Gill remodelling during terrestrial acclimation reduces aquatic ...

3 downloads 2696 Views 303KB Size Report
Aug 16, 2012 - Fish go wireless! J. Fish Biol. 57, 197-209. 441. Auld, J. R., Agrawal, A. A. and Relyea, R. A. (2010). Re-evaluating the costs and limits of. 442.
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

1

RESEARCH ARTICLE

2 3

Gill remodelling during terrestrial acclimation reduces aquatic respiratory function of the

4

amphibious fish Kryptolebias marmoratus

5

Andy J. Turkoa, Chris A. Cooperb, Patricia A. Wrightc

The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT

6 7 8

a

Department of Integrative Biology, University of Guelph, 488 Gordon Street, Guelph,

9

Ontario N1G 2W1, Canada.

10

Email: [email protected]

11

b

Department of Chemistry, Wilfrid Laurier University, 75 University Avenue West,

12

Waterloo, Ontario N2L 3C5, Canada.

13

Email: [email protected]

14

c

Department of Integrative Biology, University of Guelph, 488 Gordon Street, Guelph,

15

Ontario N1G 2W1, Canada.

16

Email: [email protected]

17 18

Keywords:

phenotypic plasticity, trade-offs, gill remodelling, mangrove rivulus

19 20 21 22 23

1 Copyright (C) 2012. Published by The Company of Biologists Ltd

24

ABSTRACT

25

The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT

26

The skin-breathing amphibious fish Kryptolebias marmoratus experiences rapid

27

environmental changes when moving between water- and air-breathing, but remodelling of

28

respiratory morphology is slower (~1 week). We tested the hypotheses that (1) there is a trade-

29

off in respiratory function of gills displaying aquatic versus terrestrial morphologies, and (2)

30

rapidly increased gill ventilation is a mechanism to compensate for reduced aquatic respiratory

31

function. Gill surface area, which varied inversely to the height of the interlamellar cell mass,

32

was increased by acclimating fish for 1 week to air or low ion water, or decreased by acclimating

33

fish for 1 week to hypoxia (~20% dissolved oxygen saturation). Fish were subsequently

34

challenged with acute hypoxia and gill ventilation or oxygen uptake was measured. Fish with

35

reduced gill surface area increased ventilation at higher dissolved oxygen levels, showed an

36

increased critical partial pressure of oxygen, and suffered impaired recovery compared to

37

brackish water control fish. These results indicate that hyperventilation, a rapid compensatory

38

mechanism, was only able to maintain oxygen uptake during moderate hypoxia in fish that had

39

remodelled their gills for land. Thus, fish moving between aquatic and terrestrial habitats may

40

benefit from cutaneously breathing oxygen-rich air, but upon return to water must compensate

41

for a less efficient branchial morphology (mild hypoxia) or suffer impaired respiratory function

42

(severe hypoxia).

43 44 45 46

2

47

INTRODUCTION

The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT

48 49

Adaptive phenotypic plasticity occurs when an organism can produce a range of

50

relatively fit alternative phenotypes in response to the environment. Alternative physiological

51

phenotypes can be expressed relatively quickly in response to an environmental change, while

52

morphological changes often take longer (Piersma and van Gils, 2011). Therefore, the

53

advantages of plasticity may be limited by lag-times between experiencing environmental

54

change and remodelling the phenotype accordingly (DeWitt et al., 1998; Pigliucci, 2001;

55

Callahan et al., 2008; Auld et al., 2010). Plasticity of functionally related traits, however, may

56

be temporally integrated in order to cope with the environmental change immediately and over

57

time (Schlichting and Pigliucci, 1998; Pigliucci, 2001; Relyea, 2003). Amphibious fishes

58

experience abrupt environmental changes when moving between aquatic and terrestrial habitats.

59

Can the temporal integration of physiological and morphological respiratory phenotypes ease the

60

transition between respiratory media?

61

Amphibious fishes require unique gills that can tolerate exposure to both water and air.

62

During air exposure (emersion) gills are vulnerable to desiccation and, when the lamellae are

63

unsupported by water, these collapse and coalesce which can cause permanent damage.

64

Therefore many amphibious fishes have gills with relatively short and thick lamellae that are

65

able to function during frequent transitions between air and water with few morphological

66

adjustments (Graham, 1997; Sayer, 2005). Conversely, the Amazonian fish Arapaima gigas

67

dramatically and permanently remodels its gills, reducing surface area, during ontogeny as the

68

fish transition from obligate water breathers to obligate air breathers (Brauner et al., 2004). The

69

amphibious mangrove rivulus (Kryptolebias marmoratus (Poey); formerly mangrove killifish

3

The Journal of Experimental Biology – ACCEPTED AUTHOR MANUSCRIPT

70

Rivulus marmoratus) is able to reversibly remodel its gill morphology in response to air exposure

71

by developing a mass of cells between the lamellae, the interlamellar cell mass (ILCM) (Ong et

72

al., 2007). The ILCM develops after 7 d in air and reduces functional gill surface area, likely to

73

protect the delicate lamellae or reduce water loss (Ong et al., 2007). Frequent voluntary

74

emersions can also cause ILCM enlargement (Turko et al., 2011). In the wild, mangrove rivulus

75

typically inhabit extremely hypoxic (