|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online January 8, 2007
Journal of Experimental Biology 210, 290-298 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02641
The energetic consequence of specific dynamic action in southern bluefin tuna Thunnus maccoyii
1 University of Adelaide, Adelaide, 5005, Australia
2 Aquafin CRC, Henley Beach, South Australia, 5022, Australia
3 Tuna Boat Owners Association of South Australia, Port Lincoln, 5606,
Australia
4 South Australian Research and Development Institute, Adelaide, 5022,
Australia
* Author for correspondence (e-mail: quinn.fitzgibbon{at}adelaide.edu.au)
Accepted 8 November 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
O2) of four
groups of three southern bluefin tuna Thunnus maccoyii (SBT) was
examined in a large static respirometer at water temperatures of
18.2-20.3°C. Six feeding events of rations between 2.1-8.5% body mass
(%Mb) of Australian sardines (Sardinops
neopilchardus) were recorded (two of the groups were fed twice). Before
feeding, fish swam between 0.71 and 1.4 body lengths s-1
(BL s-1) and the routine metabolic rate (RMR) was
366±32.5 mg kg-1 h-1 (mean ± s.e.m.). For
all trials, O2
was elevated post feeding, presumably as a result of specific dynamic action
(SDA). Swimming velocity was also elevated post feeding for periods similar to
that of O2
(between 20-45 h, longest for the largest rations). Post feeding swimming
velocity increased to between 0.87-2.6 BL s-1 and was also
dependent on ration consumed. It is suggested that the purpose of increased
post-feeding swimming velocity was to increase ventilation volume as a
response to the enhanced metabolic demand associated with SDA. Peak
post-prandial O2
increased linearly with ration size to a maximum of 1290 mg kg-1
h-1, corresponding to 2.8 times the RMR. When converted to its
energy equivalent, total magnitude of SDA was linearly correlated with ration
size to a maximum of 192 kJ kg-1 h-1, and as a
proportion of gross energy ingested (SDA coefficient), it averaged
35±2.2%. These results demonstrate that, although the factorial
increase of SDA in SBT is similar to that of other fish species, the absolute
energetic cost of SDA is much higher. These results support the contention
that tuna are energy speculators, gambling high rates of energy expenditure
for potentially higher rates of energy returns. The ration that southern
bluefin tuna require to equal the combined metabolic costs of SDA and RMR is
estimated in this study to be 3.5%Mb of Australian
sardines per day.
Key words: tuna, specific dynamic action, heat increment of feeding, oxygen consumption, energetics, Southern bluefin tuna, Thunnus maccoyii
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Bushnell and Jones, 1994;
Graham and Dickson, 2004). Of
particular interest are adaptations in the areas of metabolism and energetics.
Tunas are known to have standard metabolic rates (SMR, the rate when
theoretically at complete rest) and metabolic scopes that greatly exceed those
of most other well studied fish species
(Korsmeyer and Dewar, 2001).
These elevated metabolic states allow tuna to achieve physiological feats,
including rapid digestion and quick recovery from oxygen debt, that enable
them to take advantage of the ocean's patchy prey distribution. However, this
metabolic amplification comes at an energetic cost, which has led some authors
to describe tuna as `energy speculators', animals that gamble high rates of
energy expenditure on potential higher rates of energy return
(Brill, 1987;
Korsmeyer et al., 1996).
Our understanding of tuna energetics lags far behind that of smaller
species such as salmonids. Tuna's size and difficulty of handling has meant
only a small number of metabolic measurements have been possible. The majority
of research on tuna metabolism has focused on evaluation of the SMR or
quantification of swimming costs (Brill,
1979; Brill, 1987;
Dewar and Graham, 1994;
Gooding et al., 1981;
Graham and Laurs, 1982;
Graham et al., 1989;
Sepulveda and Dickson, 2000).
The metabolic cost of specific dynamic action (SDA) has yet to be examined in
any tuna species.
Specific dynamic action (often referred to as apparent specific dynamic
action, calorigenic effect or heat increment of feeding) refers to the total
energy cost involved with ingestion, digestion, absorption and assimilation of
a meal. In fish, SDA is a substantial component of total bioenergetics,
representing between 5 and 20% of gross ingested energy
(Beamish, 1974;
Carter and Brafield, 1992;
Chakraborty et al., 1992;
Fu et al., 2005c;
Muir and Niimi, 1972;
Peck et al., 2002). However
none of these studies have examined marine pelagic fish. Specific dynamic
action has been hypothesized to be a significant component of metabolism of
tuna, because of their high rates of food consumption and digestion
(Korsmeyer and Dewar, 2001).
Furthermore, it is hypothesized that rapidly growing fish, such as tuna,
should show the greatest post-prandial increase in metabolic rate
(Brill, 1996;
Jobling, 1981). This theory is
based on the consensus that a large proportion of the energetic cost of SDA is
related to metabolic work responsible for growth, i.e. protein synthesis and
turnover (Brown and Cameron,
1991a; Brown and Cameron,
1991b; Jobling,
1981; Lyndon et al.,
1992).
This study uses a large, sea-based, metabolic chamber to overcome some of
the logistical difficulties with working with large, pelagic fish
(Fitzgibbon et al., 2006). The
spacious, low-stress environment of this respirometer supports voluntary
feeding, allowing this study to make the first recording of SDA of a tuna
species, southern bluefin tuna Thunnus maccoyii (SBT), ingesting
Australian sardine Sardinops neopilchardus, an important food
component in the diets of both wild and aquaculture SBT.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). Fish were fed Australian sardine Sardinops
neopilchardus (Table 1)
and allowed 2 months to recover from the tow and transfer, and to become
accustomed to the sea-cage environment.
|
Mesocosm respirometer
The mesocosm respirometer was a large, flexible, plastic cylinder, 12
mx2.5 m (diameter x depth) manufactured predominantly from
polypropylene (Stevens Geomembranes R-PP 45, Holyoke, MA, USA; 1.14 mm thick
and reinforced with polyester), thermal bonded by Fabtech SA Pty. Ltd.
(Adelaide, Australia) (Fig.
1A). Further to the basic cylinder, the mesocosm had a wave break
wall that extended 1 m above water level and a sock-like access port (2 m
diameter, 2 m high) positioned in the roof
(Fig. 1B). Access into the
mesocosm was only possible through this access port, which could be pinched
shut to completely seal the system. Five 1 m diameter clear polyvinyl chloride
(0.75 mm) windows allowed entry of natural light, and capped polythene tank
fittings allowed sealable access for experimental equipment and manual
sampling. Once deployed into a 12 m diameter sea cage the mesocosm was pump
filled with seawater. Initially, it was filled to capacity (approximately 400
000 l) to reduce the likelihood of confinement stress; however, in subsequent
experiments, water volume was reduced to 350 000 l as the initial volume was
found to be slightly in excess of what was required to maximize available
space within the respirometer.
|
) or,
in the case of fish being hook-shy, by crowding the fish in a net and a
skin-diver securing them by hand and passing them across the soft, wet,
slipway into the respirometer. After introduction, any air bubbles that had
collected on the internal surface (from scuba-diver expiration or oxygen
injection) were rolled out of the access port, before the mesocosm was sealed.
Oxygen consumption rates
(O2) were
determined by measuring the drop in mesocosm internal dissolved oxygen (DO)
level over time. Mesocosm mixing was monitored by manual recordings of DO at
the beginning and end of each experimental trial through screw cap access
ports in the ceiling at nine positions within the respirometer (3, 6 and 9 m
from the port access side and at three depths: 0.25, 1.25 and 2.25 m).
Coefficient of variation between manual DO recordings from the nine sample
positions did not exceed 2.6% for any trial, indicating that the mesocosm
remained well mixed at all times.
Background respiration and photosynthesis of planktonic organisms in the
water column and on the respirometer surface was measured in trials
immediately before and after each experiment. Background respiration was
generally found be small; however, it was dependent on time of day
(respiration rate would flatten during the day due to photosynthesis). All
O2 recordings
were adjusted for background respiration according to the pertinent time of
day. The oxygen holding capabilities of the mesocosm was found to be
excellent, with a further two trials conducted to measure the rate of oxygen
diffusion through the respirometer material. For these trials, the
respirometer DO was reduced to either 1.90 or 2.26 mg l-1 by
injecting microbubbles of pure nitrogen with a gas diffuser (Aqua &
Co® Force 7, BOC Gases, NSW, Australia) and then removing the collected
bubbles before the mesocosm was sealed and oxygen monitored for more than 20
h. Subsequent oxygen diffusion across the respirometer wall was found to be
very low, representing an oxygen gradient of just 0.0042 mg-1
h-1 per mg l-1 DO between the respirometer and the
external environment. This rate of diffusion was nevertheless used to adjust
all trial DO recordings according to the pertinent oxygen gradient. Dissolved
ammonia concentrations were also monitored by daily analyses of water samples
before, during and after each trial, and they never exceeded 0.6 mg
l-1.
Experimental protocol
The mesocosm was installed into the marine farm pontoon for 49 days between
March and May 2005, when four trials were conducted. For each trial, three
fish (10±0.4 kg, mean ± s.e.m.;
Table 2) were transferred from
the holding sea-cage into the respirometer in the late afternoon. The fish
were left overnight to become accustomed to the respirometer environment. To
verify whether this time was sufficient for acclimation,
O2 was recorded
during the acclimation period for one trial. In this trial,
O2 was elevated
immediately after introduction, but had plateaued within 7 h and remained
steady for the subsequent 18 h (Fig.
2). This indicates that overnight was a sufficient period for
acclimation.
|
|
Measurement of the routine metabolic rate (RMR) was begun the morning
following introduction. The respirometer was sealed and
O2 was monitored
for 16-24 h. Routine metabolic rate was calculated as the mean,
post-acclimation
O2 over this
period (Fig. 2).
The following morning the mesocosm was re-opened and dissolved oxygen
returned to approximately 100% saturation by pure oxygen injected with the
diffuser. The fish were then left for roughly 1 h to recover from this
disturbance before they were offered Australian sardines through the entrance
port. All tuna consumed sardines during all attempts at feeding within the
respirometer. Attempts were made to differentiate rations consumed by
individual fish from both the surface and by a diver observing from within the
mesocosm. However these attempts proved largely unsuccessful as it was not
always possible to differentiate individual fish from the surface and fish
would often fail to ingest in the presence of a diver. After feeding, a diver
collected any uneaten sardines, and this mass was subtracted from the known
mass of bait offered to establish total consumption. Following feeding, the
respirometer was sealed and
O2 monitored for
the subsequent 40 h or more (except for one trial when logging failed after 26
h).
Dissolved oxygen and water temperature measurement
Two Hach® Luminescent Dissolved Oxygen (LDOTM) meters (HQ10;
Loveland, CO, USA) permanently installed at a depth of 1 and 2 m,
respectively, both 3 m from the wall, logged mesocosm DO and water
temperature. Meters were calibrated according to the manufacturer's
instructions at the start of the trials and calibration checked following the
completion of all trials. Meters recorded DO (to 0.01 mg l-1
resolution) that was automatically compensated for water temperature and
salinity set at 35%thou. Oxygen meters were set to log DO every 5 or 15 min,
depending on the trial-logging interval required (24 or 48 h, respectively).
All DO recordings were broken up into 3 h blocks according to time of day
(starting at midnight) and linear regressions were fitted to the change in DO
(mg l-1) representative for that 3 h period. The drop in mesocosm
DO was approx. 0.04 mg l-1 h-1 during RMR measurement
and as great as 0.12 mg l-1 h-1 during SDA measurement.
The high-resolution stability of these luminescent meters meant that the
linear regression coefficient of determination generally remained between
R2=0.96-0.99 over each 3 h period.
O2 calculations
were adjusted for the mean background respiration rate (mean of pre-and
post-SDA trial background recording) recorded for the respective time of day
(3 h block) and oxygen diffusion through the respirometer walls. A similar DO
meter was used to make daily recording of the DO in the external environment,
which remained between 7.1 and 7.4 mg l-1.
|
Video recordings were viewed in the VirtualDub video editing program (1.5.10, Avery Lee). Suitable records were defined as those containing a fish that was swimming perpendicularly to the camera and at least one frame in which body length (BL) could be measured for scaling. This sequence was imported into Video Point® software (Version 2.5, Lenox SoftworksTM) where swimming velocity was analysed by tracking movement across the field. Tuna BL was used to calibrate the image scale, accounting for variable distances between the fish and the camera. Any camera movement was corrected for by referring to a stable point within the respirometer on a frame-by-frame basis.
Data analysis
Swimming velocity data were collated within the same 3 h time periods as
DO. For each 3 h period, 4-7 video footage segments were analysed for swimming
velocity and the mean taken as representative for that period (a total of 448
footage segments were analysed). Due to poor quality footage, four suitable
footage segments were not available for some 3 hperiods. Video records after
24 h in trial 6 were lost due to video failure.
Mean swimming velocity recordings made during the RMR measurement are
subsequently referred to as the routine swimming velocity
(Ur) and velocity measurements made post feeding as the
specific dynamic action swimming velocity (Usda).
Usda duration is the time that post-feeding swimming
velocity remained one standard error (s.e.) above Ur. The
effect of meal size on metabolic rate was quantified by the following
parameters: SDA peak (maximum post-prandial
O2), SDA
factorial scope (SDA peak divided by RMR), SDA duration (duration that
post-prandial O2
remained greater than 1 s.e. above the RMR), SDA magnitude (total oxygen
consumed above the RMR within the SDA duration period) and SDA coefficient
(SDA magnitude as a percentage of gross ingested energy). Conversion from
oxygen consumed to the energy equivalent was calculated assuming 14.32 J
energy expended per mg O2 consumed
(Beamish and Trippel,
1990).
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). The
discrepancy is likely due to individual variability in voluntary swimming
speeds and the longer acclimation period used in the present study (16+ h
versus 6 h). Six feeding events of rations between 2.1 and 8.5%Mb Australian sardines were recorded (two of the experimental groups were fed twice, the other two experimental groups fed only once) (Table 2). On all occasions, swimming velocity increased post feeding. The duration before swimming velocity returned to pre-feeding levels (Ur) appeared to increase with ration size, from 20 h for the smallest ration to longer than the 45 h measurement period for the greatest two rations. Increase in swimming velocity recorded during the SDA period (Usda) was linearly related to ration size (R2=0.53) (Fig. 3B).
In all trials,
O2 was elevated
above the RMR post-feeding; however, the nature of this elevation was highly
dependent on ration size and experiment
(Fig. 4). Maximum post-prandial
O2 (SDA peak)
increased linearly with ration size (R2=0.71)
(Fig. 5A). At the greatest
ration consumed (8.5%Mb), SDA peak was 1 290 mg
kg-1 h-1, corresponding to 2.8x RMR, whilst with
the smallest ration (2.2%Mb), SDA peak was 469 mg
kg-1 h-1, or just 1.3x RMR
(Table 2). The duration of SDA
ranged between 23 and 45 h and was poorly correlated with ration size
(R2=0.38) (Fig.
5B). At the four lowest rations, SDA duration did not appear to be
affected by ration size; however, above a ration of 6%Mb,
SDA duration was greatly elevated. The magnitude of SDA ranged between 30.7
and 191 kJ kg-1 (Table
2) and was strongly linearly correlated with ration size
(R2=0.98) (Fig.
5C). SDA coefficient averaged 35±2.2% (N=6)
(Table 2).
|
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
O2 after feeding
before gradually falling back to the resting level
(Jobling, 1981). The pattern
of SDA response appears to be no different for SBT. The factorial scope and
duration of SDA is comparable to those of many fish species examined
(Chakraborty et al., 1992;
Fu et al., 2005a;
Fu et al., 2005b;
Hunt von Herbing and White,
2002; Jobling,
1981; Lyndon et al.,
1992; Peck et al.,
2002). Also like most fish species, peak, duration and magnitude
of SDA appear to be directly related to ration size
(Carter and Brafield, 1992;
Chakraborty et al., 1992;
Fu et al., 2006;
Fu et al., 2005c;
Jobling and Davis, 1980;
Muir and Niimi, 1972).
However, the energetic cost of SDA is approximately double (SDA
coefficient=35%) that recorded in other teleost species (generally between 5
and 20%). It appears that although the factorial pattern (peak and duration)
of SDA of SBT is consistent with other fish, the absolute metabolic cost of
SDA is much higher.
High metabolic cost of SDA
A complete understanding of the physiological basis of SDA remains unclear;
however, much of its effect is attributed to the metabolic cost of growth.
That is, the post-prandial influx of amino acids stimulates rapid synthesis
and turnover of tissue proteins resulting in much of the increase in metabolic
rate known as SDA (Brown and Cameron,
1991a; Brown and Cameron,
1991b; Jobling,
1981; Lyndon et al.,
1992). In fish, both protein synthesis and degradation rates have
been shown to rise linearly with growth rate
(Houlihan et al., 1988), and
therefore are likely to contribute more to the metabolic cost of SDA in fast
growing species. The growth rates of tuna, like other large pelagic fishes,
are known to be high (Brill,
1996; Glencross et al.,
2002; Sainsbury et al.,
1997; Uchiyama and Struhsaker,
1980). Furthermore, the SBT examined in the present study,
although large in comparison to typical specimens examined, were in fact
juveniles (Collette and Nauen,
1983; Schaefer,
2001). Juvenile fish have been shown to divert a proportionately
high amount of available metabolic scope to support SDA to meet the demands of
their fast growth rates (Hunt von Herbing
and White, 2002). Evidence to support that SDA is mostly a
post-absorptive effect is the probable discrepancy between SDA duration and
food gut passage time. The recorded duration of SDA (25-45 h) is far greater
than the likely gut evacuation time, which in tuna has been shown to be
greatly accelerated (
10-12 h)
(Magnuson, 1969;
Olson and Boggs, 1986). This
suggests that high protein turnover and synthesis rates associated with fast
growth rates of juvenile SBT are likely to elevate the metabolic cost of SDA.
Unfortunately, there is no information on the cost of SDA in other fast
growing pelagic fishes for comparison.
It is possible that the poor low energy value of the Australian sardines
ingested may have contributed to the high SDA coefficient recorded. The
nutritional balance of the diet can affect SDA, particularly the protein level
and its balance with non-protein energy sources. Deamination of ingested amino
acids is considered to be a significant proportion of SDA in carnivorous fish
(Beamish and Trippel, 1990;
Cho and Kaushik, 1990). Diets
with excess amounts of protein or insufficient non-protein energy sources
(i.e. fat or digestible carbohydrates) can elevate the energy expenditure of
SDA as a result of increased deamination of amino acids
(Beamish and Trippel, 1990;
Chakraborty et al., 1992;
Jobling and Davis, 1980;
LeGrow and Beamish, 1986;
Peres and Oliva-Teles, 2001).
When represented in terms of the digestible protein (P, g) and digestible
energy (E, mJ), the P:E ratio of the Australian sardines fed in the present
study (34 g mJ-1, assuming 90% and 85% digestible energy and
protein, respectively) is considerably greater than that of diets thought to
be optimal in aquaculture of salmonid species (P:E=20 g mJ-1)
(Cho and Kaushik, 1990). It is
likely that this extreme protein to energy ratio would have resulted in high
levels of amino acid deamination contributing the high SDA coefficient
recorded in the present study. However, this nutritional profile is typical
for Australian sardines caught in Southern Australian waters
(Ellis and Rough, 2005) and as
the Australian sardine is an important wild-fish food source
(Kemps et al., 1999), this
high SDA is biologically relevant.
Elevated energy expenditure associated with post-prandial visceral warming
may also contribute to SDA. Like other bluefin tuna, SBT elevate their
visceral temperature which is characterized by the rapid increase following
feeding, before slowly cooling to a basal temperature of 2°C above ambient
water temperature up to 60 h post feeding
(Gunn et al., 2001). The
primary purpose of visceral warming is thought to be to accelerate digestion
(Stevens and McLeese, 1984).
The source of heat is hypothesized to be a result of aerobic metabolism
associated with SDA, which is retained by counter-current exchange in retia
mirabilia that thermally isolate the stomach, caecum, intestines and spleen
(Carey et al., 1984). The
liver, however, is on the cold side of the rete and thus does not contribute
to visceral warming. This is surprising, as the liver is considered to have
the highest rates of protein synthesis of teleost tissues
(Carter and Houlihan, 2001)
and thus would be an obvious source of SDA-associated heat production. Protein
synthesis rates in the livers of juvenile Atlantic cod have been shown to
increase rapidly after feeding, and after 6 h theyaccount for 31% of whole
body protein synthesis compared to just 9% for the stomach
(Lyndon et al., 1992). This
suggests that only a small fraction of SDA contributes to visceral warming
(related to gastrointestinal work and absorption), leaving potential for the
involvement of another mechanism. Gunn et al. provided support for this
(Gunn et al., 2001) by finding
that, for a given ration, the magnitude of SBT visceral warming was much
greater in winter than in summer. They suggested that SBT possess a
compensatory acclimation mechanism to provide increased digestive efficiency
at low ambient temperatures, possibly facilitated by increased aerobic
metabolism and/or the heat conservation (through changes in the activity of
the visceral rete). Thus, it appears that visceral warming may not simply be
the accumulation of heat by-product of SDA, but may be an energy-consuming
mechanism to maintain optimal digestive rates.
The observed increase in swimming velocity after feeding would have
contributed to the measured metabolic cost of SDA. Fish on average swam 1.7
times faster after feeding (1.6 compared to 0.92 BL s-1).
Based on the relationship between
O2 and swimming
velocity described for 2.2 kg yellowfin tuna Thunnus albacares
(Dewar and Graham, 1994), an
increase in swimming velocity from 0.92 to 1.6 BL s-1
would increase metabolic rate from 409 to 585 mg kg-1
h-1. A potential explanation for faster swimming is to increase
ventilation volume as a response to the enhanced metabolic demand associated
with SDA. This theory is supported by the fact that the fish that consumed the
most also swam the fastest (Fig.
3B), and for most of the feeds examined, the duration of elevated
swimming velocity post feeding (Usda duration) is similar
to the duration of SDA. However, the pattern of post-feeding swimming velocity
was more difficult to distinguish than that of SDA, as for the two greatest
rations it failed to return to pre-feeding levels. At present the reason for
this discrepancy between swimming velocity and SDA is unknown; however, it may
be due to measurement error caused by individual variation in swimming speed
due to unequal ration consumption, or diurnal swimming cycles (fish appeared
to swim faster at dusk and dawn). More intensive examination of the effects of
feeding on the effect of individual tuna swimming velocity over longer
experimental period is required to verify the metabolic cost of faster
post-prandial swimming.
SDA and metabolic scope
Consistent with some fish species, SBT peak post-prandial
O2 increased
with ration size (Chakraborty et al.,
1992; Muir and Niimi,
1972); however for other species, SDA peak reaches a maximum and
plateaus with increased ingestion (Beamish,
1974; Fu et al.,
2005c). In the latter, SDA peak has a species-specific maximum
that limits the proportion of available metabolic scope devoted to SDA and
allows other metabolic activities to occur simultaneously
(Beamish, 1974). It is possible
that SBT reach this plateau at a ration size greater than that examined in the
present study (8.50%Mb). However, this appears to be
unlikely as anecdotal evidence from tuna farm managers indicates that
8.5%Mb is close to the maximum feed intake that SBT accept
in a single meal. According to cardiorespiratory models, the factorial scope
of skipjack (Katsuwonus pelamis) and yellowfin tuna is approximately
8-9 times the SMR (Brill and Bushnell,
1991; Korsmeyer and Dewar,
2001). If a similar factorial scope of 7 times the RMR is assumed
for SBT (less than that predicted above as the comparison is based on a low
RMR not the SMR), it corresponds to 2560 mg kg-1 h-1,
which is similar to the maximum-recorded
O2 of a tuna
species, 2500 mg kg-1 h-1
(Gooding et al., 1981). The
maximum recorded post-prandial metabolic rate (1300 mg kg-1
h-1) is approximately 50% of this predicted metabolic scope,
suggesting that even during the peak of SDA at the greatest ration recorded,
the SBT examined would still have had considerable metabolic scope available
to perform other tasks (i.e. oxygen debt recovery and locomotory costs beyond
the requirement for hydrostatic equilibrium and ventilation). This supports
the theory that the main benefit of high aerobic scope in tunas is to
simultaneously support multiple metabolic functions needed to sustain their
high performance requirements (Brill and
Bushnell, 1991; Korsmeyer et
al., 1996).
Energetic consequence of a high metabolic cost of SDA
To estimate minimum daily energetic cost of feeding SBT, we have plotted
the total energy expenditure as a percentage of ingested energy for the six
feeding trials (calculated as the total oxygen consumption the 24 h post
feeding) (Fig. 6). The
break-even point (feed ration at which energy expenditure was equal to
ingested energy) is approximately a ration of 3.5%Mb
day-1. However, if SBT are ultimately to grow and reproduce, their
minimum daily ration of Australian sardines needs to be greater than this, as
some ingested energy is indigestible and further energy is lost in the form of
urine, gill excretion and surface losses. Furthermore, the calculated
energetic cost is likely to be a minimum, as activity was restricted. With
wild fish, the cost of activity is likely to be much greater due to the
activity requirement of predation and competition.
|
;
Korsmeyer et al., 1996). These
show that tuna are `energy speculators', gambling high rates of energy
expenditure for potentially higher rates of energy returns. The work presented
here agrees with this conclusion; however, it shows that one aspect of tuna
energetics, the metabolic costs of SDA, may have been considerably
underestimated. Previous models have estimated the cost of SDA to be only 15%
of the ingested energy (Kitchell et al.,
1978; Korsmeyer et al.,
1996). For SBT consuming the predominant natural food source in
Australia's southern oceans, 35% of the ingested energy is lost in the SDA
process. This finding further exemplifies the risk that tuna take in balancing
performance with efficiency and highlights the importance of oceanic prey
species communities to these valuable fish.
List of abbreviations
O2
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Beamish, F. W. H. (1974). Apparent specific dynamic action of largemouth bass, Micropterus salmoides. J. Fish. Res. Board Can. 31,1763 -1769.
Beamish, F. W. H. and Trippel, E. A. (1990). Heat increment: a static or dynamic dimension in bioenergetic models. Trans. Am. Fish. Soc. 119,649 -661.[CrossRef]
Brill, R. W. (1979). The effect of body size on the standard metabolic rate of skipjack tuna, Katsuwonus pelamis.Fish. Bull. 77,494 -498.
Brill, R. W. (1987). On the standard metabolic rates of tropical tunas, including the effect of body size and acute temperature change. Fish. Bull. 85, 25-35.
Brill, R. W. (1996). Selective advantages conferred by the high performance physiology of tunas, billfish, and dolphin fish. Comp. Biochem. Physiol. 113A, 3-15.[CrossRef][Medline]
Brill, R. W. and Bushnell, P. G. (1991). Metabolic and cardiac scope of high energy demand teleost, the tunas. Can. J. Zool. 69,2002 -2009.
Brown, C. R. and Cameron, J. N. (1991a). The induction of specific dynamic action in channel catfish by infusion of essential amino acids. Physiol. Zool. 64,276 -297.
Brown, C. R. and Cameron, J. N. (1991b). The relationship between specific dynamic action (SDA) and protein synthesis rates in the channel catfish. Physiol. Zool. 64,298 -309.
Bushnell, P. G. and Jones, D. R. (1994). Cardiovascular and respiratory physiology of tuna: adaptations for support of exceptionally high metabolic rates. Environ. Biol. Fishes 40,303 -318.[CrossRef]
Carey, F. G., Teal, J. M. and Stevens, E. D.
(1984). Bluefin tuna warm their viscera during digestion.
J. Exp. Biol. 109,1
-20.
Carter, C. G. and Brafield, A. E. (1992). The relationship between specific dynamic action and growth in grass carp, Ctenopharyngodon idella (Val.). J. Fish Biol. 40,895 -907.[CrossRef]
Carter, C. G. and Houlihan, D. F. (2001). Protein synthesis. In Fish Physiology, Nitrogen Excretion. Vol. 20 (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 31-75. San Diego: Academic Press.[CrossRef]
Chakraborty, S. C., Ross, L. G. and Ross, B. (1992). Specific dynamic action and feeding metabolism in common carp, Cyprinus carpio L. Comp. Biochem. Physiol. 103A,809 -815.[CrossRef]
Cho, C. Y. and Kaushik, S. J. (1990). Nutritional energetics in fish: energy and protein utilization in rainbow trout (Salmo gairdneri). World Rev. Nutr. Diet. 61,132 -172.[Medline]
Collette, B. B. and Nauen, C. E. (1983). FAO Species Catalogue. Vol. 2, Scombrids of the World. An Annotated and Illustrated Catalogue of Tunas, Mackerels, Bonitos and Related Species Known to Date. (FAO Fisheries Synopsis 125). Rome: Food and Agriculture Organization of the United Nations.
Dewar, H. and Graham, J. B. (1994). Studies of tropical tuna swimming performance in a large water tunnel. I. Energetics. J. Exp. Biol. 192,13 -31.[Abstract]
Ellis, D. and Rough, K. (2005). Quality and Nutritional Evaluation of Baitfish used for SBT Farming (including baitfish profiles). Adelaide: Aquafin CRC.
Fitzgibbon, Q. P., Baudinette, R. V., Musgrove, R. J. and Seymour, R. S. (2006). Routine metabolic rate of southern bluefin tuna (Thunnus maccoyii). Comp. Biochem. Physiol. A doi: 10.1016/j.cbpa.2006.08.046.
Fu, S. J., Xie, X. J. and Cao, Z. D. (2005a). Effect of dietary composition on specific dynamic action in southern catfish Silurus meridionalis Chen. Aquacult. Res. 36,1384 -1390.[CrossRef]
Fu, S. J., Xie, X. J. and Cao, Z. D. (2005b). Effect of feeding level and feeding frequency on specific dynamic action in Silurus meridionalis. J. Fish Biol. 67,171 -181.[CrossRef]
Fu, S. J., Xie, X. J. and Cao, Z. D. (2005c). Effect of meal size on postprandial metabolic response in southern catfish (Silurus meridionalis). Comp. Biochem. Physiol. 140A,445 -451.[CrossRef][Medline]
Fu, S. J., Cao, Z. D. and Peng, J. L. (2006). Effect of meal size on postprandial metabolic response in Chinese catfish (Silurus asotus Linnaeus). J. Comp. Physiol. B 176,489 -495.[CrossRef][Medline]
Glencross, B. D., Clarke, S., Buchanan, J., Carter, C. G. and Van Bareveld, R. J. (2002). Temporal growth patterns of farmed juvenile southern bluefin tuna, Thunnus maccoyii (Castelnau) fed moist pellets. J. World Aquacult. Soc. 33,138 -145.
Gooding, R. M., Neill, W. H. and Dizon, A. E. (1981). Respiration rates and low-oxygen tolerance limits in skipjack tuna, Katsuwonus pelamis. Fish. Bull. 79, 31-48.
Graham, J. B. and Dickson, K. A. (2004). Tuna
comparative physiology. J. Exp. Biol.
207,4015
-4025.
Graham, J. B. and Laurs, R. M. (1982). Metabolic rate of the albacore tuna Thunnus alalunga. Mar. Biol. 72,1 -6.[CrossRef]
Graham, J. B., Lowell, W. R., Lai, N. C. and Laurs, R. M. (1989). O2 tension, swimming-velocity, and thermal effects on the metabolic rate of the Pacific albacore Thunnus alalunga.Exp. Biol. 48,89 -94.[Medline]
Gunn, J., Hartog, J. and Rough, K. (2001). The relationship between food intake and visceral warming in southern bluefin tuna (Thunnus maccoyii). In Electronic Tagging and Tracking in Marine Fisheries. Vol. 1 (ed. J. R. Sibert and J. L. Nielsen), pp. 109-130. Dordrecht: Kluwer Academic Publishers.
Houlihan, D. F., Hall, S. J., Gray, C. A. and Noble, B. S. (1988). Growth rates and protein turnover in Atlantic cod, Gadus morhua. Can. J. Fish. Aquat. Sci. 45,951 -964.
Hunt von Herbing, I. and White, L. (2002). The effect of body mass and feeding on metabolic rate in small juvenile Atlantic cod. J. Fish Biol. 61,945 -958.
Jobling, M. (1981). The influences of feeding on the metabolic rate of fishes: a short review. J. Fish Biol. 18,385 -400.[CrossRef]
Jobling, M. and Davis, J. C. (1980). Effect of feeding on the metabolic rate, and the specific dynamic action in plaice, Pleuronectes platessa L. J. Fish Biol. 16,629 -638.[CrossRef]
Kemps, H. A., Totterdell, J. A., Nishida, T. and Gills, H. S. (1999). Preliminary Analysis on the Diet and Feeding Ecology of Juvenile Southern Bluefin Tuna, Thunnus maccoyii, in Relation to the Southern Coastal Waters of Western Australia. Hobart: CSIRO Marine Research.
Kitchell, J. F., Neill, W. H., Dizon, A. E. and Magnuson, J. J. (1978). Bioenergetic spectra of skipjack and yellowfin tunas. In The Physiological Ecology of Tunas (ed. G. D. Sharp and A. E. Dizon), pp. 357-368. New York: Academic Press.
Korsmeyer, K. E. and Dewar, H. (2001). Tuna metabolism and energetics. In Fish Physiology: Tuna Physiology, Ecology, and Evolution. Vol. 19 (ed. B. A. Block and E. D. Stevens), pp. 35-78. San Diego: Academic Press.[CrossRef]
Korsmeyer, K. E., Dewar, H., Lai, N. C. and Graham, J. B. (1996). The aerobic capacity of tunas: adaptation for multiple metabolic demands. Comp. Biochem. Physiol. 113A,17 -24.[CrossRef]
LeGrow, S. M. and Beamish, F. W. H. (1986). Influence of dietary protein and lipid on apparent heat increment of rainbow trout, Salmo gairdneri. Can. J. Fish. Aquat. Sci. 43, 19-25.
Lyndon, A. R., Houlihan, D. F. and Hall, S. J. (1992). The effect of short-term fasting and single meal on protein synthesis and oxygen consumption in cod, Gadus morhua.Comp. Biochem. Physiol. 162B,209 -215.[CrossRef]
Magnuson, J. J. (1969). Digestion and food consumption by skipjack tuna (Katsuwonus pelamis). Trans. Am. Fish. Soc. 98,379 -392.[CrossRef]
Muir, B. S. and Niimi, A. J. (1972). Oxygen consumption of euryhaline fish aholehole (Kuhlia sandvicensis) with reference to salinity, swimming, and food consumption. J. Fish. Res. Board Can. 29,67 -77.
Olson, R. J. and Boggs, C. H. (1986). Apex predation by yellowfin tuna (Thunnus albacares): independent estimates from gastric evacuation and stomach contents, bioenergetics, and cesium concentrations. Can. J. Fish. Aquat. Sci. 43,1760 -1775.
Peck, M. A., Buckley, L. J. and Bengtson, D. A. (2002). Energy losses due to routine and feeding metabolism in young-of-the-year juvenile Atlantic cod (Gadus morhua). Can. J. Fish. Aquat. Sci. 60,929 -937.[CrossRef]
Peres, H. and Oliva-Teles, A. (2001). Effect of dietary protein and lipid level on metabolic utilization of diets by European sea bass (Dicentrarchus labrax) juveniles. Fish Physiol. Biochem. 25,269 -275.[CrossRef]
Sainsbury, K., Polacheck, T., Klaer, N., Gunn, J., Campbell, R., Hearn, W., Davis, T., Betlehem, A., Preece, A. and Cowling, A. (1997). Recent Developments and Methods in Southern Bluefin Tuna Fishery Assessments. Hobart: CSIRO Division of Marine Report.
Schaefer, K. M. (2001). Reproductive biology of tunas. In Tuna Physiology, Ecology, and Evolution. Vol. 19 (ed. B. A. Block and E. Donald Stevens), pp.225 -270. San Diego: Academic Press.[CrossRef]
Sepulveda, C. and Dickson, K. A. (2000). Maximum sustainable speeds and cost of swimming in juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). J. Exp. Biol. 203,3089 -3101.[Abstract]
Stevens, E. D. and McLeese, J. M. (1984). Why bluefin tuna have warm tummies: temperature effect on trypsin and chymotripsin. Am. J. Physiol. 246,R487 -R494.
Suarez, N. D., Hidalgo, M. C., Garcia-Gallego, M., Sanz, A. and de la Higuera, M. (1995). Influence of the relative proportions of energy yielding nutrients on the liver intermediary metabolism of the European eel. Comp. Biochem. Physiol. 111A,421 -428.[CrossRef]
Uchiyama, J. H. and Struhsaker, P. (1980). Age and growth of skipjack tuna, Katsuwonus pelamis, and yellowfin tuna, Thunnus albacares, as indicated by daily growth increments of sagittae. Fish. Bull. 79,151 -162.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  K.J. Millidine, J.D. Armstrong, and N.B. Metcalfe Juvenile salmon with high standard metabolic rates have higher energy costs but can process meals faster Proc R Soc B, June 7, 2009; 276(1664): 2103 - 2108. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T.D Clark, B.D Taylor, R.S Seymour, D Ellis, J Buchanan, Q.P Fitzgibbon, and P.B Frappell Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna Proc R Soc B, December 22, 2008; 275(1653): 2841 - 2850. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Battam, M. A. Chappell, and W. A. Buttemer The effect of food temperature on postprandial metabolism in albatrosses J. Exp. Biol., April 1, 2008; 211(7): 1093 - 1101. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Blank, J. M. Morrissette, C. J. Farwell, M. Price, R. J. Schallert, and B. A. Block Temperature effects on metabolic rate of juvenile Pacific bluefin tuna Thunnus orientalis J. Exp. Biol., December 1, 2007; 210(23): 4254 - 4261. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Malte, C. Larsen, M. Musyl, and R. Brill Differential heating and cooling rates in bigeye tuna (Thunnus obesus Lowe): a model of non-steady state heat exchange J. Exp. Biol., August 1, 2007; 210(15): 2618 - 2626. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
