In many air-breathing fishes, as well as in oxudercine gobies, the capacity to breathe both in water and in air (bimodal respiration) seems to be an adaptation to low environmental levels of oxygen (hypoxia) and high concentrations of carbon dioxide (hypercarbia or 'environmental hypercapnia') (Graham, 1997; Horn et al., 1999; Ultsch, 1996). This adaptations enable these fishes to live in highly organically polluted waters.

In fact, several systematically unrelated gobiid species (e.g. Typhlogobius californiensis, Gillichthys mirabilis) are capable of efficient aquatic respiration in hypoxic waters. On the contrary, amphibious mudskippers like Periophthalmodon schlosseri or Periophthalmus barbarus are poorly adapted to respire aquatically during hypoxia and minimise exposure to hypoxic stress through aerial respiration (Aguilar, 2000).

These behavioural and physiological adaptations can be very efficient. Even relatively more aquatic oxudercine species can be very abundant in waters with high organic loads (e.g. Pseudapocryptes elongatus: Takita et al., 1999).

All oxudercine gobies are burrowers that deeply penetrate in hypercarbic soft substrates almost devoid of oxygen (anoxic), like most of the probably closely related amblyopine gobies (Thacker, 2003; Akihito et al., 2000; see also Systematics & Biogeography). These sediments are characterised by low redox potential values and high ammonia, soluble phosphates and acid sulphides concentrations (e.g. in mangal sediments: Hogarth, 1999). These same conditions are found at depth inside burrows (Ishimatsu et al., 2000).

On the other hand, on exposed substrates there are rapid and extreme variations of relative air humidity, air and soil temperature and salinity of capillary water (Macintosh, 1977).

Even without taking into account the much more diverse and extreme conditions of the terrestrial environment relative to the aquatic one, in the absence of specific adaptations the emergence behaviour is a tough challenge for a fish to meet.

Just to mention some of emergence's consequences: the collapse and coalescence of branchial filaments and associated increase of vascular resistance; drastic decrease of CO2 elimination rate and consequent blood acidosis; accumulation of toxic nitrogen compounds in various tissues due to hindrance of excretory mechanisms; and finally body dehydration, whose effects impact on all the a.m. processes (Graham, 1997; Martin, 1996; Ultsch, 1996).

Air Breathing Organs (ABOs) of Pseudapocryptes lanceolatus. A: ventral view of head, pectoral and pelvic fins ; the dashed lines indicate the extension of expanded opercular pouches. B: medial view of the opercular circulatory system (arrows show the direction of blood flow). Modified from Graham, 1997, with permission from Elsevier.

If adaptations to the amphibious life of most terrestrial mudskippers (e.g. Periophthalmus spp.) are unrivalled among all living aquatic chordates, adaptations to aerial respiration are relatively simple and less efficient when compared to those of other freshwater air-breathing fishes (e.g. species included in the families Electrophoridae, Anabantidae, Belontiidae). Nonetheless, these efficient air-breathers are almost completely aquatic and only in a few cases do present rudimentary amphibious behaviours, emerging from polluted or overcrowded waters to look for better aquatic environmental conditions (Graham, 1997; Graham & Lee, 2004).

On the contrary, oxudercine gobies are not endowed with particularly complex ABOs (Air Breathing Organs): this is a general rule for all marine air-breathing fishes, including the amphibious rockskippers (Martin & Bridges, 1999) and the neotropical cyprinodontid Rivulus marmoratus (Davis et al. 1990; Grizzle & Thiyagarajah, 1987).

The few oxudercine species whose ABOs have been studied so far make use of the same gas-exchange surfaces both in air and in water: the bucco-pharyngeal epithelium, the opercular membrane, the skin of the head and body (cutaneous respiration), and the gills (Graham, 1997).

The complex and highly derived structure of the ABO of a completely aquatic and freshwater fish, the anabantoid Osphronemus sp.
Lateral view: S= suprabranchial chamber; L= labirinth; G= gill; O= operculum. Modified from Graham, 1997, with permission from Elsevier.

Such structures are often the result of adaptative trade-offs. For instance, the same gills' morphological traits that enables these species to reduce water losses and to counteract the force of gravity out of water (Low et al., 1990) considerably reduce their efficiency in water, particularly in environmental hypoxic conditions.
This further enhances the adaptive value of emergence behaviour and of cutaneous respiration (Martin & Bridges, 1999; Aguilar, 2000).

Other possible sites of respiratory gas exchange are the highly vascularised skin of pectoral fins and the esophagous (Milward, 1974). It should be noted that in contrast with many freshwater species with complex ABOs, the elimination of CO2 does not seem to be a problem for oxudercines and other marine fishes with amphibious behaviours, thanks to the wider area of their gas exchange surfaces (Martin & Bridges, 1999).

Several gobies can hold air bubbles in the oral cavity while they are in water (AG= air gulping: Gee & Gee, 1995), but more terrestrial mudskippers (i.e. Periophthalmus spp. and Periophthalmodon spp.) also do that whilst out of water, by sealing opercular chambers through a ventro-medial valve (Sponder & Lauder, 1981; Clayton, 1993; Martin & Bridges, 1999; Graham, 1997). These species mostly rely on cutaneous respiration and on highly vascularised bucco-pharyngeal mucosae in air; wereas whilst they are in water, where O2 extraction is less efficient, they make use of both branchial and cutaneous respiration (Clayton, 1993; Ishimatsu et al., 1999; Takeda et al., 1999).

On the contrary, more aquatic species like ones of the genera Boleophthalmus and Scartelaos, are endowed with less specialized structures for air breathing (Kok et al., 1998) and with greater relative gill area (Low et al., 1990; Milward, 1974): therefore, they respire more efficiently in water, mostly relying on gills.

The enigma of the long permanence in submerged burrows at high tide in almost anoxic conditions has only been recently solved. Several oxudercine species transport air bubbles into specialized chambers of their burrows, where they maintain an air phase (Ishimatsu et al., 1998; 2000; Lee et al., 2005). Burrowing seems therefore to be the pre-adaptation that enabled the ancestors of mudskippers to solve both the problems of eventual emersion and of environmental hypoxia in intertidal habitats.

However, some of these species are also capable of slowing down oxygen consumption rates while in water, beginning to produce lactate only after several hours of environmental hypoxic conditions (Ip et al., 1990; Ip & Low, 1990).

Periophthalmodon schlosseri and Pn. freycineti (the only known cases in fishes) slow down their heartbeat (bradycardia) during forced submersion and accelerate it (tachycardia) upon re-emersion, not unlike that observed in marine mammals during apnoea (bradycardic diving syndrome: Costa, 1999; Ishimatsu et al., 1999; Kok et al., 1998; Garey, 1962).

In fact, Pn. schlosseri seems unable to repay a metabolic oxygen debt while in water, where it cannot significantly increase oxygen absorption (Takeda et al., 1999).

Periophthalmodon schlosseri (dorsal view) holding a bubble of air in its mouth (note the expanded opercular pouches). This specimen emerges from a thin layer of water. From discover.com

Periophthalmodon schlosseri in a respirometer chamber, where oxigen uptake and CO2 excretion can be measured. Photo: Florian Borutta (2006), with permission