J Exp Biol Advance Online Articles. First posted online on 16 August 2012 as doi:10.1242/jeb.074831 Access the most recent version at http://jeb.biologists.org/lookup/doi/10.1242/jeb.074831
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RESEARCH ARTICLE
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Gill remodelling during terrestrial acclimation reduces aquatic respiratory function of the
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amphibious fish Kryptolebias marmoratus
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Andy J. Turkoa, Chris A. Cooperb, Patricia A. Wrightc
The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
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a
Department of Integrative Biology, University of Guelph, 488 Gordon Street, Guelph,
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Ontario N1G 2W1, Canada.
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Email:
[email protected]
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b
Department of Chemistry, Wilfrid Laurier University, 75 University Avenue West,
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Waterloo, Ontario N2L 3C5, Canada.
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Email:
[email protected]
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c
Department of Integrative Biology, University of Guelph, 488 Gordon Street, Guelph,
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Ontario N1G 2W1, Canada.
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Email:
[email protected]
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Keywords:
phenotypic plasticity, trade-offs, gill remodelling, mangrove rivulus
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1 Copyright (C) 2012. Published by The Company of Biologists Ltd
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ABSTRACT
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The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
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The skin-breathing amphibious fish Kryptolebias marmoratus experiences rapid
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environmental changes when moving between water- and air-breathing, but remodelling of
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respiratory morphology is slower (~1 week). We tested the hypotheses that (1) there is a trade-
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off in respiratory function of gills displaying aquatic versus terrestrial morphologies, and (2)
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rapidly increased gill ventilation is a mechanism to compensate for reduced aquatic respiratory
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function. Gill surface area, which varied inversely to the height of the interlamellar cell mass,
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was increased by acclimating fish for 1 week to air or low ion water, or decreased by acclimating
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fish for 1 week to hypoxia (~20% dissolved oxygen saturation). Fish were subsequently
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challenged with acute hypoxia and gill ventilation or oxygen uptake was measured. Fish with
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reduced gill surface area increased ventilation at higher dissolved oxygen levels, showed an
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increased critical partial pressure of oxygen, and suffered impaired recovery compared to
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brackish water control fish. These results indicate that hyperventilation, a rapid compensatory
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mechanism, was only able to maintain oxygen uptake during moderate hypoxia in fish that had
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remodelled their gills for land. Thus, fish moving between aquatic and terrestrial habitats may
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benefit from cutaneously breathing oxygen-rich air, but upon return to water must compensate
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for a less efficient branchial morphology (mild hypoxia) or suffer impaired respiratory function
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(severe hypoxia).
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INTRODUCTION
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Adaptive phenotypic plasticity occurs when an organism can produce a range of
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relatively fit alternative phenotypes in response to the environment. Alternative physiological
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phenotypes can be expressed relatively quickly in response to an environmental change, while
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morphological changes often take longer (Piersma and van Gils, 2011). Therefore, the
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advantages of plasticity may be limited by lag-times between experiencing environmental
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change and remodelling the phenotype accordingly (DeWitt et al., 1998; Pigliucci, 2001;
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Callahan et al., 2008; Auld et al., 2010). Plasticity of functionally related traits, however, may
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be temporally integrated in order to cope with the environmental change immediately and over
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time (Schlichting and Pigliucci, 1998; Pigliucci, 2001; Relyea, 2003). Amphibious fishes
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experience abrupt environmental changes when moving between aquatic and terrestrial habitats.
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Can the temporal integration of physiological and morphological respiratory phenotypes ease the
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transition between respiratory media?
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Amphibious fishes require unique gills that can tolerate exposure to both water and air.
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During air exposure (emersion) gills are vulnerable to desiccation and, when the lamellae are
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unsupported by water, these collapse and coalesce which can cause permanent damage.
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Therefore many amphibious fishes have gills with relatively short and thick lamellae that are
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able to function during frequent transitions between air and water with few morphological
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adjustments (Graham, 1997; Sayer, 2005). Conversely, the Amazonian fish Arapaima gigas
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dramatically and permanently remodels its gills, reducing surface area, during ontogeny as the
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fish transition from obligate water breathers to obligate air breathers (Brauner et al., 2004). The
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amphibious mangrove rivulus (Kryptolebias marmoratus (Poey); formerly mangrove killifish
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The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT
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Rivulus marmoratus) is able to reversibly remodel its gill morphology in response to air exposure
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by developing a mass of cells between the lamellae, the interlamellar cell mass (ILCM) (Ong et
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al., 2007). The ILCM develops after 7 d in air and reduces functional gill surface area, likely to
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protect the delicate lamellae or reduce water loss (Ong et al., 2007). Frequent voluntary
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emersions can also cause ILCM enlargement (Turko et al., 2011). In the wild, mangrove rivulus
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typically inhabit extremely hypoxic (
