Oxygen and fish behaviour
StŽphan G. Reebs
UniversitŽ de Moncton,
Canada
2007
One of the basic principles of good aquarium
maintenance is to make sure that the water is well aerated, so that enough
dissolved oxygen is available for fish respiration. This oxygen can be produced by the photosynthesis of aquatic
plants and algae, or it can simply diffuse from air to water. In most environments it is diffusion
from air that represents the main source of dissolved oxygen. ThatÕs certainly the case for most
aquaria. (In that respect, one
should know that filtration systems are useful not only for cleaning the water
but also for stirring it, bringing bottom water to the surface where it can
take up oxygen from the air before being pushed back to lower levels where the
fish can enjoy it. Air bubblers
perform the same function and, as an additional benefit, they increase the area
of the air-water interface.)
In contrast to the ideal conditions that normally
prevail in the home aquarium, wild fishes are sometimes faced with situations
where little oxygen is present in the water. In places such as swamps and pools, the absence of wind and water currents
prevents the mixing of the oxygen-rich upper layer with the rest of the water
column. [1]
In other places, an
overabundance of aquatic animals or decomposing matter depletes oxygen through
increased consumption. These
conditions are not uncommon, and therefore it is not surprising to learn that
fishes have evolved special behaviours to cope with low oxygen levels. Good aquarists should have no cause to
ever witness these behaviours, but biologists, being the curious lot that they
are, have sought or created hypoxic (low oxygen) conditions and catalogued the
reactions of fishes to them. Here
is what they found.
Increased ventilation
A universal reaction to low oxygen is increased
ventilation of the gills. In the
same way that people start to breathe faster in order to bring more air to
their lungs, fishes increase the rate of water flow through their gills. A convenient measure is the rate at
which gill covers open and close under different levels of dissolved
oxygen. Thus three-spined
sticklebacks have been reported to increase their rate of gill cover movements
from 95 to 165 per minute after the oxygen content of their water was
experimentally cut down to half of its normal level.[2]
One could also hypothesize that ram-ventilating sharks (fishes that bring
oxygenated water to their gills by swimming with their mouths open) would
increase their swimming speed and would open their mouths wider when oxygen is
scarce. This is indeed what has been observed.[3]
In the lab, researchers normally reduce oxygen levels
by blowing bubbles of a physiologically neutral gas – usually nitrogen
– into the water; nitrogen then becomes much more abundant than oxygen
and displaces it as a dissolved gas.[4] One has to be mindful of confounding
variables in experiments of this kind: disease, stress and strenuous activity
can also make fishes – like people – breathe faster. To eliminate the potential effect of
these variables, it is important to work with animals that are consistently
healthy, calm and not fidgety. Moreover,
fishes are ectotherms (cold-blooded), which means that warm temperatures can
raise their metabolism and consequently their breathing rate also. Comparisons between oxygen levels must
therefore be done at similar water temperatures.
Decreased activity
After encountering an area of low oxygen content, fish
often start to swim rapidly and erratically. This is probably an adaptive response to escape the danger
zone. However, if hypoxic
conditions persist, most fish will greatly curtail their general activity. The
advantage of inactivity in the face of hypoxia is simple: less muscular work
means less need for oxygen. As
part of his doctoral research at Laval University in Quebec City, Fred
Whoriskey observed sticklebacks breeding in tide pools along the St-Lawrence
Estuary, and he reported that during periods when dissolved oxygen levels
dropped, the fish became very sluggish, even failing to show normal fright
responses when an object flew over the pool (the object could be a bird or, if
nature did not oblige, a frisbee thrown by the resourceful researcher). In the same vein but this time in a lab
at McGill University in Montreal, Don Kramer and his students observed that
guppies swim less, eat less, and court less when oxygen levels are lower than
normal.[5] Inactivity can even reach extremes such
as in the South American cichlid Biotodoma cupido (the
greenstreaked eartheater) which appears to fall ÒasleepÓ when oxygen is scarce.[6]
Aquatic surface respiration
Another common response to low oxygen is aquatic
surface respiration. In this
behaviour, fish stay just below the surface, put their snout at the air-water
interface, and breathe in the film of water that is in direct contact with the
air. This thin layer of water is
comparatively rich in oxygen. Once
I have seen this behaviour done by wild sticklebacks in a tide pool. It was a
very warm summer night without wind.
The water in the pool did not hold its normal load of dissolved oxygen
because it was warm, the absence of wind prevented mixing, and aquatic plants
could not photosynthesise and therefore produce oxygen in the dark.[7]
In the lab, Don Kramer and Martha McClure studied 24
species of tropical fish common to the pet trade, from tetras to barbs to
cichlids. They found that all of
these fishes performed aquatic surface respiration when oxygen was deficient.[8] Typically, the fishes waited until a very
low threshold of oxygen concentration was reached – less than 2 ppm[9],
or about 25% of well aerated freshwater at room temperature – before
starting surface respiration. This
reluctance to breathe near the surface is easy to understand when we consider that,
in nature, many predators of fishes are terrestrial or aerial animals that
attack from above, and therefore being close to the surface is risky.
Air-breathing
Some fishes can switch from
water-breathing to air-breathing when there is not enough oxygen in the
water. These fishes break the
surface and trap air inside their mouth.
Then they use their mouth, pharynx, oesophagus, swimbladder or even in
some cases their stomach like we use lungs, that is as a site where oxygen can
diffuse into the blood. Examples
of such fishes include gouramis, goldfish, loaches, catfishes, the
algae-consuming suckermouth catfish so common in home aquaria, and the
lungfishes.[10]
Air breathing allows many fishes to
lead an amphibious lifestyle, or to temporarily move out of the water if they
are bothered by predators, competitors, or the threat that their water world
will disappear because of a drought. Among the most amphibious of these fishes
are the mudskippers, which spend most of their active lives in the air on intertidal
mudflats where they feed and mate and bicker with their territorial neighbours.
They are skittish creatures, though, and they always have the option to retreat
into burrows dug in the mud (see page on construction). At least two species
– the giant mudskipper Periophthalmodon schlosseri and the walking goby Scartelaos histophorus – exhibit the interesting behaviour of storing air inside their
burrow. They take air into their mouth, dive into their water-filled burrow,
and release the air into special chambers. If researchers experimentally
extract air from the special chambers, the fish diligently replace it. The
significance of this behaviour stems from the facts that at high tide, when
water covers the mudflats, the fish stay in their burrow to avoid predators,
and water inside the burrow is often poorly oxygenated. At such times these air-breathing
fishes can tap into the air reserve of their special chambers.[11]
There are several physiological
advantages to using air as a source of oxygen. Per unit volume, air contains about 30 times more oxygen
than water (the exact value depends on water temperature). Moreover, air is 1000 times less heavy
and 50 times less viscous than water, and therefore easier to move through the
respiratory system. To grasp the
difficulty of breathing in water rather than air we need only consider the fact
that to survive, a fish of 100 g typically must move 30 to 65 g of water per
minute through its gills – that is 1/3 to 2/3 of its own body weight, a
substantial exercise! Only the
incredibly large surface area of the gills can compensate for this
disadvantage. But breathing in air also carries a major disadvantage: air
cannot support the gills. Gills
are thin to facilitate gas exchange and to maximise their number and surface
area. Because of their thinness, the gills usually are not self-supporting. For
a strictly water-breathing fish this is not a problem because water provides
support for the gills. However, if such a fish finds itself out of water, the
gills are not supported anymore. The collapse of gills and the limited surface
area of other possible breathing organs are the reasons why most fishes
ultimately choke outside water, despite the abundance of oxygen in air. Only air-breathing fishes can manage, and
among their anatomical adaptations are thicker (but less numerous) gills, as
well as modified swimbladders, mouths, gill chambers, guts, or skin that are
more blood-rich and gas-permeable than in other species.
Some species of fishes have become
so specialized for air-breathing that their capacity for water breathing is
impaired and they cannot meet all of their oxygen demand in normally oxygenated
water. They must breathe in air at least once in a while. Surprisingly for a
fish, they will literally drown if forced to stay in water. Among such fishes
are the South American pirarucu Arapaima gigas
(this fish can get huge, at 4.5 m and 200 kg, and 95% of its large oxygen
demand is provided by air-breathing), the freshwater butterflyfish Pantodon
buchholzi (popular in the aquarium trade), the adult Lepidosiren
paradoxa (a South American lungfish), the electric eel Electrophorus
electricus, the three-spot (=blue) gourami Trichogaster
trichopterus, and the climbing perch Anabas
testudineus.
Some air breathers, like the
European eel (Anguilla anguilla) or the trahiras
(family Erythrinidae), are capable of overland treks that takes them deep into
woods. Some can catch insects on land, like the afore-mentioned mudskippers
(subfamily Periophthalminae), the mangrove rivulus Rivulus marmoratus, the reedfish Erpetoichthys (=Calamoichthys) calabaricus, and the eel catfish Channallabes apus.
Mudskippers and the eel catfish can even bend their head downward to facilitate
the capture of prey lying on the ground, an anatomical adaptation –
shared with the salamanderfish Lepidogalaxias salamandroides – that is exceptional among fishes.[12]
Other amphibious fishes, like the North African catfish Clarias gariepinus (= lazera) and the climbing perch,
take advantage of their access to land to include grain in their diet.[13]
Others, like the goby Lentipes concolor,
can surmount waterfalls as high as 130 m (about 425 feet) by climbing on the
rocks behind or next to the falls, using a special suction cup formed by the
fusion of their pelvic fins (and they do this amazing feat not as adults, but
as fry no more than 2.5 cm long).[14]
And yet another air-breathing species is the splash tetra Copella arnoldi, which can jump from water to spawn on leaves; the males then keep the
eggs moist and oxygenated by splashing water onto them every 10-15 min. In an
aquarium, splash tetras can lay eggs on glass above the waterline, or even on
the underside of the tank lid.
By the way, other species, even
though they are not air breathers, are also known to lay eggs in places that
get exposed to air.[15]
For example, in Australia and New Zealand, several species of Galaxias deposit their eggs in vegetation above the waterline. The eggs hatch
only when water rises temporarily high enough to submerge them.[16]
In Canada, populations of ÒwhiteÓ sticklebacks lay their eggs in filamentous
algae or even on bare rocks in the intertidal zone, places that get exposed to
the air at low tide; exceptionally for a stickleback, the eggs receive no
parental care.[17] Sites
chosen for terrestrial egg laying are naturally moist – or kept moist, as
in the case of the splash tetra – so that the eggs wonÕt dry up and die.
By developing in air, eggs may benefit from higher temperatures, more oxygen
available, and protection against aquatic predators.
Oxygen and predation
As with aquatic surface respiration, air-breathing
entails a substantial risk of predation because of the fishÕs necessary
proximity to the surface. To
demonstrate this risk of predation, Don Kramer and his students hand-reared a
green heron until it was 1 year old and allowed it to forage in pools stocked
with various kinds of fishes (10 species of tropical fishes, as well as
bluegill sunfish and central mudminnows).
The researchers experimentally reduced dissolved oxygen to either 1.6 or
0.5 ppm. As expected, the fishes
came to the surface, albeit not as much as they would have if the heron had not
been there – they were aware of the birdÕs presence and the danger it
represented. Yet they were still
forced to come up once in a while to perform aquatic surface respiration or
air-breathing, especially at 0.5 ppm.
The heron caught more fishes at 0.5 ppm than at 1.6 ppm because of the
preyÕs greater use of the surface at that concentration. The danger inherent to aquatic surface
respiration and air-breathing was thus confirmed.[18]
With this risk in mind, it is worth mentioning that in
many species of air-breathing fishes, individuals can synchronize the time at
which they break the surface to gulp air.[19]
Presumably, the fishes are wary of predators and delay air gulping until they
see another fish get away with it. The link between predation and synchronous
air-breathing has been demonstrated experimentally by John Gee of the
University of Manitoba. He simulated
a heron strike by plunging the wooden model of a heron head into the water of a
tank housing central mudminnows, Umbra limi, and saw that
the mudminnows started to synchronise their air breaths after such a
disturbance. Instead of each individual breaking the surface at any time as
they did before, the mudminnows experimentally scared by Gee's fake heron
tended to break the surface more simultaneously.[20]
Other students and colleagues of Don Kramer have
investigated the risk of predation by piscivorous fishes rather than
birds. Robert Poulin has found
that guppies did not run a greater risk of being caught by oscars under
hypoxia, probably because the predatory oscars were just as affected by the
lack of oxygen as their prey. In
contrast, Nancy Wolf has observed that giant snakeheads, Channa micropeltes, were
more successful at capturing dwarf gouramis, Colisa lalia, at 1
ppm than at 3 or 8 ppm, because the gouramis had to leave the cover of
submerged plastic plants to go near the surface. The difference between the two studies may be that predatory
air breathers, such as snakeheads, are not as adversely affected by hypoxia as
predatory water breathers, such as oscars.[21]
Findings of this kind allow us to predict that
oxygen-poor habitats could provide a refuge to hypoxia-tolerant prey species
relative to their not-so-tolerant predators. This idea has been put forward to
explain the disappearance of indigenous species from the open waters but not
from swamps in waters infested by the predatory Nile perch in Africa,[22]
and to explain the boldness of minnows in the presence of visibly distressed yellow
perch under hypoxic conditions.[23]
When pursued by predators, tolerant species could do
more than just seek hypoxic refuges. They could simply jump out of the water
and spend some time on land. This predator-evasion behaviour has been observed
in rivulines (family Aplocheilidae), killifishes (family Cyprinodontidae), and the
bald sculpin Clinocottus recalvus.
Winterkill
In northern lakes, whole fish populations are
sometimes wiped out during the winter.
Following a fierce winter, very few fishes are found alive in the
lake. Such massive die-offs –
called winterkill – take place when the surface of the lake gets covered
by ice, with snow on top. The ice
isolates the water from the air, while the snow screens the aquatic plants from
much of the already short daylight, curtailing photosynthesis. Oxygen eventually runs out, and the
fishes start to die. They cannot
use aquatic surface respiration or unrestricted air-breathing because of the
ice. They are reduced to gathering
around air bubbles trapped underneath the ice, as witnessed in the field by
John Magnuson and his team from the University of Wisconsin.[24] But this, obviously, can only be a
short-term measure. The fishÕs only
hope for long-term survival – beside physiological adaptations such as
the use of anaerobic metabolism, see below – is to congregate near the
mouths of inflowing tributaries that discharge well-oxygenated water (if the
current is strong enough, ice does not form over the stream, and oxygen can
diffuse into it). Such streams,
unfortunately, cannot always be found, hence the winterkill.
Bringing oxygen to the eggs
Another aspect of behaviour very much affected by low
oxygen is parental care. Many
species lay their eggs on the surface of rocks and fan them. Fanning is an activity whereby the
parent maintains a flow of water over the eggs by rhythmically moving its fins
near them. This water movement is
necessary because without it the breathing eggs would use up all of the oxygen
present in the layer of water that immediately surrounds them, and thus would
eventually suffocate. The flow
created by the parent guarantees that well oxygenated water is in constant
contact with the eggs. Given this,
one would expect fishes to fan more when dissolved oxygen levels are low. This prediction is borne out. I have taken a battery-operated oxygen
meter to tide pools where male threespine sticklebacks tended their nests full
of eggs, and have found that lower oxygen levels coincided with higher
percentages of time spent fanning by the fish.[25] Dutch ethologists working in the lab
have also been able to coerce male sticklebacks into fanning more by connecting
a tube to their nest and pumping deoxygenated water through it.[26] Higher fanning levels caused by low
oxygen represent a great expenditure of energy by parental males, to the point
that they may lose weight and be unable to successfully breed a second time
after the first stressful attempt.
This was recently demonstrated in common gobies, Pomatoschistus
microps, by Jackie Jones and John Reynolds from the
University of East Anglia.[27]
A peculiar behaviour has been documented in one
species of cichlid, the rainbow cichlid Herotilapia multispinosa. Working in the lab of Miles Keenleyside
at the University of Western Ontario, Simon Courtenay exposed parental rainbows
to oxygen concentrations of only 2 ppm.
When the eggs hatched, the parents did not gather the emerging wrigglers
into pits dug in gravel as usual.
Instead they sucked the wrigglers into their mouth and spat them into
vegetation, onto which the wrigglers attached themselves thanks to
glue-producing glands on their head.
Courtenay showed that this behaviour, called Òwriggler-hangingÓ, was
more prevalent when oxygen concentration was low. Presumably, wrigglers benefited from being close to
vegetation because of the oxygen released by photosynthesis and also because
the plants were often closer to the surface. Wriggler-hanging has also been reported in other cichlids,
such as the angelfish, the red discus, the severum and the festivum.[28]
One of my students has told me about another peculiar
behaviour, this time in the convict cichlid. He had a pair of convicts tending their eggs inside a
ceramic skull (one of those aquarium decorations sold in pet shops). The female, instead of fanning her eggs
in the usual way, used to go to the airstone, take air into her mouth, bring it
back to the nest and release it at the bottom so that the air bubble would
float upwards along the egg batch.
She did this repeatedly, to the extent that air was gathering at the top
of the skull, threatening to raise the nest and its content all the way to the
surface! Did she carry air bubbles
to provide oxygen to her eggs in the face of localised hypoxic conditions? George Barlow has another
interpretation, which is probably better: he has observed a similar behaviour
in orange chromides, Etroplus maculatus, and he sees it
as an expression of fry-retrieving behavior (see page on parental care). The
small bubbles are about the same size as fry. The parent may be fooled into
thinking that the air bubbles are fry (even though its eggs have not hatched
yet), and it tries to bring back those incredibly mobile fry back into the
nest. [29]
There is another similar case, but one in which an
oxygen-supply explanation seems more likely. Some gouramis take in air, move
below their bubble nest, and with strong opercular action they squirt bubbles
up through the nest. [30]
This behaviour probably brings oxygen to the eggs and must have evolved as an
adaptation to the warm, stagnant and therefore oxygen-poor waters in which
these species eke out a living.
The ease of ventilating eggs may be influenced by nest
shape. In the common goby, males build a nest for their future eggs by dumping
sand over downturned mussel shells. In the lab they may do it over a clay
flower pot. The accumulated sand partially occludes the objectÕs opening.
Normally the males try to make the opening relatively small because this
impedes the entry of egg predators such as crabs. But small openings also mean
less potential for circulating water. It has been observed that the owners of
nests with smaller openings fan more than others. Also, if the oxygen content
of the water is experimentally reduced the males build nests with larger
openings. Obviously the fish adapt their nest building and nest tending
behaviour to oxygen levels.[31]
In many fish species, females prefer to lay eggs in
nests that already contain other eggs, perhaps a form of copying the choice
that previous females have made for particular high-quality males. But considerations
relating to oxygen must be taken into account. In sticklebacks for example, females
prefer to spawn in nests that already contain two or three clutches, but they
disregard nests that are packed with four or five clutches.[32] This may be related to the fact that
eggs in an overcrowded nest have trouble getting enough oxygen for optimal
development. In the same vein,
female common gobies normally prefer nests that already have eggs in residence,
but if the fish are kept in oxygen-poor water the females reverse their
preference and now favour nests that are empty. This new choice is probably adaptive because competition for
oxygen is fiercer in a nest with many eggs, and such a nest should therefore be
avoided when oxygen is already in short supply.[33]
The
South American lungfish Lepidosiren paradoxa lives in swamps where hypoxia is common.
In this species the male guards eggs and developing larvae within a nest. At
such a time, the male grows long filaments on his pelvic and pectoral fins.
Work in the 1930s has shown that oxygen is released from these filaments into
the water. It is thought that the filaments act as oxygenators for the nest and
its content. The male breathes air at the surface, oxygen passes into his
blood, and from there it is released into the nest through the thin surface of
the filaments.[34]
Physiological adaptations to low oxygen levels
Adaptations to low oxygen can be not only behavioural
but also physiological. Fishes that live in frequently hypoxic habitats may
have more haemoglobin in their red blood cells, and more of those cells in
their blood, and therefore a higher blood capacity to take up and transport
oxygen. Their body tissues may contain more myoglobin, a molecule that can bind
up oxygen and therefore act as an oxygen store.[35]
But their main adaptation is anaerobic metabolism, a set of biochemical
pathways that do not require oxygen to yield energy. This type of metabolism is
not very efficient and can lead to the accumulation of relatively toxic
by-products, such as lactic acid, and therefore when oxygen is present anaerobic
metabolism is put aside in favour of its aerobic counterpart. But when oxygen
is rare and metabolic demand is low, as in a cold water fish for example,
anaerobic metabolism can contribute to survival for days, weeks, or even months. For example, through the use of
anaerobic metabolism, goldfish can survive for up to 9 days at 4 oC
and only 0.5 ppm of oxygen. Similarly, from February to April there is
virtually no oxygen at the bottom of northern lakes, and yet crucian carp, Carassius
carassius, survive there because of their anaerobic metabolism
and the cold winter temperatures that lower their energy requirements.[36]
Finally, drought is another
ecological condition that selects for anoxia tolerance via anaerobic
metabolism. For example, the killifish Austrofundulus limnaeus lives
in ephemeral ponds in Venezuela and the eggs it produces can enter diapause and
survive for up to 60 days in the complete absence of oxygen.[37]
Last word
Behavioural and physiological responses are not
sufficient to allow fishes to live indefinitely in severely hypoxic waters, but
they can contribute to survival for significant periods of time. It is a comforting thought, one to
which fish keepers can cling next time they are away from home on an extended
leave, worrying about their air pumps suddenly failing.
[1] Chapman, L.J., Chapman, C.A., Nordlie, F.G., and Rosenberger, A.E.,
2002, Physiological refugia: swamps, hypoxia tolerance and maintenance of fish
diversity in the Lake Victoria region, Comparative Biochemistry and Physiology
A – Molecular and Integrative Physiology 133, 421-437; Congleton, J.L.,
1980, Observations on the response of some southern California tidepool fishes
to nocturnal hypoxic stress, Comparative Biochemistry and Physiology A 66,
719-722.
[2]
Jones, J.R.E., 1952, The reactions of fish to water of low oxygen
concentration, Journal of Experimental Biology 29, 403-415.
[3] Carlson, J.K., and Parsons, G.R., 2001, The effects of hypoxia on
three sympatric shark species: physiological and behavioral responses,
Environmental Biology of Fishes 61, 427-433.
[4] The amount of gas that can be dissolved
in water depends on four factors: (1) the intrinsic solubility of the gas (for
example the solubility of oxygen is twice that of nitrogen but 30 times less
than CO2); (2) the
water temperature (the warmer it is, the less gas can be dissolved); (3) the
salt content of the water (the more solutes present, the less gas can be
dissolved); and (4) the partial pressure of the gas (partial means relative to
other gases; for example, the more dissolved nitrogen and CO2 there
is in the water, the less the partial pressure of oxygen, even for a fixed
quantity of it, and the less oxygen can be dissolved). By bubbling nitrogen into the water, it
is possible to drive out as much as 90% of the oxygen already there just by
reducing its partial pressure. To
lower the concentration of dissolved oxygen even further (to less than 1 ppm),
it is possible to dissolve small quantities of sodium sulphite in the water, without
harm to the fish. To check oxygen
concentration, scientists use oxygen meters (Yellow Spring Instruments is a
popular brand) or chemical methods (for example, the well-known Winkler
Titration).
[5]
Kramer, D.L., and Mehegan, J.P., 1981, Aquatic surface respiration, an adaptive
response to hypoxia in the guppy, Poecilia reticulata
(Pisces, Poeciliidae), Environmental Biology of Fishes 6, 299-313. Kramer has done a lot of work on
the effect of low oxygen levels on fish behaviour, and has written a good
review on the topic: Kramer, D.L., 1987, Dissolved oxygen and fish behavior,
Environmental Biology of Fishes 18, 81-92.
[6]
Cichocki, F., 1977, Tidal cycling and parental behavior of the cichlid fish, Biotodoma
cupido,
Environmental Biology of Fishes 1, 159-169.
[7]
Reebs, S.G., Whoriskey, F.G., and FitzGerald, G.J., 1984, Diel patterns of
fanning activity, egg respiration, and the nocturnal behavior of male
three-spined sticklebacks, Gasterosteus aculeatus L.
(f. trachurus), Canadian Journal of Zoology 62, 329-334.
[8]
Kramer, D.L., and McClure, M., 1982, Aquatic surface respiration, a widespread
adaptation to hypoxia in tropical freshwater fishes, Environmental Biology of
Fishes 7, 47-55. The species
tested were of different shapes, but it is worth mentioning here that the
flattened head shape of poeciliids and other tropical fishes common to the pet
trade could be viewed as an adaptation for aquatic surface respiration because
it allows better access to the thin layer of oxygen-rich water near the
surface. Water is often hypoxic in
the tropics because of its high temperature and, consequently, its low oxygen
solubility. This, however, does
not mean that aquatic surface respiration is limited to tropical species. It can be found at any latitude; for
example, see: Gee, J.H., Tallman, R.F., Smart, H.J., 1978, Reactions of some
Great Plains fishes to progressive hypoxia, Canadian Journal of Zoology 56,
1962-1966.
[9] ppm
means part per million, which in this case is equivalent to milligrams of O2
per litre of water.
[10] For a thorough review, including a list of all groups of fish that
breathe air, see: Graham, J.B., 1997, Air-breathing Fishes: Evolution,
Diversity, and Adaptation, Academic Press, San Diego. Also: Martin,
K.L.M., 1995, Time and tide wait for no fish: intertidal fishes out of water,
Environmental Biology of Fishes 44, 165-181; Sayer, M.D.J., 2005, Adaptations
of amphibious fish for surviving life out of water, Fish and Fisheries 6,
186-211.
[11]
Ishimatsu, A., Hishida, Y., Takita, T., Kanda, T., Oikawa, S., Takeda, T., and
Huat, K.K., 1998, Mudskippers store air in their burrows, Nature 391, 236-237;
Lee, H.J., Martinez, C.A., Hertzberg, K.J., Hamilton, A.L., and Graham, J.B.,
2005, Burrow air phase maintenance and respiration by the mudskipper Scartelaos
histophorus (Gobiidae: Oxudercinae), Journal of Experimental
Biology 208, 169-177.
[12] Van Wassenbergh, S., Herrel, A., Adraens, D., Huysentruyt, F.,
Devaere, S., and Aerts, P., 2006, A catfish that can strike its prey on land,
Nature 440, 881.
[13] Graham, J.B., 1997, Air-breathing Fishes: Evolution, Diversity, and
Adaptation, Academic Press, San Diego.
[14] Sherman, P.T., and Eason, P.K., October 2004, Climb every
waterfall, Natural History 113(8), 33-37.
[15] For a review: Martin, K.L.M., Van Winkle, R.C., Drais, J.E., and
Lakisic, H., 2004, Beach-spawning fishes, terrestrial eggs, and air-breathing,
Physiological and Biochemical Zoology 77, 750-759. For a recent example, this
time concerning an air-breather: Shimizu, N., Sakai, Y., Hashimoto, H., and
Gushima, K., 2006, Terrestrial reproduction by the air-breathing fish Andamia
tetradactyla (Pisces; Blennidae) on supralittoral
reefs, Journal of Zoology 269, 357-364.
[16] McDowall, R.M., and Charteris, S.C., 2006, The possible adaptive
advantages of terrestrial egg deposition in some fluvial diadromous galaxiid
fishes (Teleostei: Galaxiidae), Fish and Fisheries 7, 153-164.
[17] MacDonald, J.F., Bekkers, J., MacIsaac, S.M., and Blouw, D.M.,
1995, Intertidal breeding and aerial development of embryos of a stickleback
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