A Comparative Study of Terrestrial Adaptations of the Gills in Three Mudskippers—<i>Periophthalmus chrysospilos, Boleophthalmus boddaerti</i>, and<i>Periophthalmodon schlosseri</i>

Low, W. P.; Lane, David; Ip, Yuen K.

doi:10.2307/1541736

Cited by 91 publications

(81 citation statements)

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“…In air-breathing fish, the gills exhibit irreversible changes in morphology depending on the relative dependence on water or air for gas exchange (Low et al, 1988;Mattias et al, 1996Mattias et al, , 1998Perna and Fernandes, 1996;Takasusuki et al, 1998;Wilson et al, 1999;Graham et al, 2007). The smallest gill surface area has been documented for the South American lungfish, Lepidosiren paradoxa (Lepidosirenidae), which has irregularly arranged short papillar gill lamellae.…”

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confidence: 99%

Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

Ramos

Fernandes²,

Costa

et al. 2013

The Anatomical Record

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The gill structure of the Amazonian fish Arapaima gigas, an obligatory air breather, was investigated during its transition from water breathing to the obligatory air breathing modes of respiration. The gill structure of A. gigas larvae is similar to that of most teleost fish; however, the morphology of the gills changes as the fish grow. The main morphological changes in the gill structure of a growing fish include the following: (1) intense cell proliferation in the filaments and lamellae, resulting in increasing epithelial thickness and decreasing interlamellar distance; (2) pillar cell system atrophy, which reduces the blood circulation through the lamellae; (3) the generation of long cytoplasmic processes from the epithelial cells into the intercellular space, resulting in continuous and sinuous paracellular channels between the epithelial cells of the filament and lamella that may be involved in gas, ion, and nutrient transport to epithelial cells; and (4) intense mitochondria-rich cell (MRC) proliferation in the lamellar epithelium. All of these morphological changes in the gills contribute to a low increase of the respiratory surface area for gas exchange and an increase in the water-blood diffusion distance increasing their dependence on air-breathing as fish developed. The increased proliferation of MRCs may contribute to increased ion uptake, which favors the regulation of ion content and pH equilibrium. Anat Rec, 296:1664Rec, 296: -1675

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confidence: 99%

Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

Ramos

Fernandes²,

Costa

et al. 2013

The Anatomical Record

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“…Morphological alterations seen in some air-breathing fishes may help sustain blood circulation in air. For example, the mudskipper, Periophthalmodon schlosseri, has thick, fused lamellae (Low et al 1988), as was observed in P. modestus (Figure 1c'). The gill filaments of the swamp eel, Synbranchus marmoratus, are supported by hypertrophied, spirally configurated gill rays (Liem 1987), and the gills of the electric eel, Electrophorus electricus, were reported to be degenerative (Carter 1935).…”

Section: Discussionmentioning

confidence: 65%

“…In comparison, burrow-dwelling O. lacepedii experiences aquatic hypoxia for longer durations, but retains well-developed gills as shown in this study. Likewise, less terrestrial mudskippers of the genus Boleophthalmus also possess well-developed gills with no apparent modifications as evident for Periophthalmus and Periophthalmodon (Low et al 1988). These observations apparently favor the more traditional view that gill reduction is the result of increasing reliance on a novel air-breathing organ for oxygen supply (Munshi 1976).…”

Section: Discussionmentioning

confidence: 98%

“…A similar view was advanced earlier by Randall et al (1981), citing examples from the lungfish, Lepidosiren and Protopterus. However, the universality of this thesis might be put into question considering that the gills diminish also among marine air-breathing fishes, such as mudskippers (Figure 1; see also Low et al 1988), in which hypoxic exposure may be periodical and depend upon the duration of burrow confinement during high tide. In fact, hypoxic exposure is least likely for the more terrestrially adapted species such as Periophthalmus, which usually stays above water's edge during high tide (Colombini et al 1995;Ikebe & Oishi 1996).…”

Section: Discussionmentioning

confidence: 99%

“…This holds true especially for amphibious mudskippers residing in intertidal mudflats whose adaptation to terrestrial life, albeit varies widely among species, is apparently reflected in different degrees of morphological alterations of the gills to prevent them from collapsing in air (Schöttle 1931; Tamura & Moriyama 1976;Low et al 1988). The eel goby, Odontamblyopus lacepedii (family Gobiidae, subfamily Amblyopinae), is one of the recently reported brackish-marine species that breathe air using the buccal-opercular cavity when it stays in its hypoxic mudflat 4 burrow during low tide (Gonzales et al 2006).…”

Section: Introductionmentioning

confidence: 99%

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Respiratory vasculatures of the intertidal air-breathing eel goby, Odontamblyopus lacepedii (Gobiidae: Amblyopinae)

2007

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SynopsisLacking a propensity to emerge over the mud surface, Odontamblyopus lacepedii survives low tide periods by continuously breathing air in burrows filled with hypoxic water. As with most marine air-breathing fishes, O. lacepedii does not possess an accessory air-breathing organ, but holds air in the buccal-opercular cavity. The present study aimed to clarify how the respiratory vasculature has been modified in this facultative air-breathing fish. Results showed that the gills apparently lacked structural modifications for air breathing, whereas the inner epithelia of the opercula were richly vascularized. Comparison with two sympatric gobies revealed that the density of blood capillaries within 10 µm from the inner opercular epithelial surface in O. lacepedii (14.5±3.0 capillaries mm -1 ; mean±s.d., n=3) was significantly higher than in the aquatic non-air-breathing Acanthogobius hasta (0.0±0.0) but significantly lower than in the amphibious air-breathing mudskipper Periophthalmus modestus (59.1±8.5). The opercular capillary bed was supplied predominantly by the 1 st efferent branchial arteries (EBA1) and drained by the opercular veins, which open into the anterior cardinal vein. Deep invaginations at the distal end of the EBA1 and the junction with EBA2 are suggestive of blood flow regulatory sites during breath-holding and apnoeic periods. It remains to be investigated how blood flow through the gills is maintained during breath holding when the buccal-opercular cavity is filled with air. 3 IntroductionWhile many freshwater air-breathing fishes possess a wide array of specialized accessory air-breathing organs (e.g. lungs, gas bladder, stomach, intestine, and suprabranchial chambers), most brackish and marine air-breathing fishes lack such specializations but use the buccal-opercular epithelia, skin and possibly the gills for aerial gas exchange (for review see Graham 1997;Martin & Bridges 1999;Sayer 2005). Typical fish gills are highly efficient gas exchangers in water but not in air since the lamellae are prone to gravitational collapse, resulting in a significant reduction of their functional respiratory surface area and an elevation of vascular resistance (Maina 2000). This is partly the reason Randall et al. (1981) attributed the non-existence of a single terrestrial vertebrate species that exclusively relies on gills for aerial respiration.It is a general perception that the gills of air-breathing fishes reduce their surface area with increasing reliance on aerial gas exchange (Munshi 1976;Graham 1997). This holds true especially for amphibious mudskippers residing in intertidal mudflats whose adaptation to terrestrial life, albeit varies widely among species, is apparently reflected in different degrees of morphological alterations of the gills to prevent them from collapsing in air (Schöttle 1931; Tamura & Moriyama 1976;Low et al. 1988). The eel goby, Odontamblyopus lacepedii (family Gobiidae, subfamily Amblyopinae), is one of the recently reported brackish-marine species that breathe air using t...

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The mudskipperPeriophthalmodon schlosseri respires more efficiently on land than in water and vice versa forBoleophthalmus boddaerti

et al. 1998

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A Comparative Study of Terrestrial Adaptations of the Gills in Three Mudskippers—Periophthalmus chrysospilos, Boleophthalmus boddaerti, andPeriophthalmodon schlosseri

Cited by 91 publications

References 10 publications

Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

Respiratory vasculatures of the intertidal air-breathing eel goby, Odontamblyopus lacepedii (Gobiidae: Amblyopinae)

The mudskipperPeriophthalmodon schlosseri respires more efficiently on land than in water and vice versa forBoleophthalmus boddaerti

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