Tuna comparative physiology
1 Center for Marine Biotechnology and Biomedicine and Marine Biology
Research Division, Scripps Institution of Oceanography, University of
California, San Diego, La Jolla, CA 92093-0204, USA
2 Department of Biological Science, California State University Fullerton,
Fullerton, CA 92834-6850, USA
* Author for correspondence (e-mail: jgraham{at}ucsd.edu)
Accepted 28 August 2004
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Summary |
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Key words: fish, evolution, phylogeny, metabolism, thunniform locomotion, regional endothermy
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Introduction |
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Tuna evolution and radiation |
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Morphological evidence has been used to define tuna evolutionary
relationships (Fig. 1).
Molecular phylogenetic analyses based on different mitochondrial genes
(Finnerty and Block, 1995;
Chow and Kishino, 1995
;
Alvarado Bremer et al., 1997
)
have not yielded consistent results with respect to relationships among
closely related species but do support a long separation of the four derived
tuna genera into at least two clades: (1) Thunnus and (2)
Katsuwonus + Euthynnus + Auxis. This relationship
is also supported by some morphological evidence and by the fossil record
(Graham and Dickson, 2000
;
Collette et al., 2001
; K. A.
Monsch, personal communication; Fig.
2).
|
Extant tuna and bonito genera appear in the early Tertiary period [60
million years ago (mya); Carroll,
1988
; Monsch,
2000
; Fig. 2]. The
earliest tunas lived in the Tethys Sea, a large circumtropical waterway that
encircled Earth for about 50 million years [Mid-Cretaceous to the late
Oligocene (
25 mya)]. Tuna and bonito radiations were influenced by
tectonically induced changes in paleoceanography, including progressive
cooling [beginning in the Eocene (
50 mya)], development of the modern
ocean's thermohaline and gyre circulations, an accentuated vertical thermal
stratification, and greater high-latitude upwelling, which increased
productivity, expanded food webs and opened potential niches
(Dickson and Graham, 2004
).
Most physical and biological features of recent ocean ecosystems have been in
place since the Miocene (
20 mya;
Macdougall, 1996
;
Fordyce and Muizon, 2001
).
Swimming is fundamental to the natural history of most pelagic fishes,
including tunas. We suggest that changes in Tertiary oceanography, in
particular the appearance of more extensive ocean areas with high productivity
and diversified food webs, selected for tuna physiological adaptations that
enhanced locomotor performance, favored migratory behavior and thus
contributed to tuna radiation (Dickson and
Graham, 2004). Tunas acquired a unique swimming mode and a level
of integration between swimming and physiological performance not matched by
other teleosts. Each of the three specializations featured in this commentary
thunniform swimming, the capacity for regional endothermy and an
elevated aerobic capacity are rooted in continuous swimming and are
integral to expanded latitudinal and vertical habitat exploitation by
tunas.
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Tuna distribution |
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Fisheries' catch statistics, acoustic and archival tag data, and laboratory
studies of thermal and respiratory physiology identify factors affecting tuna
vertical distributions (Fig.
3). In the eastern tropical Pacific, Katsuwonus up to 4
kg mass occur throughout the upper 200 m but do not enter waters cooler than
18°C or having less than 3.5 ml O2 l-1 (64%
saturation at 18°C). With higher total O2 requirements, larger
skipjack are more spatially confined; 49 kg skipjack require water
cooler than 26°C (saturated O2
4.9 ml O2
l-1), while >9 kg skipjack remain below 22°C (
5.2 ml
O2 l-1) (Barkley et
al., 1978
).
|
Resource partitioning is suggested by the distributions of the tropical
Pacific yellowfin and bigeye. Yellowfin range from 50 to 350 m (15°C)
but are also limited by the 3.5 ml l-1 oxygen barrier. By contrast,
bigeye repeatedly dive from 100 m to deeper than 500 m (
7°C) and may
enter water with a lower oxygen content (1.0 ml O2 l-1;
18% saturation at 18°C) (Brill,
1994
; Schaefer and Fuller,
2002
). On the other hand, both yellowfin and bigeye will aggregate
under floating objects and remain at the surface for long periods
(Schaefer and Fuller,
2002
).
Acoustic telemetry and archival tags (recording microprocessors affixed to
the fish and recovered at capture) show that yellowfin and bigeye routinely
dive deeper than indicated by longline data, and this has dramatically altered
concepts about the importance of vertical niche expansion
(Holland and Sibert, 1994;
Brill and Bushnell, 2001
;
Lowe et al., 2000
). Schaefer
and Fuller (2002
) report that
bigeye occasionally dive to 1000 m (
3°C), and a recently recovered
tag indicates a maximum bigeye depth of 1839 m (
2.5°C) (K. M.
Schaefer, personal communication).
Deep-diving tunas appear to be foraging in the DSL. Stomach contents and
behavioral observations show that tunas do not exploit the DSL at night when
it is near the surface (Dragovich and
Potthoff, 1972; Kitagawa et
al., 2004
). However, as daylight approaches, yellowfin and bigeye
begin feeding on the DSL and pursue it to depth
(Fig. 4). Acoustic and archival
records show repeated (1015 day-1) foraging dives by bigeye;
these fish swam relatively fast [
2 fork lengths per second (FL
s-1; FL is body length from snout to caudal fork)] both up and down
and spent considerable time in 37°C water
(Holland and Sibert, 1994
;
Schaefer and Fuller, 2002
).
Atlantic northern bluefin at 1000 m are reportedly feeding on the DSL
(Gunn and Block, 2001
).
Observations by Kitagawa et al.
(2004
) indicate that young
Pacific bluefin do not dive this deep and opt for food near the surface when
available.
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Integrated tuna physiology |
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Thunniform swimming
Thunniform swimming is a lift-based propulsion mode characterized by
minimal lateral body undulation and the concentration of thrust production at
the rapidly oscillating, lunate caudal fin
(Altringham and Shadwick, 2001;
Katz et al., 2001
;
Syme and Shadwick, 2002
).
Among teleosts, only tunas use this swimming mode, and comparisons with other
scombrids show that (1) thunniform swimming is a derived tuna characteristic
resulting from modification of ancestral features including body and
caudal-fin shape, myotomal architecture, red muscle (RM) position, and its
connections with the skin and skeleton
(Graham and Dickson, 2000
;
Westneat and Wainwright, 2001
;
Dowis et al., 2003
) and (2)
the shift in RM position favored a reduction in its thermal conductance and
may have preceded or co-evolved with endothermy
(Graham and Dickson,
2000
).
Structural modifications for thunniform swimming include a more anterior
point of maximum body thickness and accentuation of posterior body tapering,
peduncular narrow-necking, development of the dense anterior corselet scale
layer, accentuation of grooves for paired and median fins and increases in
lateral keel area and caudal-fin aspect ratio
(Fig. 5A). These body shape
modifications increase streamlining and minimize anterior body undulation and
are accompanied by alterations in myotomal architecture that affect swimming
biomechanics and kinematics (Graham and
Dickson, 2000; Westneat and
Wainwright, 2001
). Tuna myotomes have longer cones, and the RM is
in the anterior-medial body position (Fig.
5B) unique to tunas and lamnid sharks
(Bernal et al., 2001
;
Westneat and Wainwright, 2001
;
Donley et al., 2004
). Regional
connections of tuna RM to the skin are reduced, supplanted by robust tendinous
connections within the horizontal septum and longer lateral tendons connecting
to the caudal fin (Figs 5,
6). The ratio of output motion
at the tail to input motion due to RM shortening (the velocity ratio) is
greater in tunas than in other scombrids
(Graham and Dickson, 2000
;
Westneat and Wainwright,
2001
). This is reflected in the higher tailbeat frequency and
reduced lateral displacement along the body in tunas relative to comparably
sized bonitos and mackerels swimming at similar speeds
(Donley and Dickson, 2000
;
Altringham and Shadwick, 2001
;
Dowis et al., 2003
;
Fig. 6B).
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Scombrid myotomal differences extend to RM activation and strain
development patterns. In both chub mackerel and bonito, with lateral-posterior
RM tightly connected to the overlying skin, shortening results in local body
bending. By contrast, activation of yellowfin and skipjack RM, with reduced
connection locally to skin, results in greater RM strain than predicted by the
bending beam theory (Shadwick et al.,
1999; Altringham and Shadwick,
2001
; Katz et al.,
2001
). This requires that RM contracts independently of the
fast-glycolytic white muscle (WM) within the same myotome, and this is
possible because RM and WM are separated by connective tissue sheets. This
separation was demonstrated with simultaneous sonomicrometry (SMC) and
electromyography (EMG), which indicated a higher RM shear and a greater extent
of shortening than would be possible if it were bound to WM
(Katz et al., 2001
;
Syme and Shadwick, 2002
).
Work-loop studies yielded maximum performance for yellowfin and skipjack RM
fibers when they were actuated using in vivo RM activation and strain
parameters. This result, together with the SMC findings and EMG data showing
sequential onset of RM activation down one side of the body and then the
simultaneous cessation of RM contraction at all positions, suggests that
during sustained swimming maximal RM power production along one side of a
tuna's body occurs at nearly the same instant
(Altringham and Shadwick, 2001
;
Katz et al., 2001
).
Although the reduced lateral displacement characteristic of thunniform
swimming should reduce drag, Korsmeyer and Dewar
(2001) note minimal evidence
that cost of transport is reduced for tunas relative to other species. In
fact, tunas have greater total metabolic swimming costs relative to bonitos
and mackerels (Sepulveda and Dickson,
2000
; Sepulveda et al.,
2003
). Further investigations of the biological advantage of
thunniform swimming are therefore needed.
Regional endothermy
The evolutionary and ecological significance of endothermy is the expanded
thermal niche it opens for tunas, whether in deep water, at high latitudes or
both (Block et al., 1993).
Counter-current vascular heat exchangers (retia mirabilia) conserve metabolic
heat, allowing the warming of RM, WM, viscera, brain and eyes above ambient
water temperature (Ta;
Carey et al., 1971
;
Graham and Dickson, 2001
).
Because of water's high heat capacity and the in-series circulation of fishes,
elevated temperatures could not be maintained without circulatory adaptations
to regulate both heat loss and gain (Dewar
et al., 1994
). Moreover, a tuna's capacity to maintain body
temperature (Tb) in the face of changing
Ta stabilizes muscular, metabolic, sensory and digestive
functions. A tuna that swims from near the surface to 1000 m benefits from the
thermal conservation of RM power production, of visual perception and of other
processes as it undergoes a
10°C Ta reduction and
severe light attenuation.
Elevation of tuna RM temperature combines the requirement to swim
continuously with the inefficiency of muscle in chemical-to-kinetic energy
conversion, providing a steady source of heat. Retia are essential for RM heat
conservation, but the anterior-medial RM position also favors heat retention.
The developmental processes affecting the differential development and growth
patterns of RM in tunas and other scombrids are unknown. Juvenile tuna form
their anterior-medial RM before the RM retia develop
(Graham and Dickson, 2001),
but comparative studies are needed to determine if this reflects selective
forces underlying thunniform swimming or endothermy.
RM retia are arrays of intimately positioned, oppositely flowing arterioles
and venules located adjacent to the muscle
(Carey et al., 1971;
Graham and Dickson, 2001
;
Fig. 7). Retial connections to
major arteries and veins show a phylogenetic trend for the elaboration of
lateral heat exchangers in more derived tunas; the pattern also suggests the
possible independent origin of lateral retia in the Thunnus and the
Katsuwonus + Euthynnus + Auxis clades (Figs
2,
7). In most fishes, including
most scombrids, the routing of myotomal blood is via the central
circulation [dorsal aorta (DA) and post cardinal vein (PCV)]. Tunas are an
exception. Allothunnus, the most basal tuna, has a small DA and
PCV-connected central rete within its expanded hemal arch. In addition to a
large central rete, Katsuwonus + Euthynnus + Auxis
perfuse RM via retia branching from the lateral arteries (branched
anteriorly from the DA) and veins (draining to the PCV or the duct of Cuvier);
Auxis and Euthynnus have only epaxial lateral vessels and
retia whereas Katsuwonus has both epaxial and hypaxial vessels and
retia (Fig. 7). Each of the
Thunnus (neothunnus) species has two expaxial and hypaxial
vessel pairs with retia, and three species [T. n. albacares, T. n.
atlanticus and T. n. tonggol] also have a small central rete
(absent in T. n. obesus). The four Thunnus
(thunnus) species have the four vessel-set lateral circulation each
with an extensive rete but lack a complete central circulation (reduced DA, no
PCV; Fig. 7). Both central rete
size and central circulation completeness are reflected in the interspecific
differences in hemal arch structure among the tunas
(Graham and Dickson,
2000
).
|
Recent works document tuna capacity to alter whole-body thermal conductance
to minimize or maximize rates of Tb change. Archival data
for Atlantic northern bluefin indicate that Tb is
conserved (2024°C) over a range of depths and
Ta (Gunn and Block,
2001). Acoustic telemetry records suggest that bigeye `bounce
dive' behavior allows heat gain in shallower, warmer water to lengthen forays
into deeper, cooler water where, despite heat conservation, RM (and other warm
regions) gradually cools (Holland and
Sibert, 1994
). At shallower depths, the bigeye is in thermal
equilibrium and has a TRM that is warmer than
Ta. After a time in deeper water it is cooler and as it
ascends and enters water warmer than its end-dive TRM,
heating occurs 1001000 times faster than diving heat loss. Although
increased RM work during upward swimming and a faster heart rate in warmer
water augment post-dive heating, a much higher heat gain rate suggests that
the ascending bigeye may bypass its lateral heat exchangers, allowing blood
warmed and oxygenated in the gills to enter RM directly via the DA
(no central rete in T. obesus). Dewar et al.
(1994
) quantified changes in
thermal conductance by rapidly imposing dive-depth equivalent
Ta changes on yellowfin swimming steadily in a large water
tunnel. Korsmeyer and Brill
(2002
) showed that blockade of
adrenergic vascular control with bretylium in yellowfin eliminates these
conductance changes.
Future studies need to detail the control of and structural bases for
blood-flow alteration through and around retia. Questions also persist about
visceral and cranial endothermy. Heat production during prey digestion,
absorption and assimilation is used to elevate tuna
Tviscera in the species of the subgenus Thunnus,
all of which have visceral retia to conserve this heat
(Carey et al., 1984;
Gunn and Block, 2001
). A warm
viscera would speed digestion and gut evacuation for the next feeding
opportunity because of the thermal enhancement of digestive enzyme activity,
as shown for Atlantic northern bluefin trypsin and chymotrypsin
(Stevens and McLeese,
1984
).
Some tunas are similar to billfish, lamnids and the butterfly kingfish
(Gasterochisma melampus; Fig.
1) in elevating their brain and eye (retinal or optic nerve)
temperatures (Korsmeyer and Brill,
2002; Dickson and Graham,
2004
). While the brain-heating mechanisms of billfishes are well
characterized (Block, 1991
),
the cranial heat source of tunas is unknown.
Metabolic scope and related specializations
SMR and aerobic scope
The high aerobic capacity of tunas is reflected in both standard and active
metabolic rates. Tuna SMR (i.e. metabolic rate at zero velocity, an index of
maintenance metabolic costs) is 23 times greater than that of other
scombrids (Korsmeyer and Dewar,
2001; Sepulveda et al.,
2003
). [As tunas never stop swimming, SMR is estimated by
extrapolating swimming velocitymetabolic rate regressions to zero
velocity or by direct measurement (stasis metabolism) in spinally blocked
tunas; Brill and Bushnell,
2001
.] However, the estimated costs of factors contributing to SMR
[i.e. endothermy and greater aerobic maintenance requirements for
osmoregulation, WM and organs (gills, heart) having a larger mass] total less
than the twofold SMR elevation, implying the importance of other factors.
Fishes with a high SMR often have a large aerobic scope
(Priede, 1985), which appears
true for tunas (Korsmeyer and Dewar,
2001
; Brill and Bushnell,
2001
; Sepulveda et al.,
2003
). Compared with other fishes, tunas have a 210-fold
greater swimming rate of oxygen uptake
(
O2) at
comparable speeds and temperatures; they also have a much higher maximum
O2 (estimated at
2500 mg O2 kg-1 h-1). Greater locomotion
costs reflect higher SMR as well as swimming power. Tunas have a larger gill
area than other fishes and, while tunas are not unique in requiring ram
ventilation, a larger gill area should increase drag and swimming costs and
require more energy for osmoregulation. Tunas have either a small
(Thunnus) or no (skipjacks) gas bladder, making them denser than
seawater and requiring relatively rapid swimming to generate hydrodynamic
lift. Considering only the minimum speed needed to ventilate and maintain
hydrostatic equilibrium, a 1 m-long tuna must swim 0.5 FL s-1 or
43 km day-1 (Magnuson,
1978
).
The enigma of tuna energetics is that their apparently larger aerobic scope
does not translate into swimming performance; water tunnel studies indicate
tuna maximum sustainable swimming velocities in the range of other fishes
(3 FL s-1). It may be that tunas require a larger scope to
accommodate multiple aerobic costs simultaneously
(Brill and Bushnell, 2001
;
Korsmeyer and Dewar, 2001
).
Because tunas are required to swim continually, they cannot suspend RM
activity to meet other aerobic demands such as growth, gonadal production,
replenishment of a post-feeding O2 debt, lactate processing, and
breakdown and assimilation of prey
(Korsmeyer and Dewar, 2001
).
Instead, these costs must be added to swimming
O2.
O2 transport and utilization
Brill and Bushnell (2001)
document numerous tuna specializations for tissue O2 delivery, and
the biochemical poising of tunas for high aerobic energy production is
detailed by Dickson (1996
) and
Korsmeyer and Dewar (2001
).
The high tuna
O2
requires 510 times greater branchial water flow than other fishes. Tuna
gill structure maximizes contact between water and the respiratory epithelium
and minimizes anatomical and physiological dead space, enabling over 50%
O2-extraction efficiencies (compared with 2533% in other
fishes). Tunas have 79 times more gill surface area than rainbow trout
and a much smaller water to branchial capillary diffusion distance
(Brill and Bushnell, 2001
;
Olson et al., 2003
).
With a high hematocrit and mean corpuscular hemoglobin (Hb) concentration,
tuna blood O2-carrying capacities exceed those of other fishes.
Specific differences in the shapes of HbO2 dissociation
curves and P50 values correlate with habitat and behavior
(Cech et al., 1984;
Lowe et al., 2000
). The
bigeye, which penetrates hypoxic water
(Fig. 3), has a higher
HbO2 affinity (P50=1.62.0 kPa;
1525°C) than other tunas (skipjack and yellowfin
2.83.1 kPa; 1525°C; albacore 3.5 kPa; 25°C).
While bigeye, skipjack and yellowfin have sigmoidal O2-dissociation
curves, that of the albacore is hyperbolic.
The thermally independent HbO2 binding shown for Atlantic
northern bluefin (Rossi-Fanelli and
Antonini, 1960) has now been documented for several tuna species
and appears to be adaptive in compensating for rapid thermal changes during
vertical migration. Closed-system temperature changes that simulate arterial
blood warming during transit from gills through the heat exchanger to RM
capillaries reveal interspecific differences in thermal effects on
HbO2 affinity. Closed-system warming increases
HbO2 affinity in albacore and bluefin but decreases that of
bigeye and yellowfin and has no effect on skipjack
(Cech et al., 1984
;
Lowe et al., 2000
). Tuna Hb
has a large Bohr effect (O2 dissociation caused by elevated
CO2 and reduced pH). The Root effect (reduction of
HbO2-carrying capacity at low pH) has been demonstrated for
skipjack, yellowfin and bigeye but not albacore
(Lowe et al., 2000
). For
tunas, a high concentration of Hb, with differential Bohr and Root effects and
with a pronounced Haldane effect (greater CO2 content of
deoxygenated blood), has implications for respiratory gas binding and
transport, particularly in light of regional thermal differences.
Heart function
Most tunas have large hearts, a large ventricular stroke volume (1 ml
kg-1), a greater rate of ventricular pressure development
(dP/dt>700 kPa s-1) and a higher ventral
aortic pressure (1012 kPa) than other fishes
(Brill and Bushnell, 2001;
Braun et al., 2003
). The
striking pyramidal tuna ventricle, with its thick walls, a high percentage of
compact myocardium and extensive coronary circulation, allows high cardiac
output (
).
Both in vitro experiments and in vivo measurements of
heart rate and blood flow in swimming tunas show that
is modulated by changes in heart rate
and not stroke volume (Korsmeyer et al.,
1997a
; Brill and Bushnell,
2001
; Blank et al.,
2004
). This differs markedly from most other fishes, in which
3070% of
adjustment
occurs through stroke volume change. It may be that space limitations imposed
by body streamlining, a large heart, a thick ventricular wall and high heart
rate limit stroke volume range. Tuna heart rate is affected by temperature and
regulated by adrenergic stimulation and cholinergic (vagal) inhibition. The
extent of heart-rate increase elicited by vagal blockade (atropine) indicates
a greater level of cholinergic inhibition for tunas than for other fishes
(Keen et al., 1995
). At normal
temperatures and activity levels, a tuna's heart rate can approach 200 beats
min-1 (Brill and Bushnell,
2001
).
Heart enzyme profiles indicate a high aerobic capacity and are consistent
with the utilization of fatty acids and lactate as metabolic fuels
(Dickson, 1996;
Korsmeyer and Dewar, 2001
).
There is limited information about tuna cardiac myocytes
(Brill and Bushnell, 2001
);
their diameters are more similar to those of other fishes (210 µm)
than mammals (1025 µm). The sarcoplasmic reticulum (SR) of the tuna
heart does not appear to have more structural complexity than that of other
fish hearts, but studies with the SR Ca2+ cycling blocker ryanodine
suggest a greater dependence on SR Ca2+ for tuna heart contraction
compared with other species (Keen et al.,
1995
).
Because lowered temperature and hypoxia both reduce tuna heart rate, forays
into deep, cool and potentially hypoxic water
(Fig. 3) may be limited by that
organ's diminished capacity to supply the O2 requirements of the
endothermic tissues (Brill and Bushnell,
2001; Blank et al.,
2004
). On the other hand, a tuna's high venous O2
reserve (Korsmeyer et al.,
1997b
) allows a margin for sustaining RM oxidative requirements at
a reduced
that, by increasing blood
residence time in the warm tissues and retia, would also conserve heat
(Graham and Dickson,
2001
).
RM and WM biochemistry
RM specializations for a high O2 flux include small-diameter
fibers, with a high myoglobin (Mb) content and capillary density, and
capillary manifolds that increase surface area and red-cell residence time
(Mathieu-Costello et al.,
1996; Dickson,
1996
; Bernal et al.,
2003
). Metabolic enzyme assays at a common temperature show tuna
and other scombrid RM to have comparable activities of citrate synthase (CS;
which catalyzes the first Krebs' cycle reaction and correlates with
mitochondrial density). However, when adjusted to in vivo
temperatures, tuna RM CS activity is
70% greater than in ectothermic
scombrids (Dickson, 1996
).
Tuna WM has a much greater CS activity and a greater anaerobic capacity
(lactate dehydrogenase and creatine phosphokinase activities) than the WM of
other scombrids (Dickson,
1996
; K.A.D., unpublished data). Although bouts of intense
exercise, such as a feeding frenzy, result in high lactate concentrations in
tuna blood (50 mmol l-1) and WM (100 mmol l-1), lactate
clearance by the skipjack is much faster than in other fishes and approaches
the rate in mammals (Arthur et al.,
1992
).
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Conclusions |
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The richness of tuna comparative physiology lies in unanswered questions about thermal effects on RM and digestive, brain and sensory physiology, about blood flow regulation, about HbO2 transport and temperature interactions in open (gills) and closed (capillaries) exchange venues, and about scaling. New findings about tuna depth penetration renew interest in their barobiology. Differences between tunas and bonitos deepen the comparative perspective, as do the independent evolution of comparable specializations in lamnid sharks and the occurrence of cranial endothermy in other teleosts.
In several respects, tuna physiological ecology parallels that of marine mammals: both make a high metabolic energy investment to acquire energy capital needed to sustain activity and for growth and reproduction. Tunas swim steadily in search of food and, like some marine mammals, dive to feed at depth, and some make long annual migrations between fertile, high-latitude feeding grounds and warmer waters favorable for reproduction and offspring success.
Tunas are at risk of over-exploitation and are vulnerable to the effects of global climate change. As recently as three decades ago, it was thought that tuna fishing methods would never succeed to the point that populations would be threatened, as is now true for Atlantic northern bluefin (a staple seasonal food resource in Mediterranean civilizations for over 3000 years!). The Pacific bigeye, now fished intensively on fish-aggregating devices, is declining in number. Just as regions of the tropical ocean may be too warm for large skipjacks, ocean warming has the potential of making the breeding areas of the Gulf of Mexico too warm for adult bluefin, and high-latitude warming (where global change effects will be pronounced) will reduce upwelling and diminish the prey biomass important to migrating tunas.
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Acknowledgments |
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References |
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