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First published online March 16, 2007
Journal of Experimental Biology 210, 1109-1115 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.002238
Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure
Department of Integrative Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada
* Author for correspondence (e-mail: patwrigh{at}uoguelph.ca)
Accepted 29 January 2007
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CO2 was measured
in fish continuously over a 5-day period in air and compared with previous
measurements of oxygen uptake
(O2) in water.
CO2 varied
between 6 and 10 µmol g–1 h–1 and was
significantly higher on days 3, 4 and 5 relative to days 1 and 2. In contrast
to O2 in water,
CO2 in air
showed no diurnal rhythm over a 24 h period. These findings indicate that
K. marmoratus remodel their gill structures in response to air
exposure and that these changes are completely reversible. Furthermore, over a
similar time frame, changes in
CO2 indicate
that metabolic rate is maintained at a rate comparable to that of fish in
water, underlying the remarkable ability of K. marmoratus to thrive
in both aquatic and terrestrial habitats.
Key words: metabolic rate, CO2 excretion, emersion, gill lamellae, interlamellar cell mass
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Introduction |
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), although
there are true males and therefore sexual reproduction occurs in some natural
populations (Mackiewicz et al.,
2006). They are considered amphibious fish because they survive in
both aquatic and terrestrial habitats
(Sayer, 2005). K.
marmoratus have a remarkable tolerance to a wide range of aquatic
extremes and can endure over one month of exposure to air (emersion) when
among moist detritus or leaf litter (Abel
et al., 1987). K. marmoratus leave their aquatic
environment for varying periods of time in response to aggression between fish
(Huehner et al., 1985;
Taylor, 1990), as well as in
response to environmental stressors, such as high hydrogen sulfide
concentrations (Abel et al.,
1987; Taylor,
1990), low water temperature
(Huehner et al., 1985) or as a
result of constant flux between drought and flooding in the areas they inhabit
(Harrington, 1961).
Additionally, they may leave the water for short periods of time in order to
catch termites on land and then return immediately to eat their prey
underwater (Huehner et al.,
1985).
In water, most fish rely primarily on gills for gas exchange
(Evans et al., 2005). During
air exposure, the gills are no longer perfused with water and will collapse if
there are no specialized structural modifications. Respiratory adaptations
that allow amphibious fishes to live in both terrestrial and aquatic
environments include specialized lungs and gas bladders (air breathing organ,
ABO), as well as modifications of existing structures, such as the gills and
skin (Graham, 1997). The
amphibious gourami, Trichogaster trichopterus, depends mainly on the
labyrinth organs in the suprabranchial chamber for respiration during periods
of aerial exposure (Burggren,
1979). Observation of an increased capillary network in the gut of
the Chilean clingfish, Sicyases sanguineus, after 24 h of emersion
suggests that this fish respires via intestinal respiration
(Marusic et al., 1981).
Cutaneous modifications are present in many different amphibious fish
(Park et al., 2003), such as
the mudskipper Periophthalmus magnuspinnatus, in which an extensive
capillary network lies close to the surface of the skin and the middle layer
of epidermis contains modified epidermal cells that are thought to facilitate
oxygen uptake (Park,
2002).
The cutaneous surface is probably a site of respiration in K.
marmoratus because the epidermis is relatively thin and there is a high
density of capillaries near the surface
(Grizzle and Thiyagarajah,
1987). During 11 days of air exposure, a significant amount
(>40%) of ammonia is released by NH3 volatilization
(Frick and Wright, 2002a). The
site of gaseous excretion is likely the skin because both NH
+4 concentration and pH on the cutaneous surface
increase significantly after air exposure
(Litwiller et al., 2006).
Furthermore, the number of cutaneous vessels perfused on certain areas of the
dorsal surface of K. marmoratus increases significantly after 30 min
of air exposure (S. Litwiller, P.A.W. and C. Murrant, manuscript in
preparation). Taken together, these studies suggest that in the absence of
functional gills and an ABO, K. marmoratus rely on the skin as the
major respiratory surface.
Changes in gill morphology have been observed in other teleost fish in
response to developmental changes or environmental stressors. For example, in
the obligate air breather Arapaima gigas, the defined lamellae of the
water-breathing juveniles regress and the filaments become smooth columns as
they mature and become obligate air breathers
(Brauner et al., 2004). The
changes in A. gigas gills are long term and not reversible. By
contrast, the secondary lamellae of the crucian carp, Carassius
carassius, become much more defined in response to hypoxic conditions
(Sollid et al., 2003), and
similar changes have been observed in both C. carassius and in C.
auratus in response to warmer water temperatures
(Sollid et al., 2005).
Exposure to hypoxia induced apoptosis of C. carassius gills in
between the lamellae (the interlamellar cell mass, or ILCM), thus causing the
lamellae to protrude and increase the surface area for gas exchange
(Sollid et al., 2003). These
changes were completely reversible when C. carassius were returned to
normoxic water. Hence, gill morphology is plastic in two Carassius
species in response to temperature and water oxygenation. Do similar changes
occur in other fish species in response to a variety of environmental
perturbations? In particular, is gill morphology plastic in K.
marmoratus, a species that tolerates prolonged air exposure?
When K. marmoratus are exposed to air they do not appear to
aestivate; they remain responsive (K.J.O., personal observation) and there is
little change in aerobic enzyme activities
(Frick and Wright, 2002a),
suggesting that metabolic rate is not depressed as in prolonged emersion in
lungfish (Smith, 1930). Graham
reviewed the effects of air-exposure on oxygen uptake in air-breathing fish
and concluded that the active amphibious species generally maintain oxygen
uptake when exposed to air (Graham,
1997). Many of these species have specialized structures for air
breathing, whereas K. marmoratus appear to be solely dependent on the
passive exchange of gases across the cutaneous surface.
We tested two hypotheses. First, we hypothesized that mangrove killifish
gills are plastic and will undergo reversible change when exposed to air. We
predicted that the gill surface area would decrease in air and that a return
to water would reverse any changes. Scanning electron microscopy and light
microscopy techniques were used to document morphological changes in the gills
of K. marmoratus associated with air exposure for 1 h, 1 day, 1 week
and following 1 week of recovery in water. Second, we hypothesized that
metabolic rate is maintained during air exposure. If true, we predicted that
carbon dioxide excretion
(CO2) would
remain unchanged over time and be similar to previously measured values in
control killifish in water. K. marmoratus were exposed to air for 5
days and CO2 was
measured continuously.
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Materials and methods |
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, pH 8,
12 h:12 h light:dark cycle) (Frick and
Wright, 2002b). Adult killifish used in metabolic rate experiments
weighed between 0.07 and 0.16 g, and in microscopy experiments weighed between
0.07 and 0.12 g. Feeding and cleaning regimes were as described by Litwiller
et al. (Litwiller et al.,
2006).
Metabolic rate
Two days prior to experimentation, fish were placed in the respirometry
chambers in water, and food was withheld to conform with previous measurements
of oxygen uptake in water (Rodela and
Wright, 2006). Fourteen fish were exposed to air for 3 days
(N=14); for seven of these fish, the exposure continued for 5 days
(N=7). Fish were not fed in the chamber, but the chamber was opened
once or twice each day to moisten the filter paper with 16 seawater.
Lights were turned on at 08.00 h and off at 20.00 h daily. Temperature was
maintained at 25±0.5°C by placing the metabolic chambers on an
aluminum water jacket connected to a water bath. Temperature was measured with
a thermocouple in the blank chamber.
The air source was filtered external air that was scrubbed to remove CO2 and humidified to prevent desiccation of the fish. The scrubbed and humidified air was pumped through flow control valves and then into all four chambers (three containing fish, one serving as a blank). The chambers were multiplexed so that the outflow of one went through an ice bath and Drierite® column to remove any water and then to an infrared CO2 meter (Qubit S151; Qubit Systems, Kingston, ON, Canada). A gas switcher (Qubit G243) switched flow between a fish chamber and the blank chamber every 30 min. Flow was set to approximately 25 ml air min–1, but the exact flow rate was recorded continuously in all chambers with high-accuracy low flow meters (Qubit G249). The analyzer was calibrated daily using scrubbed gas as zero, and a single high point using a calibrated gas containing a known concentration of CO2 (1500 p.p.m.), balanced with nitrogen.
Metabolic rate was calculated using the Fick equation:
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CO2 is
calculated in µmol CO2 g–1
h–1, flow (ml air min–1) was calculated as
the integral of the flow rate through the chamber for the 15 min period when
CO2 levels reached steady-state, CO2 out = plateau value
of CO2 leaving the chamber containing a fish (p.p.m.),
CO2 in = plateau value of CO2 leaving the blank chamber
(p.p.m.) taken as the average of the value before and after the measurement
for each fish, 60 to convert min to h, 22.4 to convert µl to µmol, 1000
to convert ml to l, m is body mass in g.
Experimental protocol for gill structure
Five groups of fish were exposed to either control (immersed) or
experimental (emersed) conditions. Control fish (time 0 h) were directly
removed from 100 ml plastic chambers (containing 60 ml of 16 water),
immediately euthanized by spinal cord transection and placed into fixative
(see below). Fish exposed to air were placed in 100 ml chambers. Three cotton
balls were placed at the bottom of each chamber and a piece of filter paper,
cut to fit snugly into the bottom of the chamber, was placed on top of the
cotton. Water (10 ml, 16) was pipetted onto the filter paper and
allowed to soak in evenly. This provided some moisture but did not allow
immersion of gills in water. After experimental treatments of 1 h, 1 day and 1
week of air exposure, fish were euthanized and immediately fixed. An
additional group of fish, a recovery group, was exposed to air for one week,
returned to water (60 ml, 16) for a further week, euthanized and
fixed.
Scanning electron microscopy
Fish heads were fixed in 1% gluteraldehyde, 1% paraformaldehyde with
16 salt water. The left gill arch of fixed fish heads was excised 48 h
later. Gills were post fixed in 1% OsO4, dehydrated in a series of
graded ethanols (50%, 70%, 80%, 90% and three rounds of 100%) and then dried
with a critical point drier (custom made at the Physics Workshop, University
of Guelph). Samples were then mounted on carbon tape and sputter coated in 30
nm gold with an Emitech K550 Sputter Coater (Ashford, Kent, UK). A Hitachi
S-570 Scanning Electron Microscope (Tokyo, Japan) was used to capture
micrographs of the gills.
Light microscopy
After 24 h of immersion in 10% phosphate-buffered formalin fixative, the
left operculum was cut away and the second gill arch was extracted and then
routinely processed for paraffin embedding. The gill arches were serially
sectioned in 4 µm increments and then stained with hematoxylin and eosin.
The slides were viewed using an Olympus BX60 light microscope (Tokyo, Japan),
and images were recorded using Image Pro Plus 5.1 (Media Cybernetics Inc.,
Silver Spring, MD, USA).
Morphometry
Measurements of lamellar width, lamellar length and height of ILCM were
performed for each fish (Fig.
1). Width of lamellae was measured parallel to the filament at the
base of the lamellae from one edge to the other. Lamellar length was measured
from the edge adjacent to the filament to the most distal point of the
lamellae from the filament. Height of ILCM was measured parallel to the total
lamellar length, starting from the edge of the ILCM bordering the filament to
the most distal edge of the ILCM from the filament.
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CO2 values
varied between 6 and 10 µmol g–1 h–1 in
fish exposed to air for 5 days (Fig.
2A). Mean metabolic rate of the 14 fish was 8.02±0.75
µmol CO2 g–1 h–1 and decreased
with an increase in body mass (ANCOVA, F1,237=47.92,
P<0.001).
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CO2 increased
with air-exposure time over a five-day period (ANCOVA,
F4,237=13.16, P=0.000)
(Fig. 2A). Tukey's tests
revealed that there were no significant differences between metabolic rates on
days 1 and 2 or between days 3, 4 and 5. However, metabolic rate on both days
1 and 2 was significantly less than on days 3, 4 or 5 (P<0.05).
When hourly rates were averaged from different days, metabolic rate did not
change significantly with time of day (Fig.
2B) (ANCOVA, F22,237=0.28,
P=1.00).
Gill structure
Scanning electron micrographs revealed marked differences in morphological
appearance between control gills and gills emersed for 1 week
(Fig. 3). The lamellae of the
control fish were defined, not fused together, and had a relatively large
surface area for exchange with water (Fig.
3A). Conversely, the lamellae of the fish exposed to air for one
week appeared to be shorter with a decreased surface area
(Fig. 3B). Similarly, light
micrographs indicated that the lamellae became more embedded (i.e. less
surface area was exposed to the air as a result of ILCM growth) with an
increase in the time exposed to air (Fig.
4). Most samples exhibited an intermediate pattern where lamellae
were partially embedded after 1 week of air exposure
(Fig. 4D), but in one of the
fish sampled the lamellae were completely embedded
(Fig. 4E). After 1 week of
recovery in water, the gill lamellae appeared very similar to control fish
(Fig. 4F).
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Mean lamellar widths from each treatment were not significantly different (P>0.05) and ranged from 4.5 to 5.1 µm (Fig. 5A). Analysis of the lamellar length from light micrographs revealed no significant differences (P>0.05) between fish in any treatment (Fig. 5B). Short-term exposure to air (1 h and 1 day) did not yield significant changes in the height of the ILCM (P>0.05), but after 1 week of air exposure there was a significant increase (P<0.05, N=6) (Fig. 5C). After 1 week of recovery in water, there was a significant decrease (P<0.05) in ILCM height compared with air-exposed fish (1 week), and the ILCM height was not significantly different (P<0.05) from control values (Fig. 5C).
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).
The most dramatic change is no doubt the move from an aquatic to a terrestrial
habitat. In normal aquatic conditions, the gills of K. marmoratus did
not exhibit any general external features unique to many air-breathing and
amphibious fish (see below). The ILCM did not fill the areas between the
secondary lamellae in aquatic conditions. K. marmoratus gills in
water were organized in a fashion typical of aquatic teleosts with relatively
long, thin secondary lamellae projecting from the filament. The move to a
terrestrial habitat induced morphological changes in the gills that were
reversible. The embedment of the lamellae via ILCM growth during
terrestrial exposure may serve to protect lamellae from collapse, aid the fish
in aerial respiration or possibly prevent desiccation.
Many amphibious fish have developed structural modifications in their gills
to prevent lamellar collapse when emersed. Tamura et al. reported that the
mudskipper Boleophthalmus chinensis has short, widely spaced lamellae
in order to reduce coalescence during emersion
(Tamura et al., 1976). The
gills of Mnierpes macrocephalus are enlarged, thick and long, which
prevents their collapse in air (Graham,
1970). The gills of the mudskipper Periophthalmodon
schlosseri have permanent fusions between the lamellae in order to
prevent collapse, and their gills have been found to be better adapted for air
breathing than for water breathing (Kok et
al., 1998; Wilson et al.,
1999). In K. marmoratus exposed to air, there was no
change in lamellar width, indicating that thickened lamellae are not a
strategy adopted to prevent lamellar collapse. However, we did observe growth
of the ILCM in air-exposed killifish, which may serve to provide structural
support. Although significant structural changes were not detected until 1
week of emersion, more subtle changes in the ILCM may have helped prevent
collapse and coalescing of the secondary lamellae in the first few hours to
days of air exposure. Alternatively, the ILCM growth during air exposure may
have helped to prevent water loss across the gills. Water conservation is of
prime importance to K. marmoratus because death occurs after only a
few hours in air in the lab if the substratum is dry (P.A.W., personal
observation) and in the field emersed fish aggregate, which is thought to be a
mechanism to reduce water loss (Taylor,
2000).
The length of time exposed to air varies in nature depending on
circumstance. Periods of drought can leave fish stranded on land for over a
month, whereas terrestrial forays in search of food can last mere minutes.
Although there is some evidence that cutaneous respiration may be the primary
mode of respiration in air (see Introduction), we cannot rule out the
possibility that the gills may be involved in aerial respiration. Much like
P. schlosseri, K. marmoratus may partially use their gills for
respiration when in air; the growth of the ILCM between the lamellae may serve
to separate the lamellae so that they can function as respiratory structures
(Sayer, 2005). The use of both
skin and gills in respiration occurs in some amphibious fish, for example
Periophthalmus cantonensis and Boleophthalmus chinensis
(Tamura et al., 1976). Careful
observations of buccal and opercular movements in air are necessary to
establish if, indeed, branchial respiration occurs.
The difficulty of distinguishing nuclei in the light micrographs made it
impossible to tell whether the growth of the ILCM was due to hypertrophy or
hyperplasia. Hypertrophy is a more energy-efficient method of increasing size
than hyperplasia because it does not involve cell duplication
(Cheek and Hill, 1970;
Overgaard et al., 2002). A
reduced energy intake, as in the case of the mangrove killifish during air
exposure, compromises the nuclear division necessary for hyperplasia, but not
necessarily for hypertrophy (Cheek and
Hill, 1970). We do not know what type of cells comprise the ILCM,
nor whether hyperplasia or hypertrophy is involved in the ILCM growth.
However, there was an increase in
CO2 after
several days in air, which may or may not be linked partly to the gill
remodeling (see below).
In air-exposed K. marmoratus, CO2 excretion was
measured instead of O2 uptake because it is a more precise measure.
The respiratory exchange ratio (CO2 released per O2
consumed) usually varies between 0.7 and 0.9 in amphibious air-breathing fish
(Bridges, 1988;
Martin, 1993;
Graham, 1997). Using a
respiratory exchange ratio of 0.8 and our
CO2 values of
K. marmoratus in air (6–10 µmol g–1
h–1), the oxygen uptake in air is estimated to be between 7.5
and 12.5 µmol g–1 h–1. Rodela and Wright
reported that O2
in water ranged from 8 µmol g–1 h–1
(nighttime, inactive period) to 22 µmol g–1
h–1 (daytime, active period) in K. marmoratus
(Rodela and Wright, 2006),
values similar to or slightly higher than our estimated oxygen uptake in air.
The fact that our values in air correspond to the previously measured
nighttime values in water is most likely a result of the observed quiescence
when the fish were exposed to air, as well as their unfed state.
Other amphibious marine fish, such as Oligocottus snyderi, Clinocottus
globiceps and Anoplarchus pupurescens, have equivalent oxygen
uptake rates in both air and water
(Bridges, 1988), whereas
Ascelichthys rhodorus and Oligocottus maculosus have a
decreased oxygen uptake when exposed to air
(Yoshiyama and Cech, 1994).
The salt marsh killifish Fundulus heteroclitus also undergoes a
significant decrease in oxygen uptake upon aerial emergence
(Halpin and Martin, 1999).
Over a 24 h period of air exposure, there were no variations in
CO2 in K.
marmoratus. This finding contrasts with the results of our previous study
of O2 in control
K. marmoratus in water (Rodela
and Wright, 2006). Over a 3-day period,
O2 consistently
peaked at midday and decreased to the lowest rate midway through the night.
The lack of a diurnal pattern in air-exposed K. marmoratus in the
present study is likely due to inactivity during emersion. Despite no
fluctuations of daily
O2 when emersed,
there was an increase in
CO2 after two
days of emersion in K. marmoratus. Gordon et al. observed a similar
increase in small Chilean clingfish, Sicyases sanguineus, over 13 h
but could not provide an explanation for this rise in oxygen uptake
(Gordon et al., 1970). We
speculate that the increase of metabolic rate over time is due to a complex
series of changes, possibly including repaying an oxygen debt, alterations in
biochemical pathways, cutaneous structures and/or gill morphology.
Our study is the first to show that the gills of K. marmoratus are plastic and are capable of undergoing reversible changes when emersed and then returned to water. We suggest that the growth of the ILCM may prevent the lamellae from coalescing (which could render the gills non-functional when returned to water), facilitate branchial aerial respiration or have another function such as resistance against desiccation. Over the period of time of gill remodeling in air, metabolic rate is maintained at a rate similar to that of fish in aquatic conditions. Hence, K. marmoratus are supremely adapted to the challenges of respiring in air, explaining in part why they tolerate weeks of air exposure.
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Acknowledgments |
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