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First published online March 17, 2006
Journal of Experimental Biology 209, 1197-1205 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02090
Tribute to R. G. Boutilier: The effect of size on the physiological and behavioural responses of oscar, Astronotus ocellatus, to hypoxia
1 School of Biological Sciences, University of Plymouth, Devon, PL4 8AA,
UK
2 Department of Biology, McMaster University, Hamilton, Ontario, Canada L8S
4K1
3 Department of Zoology, University of British Columbia, Vancouver, Canada
V6T 1Z4
4 Department of Fisheries and Oceans, Canada Centre for Inland Waters,
Burlington, Ontario, Canada L7R 3A6
5 Laboratory of Ecophysiology and Molecular Evolution, INPA, Manaus,
Brazil
* Author for correspondence (e-mail: katherine.sloman{at}plymouth.ac.uk)
Accepted 12 January 2006
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Summary |
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O2 during
decreasing environmental oxygen tensions. Larger oscars were better able to
maintain oxygen consumption during a decrease in
PO2, regulating routine
O2 to a
significantly lower PO2 threshold (50 mmHg)
than smaller oscars (70 mmHg). Previous studies have also demonstrated a
longer survival time of large oscars exposed to extreme hypoxia, coupled with
a greater anaerobic enzymatic capability. Large oscars began aquatic surface
respiration (ASR) at the oxygen tension at which the first significant
decrease in O2
was seen (50 mmHg). Interestingly, smaller oscars postponed ASR to around 22
mmHg, well beyond the PO2 at which they
switched from oxyregulation to oxyconformation. Additionally, when given the
choice between an hypoxic environment containing aquatic macrophyte shelter
and an open normoxic environment, small fish showed a greater preference for
the hypoxic environment. Thus shelter from predators appears particularly
important for juveniles, who may accept a greater physiological compromise in
exchange for safety. In response to hypoxia without available shelter, larger
fish reduced their level of activity (with the exception of aggressive
encounters) to aid metabolic suppression whereas smaller oscars increased
their activity, with the potential benefit of finding oxygen-rich areas.
Key words: oxygen, Amazon, predation, social, aquatic surface respiration (ASR), oscar, Astronotus ocellatus
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), allowing the
use of air as a respiratory medium. Breathing air can be advantageous as it
contains a higher percentage of oxygen relative to volume than water (Dejours,
1994), but there are also many problems associated with air-breathing in
aquatic organisms as their gills need to remain functional for gas exchange,
nitrogen excretion and ionoregulation
(Gilmour, 1998).
Thus many fish respond differently to falling oxygen tensions and non
air-breathing fish demonstrate a suite of physiological, biochemical and
behavioural strategies. For example, changes in gill morphology
(Laurent and Perry, 1991)
allow more efficient extraction of oxygen from the water that can be coupled
with increased oxygen carrying capacity
(Powers, 1980) to combat
hypoxia. Many vertebrates and invertebrates have an inherent ability to
downregulate their metabolic rate to balance ATP demand and ATP supply
pathways, a subject that was explored in great depth by Bob Boutilier and his
colleagues (Boutilier and St-Pierre,
2000; Boutilier,
2001a; Boutilier,
2001b; Staples et al.,
2003). This downregulation can be brought about at the cellular
level by decreasing energy-consuming processes and/or by increasing the
efficiency of energy-producing pathways
(Boutilier, 2001b). Depression
of metabolic rate can significantly increase survival time of fish exposed to
hypoxia (Almeida-Val et al.,
2000). Additionally, changes in fish behaviour can complement
metabolic depression by minimising non-essential activities
(Israeli and Kimmel, 1996;
Crocker and Cech, 1997;
Dalla Via et al., 1998) or by
exploiting spatial heterogeneity of dissolved oxygen through increased
activity (Dizon, 1977;
Domenici et al., 2000).
Another behaviour performed in response to hypoxia is aquatic surface
respiration (ASR), where fish choose to move to surface waters where oxygen
diffusion from the air results in a thin layer of well-oxygenated water
(Kramer and Mehegan, 1981;
Kramer and McClure, 1982;
Verheyen et al., 1994;
Shingles et al., 2005). Rather
than a `last gasp' attempt to escape hypoxia, ASR is a clear behavioural
adaptation displayed by many fish species
(Kramer and Mehegan, 1981;
Kramer, 1987). Although an
efficient method of maintaining oxygen consumption
(Val, 1995), ASR necessitates
excursions to the water surface to ventilate in the oxygen-rich surface layer,
which can dramatically increase susceptibility to aerial predators
(Kramer et al., 1983;
Randle and Chapman, 2005) and
air-breathing predatory fish (Wolf,
1985).
So, on the one hand ASR can decrease the physiological demands imposed by
hypoxia but may increase susceptibility to predation. On the other hand,
remaining in hypoxic waters necessitates either physiological or biochemical
responses but can decrease the risk of both aerial predation and predation by
aquatic predators less tolerant of hypoxia
(McIntyre and McCollum, 2000;
Robb and Abrahams, 2003). The
idea of hypoxia as an ecological refuge in which animals can avoid predators
less tolerant of low oxygen levels is based on the premise that many larger
predatory fish are physiologically excluded from hypoxic conditions available
to the smaller fish that they eat (Kolar
and Rahel, 1993; Chapman et
al., 1996; Robb and Abrahams,
2003). Indeed, it has been documented within several fish species
that smaller individuals are more tolerant of hypoxia than larger individuals
(Smale and Rabeni, 1995;
Burleson et al., 2001;
Robb and Abrahams, 2003).
For non air-breathing species that perform ASR, it therefore seems possible
that smaller individuals, which by virtue of their size are more vulnerable to
predation (Abrahams, 2005), should have evolved a greater physiological
capacity for using hypoxia as an escape from predation. In contrast, larger
individuals, less susceptible to predation, could supplement their oxygen
uptake by performing ASR. It is then perhaps surprising to find examples of
fish species known to perform ASR, where hypoxia tolerance is greater in
larger individuals. Interestingly, in the oscar Astronotus ocellatus,
characterised as an extremely hypoxia-tolerant species
(Almeida-Val and Hochachka,
1995), measurements of two key glycolytic and oxidative flux
enzymes suggest that anaerobic potential actually increases during growth
(Almeida-Val et al., 2000).
Thus a scaling effect on hypoxia tolerance has been proposed where larger
oscars are better physiologically equipped for coping with hypoxic conditions.
By reducing standard metabolic rates and postponing anaerobic glycolysis,
adult oscars are able to tolerate complete anoxia for up to 4 h
(Muusze et al., 1998), unlike
smaller juvenile oscars.
The present study therefore aimed to investigate the interplay between size and the physiological and behavioural responses of oscars to hypoxia. The physiological responses of oscars to hypoxia were assessed by measuring the rate of oxygen consumption of fish in relation to decreasing environmental oxygen and the behavioural responses by quantifying movements with regard to ASR, hypoxia avoidance, activity levels and social interaction.
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Materials and methods |
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Experiment 1: The effect of declining PO2 on O2
Experiments were performed on 35 oscars covering the mass range
8.8–308 g. Approximately 12 h before an experiment, the fish were placed
in sealable Nalgene® containers, and allowed to settle overnight. The
containers were placed in a water-bath to control temperature and were covered
with black plastic to minimize visual disturbance. The containers were chosen
so as to have a volume equivalent to 50–80 times the mass of the fish,
and were vigorously aerated to maintain air-saturated conditions during the
settling period. The following morning, the water was renewed with minimal
disturbance, and the experiment started 2 h later by ceasing aeration and
sealing the containers. Water samples (0.5 ml) were drawn by syringe at 15 min
intervals until the PO2 had fallen below 10
mmHg, a process that took 4–8 h. The small volume of water that was
removed at each sample time was replaced. Plots of
PO2 versus time were constructed, and
O2 values
calculated from the slopes over 20 mmHg intervals interpolated to
PO2=150, 130, 110, 90, 70, 50, 30 and 10 mmHg,
factored by fish mass, water volume and O2 solubility coefficient
at the exact temperature, the latter taken from Boutilier et al.
(Boutilier et al., 1984).
Experiment 2: Relationship between oxygen tension and ASR
Fish were placed individually into a glass tank (34 l) containing water
that was continuously aerated through an air stone situated at the bottom of
the tank. The fish were allowed 1 h to acclimate to the tank prior to the
start of the experiment. A piece of opaque plastic floating on the water
surface largely eliminated any contact of the water with the air. The tank was
divided into vertical sections marked on the outside of the tank. The first
section was from the bottom of the tank (0%) to a quarter of the way to the
surface (25%), the second from 25–50%, the third from 50–75%, the
fourth from 75% to 90% and the final section consisted of the water within 10%
of the surface (90–100%). Following acclimation, the air supply to the
tank was switched to nitrogen and the oxygen tension gradually reduced. Oxygen
tensions were measured as above every 5 min in each vertical section (see
Fig. 3A in the Results
section). No significant vertical zonation of oxygen occurred
(P=0.771). Throughout the experiment the vertical movements of the
fish were recorded and every 5 min the breathing frequency of the fish was
recorded as beats min–1. When the snout of the fish touched
the water surface this was considered the end of the experiment, the gas
supply was switched back to air and the fish allowed to recover.
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65 mmHg). The fish was then observed from a distance
and the time spent under the shelter (i.e. in the lowest oxygen tension) was
noted. Each trial lasted for 10 min. After this time the fish was removed, the
gradient allowed to re-establish and the next fish tested. Four different
experimental treatments of fish (N=7 for each treatment) were tested.
The first two treatments were either large or small oscars taken directly from
their respective stock tanks. For the third and fourth treatments, large or
small oscars were held in hypoxic water (30 mmHg) for 1 h prior to testing in
the experimental set-up. Within each size group, different individuals were
used to test for the prior effects of holding in normoxia or hypoxia, so that
each individual was naïve to the system. However, there were no
significant intragroup differences in size between these treatments
(P=0.9).
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Prior to each observation the observer sat for 10 min in front of the tank to allow the fish to acclimate to the observer's presence. Fish were then watched for 10 min. For the recording of activity, the tank was divided horizontally into quarters (drawn on the outside of the tank). Each time the snout of a fish crossed into another section of the tank this was counted as one horizontal movement. The tank was also divided into three vertical sections (marked on the outside). The first section was from the bottom of the tank (0%) to half way to the surface (50%), the second from 50–90% and the final section consisting of the water within 10% of the surface (90–100%). Each time the snout of a fish crossed into another vertical zone this was counted as one vertical movement. The number of horizontal and vertical movements of each fish was therefore calculated throughout the observation periods. Aggression was also calculated, with an attempted or actual bite of one fish against another counting as one aggressive action.
Following the initial 10 min observation period, tanks were allocated to either control or experimental treatments. Control tanks were left for 1 h, and in the experimental tanks oxygen tensions were reduced from normoxia (136.4±1.3 mmHg) to a nominal concentration of 80 mmHg (79.8±0.8 mmHg) by bubbling nitrogen into the tank. The required PO2 in experimental tanks was achieved by a steady reduction over the 1 h period. Behavioural observations were then repeated in both treatments. Oxygen levels were measured during the observation time with water samples being taken from all three vertical zones. No significant vertical zonation of PO2 was noted within the tanks (P>0.1).
Following the second behavioural observation the control tanks were left for a further 1 h while the oxygen level in the experimental tanks was gradually reduced as before to a nominal PO2 of 40 mmHg (39.7±0.6 mmHg). A final set of behavioural observations was then made on both the control and experimental tanks.
To investigate whether the socially mediated differences in plasma cortisol
concentrations documented in other fish species
(Sloman and Armstrong, 2002;
Gilmour et al., 2005) occurred
among social groups of oscars, six control groups of large oscars were sampled
for cortisol at the end of the experiment. Fish were killed by a lethal dose
of anaesthetic (0.5 mg ml–1 benzocaine) and a blood sample
withdrawn by caudal venipuncture. Blood samples were centrifuged, the plasma
removed and stored at –80°C for later analysis of cortisol by
radioimmunoassay (ICN Pharmaceuticals, Costa mesa, CA, USA).
Statistical analyses
Data were checked for normality using the Kolmogorov–Smirnov test.
Where data were normally distributed, parametric analyses of variance (ANOVA:
post hoc Tukey and Student's t-test) were used to test for
statistical differences among treatments in physiological and behavioural
parameters. In some cases significant interaction effects in two-way ANOVA
analyses masked differences between size groups so the data were subsequently
analysed separately for post hoc effects. Where data were not
normally distributed the non-parametric Kruskal–Wallis test was used to
look for statistical differences among treatments.
In experiment 1, the relationships describing
O2 as a function
of body mass and water PO2 were analysed by
multiple regression, analysis of covariance (ANCOVA; logarithmic and linear
models) and also by a two step-procedure in which log
O2 was first
regressed against log mass
[logO2=log(a)+b(log
mass)], and an asymptotic equation was fitted to the residuals (m)
from the first equation which described them as a function of
PO2
[m=x–y.zPO2].
The two equations were then combined
{logO2=[log(a)+x]+b[log(mass)]–y.zPO2}.
This latter approach yielded the highest r2 and was the
procedure chosen to derive the reported model.
In experiment 4, an overall behaviour score for individual fish was calculated by combining each behavioural parameter measured (i.e. vertical activity, horizontal activity, aggression) in a Principal Components Analysis and a correlation was used to analyse the relationship among behaviour scores of fish at varying levels of PO2. All data are presented as means ± s.e.m.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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O2O2
and the response of
O2 to declining
PO2 varied with fish size
(P<0.001). In large oscars, mass-specific
O2 remained
unchanged until a PO2 of 50 mmHg, where it fell
significantly to 74% of the value in air-saturated water
(Fig. 1). By 10 mmHg,
O2 had declined
to about 30%. In small oscars, mass-specific
O2 was much
greater, but fell gradually with PO2, the first
significant decline occurring at a higher threshold, 70 mmHg, where it was 73%
of the value in air-saturated water (Fig.
1). By 10 mmHg,
O2 had fallen to
about 20%. The overall range in body mass was sufficient to construct a model
(Fig. 2) describing the
three-dimensional response surface relating mass-specific
O2 to body mass
and water PO2, which explained 94.8% and 92.8%
of the variance, respectively, for fish of mass 10–50 g and 50–300
g. In both small and large fish, mass-specific
O2 explained
81.6% of the variability in the data, while water
PO2 explained the additional 13.2% and 11.2%,
respectively.
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Experiment 2: Relationship between oxygen tension and ASR
Size significantly affected the PO2 at which
oscars made an attempt to break the water surface with their snouts
(P=0.02; Fig. 3B).
Large fish surfaced at a higher PO2
(49.6±9.8 mmHg) than small fish (22.3±3.7 mmHg). Fish mass was
positively correlated with the PO2 at which the
fish broke the water surface with its snout (P=0.04,
r2=0.207). In general, small oscars showed a greater
(48.1±5.3%) decrease in breathing frequency than large oscars
(22.3±4.3%; P=0.002) during hypoxia, probably due to the
earlier surfacing of larger fish.
Experiment 3: Position choice in an oxygen gradient
For fish previously held in normoxia (130 mmHg), size significantly
affected time spent under the plant shelter, with smaller individuals spending
significantly more time (essentially the entire 10 min test period) in the
hypoxic, sheltered water (Fig.
4B; P<0.01). However, small oscars reduced the amount
of time under the shelter when held in hypoxic water (30 mmHg) for 1 h prior
to testing in the experimental set-up (Fig.
4B; P<0.01). Large oscars did not.
Experiment 4: Group activity during hypoxia
The behaviour of control groups of fish was observed over time in the
absence of hypoxia. For control groups of both small and large oscars, there
was no observed change in behaviour among observation periods
(P>0.5). However, there were differences in control group
behaviours according to size. Groups of large fish displayed more horizontal
activity than groups of smaller fish and were more aggressive
(P<0.001). Indeed no aggressive acts were observed among control
groups of small oscars in comparison with a total of 147 acts in control
groups of large oscars. Among groups of large oscars, clear social hierarchies
were observed, with high levels of aggression generally displayed by one fish
within the group. However, no socially mediated differences in cortisol were
observed [P=0.8; mean cortisol value (± s.e.m.) =
6.35±0.85 ng ml–1].
Hypoxia significantly affected the group behaviour of both large and small oscars, but with large and small oscars responding in different ways (P<0.05). Groups of large oscars showed a decrease in horizontal activity with decreasing PO2 (Fig. 5A; P<0.01) while small oscar did not (P>0.1). In contrast groups of small oscars showed an increase in vertical activity (up to the 50% line) with decreasing PO2 (Fig. 5B; P<0.05) unlike larger oscar (P>0.1). Aggression was not significantly affected by hypoxia in either size group (P>0.1) although, as for the control groups, aggression was significantly higher among groups of larger fish (P<0.001; Fig. 5C).
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Interestingly, a positive correlation existed among the individual activity scores for each fish at varying levels of PO2 (P<0.001; Fig. 5D). Therefore the activity of each individual fish in relation to its group members did not vary with changing oxygen tensions (i.e. the most active member of each group remained the most active at each oxygen level).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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O2 than large
oscars in experiment 1 and initially both small and large oscars displayed
independent respiration (Hughes,
1981), with rate of oxygen consumption
(O2) remaining
constant despite a fall in the oxygen tension of the water
(PO2). However, at 70 mmHg, the
O2 of small
oscars ceased to be independent of environmental oxygen tension and a
significant decrease in
O2 was noted. At
50 mmHg a similar effect was seen in large oscars, suggesting that large
oscars are able to regulate their oxygen consumption by adjustments in
respiration and circulation to a lower oxygen threshold than small oscars.
Large oscars also have a much greater ability to survive exposure to extreme
hypoxia, as previously demonstrated
(Almeida-Val et al., 2000).
Fish around 16 g in mass (equivalent to `small' in our study) survived extreme
hypoxia for about 9 h (Almeida-Val et al.,
2000) and the respective larger individuals of 230 g survived for
approximately 35 h. Thus while larger oscars appear to tolerate falling
PO2 levels slightly better than their smaller
counterparts, this difference is magnified considerably once extreme hypoxia
is reached and anaerobic metabolism becomes necessary. The greater anaerobic
potential of large oscar, as indicated by higher concentrations of lactate
dehydrogenase and malate dehydrogenase
(Almeida-Val et al., 2000),
also fits with this scenario. In summary, unlike many other species, e.g.
yellow perch Perca flavescens
(Robb and Abrahams, 2003) and
largemouth bass Micropterus salmoides
(Burleson et al., 2001), the
oscar shows a positive relationship between physiological tolerance of hypoxia
and size.
A behavioural ecology approach might predict that when faced with
decreasing oxygen, fish should choose the response that minimises the costs of
obtaining the required amount of oxygen
(Kramer, 1987). So, one might
expect that if ASR, like the air-breathing response in other species, is
evoked by the environmental oxygen tension at which respiratory mechanisms
fail to compensate for environmental hypoxia
(Takasusuki et al., 1998),
then smaller oscars would perform ASR at a higher oxygen tension than adults.
In experiment 2, larger oscars did perform ASR at approximately 50 mmHg, the
tension at which the first significant drop in their
O2 was seen.
Surprisingly, smaller oscars postponed ASR to around 22 mmHg, well beyond the
PO2 at which they switched from oxyregulation
to oxyconformation (70 mmHg).
Claireaux et al. (Claireaux et al.,
1995) stated that in responding to environmental factors fish may
simply be constrained into choosing the lesser of two evils, and for smaller
oscars it appears that, at least at oxygen tensions above 22 mmHg, ASR has
greater negative consequences for fitness than remaining in a hypoxic
environment. Susceptibility to aerial predators
(Kramer et al., 1983; Randle
and Chapman, 2004) and other predatory air-breathing fish
(Wolf, 1985) is a likely
explanation, as supported by the results of experiment 3. In an oxygen
gradient where shelter from floating plants was only available in hypoxic (30
mmHg) water, small oscars chose to move under the shelter for virtually the
entire experimental period and accept the associated physiological cost of
exposure to hypoxia. In contrast, large oscars spent approximately 50% of
their time in normoxia and 50% under the shelter. However, if small oscars
were held for 1 h at 30 mmHg prior to placing in the gradient, then they were
forced to choose more oxygenated waters that did not contain shelter. As oscar
are known to accumulate significant amounts of lactate during hypoxia
(Muusze et al., 1998) it is
likely that these small oscar were no longer able to physiologically tolerate
hypoxia. Predators of oscar include examples of air-breathing fish (e.g.
pirarucu; Arapaima gigas) and other vertebrates such as alligators
(V.M.F.A.-V., personal observations). It is not yet known whether there is a
difference in predator species that prey on large and small oscar.
Oxygen chemoreceptors on the gill epithelia mediate physiological changes
in response to hypoxia (Reid and Perry,
2003). Similar receptors are believed to stimulate air-breathing
fish to surface in hypoxia (McKenzie et
al., 1991; Taylor et al.,
1996) and it has been suggested that they also play a role in
eliciting ASR (Shingles et al.,
2005). In the flathead grey mullet Mugil cephalus,
Shingles and colleagues (Shingles et al.,
2005) demonstrated that ASR is a behavioural
O2-chemoreflex that can be modified by the risk of predation. The
choice of juvenile oscars to remain in hypoxic waters appears to be another
example of behavioural modulation of hypoxic chemoreflexes affording them a
reduction in susceptibility to potential predators.
ASR is but one behavioural adaptation in a suite of many and a complex
combination of behavioural responses to hypoxia should be expected, designed
to match oxygen supply and demand by the least costly means
(Kramer, 1987). In experiment
4, changes in activity were considered as another behavioural response to
hypoxia, both as the simple amount of horizontal and vertical movement and
also as more complex social interactions. The effects of hypoxia on
spontaneous locomotor activity documented within the literature appear to be
species- and situation-specific (Kramer,
1987). Here a clear difference between sizes was seen in the
effect of hypoxia on activity level. Large oscars were more active than small
oscars under control conditions and showed a decrease in movement in the
horizontal plane with decreasing oxygen tensions, whereas small fish showed an
increase in activity during hypoxia. The increase in activity in smaller fish
was recorded in the vertical plane although it should be noted that the fish
only increased their number of excursions around the 50% line, not up to the
water surface (as might be expected at tensions less than 22 mmHg). Thus it
seems likely that larger fish reduce their level of activity to aid metabolic
suppression (Boutilier and St-Pierre,
2000) whereas smaller fish increase their activity, potentially in
the hope of finding areas less devoid of oxygen
(Domenici et al., 2000).
Oscars live in small schools forming monogamous pairs for reproduction,
where both sexes will establish and defend breeding sites
(Santos et al., 1984;
Beeching, 1995). Aggressive
interactions between mature adults have been documented
(Beeching, 1997), with combat
defeat eliciting a colour pattern change from the normal olive-green-brown
body colouration to a near black colour interrupted with irregular white
barring (Beeching, 1995).
Aggressive interactions were noted among the groups of large fish whereas no
instances of aggression were noted among the groups of small fish. The lack of
aggression among smaller oscar is supportive of their known schooling
behaviour prior to reproductive maturity
(Santos et al., 1984). Among
large fish, although activity was seen to decrease with falling oxygen
tensions the level of aggression remained constant. Additionally, the activity
of each individual fish in relation to its group members was not affected by
hypoxia, suggesting that group social structure remained intact. Hypoxia is
known to decrease stability of dominance hierarchies in stickleback
Gasterosteus aculeatus (Sneddon
and Yerbury, 2004) and decrease the duration of aggressive
encounters in the shore crab Carcinus maenas
(Sneddon et al., 1999).
However, in large oscars, although a general decline in activity would have
allowed a reduction in metabolic activity, aggression and defence seemed to be
behaviours worthy of persistence, at least down to 40 mmHg.
In conclusion, unlike many other species, the oscar shows a positive
relationship between physiological tolerance to hypoxia and size, with large
oscars withstanding the effects of falling PO2
better than smaller oscar, supported by a greater anaerobic potential to allow
prolonged survival in extreme hypoxia. Contrary to physiological predictions,
small oscars chose to remain in hypoxic waters to lower oxygen tensions than
large oscars affording the former a reduction in susceptibility to potential
predators. We have clearly demonstrated in the present study the need to
consider both the behavioural and physiological response of these fish to
hypoxia to fully understand their mechanisms of adaptation. Little is known
about the distribution of these fish within their Amazonian habitat, although
some preliminary data suggests that large and small oscar may occupy different
areas of the water column (Junk et al.,
1983) with juveniles tending to associate with floating plants
(Botero, 2000). Oscar live
mostly in Amazon lakes and at the margins of rivers, with a strong preference
for lentic environments (Santos et al.,
1984). Oxygen gradients are known to develop, particularly at
night, between hypoxic flooded areas and the normoxic main river, which are
likely to influence distribution of oscars. Kramer et al.
(Kramer et al., 1978)
highlight the amazing diversity of aquatic habitats within the Amazonian
rainforest, from `strongly flowing rivers' to `stagnant puddles', and future
work should now strive to take our knowledge of the behavioural and
physiological responses of oscars into the field to understand how they are
executed within an ecological context.
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Acknowledgments |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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