Coward or braveheart: extreme habitat fidelity through hypoxia tolerance in a coral-dwelling goby
1 Department of Biology, University of Oslo, PO Box 1051 Oslo,
Norway
2 School of Marine Biology and Aquaculture, James Cook University,
Townsville, Australia
* Author for correspondence (e-mail: g.e.nilsson{at}bio.uio.no)
Accepted 9 September 2003
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Summary |
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Key words: hypoxia, Gobiidae, air breathing, Great Barrier Reef, Gobiodon histrio
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Introduction |
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Species of Gobiodon are arguably exceptionally cowardly fishes.
They secrete a poisonous mucus, and are therefore probably inedible to most
predators (Schubert et al.,
2003). Nevertheless, they spend virtually their whole adult life
in narrow spaces formed between the branches of Acropora, a shelter
that should make them inaccessible to most predators. Moreover, the need to
leave the coral to find a breeding partner is minimized by the ability to
change sex in either direction. Thus, if two individuals of the same sex end
up in a coral colony, one of them will change its sex unless other breeding
partners are nearby (Munday et al.,
1998
).
In addition to shelter, corals also provide a site for reproduction, and
for some gobies, a source of food (Patton,
1994; Nakashima et al.,
1996
). Coral colonies are a limited resource and there are
significant consequences to individual fitness to inhabiting different species
of coral (Munday et al., 1997
;
Munday, 2001
). Consequently,
there is intense competition for colonies of preferred coral species
(Munday et al., 2001
).
Although coral colonies are an essential resource for coral-dwelling
fishes, they may also present unique problems that could jeopardize the
survival of its inhabitants. Physiological studies have shown that coral
tissue becomes hypoxic at night (Jones and
Hoegh-Guldberg, 2001). It is therefore possible that water between
the coral branches becomes hypoxic on calm nights because of the combined
effects of the nocturnal cessation of photosynthesis, continued respiration of
the coral (and associated organisms), and lack of convective water movements.
Furthermore, the entire coral colony may be exposed to air during spring
tides. For example, coral colonies on the reef flat at Lizard Island (Great
Barrier Reef) may be completely air exposed for 14 h during
exceptionally low tides that occur up to 30 times per year. Despite these
potential problems, coral gobies rarely leave the shelter of their host coral
colonies, even when corals are fully exposed at low tide. Staying there under
such conditions could be considered an act of bravery.
In this study we investigated hypoxia tolerance in the broad-barred goby,
Gobiodon histrio, a common coral-dwelling goby on the Great Barrier
Reef (Munday et al., 1999).
This goby exhibits a strong preference for colonies of Acropora
nasuta (Munday et al.,
1997
,
2001
). First, we estimated the
nocturnal water O2 level likely to be experienced by gobies
inhabiting A. nasuta on calm nights. We then used closed-system
respirometry to test the ability of G. histrio to tolerate these
levels of hypoxia and to tolerate the extended periods of air exposure
experienced during low tides.
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Materials and methods |
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The experiments were conducted in October 2002 at Lizard Island Research Station (LIRS) on the northern Great Barrier Reef (14°40' S 145°28' E). G. histrio, of both forms, weighing 0.432.02 g (histrio form) or 0.61.51 g (erythrospilus form), where collected by anaesthetizing them with a dilute solution of clove oil (50 ml clove oil, 40 ml ethanol and 400 ml of sea water) sprayed into the coral colonies they occupied. Anaesthetized fish were carefully placed in plastic bags and transported to the laboratory, where they rapidly recovered. The fish were kept in shaded out-door aquaria with a continuous supply of water pumped directly from the ocean (2728°C). The water O2 level varied between 86% and 101% of air saturation. They were fed daily with mysid shrimps ad libitum, but were starved for 24 h before any experiments. The fish were kept in the laboratory for at least one week before the experiments, which were carried out outdoors in shaded daylight (10.00 h to 18.00 h). Oxygen concentrations are given as percentage of air saturation (100% equals a PO2 of 151 mmHg or 20.1 kPa). The collecting of fish and coral was approved by the Great Barrier Reef Marine Park Authorities and the experiments followed ethical guidelines from the University of Queensland.
Fish respirometry
Closed respirometry was conducted as described by Nilsson
(1992,
1996
). In this method, the
test animal is placed in a sealed container and the rate at which the water
O2 level declines is measured continuously using an O2
electrode (Fig. 2A). The closed
respirometer used for water breathing was custom-made out of a Perspex
cylinder (inner
=80 mm) with a variable volume of 150250 ml. Each
experiment took approximately 69 h. The O2 level was
monitored using a galvanometric O2 electrode (a microprocessor
controlled Oximeter 323A from WTW, Weilheim, Germany) and recorded with a
Powerlab 4/20 (AD instruments, Castle Hill, Australia) connected to a
Macintosh Power Book, using the program Chart 4.0 (AD instruments).
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|
O2 in mg
O2 h1 kg1 fish wet mass, was
plotted against water O2 concentration ([O2]), given as
a percentage of air saturation. The critical O2 concentration
([O2]crit) was determined by fitting two linear
regression lines to the curve, one for the normoxic,
O2-independent, part of the curve, and one for the steeply falling
hypoxic part (Fig. 2B). The
point where these lines crossed was taken as the
[O2]crit. The [O2]crit is the
concentration below which the fish is unable to maintain a resting
O2 that is
independent of the ambient [O2]
(Beamish, 1964
). The mean
O2 between 70%
and 100% of air saturation was considered to be the normoxic
O2. The short
period of activity-related increase in
O2 that was
sometimes seen immediately after the fish was introduced into the respirometer
was excluded from the measurements used to determine normoxic
O2.
For measuring
O2 in air, we
used the same set up, but the O2 electrode was connected to a 12 ml
air filled glass chamber (submerged in the aquarium). The fish was placed in
the chamber together with 0.3 ml of water. This small amount of water was
necessary to avoid distress and excessive mucous production by the fish. With
the droplet, the fish rapidly settled down, pointing its mouth into the
droplet. The partial pressure of O2 in the chamber never fell by
more than 10% (from 151 mmHg to 136 mmHg).
The ventilation rate of the fish was estimated by counting the opercular movements during respirometry.
In the measurement of O2 debt after air exposure, six fish (both forms) were kept in the air respirometry chamber for 2 h, whereupon they were transferred to the water filled respirometer. The respirometer volume was set to 250 ml, and by opening valves, the water was exchanged repeatedly, every 11.5 h so that the [O2] never fell below 60% of air saturation.
Oxygen levels in coral
To estimate O2 levels among the coral branches overnight, three
colonies of A. nasuta (23, 25 and 26 cm in diameter, all
approximately 9 cm high, and weighing 2.76, 2.84 and 3.22 kg, respectively)
were collected on the reef by carefully breaking them lose at the base. Each
coral colony was kept in a 240 liter plastic tank (105 cm diameter, 28 cm
high) continuously supplied with fresh sea water (2728°C). To
estimate O2 levels between the coral branches, an O2
electrode (as described above) was inserted 6 cm into the center of the coral,
between the branches. Because the inter-branch distance was only 510
mm, while the electrode has a diameter of 15 mm, one branch was removed to
accommodate the electrode. Another electrode was placed in the tank 30 cm from
the coral. No stirrers were attached to the electrodes (to avoid creating
water movements). Consequently, they were found to give readings that were
37.5% lower than those from stirred electrodes. The data were corrected for
this deviation, which was found to be constant over the [O2] range
of interest.
To simulate calm nights when the most severe nocturnal hypoxia is likely to occur, O2 measurements were conducted in an outdoor tank with the water supply turned off to prevent convective water currents. Two measurements, on subsequent nights, were taken for each of the corals. Corals were returned to their original sites and secured to the reef.
Statistics
All values given are means ± S.E.M. Possible differences
between the two forms were tested with the Wilcoxon test, while points in time
series were compared using Friedman's non-parametric test for repeated
measures followed by Dunn's post test (InStat 2.01 for Macintosh).
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Results |
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Respiration in water
From the respirometric measurements in water, we determined four variables:
normoxic O2,
[O2]crit, the O2 level where the fish lost
its equilibrium, and the time that elapsed between
[O2]crit and loss of equilibrium
(Fig. 2A,B). These data are
summarized in Table 1.
G. histrio was extremely hypoxia tolerant. Its [O2]crit was 18.3±1.4% of air saturation, and it tolerated a further 2 h of falling O2 levels before showing signs of equilibrium loss at approximately 3% of air saturation (Table 1). All fish recovered their ability to maintain equilibrium within a few minutes in normoxic water.
G. histrio increased its ventilatory rate significantly in response to falling water [O2] until [O2]crit was reached, whereupon the rate fell (Fig. 2C). As with the earlier results, there were no significant differences between the two forms of G. histrio (Fig. 2C includes both forms).
Respiration in air
G. histrio showed a remarkable ability to take up O2 in
air, only accompanied by a drop (0.3 ml) of water. The ventilatory movements
apparently circulated this small volume of water, by moving it over the gills
and out through the opercular openings, from where it flowed back to the
mouth.
O2 and
ventilatory rate were maintained in air for at least 3 h
(Fig. 3). The fish did not
display any aberrant behavior when returned to water, which also applied to
one individual that was kept in air for 4.5 h. The mean
O2 of 11
individuals kept in the air filled respirometer for an hour was 145±11
mg kg1 h1
(Table 1), which was about 40%
lower than that in water.
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Oxygen debt
Since the O2
in air was 40% lower than that in water, we examined the possibility that the
fish accumulate an O2 debt during air exposure. After 2 h in air,
G. histrio showed a significantly elevated
O2
(P<0.001) during the first hour in water, as compared to the
fourth, fifth and sixth hour (Fig.
4).
O2 appeared
slightly elevated during hours two and three, while by the fourth hour, it was
virtually identical to the
O2 of
247±20 mg kg1 h1 previously
measured (Table 1). The total
overshoot in O2 consumed during the three first hours was
181±34 mg kg1. This was very similar to the expected
O2 debt of 204 mg kg1 accumulated over 2 h in air
(calculated by subtracting the
O2 in air from
the
O2 in water
and multiplying by the number of hours in air).
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Discussion |
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With regard to [O2]crit, there seems to be few
comparable measurements of hypoxia tolerance in tropical sea fishes at
temperatures close to 30°C (but see
Nilsson and
Östlund-Nilsson, in press). Data in the literature allow an
interesting comparison with some species of cichlids living in African lakes
(Verheyen et al., 1994
;
Chapman et al., 1995
). These
fishes, which are renowned for their hypoxia tolerance, have a
[O2]crit of about 20% of air saturation at 25°C
very similar to that displayed by Gobiodon histrio.
Coral colonies are an essential resource for coral-dwelling gobies. Owing
to their small body size, coral gobies could experience a high risk of
predation (if edible to some predators) or hazardous predation attempts
outside their host coral colonies. Thus, the ability to remain within the
coral colony at night is likely to be a distinct fitness advantage. Coral
colonies are also a limited resource for coral-dwelling gobies and there is
intense competition for preferred corals at Lizard Island
(Munday et al., 2001). Leaving
the host coral during periods of hypoxia would provide opportunities for other
individuals to usurp habitat space. Therefore, it would be advantageous for
G. histrio to remain within the host coral colony at all times to
defend it from competitors. Consequently, it appears that hypoxia tolerance in
this goby is an important attribute to both reduce the risk of predation or
predation attempts and limit the potential of losing vital habitat space.
There are other noteworthy examples of fishes that utilizes hypoxia
tolerance for predator avoidance. The hypoxia tolerance of fishes of deep
swamp refugia in the Lake Victoria region is probably important for modulating
the impact of the predatory Nile perch (Lates niloticus)
(Chapman et al., 2002). The
most extreme example of predator avoidance through hypoxia tolerance is that
of the crucian carp (Carassius carassius). Owing to its exceptional
anoxia tolerance (Nilsson,
2001
), the crucian carp is often the only piscine inhabitant in
small lakes and ponds in Northern Europe, thereby completely avoiding
predatory fish (Poleo et al.,
1995
; Holopainen et al.,
1997
).
Hypoxia tolerance is known in some gobiids, particularly estuarine species
in temperate water (Graham,
1976; Gee and Gee,
1995
; Martin,
1995
). Tolerating hypoxia is less challenging in temperate waters
than in tropical waters because
O2 increases and
water O2 content falls with increasing temperature. The most
hypoxia-tolerant gobiid is probably the Californian blind goby,
Typhlogobius californiensis, that can survive 80 h of anoxia at
15°C (Congleton, 1974
).
However, hypoxia tolerance has also been reported in Valenciennea
longipinnis, a burrowing goby that lives in sandy areas near coral reefs
(Takegaki and Nakazono, 1995). The presence of hypoxia tolerance in both
tropical and temperate gobies, from a wide range of genera, suggests that this
may be an ancestral trait. Being phylogenetically pre-adapted to a hypoxic
habitat may have been a prerequisite for the Gobiodon ancestors to
become coral dwellers.
G. histrio was able to tolerate many hours in air. Mudskippers are
the best known gobiid air breathers, some of which show specialized
respiratory epithelia in the buccal cavity
(Al-Kadhomiy and Hughes, 1988).
A preliminary examination of the buccal cavity of G. histrio did not
reveal any specialized respiratory epithelium or highly vascularized areas in
the buccal cavity that would indicate morphological adaptations to air
breathing. The likely mechanism used by G. histrio for O2
uptake in air is the circulation of a small volume of water through the mouth
and over the gills, as was observed in the respirometer. When water moves on
the outside, from the opercular opening to the mouth, it would be oxygenated
through diffusion from air. G. histrio, and some other coral-dwelling
gobies, have a groove under each side of the jaw, running from near the
opercular opening to near the front of the mouth
(Harold and Winterbottom,
1999
). This groove may assist in the circulation of water between
the mouth and operculum.
Uptake of O2 in air may also occur through the skin. Under the
stereo microscope, we observed superficial capillaries in the skin, and many
fishes, including gobies, have been shown to utilize cutaneous respiration
both in water and air (Graham,
1976; Martin,
1995
).
In G. histrio,
O2 in air was about
40% lower than
O2 in water, and
during air exposure, this goby accumulated an O2 debt that very
closely correlated to the reduced uptake of O2 during air exposure.
This indicates that it relied on anaerobic metabolism to some degree during
air exposure. The accumulation of an anaerobic end product (most likely
lactate) will limit the time this fish can remain in air.
To conclude, tolerance to hypoxia and air exposure in G. histrio appear to reflect important adaptations that are needed to allow the highly specialized life style of most coral gobies. These abilities should make it possible for these fish to stay indefinitely in the shelter of their host corals, regardless of nocturnal hypoxia and periodic air exposure during very low tides.
To our knowledge, this is the first report of an extremely hypoxia-tolerant
teleost intimately connected to coral reefs. However, recent results suggest
that hypoxia tolerance, albeit to a lesser degree than that displayed by
Gobiodon histrio, may be widespread among coral reef fishes
(Nilsson and
Östlund-Nilsson, in press). Moreover, a coral reef
elasmobranch, the epaulette shark (Hemiscyllium ocellatum), has
proved to be hypoxia tolerant. On Heron Island (Great Barrier Reef), the
epaulette shark survives several hours of hypoxia (1020% of air
saturation) as the water of the shallow reef platform becomes cut off from the
ocean at nocturnal low tides (Routley et
al., 2002
). In view of the exceptionally diverse life styles and
habitats found on coral reefs, it is possible that hypoxia, and hypoxia
tolerance, are more common phenomena on coral reefs than generally
imagined.
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Acknowledgments |
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