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First published online March 2, 2006
Journal of Experimental Biology 209, 1085-1092 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02092
Air breathing of aquatic burrow-dwelling eel goby, Odontamblyopus lacepedii (Gobiidae: Amblyopinae)
1 Institute for East China Sea Research, Nagasaki University, Tairamachi,
Nagasaki 851-2213, Japan
2 Southeast Asian Fisheries Development Center, Aquaculture Department
(SEAFDEC/AQD), 5021 Tigbauan, Iloilo, Philippines
3 Ishigaki Tropical Station, Seikai National Fisheries Research Institute,
Fisheries Research Agency, 148-446 Fukai-Ohta, Ishigaki, Okinawa 907-0451,
Japan
* Author for correspondence (e-mail: d705144k{at}stcc.nagasaki-u.ac.jp)
Accepted 12 January 2006
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2.8 kPa, with an
air-breathing frequency (fAB) of 7.3±2.9 breaths
h–1 (mean ± s.d., N=5). Laboratory
experiments revealed that the fish is a facultative air breather. It never
breathed air in normoxic water (PO2=20.7 kPa) but started
bimodal respiration when water PO2 was reduced to
1.0–3.1 kPa. The fish held air inside the mouth and probably used the
gills as gas-exchange surfaces since no rich vascularization occurred in the
mouth linings. As is known for other air-breathing fishes,
fAB increased with decreasing water
PO2. Both buccal gas volume (VB) and
inspired volume (VI) were significantly correlated with
body mass (Mb). At a given Mb,
VI was nearly always equal to VB,
implying almost complete buccal gas renewal in every breathing cycle. A
temporal reduction in expired volume (VE) was probably due
to a low aerial gas exchange ratio (CO2 elimination/O2
uptake). Air breathing appears to have evolved in O. lacepedii as an
adaptation to aquatic hypoxia in the burrows. The acquisition of the novel
respiratory capacity enables this species to stay in the burrows during low
tide and extends the resident time in the mudflat, thereby increasing its
chances of tapping the rich resources of the area.
Key words: Gobiidae, intertidal mudflat, aquatic hypoxia, air-breathing fish
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). Many
air-breathing fishes occur in freshwater, estuarine and marine habitats
(Randall et al., 1981;
Graham, 1997;
Martin and Bridges, 1999).
Estuarine and marine air-breathing fishes, in general, are dominated by highly
derived groups of amphibious species (e.g. mudskippers and rockskippers),
which routinely emerge during low tide
(Graham, 1976). Such a
conspicuous lifestyle arguably makes them the most extensively studied group
among marine air-breathing fishes (Graham,
1976; Sayer and Davenport,
1991; Bridges,
1993; Clayton,
1993; Martin,
1995). Nevertheless, there appears to be a gap in knowledge
concerning the evolutionary transition from aquatic (i.e. does not emerge from
water) to amphibious air breathers in marine fishes. Furthermore, there are no
well-established reports on the occurrence of aquatic air breathers in the
intertidal mudflat partly because of their fossorial character and the
inability to emerge, which make them hardly noticeable in their natural
habitat.
The eel goby, Odontamblyopus lacepedii (Temminck and Schlegel)
(Gobiidae: subfamily Amblyopinae), does not emerge from water but stays inside
the burrows during low tide. This fish is widely distributed in East Asia,
including southern China, Japan, Korea and Taiwan
(Murdy and Shibukawa, 2001).
In Japan, the distribution of O. lacepedii is limited to Ariake Bay
(Dotsu, 1957). Although the
physical characteristics of O. lacepedii burrows are known –
having 4–9 openings and extending to a depth of up to 90 cm
(Dotsu, 1957) – the
burrow microenvironment has not been previously described. Since fish burrows,
in general, contain hypoxic water (Gordon
et al., 1978; Atkinson and
Taylor, 1991; Ishimatsu et
al., 1998a), burrow-dwelling fishes, including O.
lacepedii, therefore, have to develop a suite of behavioral,
morphological and physiological adaptation mechanisms to maintain their
metabolic requirements (Johansen,
1970; Graham,
1997).
Anecdotal evidence suggests the possibility of air breathing in the eel
goby. In 1997, Graham classified a species of eel goby from India,
Taenioides rubicundus, as an air breather
(Graham, 1997) based on Hora's
description (Hora, 1935) of a
group of fish floating with inflated gill chambers at the surface of an
aquarium containing foul water. Native fishermen of O. lacepedii in
the Saga Prefecture, Japan have also constantly observed a similar behavior
when they transport live individuals to markets, suggesting the presence of
air in the buccal cavity.
The main purpose of the present study was to determine if the eel goby, O. lacepedii, breathes air under natural conditions in the mudflat burrows and to examine the effects of aquatic hypoxia as a trigger to switch from aquatic to bimodal gas exchange by laboratory experiments. We also investigated the air-breathing behavior and selected air-breathing variables, such as buccal gas (VB), inspired (VI) and expired (VE) volumes, in order to obtain insights into the aerial respiratory performance of the fish.
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10 cm above the water surface of the
burrow, and recording instruments were situated in a vehicle on a nearby
platform 3 m above the mudflat surface to avoid interference with the fish.
Video images were saved in a 250-GB HDD DVD video recorder (model DR-MX5;
Victor Co., Kanagawa, Japan) and analyzed for air-breathing behavior and
frequency (fAB). Measurements of burrow-water PO2 were made during low tide concurrent with the months of field-burrow observations. Water samples were slowly withdrawn at depths of 10–15 cm below the surface into a 5 ml glass syringe tipped with plastic tubing. The syringe was previously cleared of its dead space volume by flushing with burrow water. Samples were placed in an icebox and quickly transported to the Saga Prefectural Ariake Fisheries Research and Development Center for PO2 analysis (5–10 min after sampling). Burrow-water PO2 was measured with a Blood Gas Meter (Cameron Instruments Co., Port Aransas, TX, USA) thermostatically regulated to the temperature of the burrow water, which ranged from 20 to 24°C.
Laboratory investigations of air breathing in O. lacepedii
Collection and maintenance of fish
Specimens of Odontamblyopus lacepedii were captured by set nets at
3–5 m depths in an estuary at Ariake Bay, Japan (33°10' N;
130°15' E) between August and October 2003. The area can be
characterized as having high-turbidity water with salinity varying from 0.1 to
31.6
and temperature from 10.3 to 33.0°C during the collection
period. Fish were transported to the Institute for East China Sea Research,
Nagasaki University and kept individually in a 60-l glass aquarium,
half-filled with 50% seawater (17). Each aquarium was provided with an
artificial shelter of either clay or polyvinyl chloride (PVC) pipes and was
attached to a recirculating system equipped with a thermostat
(25±1°C) and aeration supply. Fish were fed chopped fish or squid
to satiation 4–5 times per week. They were kept in these conditions for
at least a month before being subjected to experimentation. All experiments
were conducted in 50% seawater (17) at a temperature of
25±0.5°C. Fish were starved for 24 h prior to use. We did not
differentiate between sexes.
Observation of air-breathing behavior
Air-breathing behavior was observed in a perforated L-shaped fish chamber
submerged in a temperature-controlled water bath. The length (45 cm) and
diameter (5.2 cm) of the horizontal bottom section provided enough space for
the fish to move freely inside the chamber. The vertical section (length, 25
cm) had a tapered opening (diameter, 3.6 cm) at the top where fish could
access air. Two digital video cameras (model DCR-TRV20; Sony Corp., Tokyo,
Japan) were mounted on the top and side of the chamber for video observation
and recording. The water bath (65x16x30 cm depth) was screened off
with a black plastic sheet to shield the fish from laboratory activities.
Fish (23.1–128.3 g body mass; N=14) were acclimated overnight in the chamber before experiment. A steady flow (5 l min–1) of well-aerated water was gently circulated during acclimation. The same flow rate was used during stepwise exposure to aquatic hypoxia (PO2=20.7, 10.4, 6.2, 3.1 and 1.0 kPa) by bubbling N2 into the equilibration column (see Fig. 1). Water PO2 was regulated and maintained with a DO controller (model MC-7W; Iijima Electronics Corp., Aichi, Japan) and continuously monitored with an O2 meter (model DO-14P; TOA Electronics Ltd, Tokyo, Japan). Observation of air-breathing behavior was made for 2 h at each PO2 level. Transition time between PO2 levels was 3–8 min. The air-breathing behavior of individual fish was analyzed with a video cassette recorder (model WV-D9000; Sony Corp., Tokyo, Japan).
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Measurement of VB
Fourteen fish weighing 20.8–113.5 g were placed individually in a PVC
pipe (length x diameter; 34x3.8 cm or 44x4.4 cm, depending
on fish size). The pipe was diagonally immersed in a water tank
(80x60x50 cm depth), and the lower opening was covered with a
plastic screen to hold the fish inside while allowing water to flow in and out
of the pipe. A portion of the upper opening was positioned above the water
level so that fish had access to air and at the same time preventing the fish
from escaping. After 3–4 h acclimation, water PO2
was rapidly lowered and maintained at 1 kPa. When fish gulped a mouthful of
air, the whole PVC pipe was slowly immersed in a vertical position, and an
inverted glass funnel filled with water was immediately positioned above the
upper opening. The funnel was fitted with a 20-gauge syringe needle attached
to PE-90 tubing. Because the fish has a tendency to hold its breath for a long
period of time and the volume of gas reduces with time (see Results), the
mouth was poked with a blunt rod immediately after inspiration to forcibly
expel the newly inhaled air. The gas trapped in the funnel was withdrawn and
its volume measured in a 5 or 10 ml plastic syringe. Suctioning of gas from
the funnel was done rapidly after expiration to prevent the fish from
re-gulping the air. Air in the buccal cavity was considered to be completely
expelled when fish started gill ventilation. Buccal gas volume was measured
5–7 times in each fish.
Measurement of VI and VE
VI and VE were measured in an
L-shaped fish chamber (Fig. 1).
After overnight acclimation in recirculating normoxic water, the fish
(21.2–113.9 g body mass; N=14) was exposed to aquatic hypoxia
(PO2=1.0 kPa) by bubbling N2 into the
equilibration column. When fish commenced air breathing, both inlet and outlet
valves of the L-shaped chamber were closed.
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). Statistical
differences of air-breathing frequency (fAB) and
breath-holding duration at different levels of hypoxia were analyzed using
one-way analysis of variance (ANOVA) followed by Dunnett's test to identify
the data that significantly differed from control values. Significant
correlation was determined between body mass (Mb) and
VB and between Mb and
VI by linear regression analysis. The slopes and
y-intercepts of VB and VI
were compared using analysis of covariance (ANCOVA) and t-test for
comparing two elevations (Zar,
1984), respectively. Results were considered statistically
significant at P<0.05. |
Results |
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Effects of aquatic hypoxia on air breathing
Aquatic hypoxia triggered air breathing in O. lacepedii. The air
breathing observed at a water PO2 of 6.2 (five fish) and
10.4 (three fish) kPa probably has little respiratory significance considering
the short breath-holding duration (Table
1). At a water PO2 of 3.1 kPa, five out of 14
fish breathed air with highly variable breath-holding duration ranging from 1
to 88% of the total time. At a water PO2 of 1.0 kPa, all
fish breathed air, with much smaller variability in breath-holding duration
ranging from 76 to 97%. Although only at a water PO2 of
1.0 kPa did all fish breathe air, a significantly higher
fAB and breath-holding duration were found at 1.0 and 3.1
kPa than in normoxia (Table 1).
There was no significant difference in fAB
(t-test, t=–0.22, P>0.05) or
breath-holding duration (t-test, t=–0.22,
P>0.05) between the burrow water (PO2=2.5 kPa)
and the laboratory condition of 3.1 kPa water PO2, which
implies that our laboratory protocol did not impose noticeable stress on the
fish. Furthermore, the air-breathing behavior observed in the laboratory was
comparable with the endoscopic data (Fig.
3). There was no significant correlation between
fAB and Mb (P>0.05). On
return to normoxia, fish immediately stopped air breathing and resumed gill
ventilation.
Laboratory air-breathing behavior
When preparing to inhale air, the fish approached the water surface with
the mouth closed and the buccal floor and opercula adducted
(Fig. 3A). After breaking the
surface, the mouth opened and air was taken in quickly by the sudden
distension of the buccal floor and expansion of the opercular cavity
(Fig. 3B). The mouth closed,
with the buccal floor and opercula fully abducted, while still above the water
surface (Fig. 3C).
Four distinct types of behavior were observed following inspiration. First, the fish immediately descended while releasing bubbles through the mouth and instantaneously started gill ventilation (type 1). This was the exclusive air-breathing behavior at a water PO2 of 6.2 and 10.4 kPa, where only a small percentage of fish breathed air (Table 1). Second, the fish descended and rested all the way to the horizontal section of the chamber while holding its breath (type 2). When maneuvering to position itself underwater, several bubbles could be released through the gill slits (Fig. 2B), while some fish retained the full volume of air in the buccal cavity until expiration in the water (Fig. 2A). Third, the fish descended while holding its breath, then slowly returned to the surface and stayed motionless with part of the snout protruding out of the water until expiration in air (type 3). Fourth, the fish remained breath holding at the surface, protruding its snout out of the water until expiration in air (type 4; Fig. 3). In all cases, expiration was through the mouth and opercular pumping was often observed prior to the next inspiration. Some individuals (eight of 14) exhibited a combination of the latter three types of post-inspiratory behavior under severe aquatic hypoxia (PO2=1.0 kPa).
Fig. 5 shows the relationships of Mb and VB and VI. A significant correlation was found between VB and Mb (VB=0.045Mb+1.621; r2=0.96, P<0.001, N=14) and between VI and Mb (VI=0.043Mb+1.472; r2=0.90, P<0.001, N=14). There was no significant difference between the slopes (ANCOVA, F=0.14, P>0.05) or the y-intercepts (t-test, t=1.92, P>0.05) of the regression lines of VB and VI.
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30 min. |
Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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2.8 kPa
(Fig. 4). Similar to some
freshwater aquatic mouth breathers [e.g. Synbranchus marmoratus
(Johansen, 1966),
Amphipnous cuchia (Lomholt and
Johansen, 1974)], O. lacepedii inspires first and,
following variable periods of breath holding, expires through the mouth
leaving no residual gas.
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). During the
early phase of air-breathing episodes, the type 2 post-inspiratory behavior
was usually observed, but there was an apparent tendency to shift to types 3
and/or 4 when the air-breathing cycle continued. These three types of
air-breathing behavior were similarly observed in the field burrows. The shift
in respiratory behavior is probably employed to minimize energy expenditure
associated with movement in the water column and maintenance of buoyant head
under water. Aerial exposure, however, could be highly dangerous in the field
unless the fish can hide itself in some shelter (e.g. burrows). The presence
of several openings in one burrow system of the eel goby
(Dotsu, 1957) may also provide
alternative outlets for air breathing when situation in the other openings
becomes precarious for predators such as wading birds.
Like most brackish water and marine air-breathing fishes
(Graham, 1997), O.
lacepedii does not possess any diverticulum specialized for aerial gas
exchange (Fig. 7).Furthermore,
visual examination of the buccal cavity of freshly sacrificed O.
lacepedii revealed the apparent lack of vascularization on the palatine
and tongue epithelia (Fig. 7).
The gills therefore can be inferred as the potential sites of O2
absorption, as similarly suggested in more than 30 species of marine
air-breathing fishes (Graham,
1976). However, the gills are generally considered not to be
suitable for aerial gas exchange due to a reduction of functional surface area
caused by gravitational collapse of the filaments. When hypoxic stress is not
severe enough to necessitate bimodal respiration, such as during migration
(see the section below on burrowing behavior and air breathing in O.
lacepedii), the gills of O. lacepedii must meet most, if not
all, respiratory and other functional requirements (e.g. ammonia release,
acid–base regulation and ionic transfer). However, once O.
lacepedii is subjected to severe hypoxia, such as during burrow
confinement, the gills probably engage in aerial gas exchange, while other
functions of the gills might be translocated to other sites or suspended
momentarily.
The reduction in VE further supports the capacity of
O. lacepedii to extract O2 from air. The temporal
decline in VE during aquatic air breathing is generally
attributed to the low gas respiratory exchange ratio (RER=CO2
elimination/O2 uptake) through the gas-exchange surfaces in the
air-breathing organ (ABO), as shown for many freshwater air-breathing fishes
(Abdel Magid et al., 1970;
Rahn et al., 1971;
Lomholt and Johansen, 1974).
On the contrary, some intertidal fishes, especially the amphibious air
breathers, have high aerial RER (Bridges,
1993), indicating the efficiency of their ABO not only in
O2 extraction but also in CO2 excretion. It should
however be noted that the aerial RER of these amphibious marine species was
determined while the fish were exposed to air. The air breathing of O.
lacepedii shares the same functional trait as in freshwater species,
demonstrating that the early role of air breathing in fishes is oxygen uptake
irrespective of the habitat salinity conditions.
Air-breath variables
The gradual increase of fAB in O. lacepedii
with decreasing water PO2 is in agreement with
observations for other facultative air-breathing fishes
(Graham and Baird, 1982;
Mattias et al., 1998;
Takasusuki et al., 1998).
Fishes have O2 receptors in the gills
(Perry and Gilmour, 2002),
which may be particularly important in signaling a shift from gill ventilation
to air breathing. When confronted with extreme aquatic hypoxia, a facultative
air-breathing fish normally shifts to aerial respiration, and subsequent
modulation of its aerial ventilatory responses is employed (e.g.
VB or VI). Since
VI is equal to VB in O.
lacepedii, air ventilation can be augmented exclusively by way of
increasing fAB, assuming that the fish fully distends the
buccal cavity.
The complete expiration (VI=VB)
found in O. lacepedii can be explained by the vertical position
assumed by the fish during air breathing and the apparent lack of anatomical
dead space of the buccal cavity (Fig.
7). The large renewal of gas may favor its intermittent breathing
pattern, which is characterized by extended periods of breath holding
following inspiration. Complete expiration of each breath is common in many
aquatic air-breathing species with the ABO situated in the mouth or the buccal
cavity [e.g. Synbranchus marmoratus
(Johansen, 1966),
Electrophorus electricus (Farber
and Rahn, 1970), Amphipnous cuchia
(Lomholt and Johansen, 1974),
Ctenopoma kingsleyae and Osphronemus goramy
(Peters, 1978) and four
species of Channa (Liem,
1984)]. The mudskipper, Periophthalmodon schlosseri, has
a gas renewal of 54% (Aguilar et al.,
2000). Even though it uses the buccopharyngeal cavity as its ABO,
this fish normally breathes air in a horizontal position
(Aguilar et al., 2000) so that
incomplete expiration is highly possible.
Burrowing behavior and air breathing in O. lacepedii
Odontamblyopus lacepedii appears both in the coastal water, where
exigency for air breathing is unlikely, and in the intertidal mudflat burrows,
where strong selection for air breathing exists. Presently, it is unclear
whether there are two distinct populations (one migrating and the other
burrowing) or the same individual switches between the two modes of existence
depending on some internal and/or external conditions. Our limited
observations demonstrated seasonal changes in burrow density on the mudflat,
being high in June to August. Since these months correspond to the breeding
season of the species (Dotsu,
1957), it is possible that the burrowing behavior of O.
lacepedii is related to reproduction. Many intertidal burrowing fishes
have been reported to spawn in the burrows
(Clayton, 1993;
Ishimatsu et al., 1998a;
Ishimatsu et al., 1998b).
However, as shown in this study, the water in O. lacepedii burrows is
severely hypoxic so that eggs may not be able to develop normally without some
mechanisms to ensure O2 supply. If O. lacepedii does
indeed spawn in the burrows, then air breathing offers a potential advantage
not only for sustaining respiratory requirements of the adult during burrow
confinement but also for maintaining adequate supply of O2 to the
developing embryos, as has been suggested for the mudskippers
(Ishimatsu et al., 1998a;
Ishimatsu et al., 1998b).
Another potential benefit of burrowing is to extend the resident time in
the intertidal mudflat in order to increase the chance of tapping the rich
resources of the area. Intertidal zones, including estuaries, are among the
most biologically productive ecosystems in the world but, at the same time,
are characterized by strong physico-chemical gradients
(Levinton, 2001). By staying
in the burrows during low tide, O. lacepedii could avoid both the
fluctuations in environmental conditions (such as salinity and temperature)
and the threat of aquatic predations in the estuary. Thus, air breathing is a
necessary trade-off to ensure survival in the hypoxic burrow environment. The
elongated body shape and highly degenerated eye structure
(Murdy and Shibukawa, 2001)
both suggest that selective pressure on this species has been towards a
fossorial mode of life and not towards amphibious existence. The fact that
O. lacepedii does not emerge from its burrow during low tide
indicates that the fish feeds on either entrapped organisms in the burrow, as
suggested for a similar eel goby, Taenioides rubicundus
(Hora, 1936), or on some
infauna of the mudflat. Alternatively, O. lacepedii may come out from
the burrows and feed during high tide. In either case, the fish exploits the
rich biological resources of the mudflat in such a way that competition with
sympatric mudskippers (Boleophthalmus pectinirostris and
Periophthalmus modestus) is minimized. The limited knowledge on the
ecophysiology of this fish necessitates more field studies.
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Acknowledgments |
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Footnotes |
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