Theme and variations: amphibious air-breathing intertidal fishes.

Journal of Fish Biology (2014) 84, 577–602 doi:10.1111/jfb.12270, available online at wileyonlinelibrary.com

Theme and variations: amphibious air-breathing intertidal fishes K. L. Martin Department of Biology, 24255 Pacific Coast Highway, Pepperdine University, Malibu, CA 90263-4321, U.S.A.

Over 70 species of intertidal fishes from 12 families breathe air while emerging from water. Amphibious intertidal fishes generally have no specialized air-breathing organ but rely on vascularized mucosae and cutaneous surfaces in air to exchange both oxygen and carbon dioxide. They differ from air-breathing freshwater fishes in morphology, physiology, ecology and behaviour. Air breathing and terrestrial activity are present to varying degrees in intertidal fish species, correlated with the tidal height of their habitat. The gradient of amphibious lifestyle includes passive remainers that stay in the intertidal zone as tides ebb, active emergers that deliberately leave water in response to poor aquatic conditions and highly mobile amphibious skipper fishes that may spend more time out of water than in it. Normal terrestrial activity is usually aerobic and metabolic rates in air and water are similar. Anaerobic metabolism may be employed during forced exercise or when exposed to aquatic hypoxia. Adaptations for amphibious life include reductions in gill surface area, increased reliance on the skin for respiration and ion exchange, high affinity of haemoglobin for oxygen and adjustments to ventilation and metabolism while in air. Intertidal fishes remain close to water and do not travel far terrestrially, and are unlikely to migrate or colonize new habitats at present, although in the past this may have happened. Many fish species spawn in the intertidal zone, including some that do not breathe air, as eggs and embryos that develop in the intertidal zone benefit from tidal air emergence. With air breathing, amphibious intertidal fishes survive in a variable habitat with minimal adjustments to existing structures. Closely related species in different microhabitats provide unique opportunities for comparative studies. © 2013 The Fisheries Society of the British Isles

Key words: beach spawning; Blenniidae; Cottidae; Gobiidae; hypoxia; Stichaeidae.

ECOLOGY OF INTERTIDAL FISHES Terrestrial and marine influences combine to make the narrow coastal margin between the lowest and highest tides, one of the most productive marine habitats worldwide (Stevenson & Stevenson, 1972; Leigh et al., 1987). It comes as no surprise that many fish species have evolved to take advantage of the opportunities for feeding, interacting, avoiding large predators, mating and nesting in this life-filled zone (Horn & Gibson, 1988; Bridges, 1993; Horn et al., 1999). Over 70 species of teleosts from 12 families emerge from water and breathe air as tides recede in the marine intertidal Tel.: +1 310 506 4808; email: [email protected]

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zone, for a variety of biotic purposes, in a multitude of forms (Bridges, 1988; Sayer & Davenport, 1991; Graham, 1997; Martin & Bridges, 1999; Horn & Martin, 2006). Inger (1952), Romer (1967), Randall et al. (1981) and Janis & Farmer (1999) have suggested that fishes evolved adaptations for air breathing in part as a response to hypoxic aquatic conditions in freshwater swamps and that this was an essential first step in the evolution of a terrestrial lifestyle by vertebrates. In the past, evolutionary biologists have not addressed the selection pressures of low aquatic oxygen for most marine habitats, because as a rule, in most areas of the ocean, dissolved oxygen is relatively high and constant (Graham et al., 1978). Temporarily hypoxic or even anoxic dead zones that may suffocate and kill most living creatures, however, occur in response to eutrophication of the benthos along coasts or in estuaries (Diaz & Rosenberg, 2008). The frequency and extent of these events have been increasing in recent years, often marked by dramatic fish kills (Martinez et al., 2006). In contrast, less extreme, temporary hypoxic conditions occur on a regular basis on a small scale within the marine intertidal zone and this led to consideration of the intertidal zone as a source of the vertebrate transition to land (Schultze, 1999; Clack, 2007; Niedzwiedzki et al., 2010). The daily ebb and flow of tides expose to air and then submerge some portion of the coast. The retreat of the water level also isolates small pools from the open ocean, providing refuge to aquatic animals. In this predictably changing environment, conditions may depart greatly from the surrounding ocean (Truchot & Duhamel-Jouve, 1980) with hypoxia, hypercarbia and rising acidity. Temperature and salinity are more variable in the intertidal zone than in the surrounding ocean. Many intertidal teleost species adapt to these conditions by emerging onto land and breathing air (Graham, 1976, 1997; Bridges, 1988; Martin & Bridges, 1999; Graham & Lee, 2004). Some teleost species are only present in the intertidal zone during high tides and move out as the tide falls (Congleton, 1980; Gibson, 1982; Yoshiyama et al., 1986; Bridges, 1993; Davis, 2001). Other teleost species are resident within the intertidal zone and remain there to cope with the habitat under all tidal conditions (Yoshiyama, 1981; Pfister, 1992; Yoshiyama et al., 1992; Horn & Martin, 2006). The progression of moon phases creates tidal oscillations of variable height, such that on a rocky shelf of bedrock, intertidal plants and animals in the high zone on the shore are exposed to air much more frequently, for longer periods of time, than species in the mid-intertidal zone. Organisms in the low intertidal zone may only be exposed to air briefly during a few of the lowest tides of the year. These reliable microhabitat exposures result in vertical zonation of different species of invertebrates, plants and fishes at different heights on the shore (Stevenson & Stevenson, 1972; Benson, 2002). Although fishes are highly mobile, resident species show fidelity to intertidal habitats within particular tidal heights (Richkus, 1978; Barton, 1982; Yoshiyama et al., 1992; Gibson, 1999; Zander et al., 1999), which may differ between sexes (Williams, 1954), with temperature (Nakamura, 1976) or seasonally (Moring, 1986; Davis, 2000). Rocky habitats, crevices and basins, where sea water collects in pools during low tides, offer a refuge from air exposure for mobile marine intertidal animals. These tide pools teem with life. The timing of low tides affects the dissolved oxygen (Truchot & Duhamel-Jouve, 1980). During the day, photosynthesis by plants keeps oxygen levels high but, during nocturnal low tides, pools separated from the open ocean may become hypoxic, hypercarbic and more acidic owing to respiration of the many

© 2013 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 84, 577–602

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denizens taking refuge within the pool, coupled with the lack of photosynthesis. Teleost species of Cottidae, Stichaeidae, Clinidae, Gobeisocidae, Blenniidae, Gobiidae, Tripterygiidae and others are found in rocky intertidal habitats (Horn & Gibson, 1988; Horn et al., 1999). Estuaries and mudflats are also home to amphibious teleosts. In these environments, wave action is low and there may be daily fluctuations in salinity, temperature, depth and dissolved oxygen (Polgar & Crosa, 2009). Among the estuarine fishes, numerous species of oxudercine gobies and cyprinodonts in particular have adaptations for terrestrial emergence and air breathing, some at times of both high and low tides. Although burrows in mudflats may prevent desiccation, the hypoxic water that fills these refuges during low tides may result in selection pressure for air emergence by these fishes (Ikebe & Oishi, 1996). Mangrove habitats are tropical intertidal forests that are diverse and have a high density of organisms. As in rockpools, the waters around the mangrove roots may become hypoxic, particularly at night. Beaches with sand, gravel or other unconsolidated substrata may house spawning runs of some teleosts and some species emerge from water to spawn (DeMartini, 1999). Although the eggs of these species are tidally exposed to air, the adults rarely stay emerged for long periods (Martin et al., 2004).

EMERGENCE AND AIR BREATHING BY INTERTIDAL FISHES Air-breathing marine intertidal fishes are typically amphibious and partially or fully emerge from water. In contrast, most freshwater air-breathing fishes remain aquatic while gulping air at the water surface (Graham, 1976, 1997). Adaptations for amphibious behaviour and air emergence follow a vertical gradient for these negatively buoyant and relatively inactive fishes (Horn & Gibson, 1988) at different tidal heights within the intertidal zone (Zander, 1972; Horn & Riegle, 1981; Martin, 1996; Mandic et al., 2009). Most intertidal fish species are cryptic in appearance and may be difficult to see even when emerged during low tides (Horn & Martin, 2006), especially when this emergence is hidden under a rock or in vegetation. Within these generalities, three major types of amphibious emergence behaviours are seen in marine intertidal fishes (Fig. 1). The first emergence type is the passive remainer (Table I). This deliberate, reliably observed emergence is seen in resident intertidal fish species that remain at their home shore height at all tides and passively emerge into air because they do not move as the tide ebbs. These species are regularly and routinely found either in shallow pools or emerged from water under boulders or in vegetation. They are relatively quiet and inactive while out of water, and do not appear to be distressed. Passive remainer species generally exchange oxygen and carbon dioxide in air at similar rates to their respiration in water (Daxboeck & Heming, 1982; Edwards & Cech, 1990; Martin, 1993, 1995). Examples include many stichaeids (Horn & Riegle, 1981; Daxboeck & Heming, 1982; Martin, 1993, 1995) on the North American Pacific Coast, the shanny Lipophrys pholis (L. 1758) in Europe, the Mediterranean Sea and Africa (Zander, 1972; Bridges, 1988) and tripterygiid species in New Zealand (Innes & Wells, 1985; Hill et al., 1996). This behaviour allows the fishes to remain in the intertidal zone


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Fig. 1. Vertical height in the intertidal zone is correlated with type of amphibious behaviour and air emergence. Three examples are shown: the passive remainer, a stichaeid Xiphister atropurpureus, remains with an egg clutch beneath a boulder in the low or mid intertidal; the active emerger, a cottid Clinocottus analis, leaves a tidepool and the skipper, a mudskipper Periophthalmus barbarus, fully emerges for activity in the supralittoral zone on a mudflat.

during low tides and may assist these small teleosts in avoiding large predators they might encounter if they migrated temporarily out into the open ocean. Passive remainers also include the deliberate but passive emergence characterized by a parent remaining near a nest or clutch (Fig. 1), as seen in some stichaeids (Marliave & DeMartini, 1977; Coleman, 1992, 1999), the midshipman Porichthys notatus Girard 1854 (Crane, 1981; Brantley & Bass, 1994) and the northern clingfish Gobiesox maeandricus (Girard 1858) (Coleman, 1999). In contrast, the sharpnose sculpin Clinocottus acuticeps (Gilbert 1896) provides parental care to intertidal eggs only during higher tides when the adults can be aquatic (Marliave, 1981), although this species has occasionally been found emerged during low tides (Yoshiyama & Cech, 1994). Some species found low in the intertidal zone of temperate waters may endure accidental emergence when trapped by an outgoing tide. Fishes found low in the intertidal zone rarely face exposure to air, although some may tolerate accidental stranding and exchange respiratory gases in air even though they do not actively emerge (Zander et al., 1999). Their behaviour is calm and stoic, as in the rockpool blenny Hypsoblennius gilberti (Jordan 1882) (Luck & Martin, 1999) and juvenile opaleye Girella nigricans (Ayres 1860) (Martin, 1993) on the North American Pacific Coast and the estuarine mummichog Fundulus heteroclitus (L. 1766) on the North


Europe, U.K. Pacific Coast, California to Alaska California, U.S.A. Pacific Coast, Mexico to Alaska Pacific Coast, U.S.A. and Canada

Zoarces viviparous Anoplarchus purpurescens

Cebidichthys violaceus

Xiphister atropurpureus Xiphister mucosus

Stichaeidae

Kyphosidae Pholididae

Fundulidae Gobisocidae

Pacific Coast, U.S.A. and Canada California, U.S.A. Pacific Coast, U.S.A. British Columbia, Canada California, U.S.A. Europe Delaware Bay, Atlantic Coast, U.S.A. Pacific Coast, U.S.A. Northern Gulf of California Northern Gulf of California Northern Gulf of California Northern Gulf of California California, U.S.A. Pacific Coast, U.S.A. and Canada Pacific Coast, U.S.A. Pacific Coast, U.S.A. Pacific, Mexico to Canada

Porichthys notatus Hypsoblennius gilberti Artedius lateralis Clinocottus acuticeps Leptocottus armatus Taurulus bubalis Fundulus heteroclitus Gobiesox meandricus Gobiesox pinniger Pherallodiscus funebris Tomicodon boehlke Tomicodon humeralis Girella nigricans Apodichthys flavidus Pholis gunnnellus Pholis laeta Xererpes fucorum

Batrachoididae Blenniidae Cottidae

Location of study population

Genus species

Family

Crane (1981); Martin (1993, 1995) Luck & Martin (1999) Lamb & Edgell (1986) Marliave (1981); Yoshiyama & Cech (1994) Martin (1993) Davenport & Woolmington (1981) Halpin & Martin (1999) Cross (1981); Martin (1993) Eger (1971) Eger (1971) Eger (1971) Eger (1971) Martin (1993, 1995) Cross (1981); Lamb & Edgell (1986) Laming (1983); Bridges (1988); Coleman (1999) Lamb & Edgell (1986) Horn & Riegle (1981); Lamb & Edgell (1986); Martin (1993) Hartvig & Weber (1984) Cross (1981); Horn & Riegle (1981); Yoshiyama & Cech (1994); Martin (1996) Horn & Riegle (1981); Edwards & Cech (1990); Martin (1993) Daxboeck & Heming (1982); Martin (1993) Horn & Riegle (1981); Martin (1993)

References

Table I. Passive remainers are from temperate waters. Some of these species remain in the intertidal zone during low tides for parental care. Some species can survive out of water but are not usually found out of water during low tides. This type of amphibious emergence is seen most frequently in the low intertidal zone



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American Atlantic Coast (Halpin & Martin, 1999). Other species that may occur in lower tidepools but are not typically found out of water, may have difficulty surviving a few hours of tidal exposure when accidentally stranded (Congleton, 1980; Davenport & Woolmington, 1981; Martin, 1996). Intertidal fishes with the second type of emergence, active emergence (Table II), may typically be found in tide pools but will volitionally emerge when aquatic conditions become unpleasant, with hypoxia or increased acidity due to hypercarbia during nocturnal low tides (Truchot & Duhamel-Jouve, 1980). These species choose to actively leave the water and emerge, either partially with just the head (Fig. 1) or fully into air (Wright & Raymond, 1978; Martin, 1991, 1995; Yoshiyama et al., 1995; Sloman et al., 2008). This allows them to respire in the abundant atmospheric oxygen (Congleton, 1980; Davenport & Woolmington, 1981; Martin, 1993; Watters & Cech, 2003). Many of these species, e.g. the tidepool sculpin Oligocottus maculosus Girard 1856, the fluffy sculpin Oligocottus snyderi Greeley 1898 and the woolly sculpin Clinocottus analis (Girard 1858), are not typically found emerged in the field except during nocturnal low tides or in caves (Wright & Raymond, 1978) but they can be artificially induced to emerge in the laboratory under hypoxic conditions (Yoshiyama et al., 1995; Martin, 1996; Sloman et al., 2008), perhaps after engaging in aquatic surface respiration (Martin, 1996; Sloman et al., 2008). Species found in temperate waters (Fig. 2) include many Cottidae in the intertidal zone of the North American Pacific Coast. Similar temperate species that also emerge during hypoxia include the twister Bellapiscis medius (Günther 1861) of New Zealand (Innes & Wells, 1985) and some blennids in the Mediterranean Sea (Zander, 1983). Among the Gobiesocidae, the Chilean clingfish Sicyases sanguineus Müller & Troschel 1843 emerges from water adjacent to rocks as tides decline (Ebeling et al., 1970; Gordon et al., 1970; Eger, 1971) and has been reported to move ahead of the tide line in order to resist returning to water (Gordon et al., 1970). Teleosts from estuaries or mudflats may actively emerge at times to avoid hypoxic water, including gobids such as Andamia spp. (Zander, 2011) and the mangrove killifish Kryptolebius marmoratus (Poey 1880) (LeBlanc et al., 2010). Both passive remainers and active emergers show varying degrees of affinity to air emergence, correlated with tidal height at which the species is likely to be found (Zander, 1972; Congleton, 1980; Horn & Riegle, 1981; Martin, 1996; Zander et al., 1999; Mandic et al., 2009; Richards, 2011). The ability to actively emerge may also be correlated with the ability to maintain an upright posture out of water. The eel-like shape of stichaeids and the large pectoral fins of blennids and cottids assist in this regard. The third type of emergence by amphibious intertidal fishes is seen in skippers (Table III), active, highly amphibious fishes that emerge from water for most of their daily activities and are well adapted for terrestrial movement and aerial respiration (Zander, 1972, 1983; Clayton & Vaughan, 1986). They must stay close to water in order to keep the respiratory surfaces moist by behavioural means but they also engage in feeding, courtship, nesting and intraspecific interactions out of water (Graham & Rosenblatt, 1970; Graham et al., 1985; Brown et al., 1992). This type of emergence appears to be restricted to only a few families (Table III), each with multiple amphibious species (Graham, 1997). Blennids and Labrisomids that occupy the supralittoral zone and are well adapted for air emergence are colloquially called rockskippers (Graham et al., 1985; Martin


Pacific Coast, U.S.A. Pacific Coast, U.S.A. and Canada Pacific Coast, U.S.A. Pacific Coast, U.S.A. and Canada

Clinocottus recalvus Oligocottus maculosus

Oligocottus rimensis Oligocottus snyderi


Gobiesocidae Plesiopidae Rivulidae Tripterygiidae

Gobiidae

India, Bangladesh and Myanmar Pacific Coast, U.S.A. Japan, Korea, China and Taiwan India Chile New Zealand Atlantic Coast, South America, Caribbean New Zealand New Zealand

California, U.S.A. Pacific Coast, U.S.A.

Clinocottus analis Clinocottus globiceps

Apocryptes bato Gillichthys mirabilis Odontamblyopus lacepedii Pseudapocryptes elongatus Sicyases sanguineus Acanthoclius fuscus Kryptolebius marmoratus Forsterygion nigripenne Bellapiscis medius

Europe, Mediterranean Sea Pacific Coast, U.S.A. and Canada

Lipophrys trigloides Ascelichthys rhodorus

Cottidae

Mediterranean Sea, Europe, Africa Indo-Pacific, Red Sea Europe

Coryphoblennius galerita Istiblennius edentulous Lipophrys pholis

Blenniidae


Genus species

Family

Zander (1983) Zander (1972) Davenport & Woolmington (1981); Laming et al. (1982); Pelster et al. (1988) Zander (1983) Cross (1981); Yoshiyama & Cech (1994); Yoshiyama et al. (1995); Martin (1996) Martin (1991); Watters & Cech (2003) Martin (1993); Yoshiyama & Cech (1994); Yoshiyama et al. (1995) Wright & Raymond (1978); Martin (1993) Martin (1993); Yoshiyama & Cech (1994); Yoshiyama et al. (1995); Sloman et al. (2008) Yoshiyama & Cech (1994) Martin (1993); Yoshiyama & Cech (1994), Yoshiyama et al. (1995) Zander (2011) Todd (1968); Todd & Ebeling (1966) Gonzales et al. (2006) Zander (2011) Ebeling et al. (1970); Gordon et al. (1970) Mayr & Berger (1992); Hill et al. (1996) Leblanc et al. (2010) Berger & Mayr (1992); Hill et al. (1996) Innes & Wells (1985); Hill et al. (1996)

References

Table II. Active emergers are from temperate waters and emerge in response to changes in aquatic conditions. Different propensities for emergence are found among these species. They may be found at any tidal level but are more likely in the middle and high zones


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Fig. 2. Amphibious intertidal fishes are known in all continents except Antarctica ( , intertidal remainers; , tidepool emergers; , skippers). Opportunities for future comparative studies and discoveries about the biogeography of amphibious behaviour and air-breathing ability abound. Map locations are adapted from Froese & Pauly (2011).

& Lighton, 1989; Brown et al., 1992; Zander et al., 1999; Nieder, 2001; Bhikajee & Green, 2002). These are found in tropical areas, splashed by waves as they move with great agility over the rock faces. Their habitats include many areas of the IndoPacific Oceans, as well as numerous oceanic islands (Table III and Fig. 2). Some of these species, e.g. Kirk’s Blenny Alticus kirki (Günther 1868), may be out of water for up to 90% of the time (Brown et al., 1992) and feed, court, nest and interact actively out of water. Among these communities are some blennids that emerge only at night (Zander, 1983). Mudskippers are a speciose group of tropical and temperate oxudercine gobids (Murdy, 1989; Clayton, 1993) found mostly in the Indo-Pacific and Africa. They are active out of water on mudflats whenever terrestrial habitat is available (Tamura et al., 1976; Low et al., 1990; Randall et al., 2004). In mudflats, anoxia occurs within a few cm from the benthic surface. During an ebb tide, animals must cope with either air emergence or aquatic hypoxia until the incoming tide. Skippers are well adapted for air emergence and amphibious life. Terrestrial behaviours include feeding, territoriality and reproductive displays. Mating and nesting may also occur out of water (Clayton & Vaughan, 1986; Clayton, 1993; Graham, 1997; Ishimatsu et al., 2007). These energetic species emerge from normoxic water as well as from hypoxic water as part of daily life and not solely as an escape from unpleasant aquatic conditions. Some of these species spend significantly greater time out of water than submerged (Graham et al., 1985; Brown et al., 1992; Pace & Gibb, 2009), although they never stray far from a source of liquid water and may have characteristic behaviours to rehydrate respiratory membranes (Ip et al., 1991; Nieder, 2001). They generally do not venture shoreward from their intertidal habitat when feeding or interacting with conspecifics or predators, although some mudskippers may move up onto mangrove roots or other exposed plants during low tides. No


Periophthalmus gracilis Periophthalmus kalolo Periophthalmus minutes Periophthalmus modestus Periophthalmus novaeguineaensis Periophthalmus variabilis Periophthalmodon freycineti Periophthalmodon schlosseri Periophthalmodon septemradiatus Scartelaos histophorus Scartelaos tenuis Labrisomidae Dialommus fuscus Dialommus macrocephalus

Ctenogobius sagitulla Kellogella cardinalis Periophthalmus argentilinatus Periophthalmus barbarus Periophthalmus chrysospilos

Alticus arnoldorum Alticus kirki Alticus monochrus Alticus saliens Andamia tetradactylus Entomacrodus nigricans Entomacrodus vermiculatus Boleophthalmus birdsongi Boleophthalmus boddarti Boleophthalmus caeruleomaculatus Boleophthalmus dussumieri Boleophthalmus pectinirostris

Blenniidae

Gobiidae

Genus species

Family

References

Hsieh (2010) Zander (1972); Martin & Lighton (1989); Brown et al. (1992) Bhikajee & Green (2002) Abel (1973) Shimizu et al. (2006) Graham et al. (1985) Abel (1973) Murdy (1989) Teal & Carey (1967); Polgar & Crosa (2009); Ip et al. (2011) Murdy (1989) Froese & Pauly (2011) Tamura et al. (1976); Graham et al. (2007); Polgar & Crosa (2009) California to Peru Todd (1976) Ryuku Islands to Australia Larson (1983) Indo-Pacific, Red Sea to Australia and Japan Teal & Carey (1967); Gordon et al. (1969) Africa and Western Central Pacific Hillman & Withers (1987) India to Indonesia Natarajan & Rajulu (1983); Lee et al. (1987); Polgar & Crosa (2009) Indo-Pacific, Malaysia to Australia Nursall (1981); Polgar & Crosa (2009) East Africa to Samoa Murdy (1989) Western South Pacific Gregory (1977) Vietnam to Japan Ishimatsu et al. (2007) Australia, Indonesia Tamura et al. (1976) Indo-Pacific, Malaysia Polgar & Crosa (2009) Western Pacific, Papua New Guinea Bandurski et al. (1968); Milward (1974) Indo-West Pacific, South-east Asia Polgar & Crosa (2009); Gonzales et al. (2011); Ip et al. (2011) India to Indonesia Zhang et al. (2003) Indo-Pacific, Malaysia Tamura et al. (1976); Gregory (1977); Polgar & Crosa (2009) Pakistan, Persian Gulf Ishimatsu & Gonzales (2011) Galapagos Islands Nieder (2001) Baja California to Columbia Graham & Rosenblatt (1970); Graham (1973)

South Pacific Islands Indo-Pacific, East Africa, Red Sea Indian Ocean, Madagascar, Africa South-east Asia, Japan, Australia Western Pacific, Japan to Indonesia Pacific Coast, Central America Indo-Pacific, Malaysia, Africa Papua New Guinea Indo-Pacific, India and China Australia Iraq, Pakistan and India China, Korea, Japan and Taiwan


Table III. Skippers are found in tropical and temperate waters. There are different propensities for emergence and terrestrial activity within this group but as a whole these species are quite active out of water and frequently found emerged



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known species of amphibious intertidal fishes move great distances across terrestrial habitats except during a flood tide (Graham et al., 1985; Hsieh, 2010). They do not appear to make extensive overland excursions that may be seen in some freshwater amphibious fishes (Graham, 1997; Graham & Lee, 2004). Given the current state of their adaptations, these fishes appear to be unable to colonize land beyond the intertidal zone (Graham & Lee, 2004; Horn & Martin, 2006; Ishimatsu & Gonzales, 2011). During the time intertidal fishes are active out of water, they maintain moist skin and gills with certain behaviours even with a very shallow-water source, although not necessarily fully submerged. These behaviours facilitate maintenance of moisture on respiratory surfaces, including rolling on the side in a shallow pool, increasing the rate of opercular pumping with the mouth in contact with water even if the rest of the body is emerged, and quick dips and jumps in and out of water (Ip et al., 1991; Brown et al., 1992). Alticus kirki has stereotyped behaviours to maintain skin moisture such as returning to shallow pools and rolling on each side in turn in the pool and moving the mouth to draw up water from shallow depressions into and through the mouth and over the gills (Brown et al., 1992). Skippers are known from tropical and temperate habitats, while passive remainers and active emergers are known mostly from temperate waters (Fig. 2). It is likely that there are tropical remainers and emergers that have yet to be discovered. This biogeographical separation may indicate the local presence of ichthyologists more than the occurrence of aerially emerging fishes; there are many species of intertidal blennids in Africa, for example, that warrant study in this regard (Zander et al., 1999). The greater tendency for emergence in tropical species may follow the effects of temperature on ectotherms, as higher temperatures both increase the metabolic demand and decrease the solubility of oxygen in sea water (Martin & Bridges, 1999). Increased exposure to heat stress during aerial exposure triggers the production of heat shock proteins in some temperate zone intertidal fishes (Nakano & Iwama, 2002). Microhabitat choices made by amphibious intertidal fishes during tidal emergence can reduce exposure to desiccation. In addition to returning to pools regularly, fishes that shelter under boulders or within crevices often do so in the presence of small amounts of sea water that remain after the tide recedes. Irrespective of whether the water becomes hypoxic, a fish must maintain adequate moisture on the respiratory surfaces to access the unlimited reservoir of oxygen in the atmosphere (Graham, 1997; Martin & Bridges, 1999). Desiccation can lead to hyperosmolarity of body fluids, causing impaired cardiovascular and renal functions (Dall & Milward, 1969). Water lost through evaporation in air may take a long time to replace following return to sea water (Horn & Riegle, 1981; Luck & Martin, 1999), as sea water is hyperosmotic to teleost tissues. Intertidal fishes stay close to water and do not seem to have much resistance to desiccation (Horn & Riegle, 1981; Luck & Martin, 1999). Desiccation can exacerbate removal of nitrogenous wastes for intertidal fishes; they do not switch from ammonotelism to ureotelism (Evans et al., 1999; Ip et al., 2004) but are very tolerant of high levels of ammonia. This important topic is vital for understanding the full adaptations to the amphibious lifestyle (Chew & Ip, in press). For respiratory organs to work effectively, they must have sufficient surface area for diffusion and the membrane in direct contact with the respiratory medium must



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be very thin and kept moist. This creates a potential conflict between respiratory gas exchange and water balance in terrestrial habitats (Dall & Milward, 1969; Horn & Riegle, 1981). Moisture and skin mucus serve important protective functions in addition to enabling respiratory gas exchange. Modifications of skin morphology such as lack of scales and increased vascularization aid cutaneous respiratory gas exchange (Feder & Burggren, 1985), although respiratory capillaries occur in epithelia over the scales (Zhang et al., 2000). Blood vessels around the head of some skippers redden during air exposure (Zander, 1972; Zander et al., 1999; Zhang et al., 2000), indicating increased blood flow to the skin. Prickles and skin ornamentation on cottids may trap water and reduce water loss.

ABOS FOR AMPHIBIOUS INTERTIDAL FISHES Intertidal fishes typically lack a swimbladder and do not have a unique airbreathing organ (ABO) (Graham, 1976). Instead, these amphibious fishes use gills, skin and linings of the buccal and opercular cavities, more or less modified, for respiratory gas exchange of both oxygen and carbon dioxide in both air and water (Low et al., 1990; Graham, 1997; Gonzales et al., 2011). Modifications of the gills to improve aerial respiration in amphibious fishes appear to be correlated with the level of terrestrial activity and the duration of terrestrial exposure (Low et al., 1990; LeBlanc et al., 2010; Gonzales et al., 2011). In water, gills can be highly elaborate and filamentous, providing high surface area when moisture is omnipresent. In air, however, gills tend to collapse, reducing surface area for diffusion and gas exchange. Decreased surface area of the gills helps prevent collapse when a fish is in air, but reduces the area for diffusion of respiratory gases and also the capacity for ion transport. Temperature and ambient oxygen influence gill remodelling (Sollid & Nilsson, 2006) in water as well as in air. Plastic responses may increase over time of emergence, particularly in the case of K. marmoratus that may remain emerged for weeks at a time (Leblanc et al., 2010). Within the gobiids, species with air breathing ability decreased the use of the gills and increased vascularization of bucco-opercular epithelia (Gonzales et al., 2011). The most highly modified gills of amphibious fishes are seen in those that are either the most active when emerged or those that may remain emerged for long periods of time (Low et al., 1990; Zhang et al., 2000; LeBlanc et al., 2010; Gonzales et al., 2011). These fishes may have very low activity when in water, so this loss of capacity may not be a great constraint, or conversely this loss of surface area may preclude high activity in water. Decreased gill surface area in species that emerge into air, in addition to protection against collapse, may reduce desiccation (Low et al., 1990; Graham, 1997). To compensate for desiccation in air, some oxudercine gobids can temporarily seal up the opercular chamber during terrestrial excursions, holding a small amount of water that moves around to maintain gill hydration (Graham, 1997; Aguilar et al., 2000). This mechanism may also be used to hold air for tidal respiration and to deliver mouthfuls of air to nesting chambers within burrows (Graham et al., 2007; Ishimatsu et al., 2007, 2009) that protect incubating embryos from aquatic hypoxia. Some amphibious fishes show structural cartilage within or between the gill filaments


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to increase support when out of water (Low et al., 1990; Graham, 1997; Martin et al., 2004).

AEROBIC AND ANAEROBIC METABOLISM DURING EMERGENCE FOR INTERTIDAL FISHES It has been hypothesized that survival in air for some intertidal fishes is a byproduct or non-adaptive exaptation to passive exposure, by a sluggish, inactive animal with low metabolic demand that can simply wait out a tidal cycle (Graham, 1976). Certainly, there are examples of fully aquatic air-breathing fishes that nevertheless can survive hours or days out of water if kept cool and damp in a market or transport carrier (Nakamura, 1994; Graham, 1997). Laboratory studies, however, indicate that amphibious intertidal fishes possess adaptations for emergence, adaptations that are not present in closely related subtidal fishes (Congleton, 1974, 1980; Martin, 1993, 1996; Yoshiyama & Cech, 1994; Yoshiyama et al., 1995; Zander, 2011). Respiratory gases follow partial pressure gradients for diffusion and oxygen consumption by metabolism maintains a high gradient for influx of oxygen into animals’ blood whether they are in water or in air. Air is much less viscous and oxygen makes up a much higher portion of the volume of the medium than in water but the partial pressures are the same if both water and air are in equilibrium (Dejours, 1994). Intertidal fishes respiring aquatically cope with the low solubility and slow diffusion rate of oxygen in water with a higher opercular rate of pumping water across the gills than the opercular rate when breathing air (Martin & Bridges, 1999) even under normoxic conditions. Carbon dioxide is much more soluble in water than oxygen (Dejours, 1994). Carbon dioxide produced metabolically can easily diffuse out across the gills following its partial pressure gradient when fishes are in water that is in equilibrium with air. During a low tide, however, aquatic hypercarbia and lower pH can occur in tide-pools, particularly at night, when many animals and plants are respiring and no photosynthesis is replacing oxygen or removing carbon dioxide (Truchot & DuhamelJouve, 1980). This can alter aquatic release of carbon dioxide and increase internal acidity. If a fish emerges from the water and breathes air, the same respiratory surfaces that exchange oxygen aerially also exchange carbon dioxide following their partial pressure gradient (Martin, 1993). Most amphibious intertidal fishes have aerial metabolic rates that are equivalent to their aquatic metabolic rates (Graham, 1976, 1997; Bridges, 1988; Martin & Bridges, 1999). Intertidal amphibious fishes have the capacity for aerobic respiration in air over many hours during tidal exposure, taking up oxygen and releasing carbon dioxide (Teal & Carey, 1967; Edwards & Cech, 1990; Martin, 1991, 1993, 1995). Amphibious species are less likely to need assistance from anaerobic metabolism during air exposure than closely related species from the subtidal zone (Martin, 1996). Upon return to water after a period of time in air, the metabolic rate is the same as it was before emergence, indicating a lack of oxygen debt (Halpin & Martin, 1999). The possibility that amphibious fishes have reduced metabolic rates out of water has been suggested for several intertidal species, including the oxudercine gobid



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Periophthalmodon freycineti (Quoy & Gaimard 1824) (Garey, 1962), blennid A. kirki (Brown et al., 1992) and gobeisocid S. sanguineus (Gordon et al., 1970), in a sort of reverse diving response. The rate of opercular movement when a fish is breathing with gills in air is much lower than when it is using the gills in water, and some fishes cease opercular movements or seal the operculum when emerged in air (Bridges, 1988; Graham, 1997; Martin & Bridges, 1999). The only accurate way to compare metabolism in both media is respirometry (Graham, 1997). In existing studies, however, methods are different and the conditions of the studies are not equivalent, so it is difficult to generalize. The barred mudskipper Periophthalmus argentilinatus Valenciennes 1837 ventilates intermittently while in normoxic water and this might affect measurement of the metabolic rate (Martin & Bridges, 1999). A high aerial respiratory rate for the black prickleback Xiphister atropurpureus (Kittlitz 1858) was observed that was double the rate measured in water (Daxboeck & Heming, 1982), although labelled a resting rate, but a later study found aquatic and aerial respiratory rates at rest to be equivalent (Martin, 1995), suggesting that the animals in the earlier study may have not fully adjusted to the aerial respirometer before measurements were taken. Ambient oxygen tensions are far more variable in water than in air (Randall et al., 1981; Dejours, 1994). Intertidal fishes have increased ventilation rate during aquatic hypoxia (Congleton, 1980; Yoshiyama et al., 1995; Martin, 1996; Sloman et al., 2008) but emerging from water may be more advantageous, when that option is available, than physiological adaptations to survive poor aquatic conditions. An enclosed ABO may be unable to expel all the air tidally between breaths, leading to decreased oxygen and increased carbon dioxide at the respiratory membranes in comparison with air (Johansen & Lenfant, 1968; Piiper & Scheid, 1975). Although a lung provides protection from desiccation by enclosing the respiratory organ, sufficient oxygen may be obtained with relatively few, infrequent breaths, a residual level of pulmonary carbon dioxide may develop, resulting in respiratory acidosis (Graham, 1976, 1997). If the fishes that breathe air with an enclosed ABO remain aquatic, they can get around this constraint by expelling carbon dioxide into water, mostly via the gills or skin (Graham, 1976; Feder & Burggren, 1985), relying on the ABO primarily for oxygen uptake. While out of water, however, a burrowing African lungfish Protopterus aethiopicus Heckel 1851 must only rely on the ABO as it is encased in a mucous cocoon and over time it develops respiratory acidosis and blood hypercarbia (Delaney et al., 1974). On the other hand, one-way flow of air over the gills through the mouth and opercular chambers can lead to rapid desiccation of respiratory membranes, yet it does occur, particularly in active emergers (Table II) such as C. analis (Martin, 1991). The use of gills, buccal and opercular mucosae, and skin for aerial respiration by amphibious fishes (Low et al., 1990; Martin, 1991; Zhang et al., 2000) is advantageous over sole reliance on an enclosed ABO (Randall et al., 1981; Feder & Burggren, 1985; DeJours, 1994), allowing the respiratory system to be in direct contact with the respiratory medium (Piiper & Scheid, 1975). The efficiency of gas exchange is revealed by the respiratory exchange ratio (RER), the ratio of carbon dioxide expelled to the oxygen consumed. This ratio can be calculated for the whole animal, either instantaneously or over a long period of time, or for different respiratory organs of the same animal (Graham, 1976). Across all respiratory structures of the entire organism, RER is between 0·7 and 1·0, depending


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on metabolic fuel. For intertidal fishes, measured whole-body RER is generally within that range during emergence (Martin & Lighton, 1989; Martin, 1993), indicating that respiratory acidosis does not occur. On the other hand, breathing air while aquatic, P. aethiopicus has a low RER at the lung, where oxygen is consumed but little carbon dioxide is released, and a high RER at the gills, indicating significant carbon dioxide release but little oxygen exchange (Johansen & Lenfant, 1968). In comparing temperate zone cottid sculpins across an intertidal habitat gradient, Martin (1996) found different propensities for emergence behaviours and aerial respiration. Sloman et al. (2008) and Mandic et al. (2009) found increased ability to take up oxygen provided greater tolerance of aquatic hypoxia. This was accomplished with changes in gill surface area, increased haemoglobin affinity for oxygen and decreased metabolic rate. The phylogenetic comparison within one family makes this approach particularly powerful (Richards, 2011) and this approach could be fruitful for study of other intertidal fish communities. The twin strategies of hypoxia tolerance and aerial emergence may work synergistically for intertidal fishes (Gracey et al., 2001, 2011).

M E TA B O L I C S U P P O RT F O R T E R R E S T R I A L A C T I V I T Y O F I N T E RT I D A L F I S H E S

Most intertidal fishes do not engage in sustained levels of high activity, whether in or out of water (Ralston & Horn, 1986; Horn & Gibson, 1988; Horn & Martin, 2006). The highly amphibious skippers apparently power their usual levels of terrestrial activity primarily with aerobic metabolism, without incurring an oxygen debt (Graham et al., 1985; Hillman & Withers, 1987; Martin & Lighton, 1989). Oxygen consumption during periods of high activity has been examined for only three skipper species of intertidal fishes, P. argentilinatus (Hillman & Withers, 1987), A. kirki (Martin & Lighton, 1989) and the giant mudskipper Periophthalmodon schlosseri (Pallas 1770) (Takeda et al., 1999). All were able to increase their oxygen consumption rates in air greatly above resting levels during activity. Xiphister atropurpureus, a passive remainer, can double its rate of oxygen consumption in air (Daxboeck & Heming, 1982; Martin, 1995), suggesting that aerobic scope for activity exists in many amphibious fishes, even in those that are relatively inactive. If intertidal fishes are forced into exhaustive activity on land, they generate lactic acid through anaerobic metabolism (Scholander et al., 1962; Martin et al., 2004). In fishes, rapid bouts of exercise that are fuelled anaerobically may require recovery over many hours because of the accumulation of lactate (Teal & Carey, 1967). The ability to recover from an oxygen debt for P. schlosseri is more readily accomplished in air than in water (Takeda et al., 1999), suggesting the respiratory system of this skipper is better adapted for air breathing than aquatic life. An increased RER above 1·0 may be an indication of similar metabolic effort in A. kirki (Martin & Lighton, 1989).



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AIR BREATHING AND EMERGENCE FOR SPAWNING IN THE INTERTIDAL ZONE Beach spawning has evolved multiple times in teleost lineages (Martin & Swiderski, 2001; Martin et al., 2004) on gravel or rocky beaches (Frank & Leggett, 1981; MacDonald et al., 1995; Yamahira, 1996), on sandy shores (Walker, 1952; Thomson & Muench, 1976), in vegetation or shells (Taylor et al., 1977; Middaugh, 1981) or in mud burrows (Swenson, 1999; Ishimatsu et al., 2007). Oviposition in the intertidal zone provides many benefits to embryos related to tidal aerial exposure (Martin & Strathmann, 1999; Martin et al., 2004), along with some obvious potential disadvantages (Strathmann & Hess, 1999). The advantages are sufficient that numerous species of teleosts that live subtidally visit the intertidal zone solely for the purpose of spawning (DeMartini, 1999; Martin et al., 2004). Resident intertidal fishes spawn and nest within the intertidal zone as expected in their local tidal height (Morris, 1952, 1956; Wells, 1986; Coleman, 1992; DeMartini, 1999). After spawning, some intertidal species leave one parent to guard the clutch. Fishes guarding eggs or protecting young ones may be passive remainers (Fig. 1), staying with the nest and emerging into air as tides recede (Marliave & DeMartini, 1977; Crane, 1981; Coleman, 1992, 1999). Parental care is seen among stichaeids, cottids, clingfishes, pholids and blennids in shallow pools under boulders in rocky intertidal habitats (Coleman, 1999). Not all teleosts that spawn in the intertidal zone guard their clutches; some only guard aquatically when tides are sufficiently high (Marliave, 1981). More research needs to be done on species with parents caring for their offspring in intertidal habitats (Coleman, 1999) but it is clear that many of those parents are exposed to air tidally and are able to breathe air, although they emerge only at certain times of the year (Martin, 1993, 1995). In addition to their amphibious air-breathing capabilities, the adults may have an increased tolerance for aquatic hypoxia (Congleton, 1980; Ishimatsu et al., 2007; Richards, 2011). Tolerance of hypoxic aquatic conditions is adaptive for intertidal fishes but the eggs must avoid aquatic hypoxia. To avoid the potential problem of embryos being exposed to aquatic hypoxia, some intertidal species including P. notatus, the northern clingfish Gobiesox meandricus (Girard 1858) and the cottid C. acuticeps glue their clutches to the walls or ceiling of the incubation chamber, at the bottom of a boulder that shelters a shallow pool at its base (Marliave & DeMartini, 1977; Crane, 1981; Marliave, 1981; Coleman, 1999; Ishimatsu et al., 2007). The eggs are exposed to air either by the low tide or by the guarding adult’s deliberate introduction of mouthfuls of air into a mud burrow (Ishimatsu et al., 2009; Ishimatsu & Graham, 2011). The small amount of water that remains provides humidity but may not be in direct contact with the developing embryos or their eggs. The mobile adults may also be able to avoid or recover from hypoxia exposure by moving into either air or well-aerated water. Teleosts that are transient visitors to the intertidal zone tend to visit mainly during high tides and move out to sea during low tides when the area is exposed to air (Gibson, 1982; Horn & Gibson, 1988). Air exposure for most intertidal fishes occurs mainly during low tides. In contrast, spawning in the intertidal zone typically is synchronized around the highest tides, to place the clutches vertically on shore for tidal exposure of embryos to air (Jones, 1972; Taylor et al., 1977; Frank & Leggett, 1981; Middaugh et al., 1983; Tewksbury and Conover, 1987; DeMartini, 1999; Martin &


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Swiderski, 2001; Martin et al., 2004). Most species that engage in this activity do not emerge from water, or emerge only partially and accidentally. Some species, e.g. F. heteroclitus, have some ability to breathe air when emerged (Halpin & Martin, 1999), while others, including the subtidal fugu puffer Takifugu niphobles (Jordan & Snyder 1901) (Yamahira, 1996), the capelin Mallotus villosus (Müller 1776) (Frank & Leggett, 1981) and the California grunion Leuresthes tenuis (Ayres 1860) (Martin et al., 2004) apparently do not breathe air. The Atlantic silverside Menidia menidia (L. 1766) spawns aquatically in shallow water during high tides but suffers local hypoxia followed by a spawning stupor that leaves fish vulnerable to predators (Middaugh, 1981). Fishes that emerge into air during spawning activity have the adaptive benefit of escaping from increasingly hypoxic water. Some beach-spawning fishes reduce their metabolic rate or heart rate while emerged in air (Garey, 1962; Martin et al., 2004). Leuresthes tenuis spawns completely out of water, while its congener the gulf grunion L. sardina (Jenkins & Evermann 1889) spawns at the water’s edge (Walker, 1952; Thomson & Muench, 1976). Neither species can survive for a long period in air. Normal spawning activity does not require anaerobic metabolism for either male or female L. tenuis (Martin et al., 2004). If forced into exhaustive activity by experimental manipulation on land, however, L. tenuis accumulates lactic acid (Scholander et al., 1962; Martin et al., 2004). Embryos with aerial incubation and oviposition high in the intertidal zone may rely on environmental cues to hatch (Martin, 1999; Martin et al., 2011). Within burrows in mudflats, the gobid skippers P. schlosseri and Periophthalmus modestus Cantor 1842 generate an air chamber for the clutch of eggs during development (Ishimatsu et al., 2007, 2009). The parents deliver gulps of air from the opercula and mouth to the nest site until a bubble of air is formed around the clutch. When it is time for the eggs to hatch, the guarding parent removes the air by reversing the process to allow the hatchling larvae to swim freely into the water (Ishimatsu & Graham, 2011).

AIR-BREATHING MARINE FISHES IN ESTUARIES Estuarine habitats are tidally influenced but typically retain areas of open water during low tides and may experience aquatic hypoxia to a greater degree than tidepools. Egg-laying cyprinodontids are common in temperate and tropical estuaries. The gulf killifish Fundulus grandis Baird & Girard 1853 (Martinez et al., 2006) and F. heteroclitus (Richards et al., 2008) are tolerant to hypoxia, and F. heteroclitus also breathes air when emerged (Halpin & Martin, 1999). Kryptolebius marmoratus may emerge in response to aquatic hydrogen sulphide (Abel et al., 1987) as well as hypoxia. It can survive extended aerial emergence of weeks or months by taking refuge in tree trunks and vegetation (LeBlanc et al., 2010). In air, the gills undergo extensive remodelling that reduces the surface area and the skin takes on more respiratory function in air through angiogenesis. When aerial exposure is prolonged beyond a few hours of a tidal cycle, morphological effects increase (LeBlanc et al., 2010), including a profound reorganization of the gill and skin structure during periods of terrestriality that may last months. Some teleosts living in estuarine habitats are able to breathe air in response to hypoxia, in a manner different from that of the amphibious intertidal fishes discussed



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so far. The family Gobiidae, well represented in the skippers, includes an estuarine longjaw mudsucker Gillichthys mirabilis Cooper 1864 (Todd & Ebeling, 1966). This species has been observed out of water but it also gulps air at the surface and shows reddening of cutaneous surfaces of the head and lips, indicating increased cutaneous blood flow (Todd, 1968). This species tolerates aquatic hypoxia well (Gracey et al., 2001, 2011). A similar manner of air breathing at the water surface is seen in the Australian goby Arenigobius bifrenatus (Kner 1865) (Zander, 2011). The tidewater goby Eucyclogobius newberryi (Girard 1856) has been observed in hypoxic water gulping air (C. Swift, pers. comm.). This protected species nests in mud burrows with parental care (Swenson, 1999). Among marine teleosts, only the tarpons Megalops atlanticus Valenciennes 1847 and Megalops cyprinoides (Broussonet 1782) use the swimbladder as a respiratory organ (Geiger et al., 2000; Wells et al., 2003), unless one also includes the gar (Lepisosteus sp.) that are reported to enter estuaries. Both M. atlanticus and M. cyprinoides breathe air facultatively, under conditions of hypoxia or other aquatic stressors when they venture into brackish water. The ability to breathe air while aquatic allows increased metabolism and more rapid recovery from activity in these species than if only aquatic respiration is used (Geiger et al., 2000; Wells et al., 2003). Finally, the only known marine teleost that breathes air with the assistance of a non-respiratory swimbladder is the Pacific fat sleeper Dormitator latifrons (Richardson 1844). This animal is not amphibious. Remaining in the water, it uses the air bladder not as scuba tank but as a flotation device, becoming positively buoyant to rise to the surface of hypoxic water (Todd, 1973; Graham, 1997). Respiratory gas exchange takes place cutaneously as the top of the head is held in the air above the water surface.

FUTURE DIRECTIONS Intertidal fishes show a variety of adaptive ecological niches for air breathing and amphibious behaviour. They emerge from water to reproduce, care for offspring, defend territories, feed or escape harsh aquatic conditions. The triggers for emergence and air breathing may be different for intertidal fishes than for freshwater air-breathing fishes or those from estuaries (Sayer & Davenport, 1991). The numerous species and diverse families of amphibious teleosts provide a wealth of examples for adaptation to variable habitats near the ocean’s edge and excellent opportunities for comparative studies of phylogenetically close species across habitat gradients (Zander, 1972; Horn & Riegle, 1981; Low et al., 1990; Martin, 1996; Ip et al., 2002; Mandic et al., 2009; Richards, 2011). These studies may provide scenarios for the tetrapod land invasion (Schultze, 1999; Graham & Lee, 2004; Clack, 2007). The geographic extent of amphibious fishes may be far greater than is generally appreciated. It is likely that many additional species of intertidal fishes are amphibious to some degree and are awaiting discovery and study by physiologists and behavioural ecologists. Intertidal fishes lack special respiratory structures to exchange oxygen and carbon dioxide in air. Gill remodelling affects aquatic respiration to the extent that in air, gills may be unimportant and cutaneous respiration may play a large role in some


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amphibious fishes. Additional studies of morphology combined with regulation and expression of ion channels for permeability and transport systems in the gills and skin of amphibious fishes will help to elucidate adaptations for these animals, which must balance the challenges of surviving in two different respiratory media. In addition, longitudinal studies of individuals exposed to different aquatic and aerial oxygen tensions can help clarify the control mechanisms for these morphological changes. Aerobic metabolism appears to be sufficient to power most terrestrial bouts for active emergers and skippers, although anaerobic metabolism can be called upon if needed. Some skipper fishes can recover from activity powered by anaerobic metabolism while terrestrial but it is not known whether active emergers or passive remainers must return to water to recover an oxygen debt, for example, following a predator attack. Many passive remainer fishes provide parental care and the behaviours and metabolic costs, as well as predation risks of this, have not been fully examined. Many species in multiple lineages of fishes spawn in the intertidal zone to provide the benefits of some exposure to air of the embryos during incubation and early development. The environmental cues that trigger this behaviour are not known and could be very different than the cues that trigger amphibious emergence of fishes during low tides. How embryos cope with aquatic hypoxia is not known. Adaptations to prevent or survive aquatic hypoxia for clutches and nests should be examined for burrow-nesting species. An interesting research question might be to examine the trade-off or competing selection pressures between the potential for desiccation in air and the danger of aquatic hypoxia during a low tide. Comparative analysis of the physiology and behaviour among different gobies would provide insights into different nesting habitats. The limited knowledge about the ecology and physiology of marine intertidal fishes prompts concern about identifying and protecting these species during a time of coastal development and sea-level rise. These hardy denizens that live on the edge between two habitats have much to teach us about adaptation and change. I am grateful to the organizers for the invitation to submit this paper. J. B. Graham, M. H. Horn and C. Bridges shared many interesting ideas and great enthusiasm for the intertidal fishes. A. Lim created the figures. Thanks to NOAA-National Marine Fisheries Service, Contract WRAD 8-819, National Geographic Society CRE 8105-07, California Coastal Commission and Pepperdine University for support.

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Alcohol and narcotic abuse: variations on an addictive theme.

Integrated care in the UK: variations on a theme?

Kinase Regulation in Mycobacterium tuberculosis: Variations on a Theme.

Prokaryotic Argonautes - variations on the RNA interference theme.

Variations on a theme: Topic modeling of naturalistic driving data.

Variations on the theme: allosteric control in hemoglobin.

Breast self-examination and the health belief model: variations on a theme.

Theme and variations: evolutionary diversification of the HET-s functional amyloid motif.