Air-Breathing Fishes, Design and Physiology of Arteries and Veins: Anatomical Pathways and Patterns, Branchial Anatomy, Circulation: Circulatory System Design: Roles and Principles, Design and Physiology of the Heart: The Coronary Circulation, and Ventilation and Animal Respiration: Plasticity in Gill Morphology). An ABO that develops within the bran­ chial chamber can, for example, occlude the gills or restrict their size. Reductions in gill area can also be caused by the functional conflict between the in-series circulation typi­ cal of fishes and the positioning of the ABO. In most aquatic air breathers, oxygenated blood exits the ABO via the venous circulation and passes through both the heart and gills before entering the systemic circulation. The exposure of oxygenated blood to hypoxic water in the gills increases the potential for the trans-branchial loss of O2 and this is often countered by reduction in gill surface area or the permanent shunting of blood through nonex­ change surfaces within the gill. Amphibious Air Breathing There are three grades of amphibious air breathers: species that endure seasonal exposure in drying mud, those that endure brief stranding by a receding tide, and those that volitionally emerge from the water. Fishes subject to long-term exposure in drying mud include the African and South American lungfish (Protopterus and Lepidosiren), swamp eels (Synbranchidae), armored catfish (Liposarcus, Hypostomus, and Callichthys), anaban­ toids (Anabas and Ctenopoma), snakeheads (Channa), clariid catfishes (Clarias), and many other species,

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including non-air-breathers inhabiting lowland tropical streams that stagnate and disappear during the dry sea­ son. Many intertidal fish species including Fundulus majalis (and other species in this genus) can become trapped on land during low tide and fishes residing in congested littoral tidepools that become progressively hypoxic during low tide may, under extreme conditions, emerge from the water (e.g., the sculpins Clinocottus globiceps and Oligocottus snyderi). The estuarine mudsucker goby G. mirabilis also does this. The mangrove killifish (Kryptolebias (¼Rivulus) marmoratus and other species in this genus) occupies unique, above-the­ water-line habitats such as in leaf litter and termite burrows in floating logs. While amphibious air breathing is often associated with hypoxic stress and disappearance of water from a habitat, the natural behavior of a number of tropical and subtropical intertidal fishes such as the rockskipper Dialommus (¼Mnierpes) macrocephalus, numerous blennies (Blennius pholis, Entomacrodus nigri­ cans, Alticus kirki, and Andamia tetradactyla, there several species in each of these genera), and the mudskippers (Scartelaos histophorus, Boleophthalmus pectinirostris, Periophthalmus modestus, and Periophthalmodon schlosseri, there are numerous species in each genus) make fre­ quent terrestrial sojourns for the purpose of exploiting resources above the water line.

The Evolution of Air Breathing For the majority of air-breathing fishes a close link exists between this specialization and environmental hypoxia, suggesting that natural selection for air breathing has been driven largely by the cyclic occurrence, over geologic time, of severe environmental hypoxia (about 30–40% air saturation of water). For each group in which air breathing has evolved, selection has operated on a specific combination of factors that included genetic variation and the potential advantages in terms of inter-specific compe­ tition and ecological radiation through niche expansion afforded by increased hypoxia tolerance and air breathing. The potential interaction of these factors over time is illustrated in Figure 3. The important consequence of selection for air breathing has been to preserve or open ecological access to habitats that would otherwise be inaccessible to non­ air-breathing fishes. In terms of the mechanism for selec­ tion, the initial steps toward air breathing probably emerged from hypoxia adaptations common to non-air­ breathing fishes. A key behavioral response to hypoxia is searching for nearby water having a higher O2 concen­ tration, such as more shallow areas or at the water surface. Many non-air-breathing fishes use aquatic sur­ face respiration (ASR), a behavior in which the mouth is positioned as close to the water surface as possible in

1856 Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes 100%

Amphibious life

Normoxia

Habitat access AB reversal 70%

O2 Saturation

Moderate hypoxia 50%

HIF-1α responses ponses (AB reversal) rsal) Beh

avio

ral a

c Facultative AB

nd H

IF-1

α re

spo

Severe hypoxia 30%

Facultative AB

nse

HIF-1α responses (facultative AB)

s

Searching ASR Beaching/emersion

HIF-1α response (lessens)

Continuous AB

Obligatory AB Extreme hypoxia

VO2 Hb and O2 affinity

Other limiting factors

Anaerobic metabolism 0% Hypoxia duration Geologic time

Occasional

Seasonally recurrent

Chronically recurrent

Hours–weeks

104–106 years

107–108 years

Figure 3 Integrated aspects of environmental hypoxia adaptation and the selective mechanisms operating over different periods of time leading to the evolution of air breathing and terrestriality in different fish groups and its effect of opening limited habitats for occupation and promoting radiation and diversification. Behavioral responses such as ASR that takes a fish close to the surface increased the potential for inadvertent air gulping may have been a major selective factor in the origin of air breathing. Specialization for hypoxia and air breathing would lead to down regulation of HIF-1� response mechanisms. Modified from Graham JB and Wegner NC (2010) Breathing air in water and in air: The air-breathing fishes. In: Nilsson GE (ed.) Respiratory Physiology of Vertebrates: Life With and Without Oxygen, pp. 174–220. Cambridge: Cambridge University Press.

order to ventilate the gills with the upper few milli­ meters of water that remains O2 rich because of atmospheric diffusion. A further refinement in ASR, one that directly relates to the origin of air breathing, is gulping air which is done to increase buoyancy and place the mouth in a better position for surface ventila­ tion. Whether air is gulped intentionally or inadvertently, the O2 it contains has the potential to enrich the O2 supply and could contribute to aerobic metabolism if the bubble contacts an absorptive epithe­ lial surface in the mouth or other area, or if it is held in and oxygenates the ASR ventilatory stream. In this way, initial selection for gulping to aid ASR could, in recur­ rent conditions of environmental hypoxia extending over at time frame of perhaps 104–106 years or longer, select for adaptations leading to the use of aerial O2. Activation of the hypoxia-inducible factor (HIF-1�), an ancient eukaryote adaptation predating the origin of verte­ brates, is another key hypoxia response. HIF-1� induction activates genes promoting O2 transfer (i.e., erythropoiesis, Hb affinity increases, and angiogenesis) and upregulates metabolic adaptation through expression of genes control­ ling anaerobiosis and O2 consumption rate (see also

Transport and Exchange of Respiratory Gases in the Blood: Red Blood Cell Function). The efficacy of HIF-1� has been demonstrated for both water-ventilating and air-breathing fishes and, as illustrated in Figure 3, it would play a key adaptive role during irregular and brief (i.e., hours–weeks) periods of aquatic hypoxia experienced by a non-air-breathing fish. Under such conditions, HIF­ 1� expression would be continually reinforced by natural selection (i.e., individuals having an effective HIF-1� response would survive and propagate the next genera­ tion), and, among populations of species experiencing chronic recurrences of severe hypoxia (i.e., 30–40% air saturation) over an extended time, both the suite of adap­ tive responses encompassed by HIF-1� and the threshold of its onset would likely change (Figure 3). Both the increase in blood hemoglobin (Hb) concen­ tration and the reduction of the quantity of intraerythrocytic nucleoside triphosphates (e.g., adeno­ sine and glutamine triphosphate) resulting in a left-shift (increased) Hb-O 2 affinity in facultatively air-breathing loricariid catfish (L. chagresi, Pterogoplicthys multiradiatus, and other species) are signature features of HIF-1� induction. This affinity increase enables a fish to bind

Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes

more O2 in hypoxic water, lessens the potential for trans-branchial loss, and reduces critical oxygen partial pressure (PO2) and thus increases its proficiency for aquatic respiration in hypoxia. Moreover, the annual dry-season increase in loricariid Hb concentration that occurs in advance of either drying or hypoxia suggests that there has been selection for a preadaptive change that will mitigate these conditions if they occur. Strong selection for more proficient air breathing, occurring over geologic time and driven by both the environmental change and the diversification and radia­ tion of groups into different, and more variably oxygenated habitats, would have also contributed to the origin of continuous air breathing and ushered in morphological and physiological changes, such as a reduction in gill area to lessen the potential for O2 loss, leading to obligatory air breathing (Figure 3). The respiratory specializations of different groups, brought on by regular exposure to environmental hypoxia over periods of probably 107–108 years, concomitantly reduce the importance of an aquatic-hypoxia-induced HIF-1� response; Lepidosiren and Protopterus, for example, are obligatory air breathers that are so proficient at air breathing that they are largely insensitive to the effect of aquatic conditions such as low PO2 that control respiration and trigger air breathing in most other aqua­ tic air breathers. The high degree of respiratory independence from water conditions afforded by welldeveloped air breathing expands potential habitat access to the point where it becomes limited by factors such as the absence of prey and adverse conditions such as temperature, drying, and lack of cover and H2S.

Air Breathing and Natural History Adaptive Radiations Air breathing appears to have been an important factor in the radiation and diversification of certain groups. Many of the species in the families Callicthyidae and Clariidae, and all of the species in the five families comprising the anabantoid suborder (Anabantidae, Belontiidae, Helostomatidae, Osphronemidae, and Luciocephalidae), breathe air. Taken together, these groups comprise a large fraction of the total air-breathing fish diversity (about 14% of the families, 16% of the genera, and 39% of the species). Air breathing permits populations to expand into habitats where, because of adverse conditions, ecological success is assured through limited competition from non-air-breath­ ers. In this way, formerly contiguous populations may become reproductively isolated and undergo genetic diver­ gence into separate species. The degree of diversification present among the anabantoids illustrates that, despite the requirement to sustain air breathing, extensive adaptive radiation can result in dramatic modifications in dentition,

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jaw structure, and diet, as well as body shape and size. These functional changes have not altered ABO respiratory function; however, dependence on air breathing seems to have become more relaxed in some of the anabantoids that are not obligatory air breathers (Sandelia capensis, S. bainsi, Trichogaster sp., and Colisa lalia). Another pattern of adaptive radiation is seen in the African clariid catfishes, many of which have evolved into habitats in which air breathing is not required. The ABO has regressed in species of Dinotopterus occurring in open waters and depths of Lakes Malawi and Tanganyika. Several other regressed genera (Xenoclarias, one species; Clariallabes, 16 species; Gymnallabes, three species; and Taganikallabes, one species) are small and anguilliform with reduced fins. Most of these fishes have taken up life in swift streams where they burrow in rubble and even make amphibious excursions and feed out of water (Channallabes apus), while others live in lakes at consider­ able depth. With their independence from habitat conditions, the fully bimodal clariids achieved a broad distribution across both Africa and Asia, whereas the regressive clariids are largely confined to a narrow central African distribution where they have diversified into unfilled niches. A parallel occurs in the two species of the anabantoid genus Sandelia which, having radiated into more oxygenated habitats of southern Africa, have a highly reduced ABO. An additional aspect of aquatic air breathing now demonstrated for numerous species is synchronous air breathing, a behavior characterized by the closely timed and nearly simultaneous air gulping by a group. This behavior is a form of temporal schooling that reduces the danger of predation during surfacing for air. The transition to land is another dimension of fish air breathing. Amphibious air breathers must respire without water contact and thus risk desiccation as well as the inter­ ruption of the normal functions of the gills in water such as CO2 release, ion regulation, acid–base balance, and nitro­ gen excretion (see also Design and Physiology of Capillaries and Secondary Circulation: Circulatory Fluid Balance and Transcapillary Exchange, Circulation: Circulatory System Design: Roles and Principles, and Integrated Control and Response of the Circulatory System: Integrated Control of the Circulatory System). Amphibious air-breathing fishes are seldom far from water; however, air breathing does permit littoral-zone exploitation and is reflected in attendant biochemical, phy­ siological, morphological, and behavioral adaptations for terrestriality. In the case of mudskippers, which are the most terrestrial teleosts, other facultative air breathing but mainly nonamphibious species (Pseudapocryptes lanceolatus, Apocryptes bata, and others) are members of the same clade (the goby subfamily Oxudercinae); however, for mudskip­ pers the vacant niches of the mudflat proved to be the catalyst for amphibious life. Mudskipper amphibious

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adaptations include fin and body modifications for terres­ trial crawling (crutching), skipping, jumping, and climbing. They also have prominent eyes and a good visual acuity in air. Although their lateral line is reduced, mudskippers can hear airborne sound (250–600 Hz). Also, their physiology is specialized to limit desiccation, to allow osmoregulation in different salinities, and to modify nitrogen excretion for water conservation. Some species can also sense the O2 content of the air in their burrow. While most mudskippers retain the capacity for aquatic respiration, at least one species in the genus Periophthalmodon (Pn. schlosseri) is an obligatory air breather. Amphibious life poses a problem for vision because of the refractive differences of air and water. Solutions include, for some mudskippers, reduction of lens curvature to compensate for the added corneal refraction in air or, in Dialommus macrocephalus and some blennies (E. nigricans), flat corneas reduce aerial astigmatism and allow emmetropia in air without compromising aquatic accommodation. Amphibious fishes have the capacity to orient to water by using known reference points or possibly

Emerged

Submerged

sun compass. Pit traps set at night near tropical streams demonstrate that some aquatic air breathers also leave the water. Clarias lazera was discovered to leave water at night to feed on stored grain while the amphibious, regressive air breather Channallabes apus is able to capture prey on land using a snapping (not suction) jaw action. Ancillary Air-Breathing Functions Aspects of air breathing have become integrated into func­ tions unrelated to respiration. In N. forsteri, Piabucina festae, H. thoracatum, Umbra limi, H. plecostomus, and others, the ABO contributes to static lift (see also Buoyancy, Locomotion, and Movement in Fishes: Buoyancy in Fishes). The loricariids have a stomach ABO and in some species thick, air-filled diverticulae that branch off from the esophageal– stomach junction and encircle the stomach contribute to near-neutral buoyancy which is important for foraging on vertical surfaces, submerged roots, or tree branches. Buoyancy control may also take precedence over

Emerged

Submerged

Egg chamber P O2

Tidal cycle

Burrow entrance site

N2 added to burrow

Air-adding behavior

Air-adding behavior 24 h

Figure 4 Tidal-cycle effects on the PO of the egg chamber in the mudflat burrow of the mudskipper, P. modestus. The male 2 mudskipper guards the intertidal mudflat nest and attends to the eggs, which hatch about 7 days postfertilization. During high tide, the burrow entrance is submerged and egg respiration combined with the reducing environment of the anoxic mud and possibly the respiration of the guarding fish reduce the egg chamber O2 content. When the tide level recedes below the burrow opening, the male uses air-gulp transportation to raise egg-chamber O2 content in preparation for the next high tide. The experimental injection of N2 gas into the egg chamber causes the male fish to increase its frequency of air-deposition behavior in order to raise burrow PO2 before the next incoming tide covers the burrow entrance. Modified from Ishimatsu A, Yoshida Y, Itoki N, et al. (2007) Mudskippers brood their eggs in air but submerge them for hatching. Journal of Experimental Biology 210: 3946–3954; and Graham JB and Wegner NC (2010) Breathing air in water and in air: The air-breathing fishes. In: Nilsson GE (ed.) Respiratory Physiology of Vertebrates: Life With and Without Oxygen, pp. 174–220. Cambridge: Cambridge University Press.

Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes

respiratory needs in some fishes; species of Lepisosteus and A. calva are known to regulate ABO volume for buoyancy purposes, and when in water mudskippers inflate their branchial chambers with enough air to allow them to float with their eyes in air. In anabantoids, bubbles derived from air breathing have a role in territoriality, courtship displays, and bubble-nest construction (Betta splendens and other spe­ cies), and the ABO of these fishes is used to make sounds important in courtship behavior. H. thoracatum and other callichthyids also build bubble nests; the diffusive properties of these structures remain uninvestigated. Some anabantoid species (Macropodus, Betta) are mouth brooders, as is A. gigas and some species of Channa; how this is coordinated with air breathing is unknown. Air breathing plays a role in nest oxygenation. In male Lepidosiren, aerially obtained O2 is exuded into the nests via gill-like filaments that form on their paired fins. (These were early studies that were controversial and more data are needed. Also, accounts differ as to whether the gill filaments form only on the pelvic fins or on both paired fins.) A comparable function has been suggested for the skin of Synbranchus and for cirri on the heads of male loricariids. Mudskippers incubate eggs in air-filled cham­ bers within their littoral-zone mud burrows. An eggtending male P. modestus can sense the PO2 in its air chamber. During high tide when the burrow is sub­ merged, chamber PO2 decreases and during low tide the fish restores chamber PO2 by bringing in gulps of fresh air. If air-chamber PO2 is lowered by pumping in N2, the fish responds with a greater rate of air transport (Figure 4).

Summary Air breathing is an ancient fish adaptation that has inde­ pendently evolved in many groups over 400 million years. The diversity of these fishes and their different types of ABOs and air-breathing behaviors all signify the efficacy of natural selection in achieving a nearly perfect solution to the common occurrence of environmental hypoxia in shallow water habitats throughout the long history of fish evolution. Diverse air-breathing groups demonstrate the central role of aquatic hypoxia in driv­ ing the independent origin of air breathing and for, over the expanse of geologic time, either intensifying or relaxing selection for air breathing and related adapta­ tions, all in concert with changes in environmental factors, with shifts in the patterns of expansion and ecological radiation and morphological changes in a particular group. Specifically, the capacity of fishes to breathe air was an important precondition for the evolu­ tion of amphibious life, both in the tetrapodomorphs and in many extant air-breathing fishes such as the mudskip­ pers. Although air breathing seemingly presents the perfect answer to shallow-water environmental hypoxia,

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not all fishes exposed to this environmental challenge answer it with air breathing. However, for the majority of air breathers this capacity enables them to remain in and better exploit an aquatic habitat in which they could not otherwise survive and associated with this are the examples of how air breathing has secondarily influ­ enced other aspects of natural history. Because the independent evolution of air breathing is viewed as an ongoing process, it is likely that some fishes, because of environmental change or their potential for ecological radiation into less favorable habitats, may now be under­ going the initial selective processes leading to the acquisition of this capacity.

Acknowledgments Research for this paper was supported by the UCSD Academic Senate and by NSF0922569. See also: Air-Breathing Fishes: Circulatory Adaptations for Air-Breathing Fishes; Respiratory Adaptations for AirBreathing Fishes. Buoyancy, Locomotion, and Movement in Fishes: Buoyancy in Fishes; Swimbladder Function and Buoyancy Control in Fishes. Circulation: Circulatory System Design: Roles and Principles. Design and Physiology of Arteries and Veins: Anatomical Pathways and Patterns; Branchial Anatomy. Design and Physiology of Capillaries and Secondary Circulation: Circulatory Fluid Balance and Transcapillary Exchange. Design and Physiology of the Heart: The Coronary Circulation. Gas Exchange: Respiration: An Introduction. Integrated Control and Response of the Circulatory System: Integrated Control of the Circulatory System. Transport and Exchange of Respiratory Gases in the Blood: Red Blood Cell Function. Ventilation and Animal Respiration: Plasticity in Gill Morphology.

Further Reading Burggren WW (1982) ‘‘Air gulping’’ improves blood oxygen transport during aquatic hypoxia in the goldfish, Carassius auratus. Physiological Zoology 55: 327–333. Carter GS (1957) Air breathing. In: Brown M (ed.) Physiology of Fishes, pp. 65–79. New York: Academic Press. Chapman LJ and Liem KF (1991) Papyrus swamps and the respiratory ecology of Barbus neumayeri. Environmental Biology of Fishes 44: 183–197. Clack JA (2002) Gaining Ground: The Origin and Early Evolution of Tetrapods. Bloomington, IN: Indiana University Press. Farrell AP (2007) Cardiovascular systems in primitive fishes. In: McKenzie DJ, Farrell AP, and Brauner CJ (eds.) Primitive Fishes, Fish Physiology, vol. 26, pp 53–120. San Diego, CA: Elsevier. Gonzales TT, Katoh M, and Ishimatsu A (2006) Air breathing of the aquatic burrow-dwelling eel goby, Odontamblyopus lacepedii (Gobiidae: Amblyopinae). Journal of Experimental Biology 209: 1085–1092. Graham JB (1976) Respiratory adaptations of marine air-breathing fishes. In: Hughes GM (ed.) Respiration of Amphibious Vertebrates, pp. 165–187. London: Academic Press.

1860 Air-Breathing Fishes | The Biology, Diversity, and Natural History of Air-Breathing Fishes Graham JB (1997) Air Breathing Fishes: Evolution, Diversity and Adaptation. San Diego, CA: Academic Press. Graham JB (2006) Aquatic and aerial respiration. In: Evans DH and Claiborne JB (eds.) The Physiology of Fishes, 3rd edn., pp. 85–117. Boca Raton, FL: CRC Press. Graham JB and Wegner NC (2010) Breathing air in water and in air: The air-breathing fishes. In: Nilsson GE (ed.) Respiratory Physiology of Vertebrates: Life With and Without Oxygen, pp. 174–220. Cambridge: Cambridge University Press. Greenwood PH (1987) The natural history of African lungfishes. In: Bemis WE, Burggren WW, and Kemp NE (eds.) The Biology and Evolution of Lungfishes, pp. 163–179. New York: Liss. Ishimatsu A, Aguilar NM, Ogawa K, et al. (1999) Arterial blood gas levels and cardiovascular function during varying environmental conditions in a mudskipper, P. schlosseri. Journal of Experimental Biology 202: 1753–1762. Ishimatsu A, Yoshida Y, Itoki N, et al. (2007) Mudskippers brood their eggs in air but submerge them for hatching. Journal of Experimental Biology 210: 3946–3954.

Janvier P (2007) Living primitive fishes and fishes from deep time. In: McKenzie DJ, Farrell AP, and Brauner CJ (eds.) Primitive Fishes, Fish Physiology, vol. 26, pp. 1–51. San Diego, CA: Elsevier. Liem KL (1989) Respiratory gas bladders in teleosts: Functional conservation and morphological diversity. American Zoologist 29: 333–352. Randall DJ, Burggren WW, Farrell AP, and Haswell MS (1981) The Evolution of Air Breathing in Vertebrates. Cambridge: Cambridge University Press. Sayer MDJ (2005) Adaptations of amphibious fish for surviving life out of water. Fish and Fisheries 6: 186–211. Taylor DS, Turner BJ, Davis WP, and Chapman BB (2008) A novel terrestrial fish habitat inside emergent logs. American Naturalist 171: 263–266. Wassenbergh SV, Herrel DA, Hiysentruytt F, Devaeret S, and Aerts P (2006) A catfish that can strike its prey on land. Nature 440: 881. Wells NA and Dorr JA (1985) Form and function of the fish Bothriolepis (Devonian; Placodermi, Antiarchi): The first terrestrial vertebrate? Michigan Academician 17: 157–173.