First published online May 8, 2007
Journal of Experimental Biology 210, 1673-1686 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02718
Tribute to P. L. Lutz: respiratory ecophysiology of coral-reef teleosts
Göran E. Nilsson1,*,
Jean-Paul A. Hobbs2 and
Sara Östlund-Nilsson3
1 Department of Molecular Biosciences, University of Oslo, N-0316 Oslo,
Norway
2 ARC Centre of Excellence for Coral Reef Studies and School of Marine and
Tropical Biology, James Cook University, Townsville, Australia
3 National Library of Norway, Oslo, Norway
*
Author for correspondence (e-mail:
g.e.nilsson{at}imbv.uio.no)
Accepted 15 January 2007
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Summary
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One of the most diverse vertebrate communities is found on tropical coral
reefs. Coral-reef fishes are not only remarkable in color and shape, but also
in several aspects of physiological performance. Early in life, at the end of
the pelagic larval stage, coral-reef fishes are the fastest swimmers of all
fishes in relation to body size, and show the highest specific rates of
maximum oxygen uptake. Upon settling on the reef, coral-reef fishes have to
adopt a demersal lifestyle, which involves coping with a habitat that can
become severely hypoxic, and some fishes may even have to rely on air
breathing when their coral homes become air exposed. Oxygen availability
appears to be a major ambient selection pressure, making respiratory function
a key factor for survival on coral reefs. Consequently, hypoxia tolerance is
widespread among coral-reef fishes. Hypoxia can even be a factor to gamble
with for those fishes that are mouthbrooders, or a factor that the coral
inhabitants may actively seek to reduce by sleep-swimming at night. Here, we
summarize the present knowledge of the respiratory ecophysiology of coral-reef
teleosts. From an ecophysiological perspective, the coral reef is an exciting
and largely unexplored system for testing existing hypotheses and making new
discoveries.
Key words: hypoxia, coral reef, fish larvae, Pomacentridae, Gobiidae, Apogonidae
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Introduction
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This review is dedicated to our late friend, colleague and long-term
collaborator, Peter Lutz, who devoted much of his scientific life to the
hypoxia tolerance and respiratory physiology of various animals in various
parts of the world. Like two of us, Peter came from the North but loved life
in the tropics. He was a true explorer, and had Peter still physically been
with us, we know that he would have been delighted to join us in the
exploration of the respiratory physiology of coral-reef teleosts, and to share
our beers in the evening.
Animals that take up their oxygen from water run a much greater risk of
experiencing hypoxia than air breathers. This is because the concentration of
oxygen in air-saturated water is only about 3–5% of that in air, and
because oxygen diffuses some 10 000 times faster in air than in water. Thus,
aquatic organisms may use up the oxygen in their surroundings before it is
replenished by diffusion or photosynthesis. Hypoxia is particularly likely to
occur at night, when the lack of light stops photosynthesis and forces plants
to rely on respiration for their energy supply. While it is well known that
hypoxia has a great influence on tropical freshwater habitats (e.g.
Val et al., 2006
), it has only
recently become apparent that hypoxia also shapes the teleost fauna on
tropical coral reefs. Thus, in the areas with the most diverse fish faunas,
which include tropical freshwater systems, such as that of the Amazon river,
and tropical coral reefs, hypoxia is a major abiotic selection pressure.
Still, the exploration of how hypoxia has shaped coral-reef fishes has just
begun, and the high complexity and biodiversity of this ecosystem indicate
that we can expect to find a wealth of adaptations to hypoxia. In this review,
we will summarize our present understanding of the respiratory challenges that
coral-reef teleosts have to cope with. We begin with an overview of the
prevalence of hypoxia tolerance in coral-reef fishes and identify where and
when coral-reef fishes are likely to experience hypoxia. Following this, we
highlight specific cases of respiratory adaptation and examine the respiratory
abilities of larval fish and the ontogeny of respiratory physiology. We
attempt to link physiological adaptations with the environment that presumably
promoted their evolution.
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Hypoxia tolerance in coral-reef fishes
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Hypoxia tolerance appears to be widespread in coral-reef fishes. In an
initial survey carried out on the coral reef at Lizard Island (Great Barrier
Reef, Australia), we used closed respirometry to determine critical oxygen
concentrations ([O2]crit) in 31 species of teleost fish
from several families (Nilsson and
Östlund-Nilsson, 2004). [O2]crit is the
lowest oxygen level where a fish is able to maintain its routine rate of
oxygen consumption (Prosser and Brown,
1961), and is a frequently used indicator of hypoxia tolerance. To
our immediate surprise, all species examined were found to be strikingly
hypoxia tolerant, showing [O2]crit values between 13 and
34% of air saturation, the mean being about 24%
(Table 1).
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Table 1. Hypoxia tolerance of coral-reef fishes in the lagoon at Lizard Island
Research Station, Great Barrier Reef
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At the time of our first experiments, we did not think of coral reef fishes
as inhabitants of hypoxic habitats, except in the special case of the
epaulette shark on shallow tidal flats (reviewed by
Nilsson and Renshaw, 2004),
which are known to periodically become large hypoxic tide pools at night
(Orr, 1933). Tolerating
hypoxia in warm water, like the 30°C water of a tropical coral reef,
should be more challenging than in colder water. Thus, it seems to be a
considerable physiological achievement of coral-reef fishes to maintain
O2 uptake in hypoxia, due to the combined effects of a low
solubility of O2 in warm seawater, and the high rate of oxygen
consumption of a small fish at such a high temperature. Most of the fishes
studied weighed less than 10 g and had routine rates of oxygen consumption
(
O2) of
200–700 mg O2 kg–1 h–1,
which is about 2–5 times higher than that of fishes living at
10–20°C in temperate waters (see
Clarke and Johnston, 1999).
The [O2]crit values shown by the coral-reef fishes
were similar to those of tropical freshwater fishes that inhabit hypoxic
waters and are renowned for their hypoxia tolerance. For example, African
cichlid species, including tilapia (Oreochromis niloticus), show
[O2]crit values of about 20% of air saturation at
25°C (Verheyen et al.,
1994). The elephant nose fish (Gnathonemus petersii) from
central Africa has a [O2]crit as low as 10% at 26°C
(Nilsson, 1996), while adults
of the hypoxia tolerant oscar cichlid (Astronotus ocellatus) of the
Amazon river have an [O2]crit value of 30%
(Sloman et al., 2006). In
those measurements, like in our measurements on reef fish, closed respirometry
was used. This method mimics the hypoxic situation in nature, where oxygen is
used up by aerobic organisms converting O2 into CO2,
thereby creating hypoxia as well as hypercapnia. Moreover, a closed
respirometer is relatively simple, lightweight and transportable, making it
ideal to use in the field.
Although hypercapnia (high PCO2) is associated with low
oxygen environments, both in a closed respirometer and in the field, we have
focused our research on hypoxia, since hypercapnia is unlikely to be a major
challenge in warm seawater because it is well buffered (see
Kalle, 1972) and holds
relatively little O2 that can be converted into CO2 even
when air saturated. Thus, in marine tide pools that are supersaturated
(200–300%) with O2 in the day, PCO2 does
not reach levels much higher than 2 mmHg, and pH stays above 7.5, when all
this O2 has been consumed at night
(Truchot and Duhamel-Jouve,
1980). Consequently, PCO2 values in the
respirometer should not reach higher values than about 1 mmHg, which should
not be a major threat to the CO2 excretion of fishes, which
normally have a blood PCO2 near 4 mmHg
(Ishimatsu et al., 2005).
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Anaerobic energy production – the second line of defence
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Low oxygen environments pose significant challenges to an animal's
physiology, and without specialized adaptations hypoxia is likely to lead to
death. When ambient oxygen levels fall below [O2]crit, the tissues
become starved for oxygen. At low cellular oxygen levels, the ATP production
from oxidative phosphorylation slows down and eventually stops. A fall in
[ATP] rapidly becomes life threatening to fish, like to most animals, since
ion-pumps stop, leaving the cells in a depolarized state
(Nilsson et al., 1993;
Nilsson and Lutz, 2004).
Still, most of the coral-reef fishes we studied did not show any signs of
distress or loss of coordination until the O2 level in the closed
respirometer had fallen well below [O2]crit. In fact,
these signs were usually not seen until water [O2] had fallen below
10% of air saturation, or even as low as 1–3% of air saturation in
several gobiids, blenniids, scorpaenids and a pinguipedid. These are the
values denoted [O2]out in
Table 1 (at which point the
fish was taken out of the respirometer and allowed to recover). After
[O2] had fallen below [O2]crit, it often took
1–2 h before [O2]out was reached (see
Nilsson et al., 2004). Thus,
our data indicate that when the [O2] in water falls below the
[O2]crit, coral-reef fishes are, at least temporarily,
able to maintain ATP levels in spite of the impaired oxidative ATP production.
This is likely to be achieved by boosting anaerobic ATP production (i.e.
glycolysis), and it may also involve mechanisms for reducing ATP demand
(metabolic depression) (see Hochachka and
Somero, 2002; Lutz and
Nilsson, 2004). Suppressing ATP demand has been found in other
fish to involve suppressed brain activity
(Johansson et al., 1995;
Nilsson, 2001) correlated with
increased levels of inhibitory neurotransmitters
(Nilsson et al., 1991;
Nilsson, 1992;
Lutz and Nilsson, 2004). To
what extent coral-reef teleosts are utilizing anaerobic glycolysis and
metabolic depression when faced with critically low O2 levels
remains to be studied.
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Where is the hypoxia?
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The low [O2]crit of coral-reef fishes clearly
indicates that hypoxia is an important selective pressure on coral reefs.
However, identifying hypoxic habitats utilized by coral-reef fishes was not
obvious at first. The clear, well-lit waters of coral reefs is as far as one
can imagine from the turbid or shaded waters normally associated with hypoxic
waters. So where and when do coral-reef fishes encounter hypoxia? The fishes
that exhibited hypoxia tolerance were collected in close proximity to living
coral on 2–5 m deep reefs (Fig.
1) in the lagoon at Lizard Island, and were indicative of the
coral-reef fish community present in this habitat. During the daytime, we
found that these coral-reef waters have oxygen levels around 100% of air
saturation. However, at night these waters may become hypoxic because
photosynthesis ceases while the reef inhabitants will continue to consume
oxygen.
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Fig. 1. Coral reef at Lizard Island, Great Barrier Reef, Australia. This picture
depicts daytime behaviour of damsefishes (here mainly represented by the
genera Pomacentrus and Chromis) hovering above a colony of
Acropora nasuta. At night, these fishes shelter between branches in
the coral, a microhabitat that can be severely hypoxic. Photo by G. E.
Nilsson.
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By focusing on the possibility of nocturnal hypoxia, we envisaged two major
scenarios that could result in coral-reef fishes experiencing hypoxia
(Nilsson and Östlund-Nilsson,
2004): (i) when fishes hide from predators at night by moving into
the coral colonies and residing between coral branches, or (ii) when fishes
get trapped in tidal pools during nocturnal low tides. While the first
situation could be a ubiquitous cause of hypoxia in coral reef environments,
the latter situation is of course only possible on shallow reefs. It is well
known that hypoxia can occur in tide pools in all kinds of marine ecosystems
(e.g. Horn et al., 1999), and
with regard to coral reefs, it was noted by European expeditions to Australia
and Java in the 1920s that oxygen levels could fall to about 20% of air
saturation during the dark hours in tidal pools on shallow reefs, or in reef
lagoons temporarily cut off from the ocean
(Verwey, 1931;
Orr, 1933).
To test the first hypothesis, we collected live colonies of Acropora
nasuta from the Lizard Island reef, placed these colonies in outdoor
aquaria, and monitored the water oxygen levels between the coral branches. The
recordings showed a progressive reduction in [O2] during the night,
with the average [O2] between the branches falling to 20% of air
saturation just before sunrise (Fig.
2) and, for short periods, [O2] as low as 2% of air
saturation was measured (Nilsson et al.,
2004).
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Fig. 2. Coral colonies can be severely hypoxic habitats at night. The graphs show
the oxygen levels (A) outside and (B) between branches of Acropora
nasuta colonies from dusk to dawn. Values are means ± s.e.m. from
six measurements on three corals in an outdoor tank at Lizard Island Research
Station. Sunset and sunrise are indicated by broken lines. From Nilsson et al.
(Nilsson et al., 2004).
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Similarly, in colonies of Stylophora pistillata from the Red Sea,
kept in the laboratory, Goldshmid et al.
(Goldshmid et al., 2004)
showed that water oxygen levels can fall to 10–20% of air saturation in
the dark. They also made the interesting suggestion that piscine inhabitants
of the Stylophora colonies (three damselfish species: Chromis
viridis, Dascyllus aruanus and D. marginatus) perform nocturnal
`sleep-swimming' (Fig. 3),
apparently to increase the water flow through the coral, thereby reducing
nocturnal hypoxia. It was found that the presence of sleep swimming fish
increased the flow of water through coral colonies on the reef. In the
laboratory, sleep-swimming fish reduced the hypoxia occurring in coral
colonies kept in the dark (Goldshmid et
al., 2004). It remains to be studied in the field if the presence
of fish in coral does reduce the level of hypoxia within the coral
colonies.
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Fig. 3. Sleep swimming in the damselfish Dascyllus marginatus measured by
video filming them in infrared light on a coral reef in Eilat, Red Sea. The
stroke frequencies of the dorsal, pectoral and caudal fins are about doubled
at night when the fish hide inside coral (Stylophora pistillata)
compared to the `normal swimming' performed outside the coral during the day.
From Goldshmid et al. (Goldshmid et al.,
2004). Reproduced with permission from Limnology and
Oceanography.
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To confirm that the nocturnal hypoxia detected between branches in coral
colonies in the laboratory was indicative of oxygen levels on coral reefs, we
conducted night-time field measurements of oxygen levels on the reef in the
Lizard Island lagoon. The measurements were done between 02:00 h and 05:00 h
on (austral) summer low tides (G.E.N., J.-P.H. and S.Ö.-N., unpublished
observations). Inbetween the branches of coral colonies, where numerous fishes
were seen to hide, oxygen levels between 12 and 20% of air saturation were
recorded (Fig. 4), confirming
that the water inside coral colonies becomes hypoxic at night.
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Fig. 4. (A) Fishes (Chromis viridis) sheltering in the hypoxic water
inside a coral colony (Acropora sp.) on the Lizard Island reef at
night during low tide. Oxygen levels between the coral branches varied between
12 and 20% of air saturation. (B) A predatory rockcod (Epinephelus
spilotoceps) lies outside the coral and provides a good reason for the
smaller fishes to use the coral as nocturnal shelter. Photo G. E. Nilsson.
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These nocturnal surveys confirmed that fishes do reside in these hypoxic
environments. For example, one coral colony (Acropora yongei; about
1.3 m in diameter and with a water [O2] of about 13% between the
branches), was sprayed with clove-oil to temporarily anaesthetize some of its
inhabitants so that they would drift out of the coral and be positively
identified. We counted 77 Chromis viridis, two Pomacentrus
pavo, and one each of Pomacentrus mollucensis, Dascyllus aruanus,
Acanthochromis polyacanthus, Chelmon rostratus and Ostracion
cubicus. The first five species are damselfishes (Pomacentridae), while
the latter are a butterflyfish (Chaetodontidae) and a boxfish (Ostraciidae),
respectively. It was clear that these fishes only made up a fraction of the
fishes hiding in this coral colony and that there may have been hundreds of
fishes residing in about 1 m2 of living coral. It is probable that
these fishes are sheltering in corals at night to avoid predators. This habit
of hiding in coral at night has previously been described
(Fishelson et al., 1974;
Hixon, 1991;
Holbrook and Schmitt, 2002;
Goldshmid et al., 2004), and
is well known to many night divers. Apparently, to use these nocturnal
shelters, the fishes need the capacity to endure severely hypoxic
environments.
The second scenario where coral-reef fish would experience hypoxia is
through nocturnal occupation of tide pools. The stop of inflow of oceanic
water combined with continued respiration and the lack of photosynthesis at
night will result in tidal pools becoming hypoxic. Oxygen levels as low as
17.8% of air saturation were registered in tide pools at Low Isles (Great
Barrier Reef) at nocturnal low tide (Orr,
1933). However, it has been unclear to what extent fishes remain
in such hypoxic tide pools. We found the tidal pools formed at nocturnal low
tides at Lizard Island to be severely hypoxic, with oxygen levels typically
within the range of 8–12% of air saturation. A range of coral-reef
fishes were seen occupying these hypoxic tidal pools, including surgeonfish
(Acanthurus grammoptilus), emperors (Lethrinus sp.), coral
bream (Scolopsis bilineatus), rockcod (Epinephelus
spilotoceps), damselfishes (Chromis viridis, Pomacentus ambionensis,
P. nagasakiensis, P. wardi), butterflyfishes (Chaetodon auriga),
wrasses (Coris batuensis), shrimp goby (Amblyeleotris
steinitzi), sandperch (Parapercis cylindrica) and cardinalfishes
(Apogon spp.). This appears to be a fairly random selection of
coral-reef fishes, rather than a subset of species particularly well adapted
to survival in tide pools. (The exceptions may be the shrimp goby and the
sandperch, which both live in sand burrows on shallow water.) Thus, in
addition to residing within hypoxic coral colonies at night, some coral-reef
fishes also run the risk of encountering severe hypoxia when they venture into
shallow water and get trapped in nocturnal tidal pools.
Further research is likely to unveil coral-reef fishes living in other
hypoxic microhabitats. Many gobiids and blenniids live in sand burrows close
to coral reefs, and are likely to be exposed to hypoxia in their burrow. These
include Amblygobius phalaena
(Table 1), Asterropteryx
semipunctatus (Table 1),
Valenciennea longipinnis (studied by
Takegaki and Nakazono, 1999)
and V. strigata (Table
1), which all show a considerable hypoxia tolerance.
Interestingly, Amblygobius rainfordi, which live in sandy areas but
does not reside in burrows, shows the highest [O2]out of
the gobiids examined (Table 1).
With regard to parrotfishes (Scaridae) and wrasses (Labridae), their habit of
spending the night in a mucus-cocoon or buried in the sand may lead to
impaired oxygen exchange that demands hypoxia tolerance. Both wrasse species
that we have examined (Halichoeres melanurus, which we observed
burrowing in the aquarium, and Labroides dimideatus, which makes a
cocoon at night) showed a level of hypoxia tolerance that was similar to that
of most other coral reef fishes examined
(Table 1).
Overall, to live on a coral reef means more or less regular encounters with
hypoxia for many teleosts. As we shall see next, some may have to endure more
than others.
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The obligate coral-dwellers: hypoxia tolerant air breathers
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It is well known that many fishes living in tropical freshwaters, estuarine
habitats, or rocky intertidal zones have evolved air-breathing capacities to
cope with hypoxia or air exposure (Graham,
1997; Martin and Bridges,
1999). Also recently some fishes intimately connected to living
coral have been found to be excellent air-breathers. Apparently, for some
fishes, it is not enough to be hypoxia tolerant to survive in a coral habitat,
they also need the ability to breathe air. The need for air breathing probably
does not relate to aquatic hypoxia. It appears to have evolved to allow the
fishes to endure air exposure during the lowest of tides. In contrast to
fishes inhabiting intertidal rocky shores, air exposure in coral dwellers is a
rare event, and may only occur a few times a year during the lowest of
tides.
Coral-dwelling gobies of the genera Gobiodon are obligate
inhabitants of coral colonies, particularly species of branching
Acropora (Munday et al.,
1997). Some of these coral colonies not only become hypoxic at
night (see above) but can also become air exposed during very low tides. At
Lizard Island we have observed that colonies of Acropora can become
air exposed for up to 4 h during spring tides. To test if coral-dwelling
gobies can tolerate severe hypoxia and air exposure we initially focused on
Gobiodon histrio, whose preferred coral (Acropora nasuta)
(Munday et al., 1997;
Hobbs and Munday, 2004) is
often exposed to air. It was found that G. histrio could not only
tolerate hypoxia ([O2]crit was around 19% of air
saturation, Table 1), but also
endured hours of air exposure (Nilsson et
al., 2004). The ability to remain in the coral during periods of
hypoxia and air exposure would be a distinct fitness advantage, given the risk
of predation outside the coral and the potential loss of this limited habitat
to other competing gobies (Munday et al.,
2001; Hobbs and Munday,
2004).
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Air-breathing ability and habitat choice
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To determine if the hypoxia tolerance and air breathing abilities observed
in G. histrio are indicative of all obligate coral-dwelling fishes,
we repeated the same experiments on a range of species. These obligate
coral-dwelling species included coral gobies of the genera
Paragobiodon and Gobiodon, as well as the coral croucher
(also known as velvetfish; Caracanthus unipinna, family Scorpaenidae)
(Fig. 5). Preferences for host
coral species (Lassig, 1976;
Munday et al., 1997;
Wong et al., 2005) may overlap
and preferred corals are often a limiting resource, resulting in intense
intra- and interspecific competition
(Munday et al., 2001;
Hobbs and Munday, 2004).
Therefore, tolerance to hypoxia and the ability to breathe air would be
adaptive in this habitat. However, these coral dwellers vary in their
preference for coral species, water depth and reluctance to leave their host
coral. Some of them inhabit coral species that occur in shallow water where
they will become air exposed for several hours at the lowest tides, whereas
others live in coral species that occur in slightly deeper water and never
become air exposed.
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Fig. 5. Obligate coral dwellers represented by Gobiodon axillaris (A,
left, B), Paragobiodon xanthosomus (A, middle), Caracanthus
unipinna (A, right), and Gobiodon histrio (C). These fishes
spend virtually their whole life between branches of coral, and show a high
degree of hypoxia tolerance. Moreover, G. axillaris, G. histrio and
C. unipinna have excellent abilities for air breathing, apparently
through their scaleless skin. Air breathing is needed if their coral home
becomes air exposed. C shows G. histrio in a coral colony that has
become air exposed during a nocturnal low tide at the Lizard Island reef.
Photos by G. E. Nilsson.
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By using closed respirometry to compare hypoxia tolerance and air-breathing
capacity among Paragobiodon xanthosomus, Caracanthus unipinna and
seven species of Gobiodon we found a significant variation in hypoxia
tolerance, and that air-breathing ability was correlated with habitat use
(Nilsson et al., 2007a). The
four Gobiodon species (G. axillaris, G. erythrospilus, G.
histrio and G. unicolor) that inhabit Acropora corals,
which often occur in shallow water where they may become air exposed at low
tide, were all found to be excellent air breathers. Also C. unipinna,
which live in Acropora and Pocillopora species that extend
into shallow water, showed an equally good air-breathing capacity. By
contrast, Gobiodon acicularis and G. ceramensis, which
occupy corals of the genera Echinopora, Hydnophora and
Stylophora that do not usually become air exposed, could only
maintain oxygen uptake from air for short periods (an hour or less). Also
G. okinawae, which deviates from other Gobiodon by often
venturing relatively far from the host coral, and probably leaving it during
air exposure, was found to be a poor air breather. Finally, Paragobiodon
xanthosomus, which inhabits Seriatopora hystrix in areas that do
not usually become air exposed, was unable to take up oxygen from air.
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Cutaneous air-breathing and toxin production
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For the coral dwellers, the results suggested that oxygen uptake in air
occurs primarily through the skin, which is scaleless in both
Gobiodon and Caracanthus
(Nilsson et al., 2007a). This
conclusion is based on the observation of a 50% fall in the rate of oxygen
uptake when one body half of the fish was stuck to the wall of the
respirometer. Moreover, oxygen uptake was found to be maintained even if
ventilatory movements stopped in some individuals, indicating that oxygen
uptake over the gills or oral mucosa were of minor importance. In the five
best air breathers (G. axillaris, G. erythrospilus, G. histrio, G.
unicolor and C. unipinna), the rate of oxygen uptake was similar
in water and in air and could continue in air for at least 4 h, which
corresponds to the longest periods that their coral hosts may be air exposed
around Lizard Island. It was striking that the unrelated genera
Gobiodon and Caracanthus were found to have a similar
capacity for air breathing, most likely taking up the oxygen through their
scaleless skin, while Paragobiodon, a close relative to
Gobiodon, has retained its scales and is unable to breathe air.
Martin and Bridges (Martin and Bridges,
1999) suggested that for the skin to function as a respiratory
organ in fish, its must be relatively free of scales or other obstructions.
Our finding on the air-breathing abilities of the scaleless Gobiodon,
contra the closely related scaled Paragobiodon, certainly
supports this view, but being scaleless is apparently not a pre-requisite for
air-breathing in all fishes since a well vascularised epidermis can be present
outside the scales (Feder and Burggren,
1985).
It can be concluded that a high capacity for air breathing has evolved at
least twice in coral-dwelling fishes, and at least in the gobies, this is
probably a relatively late evolutionary event that probably involve the loss
of scales. In contrast to air-breathing fishes in freshwater habitats, marine
air-breathing fishes occupying intertidal zones have generally not evolved
specialized air-breathing organs (Graham,
1976; Graham,
1997). Similarly, except for the loss of scales, specialized
organs for oxygen uptake in air appear to be lacking in the obligate coral
dwellers.
While a scaleless skin probably improves cutaneous gas exchange, it is also
likely to make the fish particularly vulnerable to ectoparasites. The species
of the genus Gobiodon secrete a toxic mucus through glands in their
skin. This mucus is highly toxic to other fish attempting to eat them,
indicating a function in predator avoidance
(Schubert et al., 2003).
However, the scaled skin of Paragobiodon does not contain toxin
glands, which has led to the speculation that the toxin secreted through
glands in the scaleless skin of Gobiodon may be aimed at fighting off
cutaneous parasites. Indeed, a study has suggested that the scales of
Paragobiodon and the toxin of Gobiodon are equally effective
in fighting off ectoparasites, since exposing these gobies to gnathiid isopods
leads to similar infection rates in both genera
(Munday et al., 2003).
Interestingly, the same study showed that in Gobiodon, body regions
with fewer toxin glands were more vulnerable to these ectoparasites. Thus, in
Gobiodon, evolving a capacity for cutaneous air breathing may have
triggered the evolution of toxin glands to protect the scaleless skin from
parasites.
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Close association with coral correlate with hypoxia tolerance
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The nine species of obligate coral-dwelling fish studied
(Nilsson et al., 2007a) were
found to have an average [O2]crit of 20.4%, and did not
show any signs of distress until the ambient oxygen level fell to 3% of air
saturation, with two species doing well down to 1% of air saturation (genera
Gobiodon, Paragobiodon and Caracanthus in
Table 1). These values revealed
a significantly higher degree of hypoxia tolerance than that of coral-reef
fish with a somewhat less intimate connection with living coral (fishes of the
families Apogonidae, Labridae, Monacanthidae, Nemipteridae, and
Pomacentridae). Thus, an obligate association with living coral appears to
demand a particularly well developed tolerance to hypoxia. As mentioned,
measurements of nocturnal oxygen levels between branches in A. nasuta
colonies inhabited by Gobiodon show that these may fall well below
20% of air saturation (even as low as 2% for short periods)
(Fig. 2). A physiological
heritage allowing a high degree of hypoxia tolerance may have been a
prerequisite for these gobiids and scorpaenids to acquire an obligate
coral-dwelling life style. This is suggested by the particularly well
developed hypoxia tolerance (low [O2]crit and
[O2]out values) shown by other members of these two
families that live in reef habitats but do not show such a close association
with living coral (exemplified by genera Amblygobius, Asterropteryx,
Valenciennea, Parascorpaena and Sebastapistes in
Table 1).
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Hyperoxia – an additional challenge?
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Coral-reef fishes may not only need physiological adaptations that enable
them to utilize a hypoxic and air exposed environment. They may also have to
tolerate very high oxygen levels (hyperoxia) in the daytime due to oxygen
produced by various plants and algae, including the coral's symbiotic
photosynthesizing algae (zooxanthellae). Oxygen levels as high as 278% of air
saturation were measured in enclosed areas rich in coral at Low Isles (Great
Barrier Reef) (Orr, 1933).
Similarly, between the branches of A. nasuta colonies kept in
sun-exposed outdoor tanks on Lizard Island, we measured supersaturated oxygen
levels around 200% of air saturation during the middle of the day (G.E.N.,
J.-P.A.H. and S.Ö.N., unpublished observation). These corals were
inhabited by Gobiodon species, suggesting that hyperoxia is a factor
that these coral dwellers have to cope with. High levels of oxygen can be a
challenge for fish, since it may cause cellular damage through the formation
of reactive oxygen species (reviewed by
Lushchak and Bagnyukova,
2006). It appears that the life of these coral dwellers, from a
respiratory point of view, is in some aspects similar to that of many marine
tide-pool fishes, which are also exposed to highly variable oxygen levels
(Truchot and Duhamel-Jouve,
1980). Whether coral-dwelling fishes have particularly well
developed mechanisms for counteracting oxygen induced damage remains to be
explored.
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Tackling hypoxia with a mouth full of eggs
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Cardinalfishes (Apogonidae), a species-rich family on coral reefs, are
faced with a particular respiratory challenge. All species of this family are
mouthbrooders, and it is always the males that take care of this task. They
keep the brood in their mouth for about 2 weeks after fertilization
(Fig. 6A). This egg mass can
make up a quarter of the male's body mass
(Östlund-Nilsson and Nilsson,
2004), and it is virtually filling up his whole oral cavity, which
constitutes about 20–30% of the body volume and is significantly larger
in males compared to females (Barnett and
Bellwood, 2005). There is a central channel in the egg mass,
rendering it doughnut shaped (Fig.
6B). This channel probably serves to let some water through to the
gills, and aides in the ventilation of the gills as well as the egg clutch.
Still, one may assume that the egg mass will reduce the ability of the fish to
ventilate its gills, which could be a problem when they face hypoxia at night.
Moreover a reduced ability to ventilate the gills could affect the capacity
for sustained aerobic swimming.
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Fig. 6. A female (A, left) and male (A, right) of the cardinalfish Apogon
leptacanthus. The male is mouthbrooding, as revealed by its expanded
lower jaw. The egg mass of this species makes up about 14% of the body mass of
the male, and constitutes a considerable respiratory obstacle. (B) A male of
Apogon fragilis spitting his brood when exposed to hypoxia in a
closed respirometer, thereby significantly increasing his ability to take up
oxygen. Photos by G. E. Nilsson.
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We compared the respiratory consequences of mouthbrooding in two
Apogon species occurring at Lizard Island: the fragile cardinalfish
(A. fragilis) and the longspine cardinalfish (A.
leptacanthus) (Östlund-Nilsson
and Nilsson, 2004). The resting metabolic rate was not
significantly affected by the presence of the egg clutch in the mouth (if the
oxygen consumption of the clutch itself was accounted for). By contrast,
[O2]crit of the mouthbrooding males was increased, being
about 32% of air saturation, as compared to 18% in non-brooding males or
females. Thus, their hypoxia tolerance was clearly reduced by having the mouth
full of eggs. Moreover, their ability for sustained aerobic swimming was also
diminished: while non-mouthbrooding males of A. leptacanthus
could maintain a maximal aerobic swimming speed of 5.1 BL
s–1 (where BL is body length), the same value for
mouthbrooding males was reduced to 3.5 BL s–1. By
contrast, the time that the males could swim anaerobically against water
moving at speed of 14 BL s–1 was not affected by
mouthbrooding, both groups being able to do this for about 50 s
(Östlund-Nilsson and Nilsson,
2004). Of course, there is no obvious reason to expect that
anaerobic capacity would be significantly affected by having eggs in the
mouth.
The two species studied were found to differ in the mean brood mass, with
males of A. fragilis and A. leptacanthus having broods that
corresponded to 20% and 14% of the body mass, respectively. This difference
clearly affected their performance in hypoxia. When faced with a continuous
decrease in the ambient oxygen level in the closed respirometer, both species
eventually spat out the clutch (Fig.
6B), thereby sacrificing their offspring while significantly
increasing their ability to take up oxygen (i.e. increasing their own chance
of hypoxic survival). However, in A. fragilis (the species with the
larger egg mass), the brood spitting occurred at a less severe level of
hypoxia, 22% of air saturation, compared to A. leptacanthus, which
spat out the eggs at 13% of air saturation. Moreover, while mouthbrooding
A. leptacanthus were able to increase their ventilatory frequency in
response to a falling ambient oxygen level, mouthbrooding A. fragilis
were already performing at their maximal ventilatory rate during normoxic
conditions. These results clearly indicate a trade-off situation between brood
size and hypoxia tolerance. Being able to successfully brood a larger clutch
should mean a correspondingly larger increase in fitness. A. fargilis
appears to be gambling on a brooding period without any severely hypoxic
episodes, attempting to maximize the fitness gained from each brood, while
A. leptacanthus does not take this risk. Interestingly, both species
occur in the same habitat at daytime, often schooling together, which suggest
that these different strategies are not the result of different environmental
constraints in the preferred habitat. However, we do not presently know how
the different mouthbrooding strategies correlate with their nocturnal
habits.
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Ontogeny and respiration: from record swimmers to hypoxia tolerance
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Most coral-reef fishes have planktonic larvae
(Thresher, 1984). Thus, after
hatching, their larvae spend a few weeks drifting in the open water before
they settle on the reef. Research in the last decade has revealed that
coral-reef fish larvae develop very impressive capacities for high-speed
sustained swimming (i.e. for hours or even days) at the end of their pelagic
phase when they need to reach and settle on suitable coral habitats
(Stobutzki and Bellwood, 1994;
Leis and Carson-Ewart, 1997;
Pain, 1997;
Fisher et al., 2005). Indeed,
coral-reef fish larvae may have more influence on their movement and
distribution in the ocean than previously assumed
(Leis, 2006).
Many of the late stage pre-settlement larvae are capable of reaching
maximal sustained swimming speeds (Ucrit) of 30–50
BL s–1
(Stobutzki and Bellwood, 1994;
Leis and Carson-Ewart, 1997;
Fisher et al., 2005). To put
this into perspective, it can be mentioned that larvae of temperate fishes do
not usually reach a Ucrit higher than 4–5
BL s–1 (Blaxter,
1986; Meng, 1993).
Similarly, most adult fishes, including salmonids, cannot attain higher
sustained swimming speeds than 5–7 BL s–1. In
fact, not even the fishes best known for exceptional swimming performance,
including swordfish (Xiphias), tunas (Thunnus and
Euthynnus), and the inconnu (Stenodus leucichthys), which
can reach maximal sustained speeds of 12–20 BL
s–1 (Aleyev,
1977; Beamish,
1978), come close to the swimming performance of many coral-reef
fish larvae. Scaling can be used to explain the extraordinary swimming
performance of coral-reef fish larvae. It appears that the smaller a fish is,
the faster it can swim in relation to body size (i.e. in BL
s–1). However, this relationship only exists for fish that
have developed a capacity for forceful swimming, and coral-reef fish larvae
are probably the smallest fishes that have such capacities
(Bellwood and Fisher,
2001).
Swimming can only be sustained if it is fully aerobic and does not lead to
a build up of lactate (Goolish,
1991). Therefore, one may assume that the extremely high,
sustained (and therefore aerobic) swimming speeds of coral-reef fish larvae
must require very high rates of maximum oxygen uptake
(O2max). We
recently constructed a miniature swim respirometer that allowed us to measure
O2max during
high-speed swimming in larvae and juveniles of two species of damselfish,
Chromis atripectoralis and Pomacentrus ambionensis
(Nilsson et al., 2007b). Our
results showed that pre-settlement larvae of C. atripectoralis and
P. ambionensis, swimming at maximal sustained speeds, reach
O2max values of
about 5000 and 4000 mg O2 kg–1
h–1, respectively, which to our knowledge is the highest
O2max values
ever measured in cold-blooded vertebrates.
C. atripectoralis is one of the fastest swimming coral-reef fish
larvae both in nature and in laboratory race tracks. Thus, Leis and
Carson-Ewart (Leis and Carson-Ewart,
1997), who had divers swim after released coral-reef fish larvae
in nature, found that pre-settlement larvae of damselfish have some of the
highest maximum sustained swimming speeds. The 17 damselfish species they
examined reached an average maximum speed of 34 BL
s–1, with the 10 mm long C. atripectoralis larvae
being the fastest swimmers observed, reaching maximal in situ
swimming speeds of 53 BL s–1. Similar results have
later been obtained in swim tunnels
(Fisher et al., 2005),
although it appears that mean Ucrit values are generally a
bit higher than the average speeds seen in situ. Still, observations
of spontaneous swimming of pre-settlement larvae suggest that they are almost
constantly swimming at high speeds, although they rarely swim at their
Ucrit (Fisher and
Bellwood, 2003). In comparison with C. atripectoralis, P.
ambionensis is a more average performer among pre-settlement larvae, with
a Ucrit of about of 30 BL s–1
(Stobutzki and Bellwood,
1994).
We also carried out comparative measurements of
O2max in
Acanthochromis polyacanthus, which is one of very few coral-reef
damselfishes showing parental care, thus lacking a planktonic larval stage
(Randall et al., 1997). The
O2max of
resident A. polyacanthus juveniles weighing 30 mg, corresponding to
the pre-settlement size of other damselfishes, was about 2000 mg O2
kg–1 h–1, which was significantly lower than
the O2max of
4000–5000 mg O2 kg–1 h–1
that we measured in C. atripectoralis and P. ambionensis
(Nilsson et al., 2007b). This
low O2max in
juvenile A. polyacanthus coincides with a comparatively poor swimming
performance of these juveniles, which at a size that is equivalent to
pre-settlement larvae of other damselfishes, only reach a
Ucrit of 12 BL s–1
(Fisher et al., 2005).
We may conclude that the extraordinarily high, sustained swimming speeds of
pre-settlement damselfish larvae are paralleled by extraordinarily high
capacities for rapid oxygen uptake, and that these traits are important
because they enable the larvae to reach a suitable reef at the end of their
planktonic period. However, high aerobic capacities of very active fish
species appear to preclude hypoxia tolerance, and vice versa (for a
review, see Burggren et al.,
1991). Thus, fishes with highly active life styles and top
swimming performance cannot tolerate low oxygen levels. Salmonids, for
example, display [O2]crit values around 50% of air
saturation (Davis, 1975), and
tuna die when water [O2] falls below 60% of air saturation
(Gooding et al., 1981). The
underlying reasons are probably the opposing demands that a high
O2max and
hypoxia tolerance put on the oxygen-carrying properties of haemoglobin. Oxygen
uptake in hypoxia require haemoglobins with high O2 affinities,
which leads to relatively low rates of O2 downloading in the
tissues (O2 has to be downloaded at a low partial pressure, leading
to a small pressure gradient from blood into the mitochondria and therefore a
slow O2 delivery). Therefore, haemoglobins of highly active fish
show lower O2 affinities than those of sedentary species (reviewed
by Burggren et al., 1991).
As discussed earlier, coral-reef fishes probably need to cope with hypoxia
when they shelter in corals at night to avoid predators. An obvious question
therefore is: have coral-reef fishes found a unique way to combine extremely
high rates of oxygen uptake with hypoxia tolerance? Or, could it be that they
change their respiratory performance when they settle on the reef?
To answer these questions, we measured [O2]crit and
O2max with
closed respirometry in pre-settlement larvae, post-settlement larvae, and
juveniles of C. atripectoralis and P. ambionensis, as well
as in juvenile A. polyacanthus of different sizes
(Nilsson et al., 2007b). For
the two species with planktonic larvae, the results revealed a striking,
almost transient, reduction in
O2max and
[O2]crit within the first 5–10 days of settlement,
which is illustrated by data for C. atripectoralis in
Fig. 7. Thus, upon settlement,
larval C. atripectoralis and P. ambionensis adjust their
respiratory capacities to increase their hypoxia tolerance at the expense of
rapid oxygen uptake. Our results indicate that it takes about a week for the
settled larvae to attain low [O2]crit values, and that
high anaerobic capacities allow them to survive hypoxic episodes during this
period. Measurements of Ucrit in two species of developing
damselfish (P. ambionensis and the clown-fish Amphiprion
melanopus) also reveal a transient drop in swimming capacity when the
fishes reach settlement size (Bellwood and
Fisher, 2001) (Fig.
8). Thus, after settlement, these fishes are no longer
exceptionally fast swimmers with high
O2max values,
but instead become hypoxia-tolerant fishes that can utilize the shelter
provided by coral colonies at night.
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Fig. 7. Coral-reef fish larvae need to make a transition from top swimming
performance to hypoxia tolerance when they settle on a reef. Relationship
between body mass and (A) oxygen consumption at maximal swimming speed, and
(B) hypoxia tolerance (measured as [O2]crit) in larvae
and juveniles of Chromis atripectoralis. Note the transient drop in
maximum oxygen uptake and simultaneous increase in hypoxia tolerance (seen as
a drop in [O2]crit) that occur when the larvae settle on
the reef and become post-settlement juveniles. Data from Nilsson et al.
(Nilsson et al., 2007b).
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Fig. 8. Transient fall in maximum sustained swimming speed
(Ucrit) when post-settlement size is reached in two
species of damselfish, Amphiprion melanopus (A) and Pomacentrus
ambionensis (B). The fishes were reared in the laboratory and tested in a
swimming flume. From Bellwood and Fisher
(Bellwood and Fisher, 2001).
Reproduced with permission from Marine Ecology Progress Series.
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At present, we can only hypothesize on the mechanisms responsible for the
rapid change in respiratory properties displayed by settling coral-reef fish
larvae. An obvious possibility is that the transition involves changes in
blood oxygen affinity. Many fishes are known to possess multiple haemoglobin
isoforms, and there are examples of ontogenetic changes in haemoglobin isoform
expression in fishes (reviewed by Jensen
et al., 1998). Thus, when fish larvae settle on a coral reef, they
may change the expression of haemoglobin isoforms to types with higher
O2 affinity that allow hypoxia tolerance at the expense of fast
O2 downloading in the tissues. Unfortunately, the small size of the
larvae (generally less than 50 mg) would preclude a study of haemoglobin's
oxygen binding properties and isoform expression pattern using
electrophoresis, but it may be possible to measure changes in mRNA expression
of haemoglobin isoforms using quantitative PCR.
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Body size and hypoxia tolerance
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After the transition to hypoxia tolerance has occurred upon settling on the
reef, coral-reef fishes maintain a steady level of hypoxia tolerance
throughout life, as seen from the lack of any change in
[O2]crit with size in juvenile and adult fishes from the
Lizard Island reef (Fig. 9A).
This suggests that the level of hypoxia tolerance needed is constant
throughout life. This is not unexpected since they probably continue to use
the coral colonies as shelter after settlement, and may also continue to run
the risk of being temporarily confined in nocturnal tide pools. Nevertheless,
the role of size in hypoxia tolerance is not an uncontroversial issue.
Fig. 9B shows that in
coral-reef fishes (like in all organisms) mass-specific metabolic rate
(measured as routine rate of oxygen consumption) falls as body size increases.
An adult coral-reef fish has a mass-specific rate of oxygen consumption that
is about 10% of what it had when it settled on the reef
(Nilsson and Östlund-Nilsson,
2004; Nilsson et al.,
2007b). Arguably, because adults need that much less oxygen,
acquiring a low [O2]crit should be less of a challenge
for adults than for juveniles. Thus, life in hypoxia may become relatively
easy as coral-reef fishes reach adult size. In the hypoxia-tolerant oscar
cichlid of the Amazon river system, large individuals do indeed show a lower
[O2]crit (about 30% of air saturation) than smaller ones
(near 50% of air saturation) (Sloman et
al., 2006). On the other hand, it has been argued that the scaling
of respiratory factors such as gill-surface area and branching of blood
vessels should make smaller individuals more hypoxia tolerant than larger ones
(e.g. Robb and Abrahams,
2003), and a higher degree of hypoxia tolerance in small
individuals has been seen in some fish species
(Burleson et al., 2001;
Robb and Abrahams, 2003).
Still, one may expect that the degree of hypoxia tolerance displayed by a fish
reflects its need for survival under hypoxic cond
TOP
Summary
Introduction
