Portal de Periódicos da CAPES

Air‐breathing fishes

2014; Wiley; Volume: 84; Issue: 3 Linguagem: Inglês

10.1111/jfb.12349

1095-8649

Sjannie Lefevre, Mark Bayley, David J. McKenzie, John F. Craig,

Aquaculture Nutrition and Growth

Physiological adaptations for air breathing have evolved multiple times in bony fishes and have fascinated researchers for well over a century (Poey, 1858; Dobson, 1874; Wilder, 1877; Day, 1878; Das, 1928; Carter & Beadle, 1931). 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, 2014); so this number is certainly an underestimate of the true total. Air breathing is believed to have evolved in response to aquatic hypoxia in freshwater habitats, and in response to periodic emersion in marine habitats (Johansen, 1968, 1970; Randall et al., 1981; Graham, 1997; Graham & Lee, 2004). All air-breathing fishes are in fact bimodal breathers because they retain gills that have a role in gas-exchange, in particular excretion of carbon dioxide and ammonia into water (Randall et al., 1981). The simplest air-breathing organ is the skin, which can only take up oxygen from air when the animals emerge, and the gills collapse and no longer function for oxygen uptake. Many air-breathing fishes have evolved an ability to gulp air and store it in well-vascularized internal organs which can be a true lung, a modified swimbladder, diverticula of the buccal, opercular or pharyngeal cavities, or the gut (Graham, 1997). These organs enable them to breathe air not only when exposed to air but also when in water. This requires excursions to the surface and provides a greater capacity to regulate respiratory partitioning and oxygen uptake from air. Although the majority of air-breathing fishes are found in the tropics, they also inhabit temperate areas and a species of umbrid, the Alaska blackfish Dallia pectoralis Bean 1880, lives above the Arctic Circle. The extent to which the various species rely on air varies on a spectrum from facultative (will not drown if denied access to the surface) to obligate (must have access to aerial oxygen), although classifying a given species as obligate has proven to be highly dependent upon experimental and environmental conditions (Graham, 1997; Lefevre et al., 2014a). A number of plesiomorphic bony fish species are air breathers, such as the birchirs Polypterus spp, the bowfin Amia calva L. 1758 and the gars Lepisosteus spp., and some primitive teleosts, osteoglossids such as the pirarucu Arapaima gigas (Schinz 1822) and elopiformes such as the tarpons Megalops spp. Bimodal respiration is of course an ancestral trait of all tetrapods. The three extant genera of sarcopterygian lungfishes are perhaps the best known air-breathing fishes. They share morphological characters with a group that dominates the fossil record from the Palaeozoic and gave rise to the modern terrestrial vertebrates (Clack, 2007, 2012; Janvier, 2007). It has often been proposed, therefore, that the study of extant air-breathing fishes could provide insights into the evolution of physiological systems in vertebrates (Randall et al., 1981; Graham, 1997), although this remains a rather speculative activity. A molecular phylogeny of air breathing in the vertebrate and bony fish Tree of Life does not yet exist (Janvier, 2007). Nonetheless, the comparative physiology of air breathing in fishes is a fascinating topic in itself, because the species are very interesting in their own right (Graham, 1997). There have been a number of extensive reviews and books dedicated to air breathing in fishes over the last 100 years culminating, ultimately, in the exceptional monograph by the late J.B. Graham in 1997 (Rauthner, 1910; Das, 1928; Carter & Beadle, 1931; Johansen, 1968; Randall et al., 1981; Graham, 1997). There have been no monographs, volumes or journal special issues specifically dedicated to air-breathing fishes since Graham (1997) although there are several more recent reviews and book chapters on elements of their physiology (Graham & Lee, 2004; Ip et al., 2004; Graham, 2006; Chapman & McKenzie, 2009; Glass & Rantin, 2009; Nelson & Dehn, 2010; Ishimatsu, 2012; Milsom, 2012). The objective of this special issue was to provide a forum to publish ongoing research and, in particular, to review knowledge in specific areas. Although there are many publications on air-breathing fish species in the literature, the majority are not related to the fact that species have bimodal respiration. Rather, they are related to the species' economic importance, e.g. siluriforms in aquaculture, or because the species is considered to occupy a particular position in vertebrate evolution, or is the focus of conservation strategies, both the case with the Australian lungfish Neoceratodus forsteri (Krefft 1870). The emphasis of this special issue is research on the physiology of air breathing in fishes; the emphasis is on physiology because air breathing is an anatomical and physiological adaptation, and many of the laboratories currently working in this area have contributed articles here. Much of the previous physiological research on air-breathing fishes has been on the respiratory and cardiovascular adaptations associated with bimodal respiration. These topics are nicely covered by two recent comprehensive reviews (Ishimatsu, 2012; Milsom, 2012) and hence are not included in this special issue. This special issue comprises seven reviews and eight research articles that cover both freshwater and marine species, temperate and tropical, and a wide range of topics. 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. The paper provides a phylogeny to family level based on the most recent molecular data; the species are mainly tropical freshwater and facultative air breathers. It then reviews the anatomy of their air-breathing organs and how they use these and other related cardiorespiratory adaptations to supplement oxygen uptake, especially in aquatic hypoxia. An interesting area for future research, which has been explored little to date, is how these species balance the digestive and respiratory functions of their gut. Martin (2014) provides a comprehensive update of knowledge on the more than 70 species of intertidal teleosts, from 12 families, which breathe air when they emerge from water. These species emerge to different extents depending on their ecology, ranging from passive remainers that are left by the tide, to active emergers that pursue a truly amphibious lifestyle. They all use vascularized mucosae and the skin to exchange both oxygen and carbon dioxide in air, rather than a more specialized air-breathing organ. The review considers, in particular, how they differ from freshwater air-breathing fishes in their morphology, physiology, ecology and behaviour. The existence of closely related species that have colonized different microhabitats should provide unique opportunities for future comparative studies. Chew & Ip (2014) have written an authoritative review of the strategies that air-breathing fishes have evolved for dealing with the buildup of toxic ammonia that is created during emersion, whether during amphibious excursions or when progressively trapped into mud during the tropical dry season. The strategies depend on the behaviour of the species and the nature of its habitat and can be broadly categorized as (1) enhancement of excretion and reduction of re-entry, (2) conversion to less toxic products that can be accumulated, (3) reduction of ammonia production and accumulation and (4) tolerance at the cellular and tissue levels. Air-breathing fishes may be particularly tolerant to ammonia; among the many strategies, conversion of ammonia to urea appears to be extremely rare in bony fishes, although it occurs in sarcopterygians notably aestivating African lungfishes Protopterus spp. The authors conclude that these species provide models to examine the adaptations that facilitated invasion of land by fishes. Future research should be aimed at revealing novel strategies and behaviours. Pace & Gibb (2014) provide the first comprehensive review of how air-breathing fishes move over land when emerged. Although appendage-based terrestrial locomotion is rare in bony fishes, the authors provide a phylogeny demonstrating how various families and species have converged upon two types of locomotion. One involves axial-based movements, with an anterior-to-posterior wave of undulation that travels down the axial musculoskeletal system; the other is axial-appendage-based, comprising side-to-side, whole-body bending in co-ordination with protraction or retraction cycles of the pectoral fins. The authors conclude that surprisingly little is known about physiological or biomechanical limits to terrestrial excursions. Also, future research should investigate how these species switch from swimming to terrestrial locomotion: they may provide models to investigate novel motor patterns and their neuro-sensory control. Lefevre et al. (2014b) provide the first dedicated review of how bimodal fishes use aerial respiration to meet metabolic demands of swimming. In all species studied, sustained aerobic exercise stimulates air breathing, with evidence of an exponential increase in surfacing frequency and oxygen uptake from air with increasing swimming speed. Facultative air breathers apparently breathe air during aerobic exercise even when they can achieve the same aerobic scope and performance by branchial ventilation alone, when denied surface access. Although it might be expected that bimodal fishes use aerial respiration to recover from metabolic imbalances incurred during anaerobic exercise, some apparently prefer to increase aquatic respiration, possibly to promote branchial ion exchange and restore acid–base balance, and avoid being seen by predators. Further research is needed to understand the mechanisms controlling air breathing during exercise, in particular why facultative air breathers surface when this is unnecessary to sustain their aerobic performance. Shartau & Brauner (2014) provide the first comprehensive review of ion and acid–base balance in bimodal fishes. An obvious consequence of bimodal respiration is that the metabolic drive for branchial oxygen uptake is relaxed, allowing separation and specialization of the otherwise multi-functional gill (Evans et al., 2005). Moreover, many of the known bimodal fishes inhabit waters that are particularly ion-poor. In clear prose, the authors investigate and present the consequences of these influences on acid–base and ion balance. They suggest that intracellular pH is more strongly regulated in air-breathers than is normally the case in fishes: it will be interesting to see if this trend, seen in five species to date, is a general adaptation. They point out that the roles of the kidney and gut are deserving of much more research attention in the future, as they may give interesting insights into the evolution of respiratory systems in vertebrates. Lefevre et al. (2014a) review aquaculture of air-breathers and the state of knowledge of their respiratory physiology, as related to further development of this source of human protein. Statistics from FAO reveal that the production of air-breathing fishes from four families (Clariidae, Channidae, Pangasiidae and Synbranchidae) has increased explosively over the past decade and now represents 8% of global fish production from aquaculture. Although water oxygenation is typically not used in aquaculture of bimodal fishes, they reach the surprising conclusion that it is likely to be highly beneficial to growth, even for species considered obligate air-breathers. Cultured air-breathing fishes appear to be significantly more tolerant to ammonia and nitrite compared to water breathers. The authors point out that the huge knowledge base supporting the development of aquaculture in water-breathing fishes is largely lacking for air breathers, pointing to a need for an intense research effort. The eight research articles cover a fairly broad range of topics and species. Brown & Green (2014) investigate how temperature influences embryogenesis during aerial incubation of eggs of the Gulf killifish Fundulis grandis (Baird & Girard 1859), a species that deposits eggs on marsh grasses at high water on spring tides. Magellan et al. (2014) and Urbina et al. (2014) provide new information about how different galaxiid species utilize adaptations for cutaneous respiration to tolerate periodic aerial exposure. Toba & Ishimatsu (2014) present novel data about the significance of air stored in burrows by the great blue spotted mudskipper Boleophthalmus pectinirostris (L. 1758), in particular for the embryonic development of its broods. Mendez-Sanchez & Burggren (2014) and Blank & Burggren (2014) investigate developmental plasticity of air breathing in various species of anabantids, specifically whether chronic aerial and aquatic hypoxia can elicit plastic responses in the timing of onset of air breathing and the morphology of their suprabranchial air-breathing organs. Porteus et al. (2014) demonstrate that acclimation to chronic aquatic hypoxia elicits significant plastic responses by the oxygen transport system in A. calva. Finally, Johannsson et al. (2014) describe air breathing behaviour by the Lake Magadi tilapia Alcolapia grahami (Boulenger 1912) in aquatic hyperoxia and the intriguing possibility that this is linked to reactive oxygen species. Being the only group of animals that can breathe both air and water efficiently, air-breathing fishes are the intriguing result of opposing evolutionary forces, with much more knowledge yet to be gained about their phylogeny, physiology and, in particular, behavioural ecology. They remain a small minority of the total number of bony fish species, indicating that bimodal respiration is not necessarily a successful strategy for fishes in general, involving trade-offs that remain largely to be explored (Kramer, 1983; 1988; Kramer et al., 1983) The editors of this special issue are very grateful to the authors for their contributions and for their forbearance with the delay in its publication.