Content uploaded by Jeffrey B Graham
Author content
All content in this area was uploaded by Jeffrey B Graham on Mar 21, 2018
Content may be subject to copyright.
998
Evolution and Consequences of Endothermy in Fishes
Kathryn A. Dickson
1,
*
Jeffrey B. Graham
2
1
Department of Biological Science, California State
University, Fullerton, Fullerton, California 92834-6850;
2
Center for Marine Biotechnology and Biomedicine and
Marine Biology Research Division, Scripps Institution of
Oceanography, University of California, San Diego, La Jolla,
California 92093-0204
Accepted 4/30/04
ABSTRACT
Regional endothermy, the conservation of metabolic heat by
vascular countercurrent heat exchangers to elevate the tem-
perature of the slow-twitch locomotor muscle, eyes and brain,
or viscera, has evolved independently among several fish line-
ages, including lamnid sharks, billfishes, and tunas. All are large,
active, pelagic species with high energy demands that undertake
long-distance migrations and move vertically within the water
column, thereby encountering a range of water temperatures.
After summarizing the occurrence of endothermy among fishes,
the evidence for two hypothesized advantages of endothermy
in fishes, thermal niche expansion and enhancement of aerobic
swimming performance, is analyzed using phylogenetic com-
parisons between endothermic fishes and their ectothermic rel-
atives. Thermal niche expansion is supported by mapping en-
dothermic characters onto phylogenies and by combining
information about the thermal niche of extant species, the fossil
record, and paleoceanographic conditions during the time that
endothermic fishes radiated. However, it is difficult to show
that endothermy was required for niche expansion, and ad-
aptations other than endothermy are necessary for repeated
diving below the thermocline. Although the convergent evo-
lution of the ability to elevate slow-twitch, oxidative locomotor
muscle temperatures suggests a selective advantage forthat trait,
comparisons of tunas and their ectothermic sister species
(mackerels and bonitos) provide no direct support of the hy-
pothesis that endothermy results in increased aerobic swim-
ming speeds, slow-oxidative muscle power, or energetic effi-
ciency. Endothermy is associated with higher standard
metabolic rates, which may result from high aerobic capacities
* Corresponding author; e-mail: kdickson@fullerton.edu.
Physiological and Biochemical Zoology 77(6):998–1018. 2004. 䉷2004 by The
University of Chicago. All rights reserved. 1522-2152/2004/7706-3108$15.00
required by these high-performance fishes to conduct many
aerobic activities simultaneously. A high standard metabolic
rate indicates that the benefits of endothermy may be offset by
significant energetic costs.
Introduction
Regional endothermy, the ability to conserve metabolically de-
rived heat to maintain the temperature of certain tissues ele-
vated above ambient temperature, has evolved in several line-
ages of fishes (Table 1; Fig. 1). Endothermy requires an internal
source of heat and a mechanism to retain that heat. The source
of metabolic heat varies, but all endothermic fishes make use
of blood vessels arranged as countercurrent heat exchangers
(retia mirabilia), interposed between the endothermic tissue
and the gills where any heat transferred by convection from
the tissue would be lost to the surrounding water across the
large and thin gill surface. Some fish species are specialized to
elevate the temperature of only one or two tissues. For example,
in istiophorid billfishes and butterfly mackerels, only eye and
brain temperatures are elevated (cranial endothermy; Carey
1982; Block 1986, 1991). Other species, including shortfin
mako, white sharks, and northern bluefin tunas, have evolved
the capacity to elevate the temperature of several core body
tissues (the viscera, the slow-twitch, oxidative myotomalmuscle
fibers, and the eye and brain), and acoustic telemetry and ar-
chival (data-logging) tagging studies have documented that
these species can maintain relatively stable tissue temperatures
when encountering large changes in ambient water temperature
(Carey and Lawson 1973; Carey et al. 1981, 1982; Goldman
1997; Block et al. 2001; Marcinek et al. 2001a). Many of these
species have some capacity for behavioral or physiological
thermoregulation.
Several reviews published within the past decade have sum-
marized many aspects of endothermy in fishes (Block 1994;
Block and Finnerty 1994; Brill 1996; Dickson 1996; Fudge and
Stevens 1996; Graham and Dickson 2000; Bernal et al. 2001a;
Block and Stevens 2001). This article summarizes recent work
on fish endothermy and brings together information on all
known or suspected endothermic fish species. With fishes, there
are two advantages in studying the evolution of endothermy:
(1) within the family Scombridae, phylogenetically based com-
parisons of extant endothermic and ectothermic sister taxa (tu-
nas and the bonitos, Spanish mackerels, and mackerels; Fig. 1)
can be used to elucidate the sequence of evolutionary changes
that led to endothermy and (2) we can compare several groups
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Table 1: Known or suspected endothermic fish species
Taxon
Ability to Elevate Temperature of
References
a
Muscle Eye/Brain Viscera
Elasmobranchii:
Order Lamniformes:
Family Lamnidae (mackerel sharks):
Lamna ditropis Hubbs and Follett salmon shark X X X 3, 8, 16, 35, 40, 42
Lamna nasus (Bonnaterre) porbeagle shark X X X 8, 15, 16, 19, 20, 42
Carcharodon carcharias (Linnaeus) white shark X X X 8, 16, 17,19, 25, 42
Isurus paucus Guitart Manday longfin mako shark ? X X 8, 16
Isurus oxyrinchus Rafinesque shortfin mako shark X X X 3, 8, 15, 16, 19, 20, 42
Family Alopiidae (thresher sharks):
Alopias pelagicus Nakamura pelagic thresher shark ? ? 8, 41
Alopias superciliosus (Lowe) bigeye thresher shark ? ? 8, 20, 41
Alopias vulpinus (Bonnaterre) common thresher shark ? ? 3, 9, 24, 41
Order Rajiformes, family Myliobatidae (manta rays):
Mobula tarapacana (Philippi) Chilean devil ray ? ? 1, 2
Manta birostris (Walbaum) giant manta ray ? 2
Teleostei:
Order Perciformes, suborder Scombroidei:
Family Xiphiidae Xiphias gladius Linnaeus swordfish ? X 4, 6, 11, 12
Family Istiophoridae (eight billfish species) X 4, 5, 6
Family Scombridae:
Gasterochisma melampus Richardson butterfly mackerel X? 4, 6, 7, 11
Tribe Thunnini (tunas):
Allothunnus fallai Serventy slender tuna ? 29
Auxis rochei (Risso) bullet tuna X nd 10, 22
Auxis thazard (Lacepede) frigate tuna X X 20, 37
Euthynnus affinis (Cantor) kawakawa tuna X X 38
Euthynnus alletteratus (Rafinesque) little tunny X X 20, 32
Euthynnus lineatus Kishinouye black skipjack tuna X X 22, 26, 36
Katsuwonus pelamis (Linnaeus) skipjack tuna X X 20, 27, 34, 38, 39
Thunnus tonggol (Bleeker) longtail tuna X nd 10, 21
Thunnus atlanticus (Lesson) blackfin tuna X nd 10, 20
Thunnus albacares (Bonnaterre) yellowfin tuna X X 20, 23, 27
Thunnus obesus (Lowe) bigeye tuna X X ? 12, 20, 31, 32
Thunnus alalunga (Bonnaterre) albacore tuna X X X 20, 28, 32
Thunnus maccoyii (Castelnau) southern bluefin tuna X nd X 30
Thunnus orientalis (Temminck and Schlegel) Pacific
northern bluefin tuna X X X 33
Thunnus thynnus (Linnaeus) Atlantic northern bluefin tuna X X X 13, 14, 18, 20, 32
Note. of endothermy includes morphological specializations and measurement of elevated tissue temperatures. morphological spe-Xpevidence ?ponly
cializations (including putative countercurrent heat exchangers) have been reported. Gasterochisma, we have found no temperature measurements, butX? pfor
cranial endothermy is assumed due to the presence of heater tissue. pertinent data for this species have been reported, but endothermy is assumednd pno
due to phylogenetic relationship with known endothermic species.
a
Data are from the following references: 1995; 1996; et al. 2001a; 1986; 1990;1pAlexander 2 pAlexander 3 pBernal 4 pBlock 5 pBlock 6 pBlock
1991; 1994; and Carey 1985; and Chubb 1983; et al. 1992; 1982; 1990;7pBlock 8 pBlock 9 pBone 10 pBushnell 11 pCarey 12 pCarey 13 pCarey
and Lawson 1973; and Teal 1966; and Teal 1969a; et al. 1985; et al. 1982; et al. 1984;14 pCarey 15 pCarey 16 pCarey 17 pCarey 18 pCarey 19 p
et al. 1981; et al. 1971; 1978; 1994; and Brill 1979; and Stevens 1996;Carey 20 pCarey 21 pCollette 22 pDickson 23 pDizon 24 pFudge 25 p
1997; 1973; 1975; and Dickson 1981; and Dickson 2000; and Block 2001;Goldman 26 pGraham 27 pGraham 28 pGraham 29 pGraham 30 pGunn
et al. 1992; and Carey 1972; et al. 2001a; et al. 1976; and Smith 1983;31 pHolland 32 pLinthicum 33 pMarcinek 34 pNeill 35 pRhodes 36 p
1984; 1985; and Fry 1971; and Neill 1978; and Block 2000; and Block 2004;Schaefer 37 pSchaefer 38 pStevens 39 pStevens 40 pTubbesing 41 pWeng
et al. 1988.42 pWolf
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1000 K. A. Dickson and J. B. Graham
Figure 1. Cladograms showing proposed phylogenetic relationships among fish groups with endothermic species (sharks of the families Lamnidae
and Alopiidae and Scombroid fishes of the families Xiphiidae, Istiophoridae, and Scombridae; see Table 1). Cladograms are based on those of
Carpenter et al. (1995), Lydeard and Roe (1997), Naylor et al. (1997), Graham and Dickson (2000), Bernal et al. (2001a), and Collette et al.
(2001), which are derived from morphological and gene sequence data. Numbers in parentheses represent the number of species in the genus.
of fishes in which endothermy has evolved by convergence
(Block and Finnerty 1994; Dickson 1995, 1996; Bernal et al.
2001a). The article focuses on phylogenetically based compar-
isons of endothermic fishes with their ectothermic relatives to
evaluate evidence for two major hypotheses about the selective
forces leading to the evolution of endothermy in fishes: thermal
niche expansion and enhancement of aerobic swimming per-
formance. We also discuss consequences and costs of
endothermy.
Which Fish Species Are Endothermic?
Unequivocally documenting endothermy in a given fish species
requires measuring significantly elevated tissue temperatures,
describing a mechanism to conserve heat within the tissue (vas-
cular countercurrent heat exchangers), and usually identifying
the source of metabolic heat. Regional endothermy has evolved
independently in four groups of fishes (lamnid sharks, billfishes
[families Xiphiidae and Istiophoridae], the butterfly mackerel,
and tunas) and possibly also in thresher sharks and manta rays
(Table 1; Fig. 1). In the latter two groups and the butterfly
mackerel, endothermy has not been confirmed by measure-
ments of elevated tissue temperatures but is proposed on the
basis of morphological characteristics, including tissues per-
fused by putative countercurrent heat exchangers that are sim-
ilar to those found in species known to be endothermic (Carey
et al. 1971; Bone and Chubb 1983; Block and Carey 1985; Tullis
et al. 1991; Alexander 1995, 1996; Fudge and Stevens 1996;
Bernal et al. 2001a; Weng and Block 2004). A number of fish
species can maintain an elevated temperature in more than one
tissue (Table 1). Because elevation of the temperature of each
tissue requires specific morphological characteristics andsome-
times physiological or biochemical adaptations, endothermy
most likely evolved more than once in those fish lineages.
Sources of Heat for Endothermy in Fishes
Slow-Oxidative, Myotomal Muscle (RM) Endothermy. All species
known to elevate RM temperatures swim continuously, and
contraction of the RM to power sustained swimming is the
source of heat for RM endothermy. In all these fishes, myotomal
RM muscle fibers are found in a more medial and anterior
position within the myotomal cones rather than in a lateral
wedge just beneath the skin, as they are in ectothermic species
(Kishinouye 1923; Carey et al. 1985; Westneat et al. 1993; Gra-
ham and Dickson 2000; Bernal et al. 2001a, 2003a). The RM
fibers are thus insulated by overlying tissues, reducing con-
ductive heat loss from the RM across the body surface.
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1001
Table 2: Comparison of selected characteristics of endothermic tunas and the shortfin mako shark with those of related
ectothermic species
Characteristic
Eastern Pacific
Bonito Tunas References
a
Ectothermic
Sharks
Shortfin Mako
Shark References
a
Characteristics of RM:
Amount (% of body mass) 4.5–6.2 4.1–12.8 8, 16, 18,
19, 22
222,5
Citrate synthase activity (IU/g at
20⬚C) 41 43–70 8, 19 22–34 32 3, 9
Mitochondrial density (volume %) 47 24–32 23, 24, 25 30–34 25–37 2, 26
Myoglobin content (mg Mb/g
tissue)
b
13 21 8 3–9 21 2
RM position
b
Lateral wedge Anterior-medial 19, 28 Lateral Anterior-medial 1, 2, 5
Locomotor mode
b
Carangiform Thunniform 7, 10, 13,
14, 15, 21
Subcarangiform Thunniform 28, 11, 12
Standard metabolic rate (mg O
2
kg
⫺1
h
⫺1
)
b
161
c
250–350
c
4, 6, 27 92
d
240
d
1
Highest metabolic rate measured
(mg O
2
kg
⫺1
h
⫺1
)
b
∼1,400
c
2,200–2,700
c
17, 20, 27 167
d
507
d
1
a
Data are from the following references: et al. 2001a; et al. 2003a; et al. 2003b; 1987; et al. 1985;1pBernal 2 pBernal 3 pBernal 4 pBrill 5 pCarey
and Graham 1994a; and Graham 1994b; 1996; et al. 1993; and Dickson 2000; et6pDewar 7 pDewar 8 pDickson 9 pDickson 10 pDonley 11 pDonley
al. 2004; and Shadwick 2003; et al. 2003; et al. 2000; and Walters 1968; 1999;12 pDonley 13 pDowis 14 pEllerby 15 pFierstine 16 pFreund 17 p
et al. 1981; and Dickson 2000; et al. 1983; and Dewar 2001; 1978; 1973;Gooding 18 pGraham 19 pGraham 20 pKorsmeyer 21 pLindsey 22 pMagnuson
-Costello et al. 1992; et al. 1992; Porcu, S. Karl, and K. Dickson, unpublished observations; Powers, S. Karl, and23 pMathieu 24 pMoyes 25 pC. 26 pA.
K. Dickson, unpublished observations; et al. 2003; and Keyes 1982. For similar comparisons of other characteristics, see tables in27 pSepulveda 28 pWebb
Bernal et al. 2001a, 2003b.
b
In both groups, the endothermic species is/are significantly greater than the ectothermic species
c
For ∼1-kg fish at 24⬚C.
d
For ∼4-kg fish at 18⬚C.
Although some tunas (e.g., Auxis,Euthynnus) have more RM
(as a percentage of body mass) than ectothermic scombrids,
others, including the most basal tuna Allothunnus fallai Ser-
venty and the more derived albacore Thunnus alalunga (Bon-
naterre), have lower amounts that fall within the range for
ectothermic scombrids (reviewed in Dickson 1995; Graham and
Dickson 2000). Relative amounts of RM in lamnid sharks, the
common thresher shark, and active ectothermic sharks are sim-
ilar (approximately 2% of body mass; Bernal et al. 2001a,
2003a). Therefore, endothermic species do not consistently
have significantly greater amounts of RM than are found in
related ectothermic fishes (Table 2).
There is no evidence that the RM of any endothermic species
has been modified to produce heat for endothermy, although
specific indices of RM heat production, including plasma
membrane Na
⫹
conductance, mitochondrial H
⫹
leak rates, and
membrane lipid unsaturation levels, have not been measured
in related endothermic and ectothermic fishes. In the RM of
tunas and lamnid sharks, the activity (measured at a given
temperature) of the mitochondrial enzyme citrate synthase and
mitochondrial densities are not significantly greater than in the
RM of closely related ectothermic species, but myoglobin con-
centration is greater (Table 2). Because Marcinek et al. (2001b)
found similar oxygen binding affinities at in vivo temperatures
for myoglobins from the RM of chub mackerel, eastern Pacific
bonito, skipjack tuna, and Pacific northern bluefin tuna, the
concentration of myoglobin will be an important determinant
of oxygen flux within these muscle cells. Mitochondria isolated
from RM of the shortfin mako were well coupled and respired
at rates comparable to those of dogfish (Squalus acanthias Smith
and Radcliffe) RM (Ballantyne et al. 1992); similar results were
obtained by Moyes et al. (1992) in comparisons of RM mi-
tochondria from skipjack tuna (Katsuwonus pelamis [Lin-
naeus]) and carp (Cyprinus carpio Linnaeus). On the basis of
these findings, it appears that the slow-oxidative locomotor
muscle of endothermic fishes is not specialized for heat pro-
duction. Therefore, the modifications required for RM endo-
thermy are the differentiation of slow-oxidative myotomalmus-
cle fibers in a more medial and anterior body position and the
perfusion of this muscle by arterial and venous vessels arranged
as countercurrent heat exchangers. These changes involve al-
terations in processes (muscle fiber type expression and angi-
ogenesis) that occur in all fishes.
Visceral Endothermy. Elevation of visceral temperatures involves
retention of heat produced by processes that normally accom-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1002 K. A. Dickson and J. B. Graham
pany feeding. Heat associated with specific dynamic action, or
the elevation of metabolic rate as a consequence of food pro-
cessing (digestion, absorption, and protein synthesis), is re-
tained in endothermic fishes by visceral countercurrent heat
exchangers. As with RM endothermy, it appears that the prin-
cipal adaptation required for visceral endothermy is the de-
velopment of retia that reduce convective heat loss from the
viscera.
The warmest visceral tissues are the pyloric caeca (caecal
mass) in tunas (Carey et al. 1984) and the spiral valve intestine
in the lamnid sharks (Carey et al. 1981, 1985; Bernal et al.
2001a), and these organs are likely to be the main site of heat
production for visceral endothermy in these fishes. In the tuna
species with visceral countercurrent heat exchangers (Table 1),
the liver is “upstream” of these heat exchangers, and they can-
not conserve metabolic heat produced in the liver. Yet, parallel
arteries and veins, which form “striations” on the liver surface,
may function as a simple two-dimensional heat exchanger (Ca-
rey et al. 1984; Fudge and Stevens 1996). By contrast, in lamnid
sharks, the large liver is served by the suprahepatic rete and is
warm (Carey and Teal 1969a; Carey et al. 1985; Bernal et al.
2001a). In thresher sharks, no visceral temperature measure-
ments that we know of have been reported, but putative coun-
tercurrent heat exchangers have been described in Alopias vul-
pinus, and, as in the tunas, the liver is not included in the
tissues perfused by the retia, and it also contains “striations”
(Fudge and Stevens 1996). As far as we know, the other thresher
shark species have not been examined for visceral retia. In
addition to enhancing food processing and speeding rates of
digestion and assimilation of food (Carey et al. 1984; Stevens
and McLeese 1984), visceral endothermy contributes to warm-
ing of the body core and, among the tunas, has been docu-
mented only in albacore and bluefin, species that dive into cool
waters.
Cranial Endothermy. The source of heat used to elevate brain
and eye temperatures varies interspecifically. In tunas, the heat
source for cranial endothermy is not known. It has been sug-
gested to be from aerobic metabolism in the brain and eyes
(Block 1987b) or in the ocular muscles (Block and Finnerty
1994) or conduction from the warm myotomal muscle (Sharp
and Vlymen 1978; Block 1987b) via the frontoparietal fenestrae
in the skull (Graham and Dickson 2000). In the lamnid sharks,
a unique “red muscle vein” transfers heat from the warm RM
to the orbital sinus that comprises the venous portion of the
orbital rete (Wolf et al. 1988; Tubbesing and Block 2000), but
heat may also be contributed by activity of the ocular muscles,
which are darker red in color and presumably more aerobic
than they are in ectothermic sharks (Wolf et al. 1988; Block
and Finnerty 1994). The apparent dependence of cranial en-
dothermy on endothermic RM in lamnid sharks means that
RM endothermy evolved before cranial endothermy in this
group or that these two traits evolved in concert.
The billfishes and the butterfly mackerel have independently
evolved specialized heater tissues from the superior rectus and
lateral rectus ocular muscles, respectively (Carey 1982; Block
1986, 1991; Tullis et al. 1991). Fish cranial heater tissue is one
of only two animal tissues known to be specialized for heat
production, the other being mammalian brown adipose tissue.
These two tissues use different mechanisms for thermogenesis,
which represent modifications of the typical function of the
tissue from which each is derived (reviewed by Block 1994).
The current model for heat production in fish heater tissue is
a modification of the Ca
⫹⫹
cycling process that normally is
involved in muscle fiber contraction and relaxation, as first
proposed by Block (1987a). The heater tissue cells have lost
the myofibrillar contractile apparatus and participate in futile
cycling of Ca
⫹⫹
between the cytoplasm and the sarcoplasmic
reticulum (SR), mediated by Ca
⫹⫹
ATPase and a physiologically
unique ryanodine receptor (a Ca
⫹⫹
release channel) within the
SR membrane (Block 1994; Franck et al. 1998; Morrissette et
al. 2003). Evidence that this thermogenic process is controlled
by cholinergic innervation was recently obtained (Morrissette
et al. 2003). Cranial endothermy involving thermogenesis
within specialized heater tissues is the only case in fishes in
which heat is generated specifically for endothermy and is not
just a by-product of other metabolic processes that would occur
whether or not the fish is endothermic.
Physiological and Behavioral Thermoregulation
Once the capacity to retain metabolic heat evolved, selection
for mechanisms to control rates of heat loss and retention by
the retia would have occurred. Empirical evidence of physio-
logical thermoregulation (the ability to adjust rates of heat
production or heat conservation by physiological means) has
been obtained in albacore tuna (Graham and Dickson 1981),
bigeye tuna (Holland et al. 1992), yellowfin tuna (Brill et al.
1994; Dewar et al. 1994), swordfish (Carey 1990), blue marlin
(Morrissette et al. 2003), and lamnid sharks (Goldman 1997;
Bernal et al. 2001b). However, the exact mechanisms involved
in modifying thermal conductance and heat exchanger effec-
tiveness have not been well characterized (reviewed in Bushnell
et al. 1992; Graham and Dickson 2001). The heat exchange
efficiency of the retia could be modified by altering blood flow
through rete blood vessels, mediated by changes in vessel di-
ameter, or by adjusting relative blood flow through alternate
routes to the endothermic tissue if heat exchange efficiency
differs between the two routes. For example, the RM of some
tunas (Auxis,Euthynnus, and Katsuwonus) is perfused both by
large central retia with many arterioles and venules and by small
lateral retia with a smaller surface area for heat exchange (Gra-
ham 1973; Stevens et al. 1974; Graham 1975; Graham and
Diener 1978; Dickson 1994); shunting more blood via the lat-
eral retia and less via the central rete could reduce RM heat
conservation in these fishes. In species with lateral but no cen-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1003
tral retia perfusing the RM (e.g., lamnid sharks and bigeye,
albacore and bluefin tunas), blood flow from the gills via the
reduced dorsal aorta would shunt blood at ambient tempera-
ture directly to the RM, thereby allowing some control of RM
heating and cooling rates (Carey et al. 1971; Graham and Dick-
son 1981; Holland et al. 1992). The blood supply to the RM
of the Pacific northern bluefin tuna Thunnus orientalis (Tem-
minck and Schlegel), to the cranial region of the Atlanticnorth-
ern bluefin tuna Thunnus thynnus (Linnaeus), and to the viscera
of the lamnid sharks includes apparent vascular shunt pathways
around the retia (Linthicum and Carey 1972; Carey et al. 1981;
Funakoshi et al. 1985). Nerves are often found to be associated
with heat exchanger blood vessels (Stevens et al. 1974; Carey
1990; Moore 1998), but no direct evidence exists for nervous
control of heat exchanger efficiency or of blood shunting in
endothermic fishes. Injection of catecholamines or adrenergic
blockers altered heat exchange efficiency in kawakawa and yel-
lowfin tunas, respectively (Brill et al. 1994; Korsmeyer and Brill
2002), but it is not known whether tunas adjust circulating
levels of catecholamines for physiological thermoregulation.
These findings, based primarily on anatomical characteristics,
should be followed up by physiological studies to understand
how heat conductance can be adjusted in endothermic fishes.
Endothermic fishes can also behaviorally thermoregulate by
swimming vertically within thermally stratified waters. This has
been demonstrated most convincingly in the bigeye tuna by
Holland et al. (1992). When not associated with floating objects,
bigeye tuna make repeated dives below the thermocline to
depths as great as 1000 m, apparently so they can feed on prey
within the deep scattering layer, and then they return to surface
waters to warm up (Holland et al. 1992; Dagorn et al. 2000;
Schaefer and Fuller 2002; Musyl et al. 2003). While bigeye were
in cold deep waters, whole-body thermal conductance was
much less than it was when they moved into warm water;
muscle temperature increased rapidly when the fish were near
the surface and dropped slowly when they dove (Holland et
al. 1992; Schaefer and Fuller 2002). By modifying thermal con-
ductance and moving vertically within thermally stratified wa-
ters, the fish prevented muscle temperature from dropping be-
low 18⬚C (Holland et al. 1992). Thus, a combination of
behavioral and physiological thermoregulatory mechanisms are
used by bigeye tuna, as has also been documented in swordfish
during dives to depths of 500–600 m (Carey 1990).
Evolution of Endothermy in Fishes
All known or suspected endothermic fish species (Table 1) are
active, pelagic predators that swim continuously, and many of
them migrate vast distances and repeatedly move vertically
within the water column, encountering wide temperature
ranges (Carey and Lawson 1973; Joseph et al. 1988; Carey 1990;
Block et al. 2001; Marcinek et al. 2001a; Boustany et al. 2002;
Schaefer and Fuller 2002; Musyl et al. 2003). There have been
many hypotheses to explain the convergent evolution of en-
dothermy in these different fish lineages. It has been proposed
that endothermy evolved to allow fishes to (1) expand their
thermal niche (Block et al. 1993; Graham and Dickson 2000);
(2) stabilize tissue temperatures in the face of changing ambient
temperatures (Carey and Teal 1969b; Neill et al. 1976; Stevens
and Neill 1978; Weng and Block 2004); (3) perceive thermal
gradients more effectively (Neill et al. 1976); (4) increase rates
of metabolic processes, including faster recovery from anaer-
obic bursts (Stevens and Neill 1978; Brill 1996); and (5) increase
rates of somatic and gonadal growth (Brill 1996). In addition,
the following advantages of elevating the temperatureof specific
tissues have been proposed: (1) cranial endothermy has been
hypothesized to enhance visual acuity and neural processing
(Carey and Teal 1966; Linthicum and Carey 1972; Block and
Carey 1985); (2) visceral endothermy is believed to increase
rates of digestion, absorption, assimilation, and clearance of
food (Carey and Teal 1966; Carey et al. 1981, 1984; Stevens
and McLeese 1984; Goldman 1997); (3) elevation of the tem-
perature of the fast-glycolytic locomotor muscle, primarily by
conduction from the RM that it surrounds, is hypothesized to
increase maximum burst swimming performance by increasing
muscle contraction rate and power output or by increasing
lactate turnover (Carey and Teal 1969a; Carey et al. 1971; Brill
1978; Wardle et al. 1989); and (4) elevation of the temperature
of the slow-oxidative locomotor muscle is hypothesized to in-
crease sustainable swimming performance by increasing muscle
contraction rate and power output (Carey et al. 1971; Johnston
and Brill 1984; Altringham and Block 1997) or by enhancing
the diffusion of oxygen to the muscle mitochondria (Stevens
and Carey 1981).
We have chosen to review the evidence for two of these
hypotheses, thermal niche expansion and increasing sustainable
swimming performance, because recent studies provide new
insight on these two in particular. Furthermore, these hypoth-
esized advantages of endothermy closely parallel those proposed
for the evolution of endothermy in terrestrial vertebrates
(Crompton et al. 1978; McNab 1978; Bennett and Ruben 1979).
Thermal Niche Expansion Hypothesis
The idea that thermal niche expansion was a key selective force
in the evolution of endothermy in fishes was first formalized
by Block (Block 1991; Block et al. 1993), although the basis
for this hypothesis can be traced back to the early work of
Carey. For example, Carey and Lawson (1973, p. 390) state that
endothermy “has enabled [the Atlantic northern bluefin tuna]
to greatly expand [its] range and take advantage of the rich
feeding areas in northern waters and warm spawning areas in
the tropics.” New insight on thermal niche expansion was
gained when Block et al. (1993) mapped endothermic char-
acters onto a molecular phylogeny of the suborder Scombroidei
and showed that cranial endothermy appears in more basal
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1004 K. A. Dickson and J. B. Graham
Figure 2. Sequences of the geological, physical, and biological changes taking place in the Cenozoic ocean in relation to the origin and radiation
of tunas and other endothermic fishes. Geological time scale is from Berger and Wefer (1996). Relative benthic oceanic temperatures are based
on oxygen isotope ratios in benthic foraminiferal tests from deep-sea sediment cores taken from the Atlantic Ocean and are consistent with
other evidence (Berger and Wefer 1996; Macdougall 1996; Lear et al. 2000; Bice and Marotzke 2001; Berger et al. 2002). Ocean conditions are
based on several sources (Berger 1981; Carroll 1988; Barron and Baldauf 1989; Berggren and Prothero 1992; Smith et al. 1994; Berger and
Wefer 1996; Macdougall 1996; Fordyce and de Muizon 2001). Size of the North Atlantic was determined from maps in an article by Smith et
al. (1994). Time of first known appearance of different genera of endothermic or suspected endothermic fishes are indicated with dots for
scombrids (Bannikov 1985; Carroll 1988; Patterson 1993; K. A. Monsch, personal communication), billfishes (Fierstine 1990, 2001), lamnid
sharks (Carroll 1988; Applegate and Espinosa-Arrubarrena 1996; Purdy 1996), and other elasmobranch fishes (Carroll 1988; Martin et al. 1992).
Records of the earliest fossil evidence for other vertebrate groups having relevance as an index of ocean productivity and carrying capacity are
also indicated: perciform fishes (Carroll 1988), penguins (Carroll 1988), pinnipeds (Berta and Adam 2001), and cetaceans (Fordyce 1992;
Fordyce and de Muizon 2001).
lineages within the Scombroidei (in the billfishes) and within
the family Scombridae (in the butterfly mackerel) than do RM
and visceral endothermy. In addition, because cranial endo-
thermy is more widespread among fishes than either RM or
visceral endothermy, Block et al. (1993) argued that niche ex-
pansion was the primary driving force for the evolution of
endothermy, since enhanced locomotor performance and ac-
tivity cannot explain elevating the temperature of just the eye
and brain, as occurs in istiophorid billfishes and the butterfly
mackerel. Yet Block and Finnerty (1994) did acknowledge that
the evolution of cranial, RM, and visceral endothermy in the
scombroid fishes may have been independent events and each
may have occurred as a result of different selection pressures.
Graham and Dickson (2000) provided additional support
for the thermal niche expansion hypothesis by considering the
selective pressures and environmental conditions that existed
during the time that the tunas radiated from a presumably
ectothermic ancestor. They integrated what was known about
the tuna fossil record and paleoceanographic conditions and
proposed that endothermy evolved in association with ocean
cooling and tropical compression to allow warm-water-adapted
tunas to migrate and dive into cooler waters to feed in zones
of high productivity. The following sections review that infor-
mation; incorporate additional findings on fossils, paleocean-
ography, and the distribution and behavior of extant species;
and broaden the discussion to consider the other endothermic
fishes.
A Summary of the Fossil Record for Endothermic Fishes. Although
it is incomplete and is subject to different interpretations, we
can use the fossil record, in combination with assessments of
paleoenvironmental conditions, to support the niche expansion
hypothesis by showing that selective pressures that favoredther-
mal niche expansion were present when endothermic fishes
evolved and radiated. The scombrid fossil record contains sev-
eral extant genera of bonitos and tunas (Bannikov 1985; Carroll
1988; Monsch 2000a, 2000b; Fig. 2). All tuna fossils are from
sediments that have been interpreted to be tropical or sub-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1005
tropical seas (Bannikov 1985; Landini and Sorbini 1996; Dine-
ley and Metcalf 1999; K. A. Monsch, personal communication).
The earliest tuna fossils occur in the Late Paleocene (55–65
Ma) or Early Eocene (50–55 Ma) epochs of the Tertiary (Ban-
nikov 1985; Carroll 1988; Monsch 2000b; K. A. Monsch, per-
sonal communication) and occur in Tethys Sea deposits from
the Middle East and southern Europe or the London Clay
formation in England. The earliest bonito that has been iden-
tified is Sarda palaeocenica Leriche from the Early Paleocene
(Bannikov 1985; Patterson 1993; K. A. Monsch, personal com-
munication). Bannikov (1985) found that the extinct Paleo-
thunnus parvidentatus Bannikov shared characteristics with ex-
tant bonitos and tunas and identified this species as the putative
common ancestor of the clade composed of tunas and bonitos.
Monsch (Monsch 2000b; K. A. Monsch, personal communi-
cation) reexamined scombrid fossils described by Bannikov
(1985) and found that Paleothunnus has primitive character-
istics relative to both bonitos and tunas. The fossil data suggest
that the split between the tunas and bonitos did not occur
before the Early Eocene. The results of Bannikov (1985) also
suggest that, within as little as 8–10 million years, the tunas
and bonitos diverged, and the derived tuna genus, Thunnus,
had appeared (Fig. 2). Auxis is known from the Eocene, but
the fossil record for Euthynnus/Katsuwonus extends only to the
Pliocene (Carroll 1988; Fig. 2). A rapid radiation of the tunas
is also suggested by molecular phylogenetic studies, based on
the rate of nucleotide base substitutions (Block et al. 1993;
Chow and Kishino 1995; Finnerty and Block 1995; Alvarado
Bremer et al. 1997).
The fossil record for billfishes has recently been reviewed and
summarized (Fierstine 1990, 2001; Fierstine and Monsch 2002).
The extant genera (Xiphias,Makaira,Istiophorus, and Tetrap-
turus) can be traced as far back as the Pliocene, Middle Mio-
cene, Late Miocene, and Early Pliocene, respectively, although
one fossil from the Late Eocene of Belgium may be an isti-
ophorid (Fierstine 1990, 2001; Fig. 2). Monsch (2000b) iden-
tified Makaira sp. fossil vertebrae from the Early Eocene, Lon-
don Clay formation, and Lower Barton Clay. The fossil data
coincide with the molecular phylogenetic analyses of Block et
al. (1993), which indicate that the istiophorids radiated rapidly,
based on the number of nucleotide substitutions occurring
along branches of a cladogram derived from cytochrome b gene
sequences. The extinct Xiphiorhynchidae, the sister group to
the present-day swordfish (Xiphiidae), are found in Eocene and
Oligocene deposits from the north Atlantic and western Tethys
Sea (Fierstine 1990; Fierstine and Monsch 2002). Fossils
of the extinct Blochiidae, which is sister to Xiphiidae ⫹
, have been identified from the Middle Eo-Xiphiorhynchidae
cene in tropical coastal sediments (Fierstine and Monsch 2002).
The fossils of extant and ancestral billfish taxa are found in
deposits representing habitats similar to those in which present-
day billfishes are found.
The fossil record for the elasmobranchs is composed largely
of teeth because the cartilaginous skeletons of elasmobranchs
rarely fossilize well. The first appearance of Alopias in the fossil
record was at 50–56 Ma (Carroll 1988; Martin et al. 1992; Fig.
2). A combination of fossil data and estimates of cytochrome b
gene sequence divergence rates based on transversion substi-
tutions indicate that the three extant lamnid genera (Carchar-
odon,Isurus, and Lamna) diverged from a common ancestor
in a relatively brief period, 35–50 Ma (Martin et al. 1992; Martin
1996). However, extinct lamnid sharks (e.g., Cretolamna and
Paleocarcharodon) were present in the Late Cretaceous and the
Paleocene, and others believe that the extant lamnid genera
evolved from different ancestral lineages (e.g., Applegate and
Espinosa-Arrubarrena 1996). Purdy (1996) summarized the oc-
currence of Carcharodon and Isurus fossils from the Tertiary in
relationship to water temperature and presence of marine
mammal fossils. He hypothesized an association between the
large-tooth shark, Carcharodon megalodon (Agassiz) and its ma-
rine mammal prey, especially in upwelling areas, as represented
in the Lee Creek Mine phosphate deposits. The putative an-
cestor of C. megalodon had a worldwide tropical distribution
(Purdy 1996). Fossils of C. megalodon have not been found
more recently than the Late Pliocene (Applegate and Espinosa-
Arrubarrena 1996; Purdy 1996), which is when global cooling
commenced (Fig. 2). The extant white shark, Carcharodon car-
charias (Linnaeus), is represented in the fossil record back to
15–16 Ma (Fig. 2); fossils of C. carcharias and its putative
ancestors are found in cooler water deposits (Purdy 1996).
Summary of Paleoceanographic Conditions during the Cenozoic.
The co-occurrence of processes likely to have influenced the
evolution and radiation of endothermic fishes and other marine
organisms in the Cenozoic is shown in Figure 2. Ocean paleo-
temperature was warmest near the end of the Paleocene (∼55
Ma) and cooled thereafter (Berger and Wefer 1996). Tectonic
events that caused the isolation of Antarctica behind the cir-
cumpolar current and the shrinkage of the Tethys Seaway, a
large tropical sea that had encircled the globe for more than
70 million years, both contributed to the global cooling trend,
as did the penetration of cold Antarctic water into the Atlantic
Basin (Berger 1981). Cooling at high latitudes and the resultant
increase in the earth’s equator-to-pole thermal gradientaffected
wind patterns, which formed oceanic gyres and initiated the
process of transporting water toward the poles. Coastal up-
welling associated with this poleward transport enhanced pro-
ductivity (Barron and Baldauf 1989; Berger and Wefer 1996).
The change in paleoclimate also likely resulted in seasonalshifts
in the location of zones of high productivity. Patterns of marine
biodiversity and abundance in the Cenozoic reveal a strong
dependence on high rates of primary production (Barron and
Baldauf 1989).
The long-term stability of the relatively warm, circumglobal
Tethys Seaway, followed by a reduction in volume of this trop-
ical habitat and global cooling accompanied by increased pro-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1006 K. A. Dickson and J. B. Graham
ductivity, appears to have had important consequences for the
evolution and radiation of several groups during the Cenozoic.
Fossils of the earliest cetaceans (Fordyce 1992; Fordyce and de
Muizon 2001) and many of the fish groups that radiated in
the Tertiary, including ancestral tunas (Bannikov 1985), occur
in Tethys Sea deposits. As a consequence of sea-floor spreading,
the physical area of the North Atlantic steadily increased during
the Cenozoic (Fig. 2), and this opened up new ecologically rich
areas for exploitation by species capable of adapting to the
conditions. Many groups such as the whales and pinnipeds,
which first appeared in the Oligocene, began to radiate in high
latitudes during the Miocene (5–20 Ma), the approximate time
of the advent of the modern ocean’s thermohaline circulation
(Fordyce and de Muizon 2001; Fig. 2). Many other groups,
including zooplankton, many of the modern perciform fishes,
and marine birds, also underwent significant radiations in the
Cenozoic (Berger 1981; Carroll 1988, 1997; Macdougall 1996).
Linking Paleoceanography, Niche Expansion, and Fish Endo-
thermy. The radiation and diversification of both the lamnid
sharks and tunas began at approximately the same time (during
the Late Paleocene and Early Eocene). We hypothesize that the
ancestral stocks of these endothermic species were ectotherms
adapted to the stable, tropical conditions within the Tethys
Seaway. Therefore, subsequent oceanic cooling and tropical
compression would have had significant evolutionary conse-
quences. These species would have had to adapt to the changing
conditions or face extinction, and we propose that these se-
lective pressures led to the convergent evolution ofendothermy.
Other fish lineages, such as that leading to the extant temperate
ectothermic bonitos, must have adapted to tolerate a reduced
body temperature, whereas others, such as Carcharodon me-
galodon, eventually became extinct. It is hypothesized that en-
dothermy evolved in response to oceanic cooling during the
Eocene or possibly more recently during the Pliocene-Pleis-
tocene when the rate of cooling was more rapid (Fig. 2). En-
dothermy would have allowed these tropical-adapted fishes to
expand their thermal niche into cooler waters to take advantage
of the highly productive regions developing in higher latitudes
and in areas of coastal upwelling. This was likely an important
selective force for these large, active predators because they
require high energy inputs to support maintenance and con-
tinuous swimming and also to grow rapidly and for repro-
duction. Selection for a high fecundity may also have been a
key factor in the evolution of these lineages and would have
been dependent on abundant forage. In addition, the ability to
migrate long distances would have allowed these fishes to take
advantage of seasonally variable regions of high productivity in
upwelling zones and to move to warm-water spawning sites.
The Thermal Niche of Extant Endothermic Fishes. If niche ex-
pansion was an important selective force in the evolution of
endothermy from ectothermic ancestors, one would expect a
relationship between the thermal niche of present-day fish spe-
cies and their adaptations for endothermy. Major advances in
our knowledge of how several endothermic fish species utilize
the oceanic environment has come from the use of acoustic
telemetry and archival (data-logging) tags (Carey and Lawson
1973; Carey 1990; Gunn and Block 2001; Boustany et al. 2002;
Brill et al. 2002). With those data, positive correlationsbetween
the extent of endothermic adaptations and the limits of the
thermal niche in extant species are evident. For example, among
billfish species, there is a correlation between mass of the heater
tissue and how much time is spent in cold water (Carey 1982;
Block 1990, 1991). Swordfish have a larger mass of heater tissue
than do blue marlin of the same size, and acoustic telemetry
data show that swordfish make extensive dives below the ther-
mocline, remaining at depths of 500–600 m in water temper-
atures below 10⬚C for up to 12 h, whereas blue marlin spend
most of the time in the warm mixed layer above the thermocline
(Block 1986, 1991; Carey 1990; Block et al. 1992). Furthermore,
swordfish have medially positioned RM that is perfused by a
small lateral rete, whereas RM in the istiophorid billfishes is
adjacent to the skin and is not served by a rete (Carey 1990;
Block 1991; Dickson 1994). Among the lamnid sharks, Carey
et al. (1985) determined that Lamna ditropis Hubbs and Follett
and Lamna nasus (Bonnaterre) had the greatest degree of mor-
phological adaptations for endothermy, and those species in-
habit the highest latitudes and coolest waters (Compagno
1984). The longfin mako, the lamnid species with the least
developed endothermic characteristics, inhabits the warmest
waters (Compagno 1984; Carey et al. 1985).
Among tunas, the species capable of elevating the temper-
ature of RM, eye and brain, and viscera (bigeye, albacore, and
bluefin) are able to forage in cool waters at higher latitudes or
greater depths (Holland et al. 1992; Laurs and Lynn 1993; Da-
gorn et al. 2000; Block et al. 2001; Gunn and Block 2001; Brill
et al. 2002; Schaefer and Fuller 2002; Musyl et al. 2003). Other
tuna species (e.g., skipjack and yellowfin), even those that grow
to a very large size, have a more restricted thermal range (Bark-
ley et al. 1978; Brill et al. 1999). This relationship is evident,
for example, in 1970s Japanese longline catch data for four
tuna species in the tropical central Pacific Ocean summarized
by Sharp (2001). The peak catches of skipjack were near the
surface; yellowfin catches peaked at depths of 125 m, followed
by albacore at 200 m, whereas bigeye were caught in the deepest
waters fished by the longlines. Although all four species main-
tain elevated temperatures in the RM, eye, and brain, albacore
and bigeye can also elevate visceral temperatures, thereby keep-
ing a greater proportion of the body warm and allowing better
modulation of temperature changes during deep diving. Thus,
the vertically stratified distributions of tuna species correlate
with their endothermic capacities.
The results of a number of tagging studies indicate that hor-
izontal movement patterns of endothermic fishes are linked to
exploitation of food resources. For example, Atlantic northern
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1007
bluefin tuna follow the Gulf Stream and migrate to productive
waters of the north Atlantic (Block et al. 2001; Gunn and Block
2001), and albacore tuna are associated with highly productive
oceanic fronts in the north Pacific (Laurs et al. 1977; Laurs and
Lynn 1993). There is also evidence that vertical movements by
endothermic fishes below the thermocline are associated with
feeding. For example, by overlaying acoustic telemetry tracks
of a swordfish with the position of the deep scattering layer,
Carey (1990) found that individual swordfish were apparently
following vertically migrating prey within the deep scattering
layer. Gunn and Block (2001) presented archival tag data show-
ing vertical movements of southern bluefin tuna associated with
feeding. Brill et al. (2002) found that movements of the Atlantic
northern bluefin tuna were more closely associated with zones
of productivity than with water temperature or oxygen levels.
And several studies of bigeye tuna in the Pacific have linked
deep diving behavior to feeding on prey within the deep scat-
tering layer (Dagorn et al. 2000; Schaefer and Fuller 2002; Musyl
et al. 2003). These data support the hypothesis that expanding
the thermal niche provides access to key food resources.
Other Adaptations for Diving into Deep Waters. Although this
review focuses on how endothermy may be linked to niche
expansion, the ability to expand the thermal niche vertically
into cool waters below the thermocline almost certainly requires
additional adaptations (e.g., see Brill et al. 1999; Lowe et al.
2000; Blank et al. 2004). Repeated diving below the thermocline
subjects tissues that are not served by retia, including the heart,
to rapid changes in temperature and requires that tissue func-
tion be maintained for considerable periods at low tempera-
tures. In addition, fish experience rapid changes in hydrostatic
pressure, light level, and oxygen concentration during dives,
and more energy may be expended in swimming up and down
within the water column. It may be that adaptations to these
other factors, rather than to temperature, are critical for niche
expansion into ocean depths and are what distinguish the en-
dothermic species capable of such diving behavior (e.g., bigeye,
bluefin, and albacore tunas and swordfish) from related en-
dothermic species that remain in the warmer mixed layer (Brill
et al. 1999; Blank et al. 2004). Less is known about such ad-
aptations, particularly from a comparative, phylogenetically
based perspective, although certain aspects of cardiovascular
physiology have been studied in different tuna species. Heart
rate and cardiac output decrease with temperature (Brill 1987;
Korsmeyer et al. 1997; Brill et al. 1999; Brill and Bushnell 2001;
Blank et al. 2003), and Brill et al. (1999) hypothesized that
temperature effects on cardiac function limit the thermal range
of at least some tuna species. In support of this idea, Blank et
al. (2002, 2003) showed that cardiac output in isolated perfused
hearts of Pacific northern bluefin tuna was less temperature
sensitive than that of yellowfin tuna, and bluefin hearts main-
tained function at temperatures as low as 2⬚C. On the other
hand, there were no interspecific differences that correlate with
the extent of the thermal niche in the temperature sensitivity
of cardiac enzymes in bigeye compared with yellowfin andskip-
jack tunas (Swimmer et al. 2001). In the Pacific Ocean, bigeye
tuna routinely experience hypoxia (∼1mLO
2
L
⫺1
) when diving;
this species is more tolerant of hypoxia than are yellowfin and
skipjack tuna, and its hemoglobin-oxygen binding affinity is
greater than that measured in kawakawa, skipjack, and yellowfin
tunas (Lowe et al. 2000). The distributions of skipjack and
yellowfin tunas are limited by water oxygen content, as well as
temperature (reviewed in Brill 1994). Future efforts should be
directed at understanding these and other adaptations that have
allowed some endothermic species to repetitively dive into
deeper waters to exploit rich food resources.
Limitations of the Thermal Niche Expansion Hypothesis. A lim-
itation of the thermal niche expansion hypothesis is that it is
difficult to test the hypothesis that endothermy was actually
required for niche expansion. Several extant ectothermic species
have extensive thermal ranges and also move vertically within
the water column. For example, the ectothermic blue shark,
Prionace glauca (Linneaus), encounters water temperature
changes of up to 9⬚C within less than 1 h while diving through
the thermocline (Carey and Scharold 1990). During those dives,
the change in muscle temperature was less than that of the
water (due to thermal inertia) but was greater than that mea-
sured in tunas experiencing similar ambient temperature
changes (Carey and Lawson 1973; Holland et al. 1992; Marcinek
et al. 2001a). In addition, the ectothermic eastern Pacific bo-
nito, Sarda chiliensis (Cuvier), which is hypothesized to have
shared a common ancestor with the tunas, has an antitropical
distribution, inhabiting temperate waters of the north and
south Pacific Ocean (Collette and Chao 1975). These examples
show that, at least for some species, it is not necessary to be
endothermic to expand into cooler water. Furthermore, ad-
aptations to rapid changes in hydrostatic pressure, light level,
and oxygen concentration, which change with depth, not just
endothermy, are most likely required for expanding the thermal
niche vertically.
There are also inconsistencies in correlating the distributions
(thermal niches) of extant species with the capacity for en-
dothermy. For example, Allothunnus fallai, the most basal tuna,
possesses minimal structural adaptations for endothermy
(anterior-medial RM perfused with a small central rete) but
inhabits the cool surface waters of the Southern Ocean (Nak-
amura and Mori 1966; Collette and Nauen 1983; Graham and
Dickson 2000). Likewise, the butterfly mackerel Gasterochisma
melampus Richardson, which warms only the eye and brain, is
also found in the Southern Ocean (Collette and Nauen 1983).
These species are able to inhabit cool waters with a minimum
of endothermic adaptations. Nevertheless, despite these limi-
tations, niche expansion remains a reasonable explanation for
the convergent evolution of endothermy in the different fish
lineages.
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1008 K. A. Dickson and J. B. Graham
Increasing Sustainable Swimming Performance Hypothesis
Elevation of RM temperature is widespread among the fishes
that are endothermic (Table 1) and has evolved by convergence
at least twice (in tunas and lamnid sharks) and possibly two
or three additional times (in swordfish, thresher sharks, and
manta rays). In all of these fishes except the manta rays, the
slow-twitch, oxidative myotomal muscle fibers are not located
laterally, just beneath the skin, as they are in ectothermic species
(Table 2), but are in a more medial and anterior position,within
the myotomal cones (Kishinouye 1923; Carey et al. 1985; Carey
1990; Westneat et al. 1993; Graham and Dickson 2000, Bernal
et al. 2001a, 2003a). This placement reduces heat loss from the
RM by conduction across the body surface to the water. More
important, convective heat loss from the RM is reduced because
in all species with anterior-medial RM, the tissue is perfused
by arterioles and venules arranged as countercurrent heat ex-
changers (Carey et al. 1971, 1985; Graham 1973, 1975; Bone
and Chubb 1983; Carey 1990; Block 1991; Dickson 1994; Bernal
et al. 2001a). The convergent evolution of this trait suggests
that there is an important selective advantage of elevating RM
temperature; therefore, this hypothesis focuses on the function
of the slow-twitch, oxidative myotomal muscle fibers in pow-
ering sustained swimming. Recent work on ectothermic scom-
brids (mackerels and bonitos) and comparisons with data for
similar-sized tunas have for the first time allowed appropriate
phylogenetically based tests of this hypothesis.
Increasing Sustainable Swimming Speed. Indirect support for the
hypothesis that endothermy enhances sustainable swimming
performance comes from studies of ectothermic fish species
that show an increase in maximum sustainable swimmingspeed
with an increase in water temperature and therefore muscle
temperature (Rome et al. 1984; Sisson and Sidell 1987; Kieffer
et al. 1998). In the chub mackerel, Scomber japonicus Houttuyn,
maximum sustainable speed increased by 30% with a 6⬚Cin-
crease in temperature (Dickson et al. 2002). Additional support
is provided by studies demonstrating an increase with tem-
perature in contraction velocity and power output of isolated
tuna RM fibers (Johnston and Brill 1984; Altringham and Block
1997). However, when compared at physiological temperatures
and stimulation frequencies, power output calculated for yel-
lowfin tuna RM is similar to or less than that of the eastern
Pacific bonito. Using tailbeat frequencies recorded for yellowfin
tuna (3.8 Hz) and the eastern Pacific bonito (3.0 Hz) swimming
at similar sustainable speeds (130 cm s
⫺1
) in a swimming tunnel
respirometer (Dewar and Graham 1994a, 1994b; Dowis et al.
2003), estimates of RM temperatures for these fishes (26⬚–27⬚C
for the yellowfin and 18⬚C for the bonito; Dewar et al. 1994;
Dowis et al. 2003), and the data of Altringham and Block
(1997), power output was estimated to be 7 W kg
⫺1
in the
yellowfin and 9 W kg
⫺1
in the bonito. When the greater amount
of RM in the yellowfin relative to the bonito (7.4% of fish mass
vs. 6.2% [Magnuson 1973]; 6.5% vs. 4.5% [Graham et al. 1983];
6.1% vs. 5.3% [Freund 1999]) is taken into account, the total
power output in comparably sized individuals of the two species
would be similar. (Although Syme and Shadwick [2002] re-
cently reported much greater power production by skipjack
tuna RM when stimulated under in vivo conditions at 25⬚C
[approximately 40 W kg
⫺1
], they attribute the difference be-
tween their values and those of Altringham and Block [1997]
to how they determined the mass of viable muscle in the muscle
fiber bundles tested. Therefore, assuming that the values for
both yellowfin and bonito are affected similarly, this difference
in absolute power would not affect the conclusion of the in-
terspecific comparison.) Although the elevated RM temperature
in the yellowfin tuna increases power output relative to what
it would be at a lower temperature, the tuna’s RM poweroutput
is not higher than in the cooler RM of its ectothermic sister
species, making it difficult to argue that an increase in power
played a role in the selection for RM endothermy.
To test the hypothesis that RM endothermy evolved to en-
hance sustainable swimming performance directly, it is nec-
essary to compare the swimming performance of endothermic
species with that of their closest ectothermic relatives and to
control for fish size and water temperature. These comparisons
have been made under controlled conditions in swimming tun-
nel respirometers but have been difficult to accomplish because
of limits on the availability of similar-sized, closely related en-
dothermic and ectothermic fishes; on capturing, transporting,
and maintaining these active pelagic fishes in good physiological
condition; and on the size of variable-speed swimming tunnels
available for such studies. As a result, only small individuals,
with modest RM temperature elevations (approximately 1⬚–
3⬚C above water temperature), have been studied, and virtually
all such investigations have been done on scombrids. Despite
these limitations, maximal sustainable speed has been quan-
tified in tunas using standard procedures in which velocity is
increased until the fish can no longer maintain position in a
swimming tunnel. No significant difference was detected in
maximal sustainable speed between juvenile kawakawa tuna
and chub mackerel of comparable sizes at 24⬚C (Sepulveda and
Dickson 2000). In addition, the highest speed recorded for
skipjack, kawakawa, and yellowfin tunas (110–140 cm s
⫺1
)did
not differ from that of eastern Pacific bonito (120–130 cm s
⫺1
)
of similar sizes (approximately 40–56-cm fork length) studied
in the same water tunnel (Dewar and Graham 1994a, 1994b;
Knower et al. 1999; Dowis et al. 2003; Sepulveda et al. 2003).
Experiments like these in swimming tunnels involve unknown
levels of fish stress, but it is the only method presently available
to determine whether endothermy extends the aerobic swim-
ming performance limits of tunas.
An increase in sustainable swimming performance as a result
of RM endothermy would also be supported if endothermic
species typically swim at higher sustained speeds in their oce-
anic habitat. Two studies (Carey and Scharold 1990; Block et
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1009
al. 1992) have used acoustic telemetry and a speedometertrans-
mitter to measure volitional swimming speeds in undisturbed,
free-swimming fishes, but they tracked blue shark and blue
marlin, respectively, two species that do not elevate RM tem-
peratures. Volitional swimming speeds have also been calculated
as distance over time from fish positions recorded by telemetry
and archival tags (Laurs et al. 1977; Brill et al. 1999; Marcinek
et al. 2001a; Schaefer and Fuller 2002). The highest sustained
speeds range from 150 to 225 cm s
⫺1
, with mean speeds of 30–
160 cm s
⫺1
(reviewed by Magnuson 1978; Block et al. 1992;
Brill et al. 1999). Although the data are limited, the volitional
speeds of endothermic species are not greater than those of
ectothermic fishes of similar sizes. Apparently, whether endo-
thermic or ectothermic, large pelagic fishes routinely swim at
moderate speeds, possibly to reduce transport costs (reviewed
in Block et al. 1992). Therefore, on the basis of the limited data
available, it is not possible to conclude that RM endothermy
increases aerobic swimming speeds in tunas or any other en-
dothermic species.
Increasing Swimming Efficiency. Rather than an increase in sus-
tainable speed, it may be that endothermy enhances swimming
efficiency, for example, by allowing RM fibers to operate closer
to the frequency at which force, power, or work is maximal.
Refuting this hypothesis is the recent finding that the energetic
cost of swimming in tunas is not less than that of their ecto-
thermic relatives, despite using a swimming mode with less
lateral undulation (Table 2) that is theoretically more efficient
(Donley and Dickson 2000; Ellerby et al. 2000; Sepulveda and
Dickson 2000; Altringham and Shadwick 2001; Korsmeyer and
Dewar 2001; Dowis et al. 2003; Sepulveda et al. 2003). The
total energetic cost of swimming at sustainable speeds was
higher in yellowfin and kawakawa tunas than in size-matched
eastern Pacific bonito and chub mackerel, due to a higher stan-
dard metabolic rate (SMR) in the tunas; the net cost of trans-
port (the total metabolic rate at a given speed minus SMR, or
the incremental cost of swimming) was similar in tunas and
ectothermic scombrids (Sepulveda and Dickson 2000; Kors-
meyer and Dewar 2001; Sepulveda et al. 2003). Therefore, the
idea that the anterior-medial position of the RM evolved before
RM endothermy due to selection for increased swimming ef-
ficiency (Graham and Dickson 2000) is not supported by the
available energetics data, although there may be a mechanical
benefit of anterior-medial position of the endothermic RM
(Westneat et al. 1993; Graham and Dickson 2000; Westneat and
Wainwright 2001; Katz et al. 2001; Katz 2002; Donley et al.
2004). Tunas do have higher optimal swimming speeds (the
speed at which the total cost of transport is a minimum; Videler
1993; Dewar and Graham 1994a; Korsmeyer and Dewar 2001;
Sepulveda et al. 2003). If fishes routinely swim at their optimal
speed, as has been suggested (Videler 1993; Korsmeyer and
Dewar 2001), then RM endothermy would be associated with
higher routine swimming speeds, which may be advantageous
for the long-distance movements characteristic of endothermic
fishes. However, the total energetic cost would be greater than
that of an ectothermic fish of the same size swimming at the
same speed.
Recently, Katz (2002) argued that tunas have adopted an
effective strategy, rather than an efficient one, in which selection
for a greater amount of RM and a higher aerobic capacity
resulted in increased endurance at speeds that allow tunas to
overtake their prey. Unfortunately, there are no studies of en-
durance in tunas or their ectothermic relatives to test this idea.
Furthermore, selection for a greater amount of RM in tunas is
not supported by mapping the relative amount of RM onto a
phylogeny of scombrid fishes (Graham and Dickson 2000,
2001).
The literature contains many references to the remarkable
swimming speeds of tunas, but recent comparisons with
similar-sized mackerels and bonitos reveal no differences be-
tween speeds achieved by tunas and closely related ectothermic
fishes. Phylogenetic comparisons of tunas with their ecto-
thermic sister groups have provided no empirical evidence of
enhanced sustainable swimming performance associated with
endothermy. Although the tests that have been doneare limited,
all comparative studies have found aerobic muscle and swim-
ming performance to be similar in tunas and ectothermic scom-
brids, despite the unusual characteristics of tunas. Thus, there
is no support for the hypothesis that selection for enhancement
of aerobic swimming performance was associated with the evo-
lution of RM endothermy. Future studies of larger individuals
and those with greater temperature elevations, careful quan-
tification of fish swimming performance in the wild, compar-
isons of endurance in tunas and their ectothermic relatives,and
investigations of other endothermic groups are needed to test
this hypothesis more rigorously.
Consequences and Costs of Endothermy
In species with specialized heater tissues to warm the eye and
brain, it is clear that there is an energetic cost associated with
thermogenesis, as the primary function of the tissue is to pro-
duce heat for cranial endothermy. On the basis of oxygen con-
sumption rates at 20⬚C of mitochondria isolated from swordfish
heater tissues, maximum heat production rates have been cal-
culated to be up to 81 W kg
⫺1
when oxidizing palmitate and
365 W kg
⫺1
when oxidizing glucose (Ballantyne et al. 1992).
These rates of heat production are more than enough to main-
tain the measured temperature gradients between the heater
tissue and the ambient water (Carey 1990; Block 1991). This
energetic cost represents an unknown proportion of the total
energy expenditure of billfishes, but the heater tissue is only
approximately 0.042% of body mass in swordfish and 0.015%–
0.020% in istiophorids (calculated from data in Carey 1982;
Block 1986).
In the species that conserve heat that is produced by met-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1010 K. A. Dickson and J. B. Graham
Figure 3. Mass-specific standard metabolic rate (SMR) at 24⬚C versus
fish mass data that show that the SMR of tunas is greater than that
of their ectothermic relatives. Values are . Open symbolsmeans ⫹SD
are tunas ( , Thunnus albacares;squares pyellowfin circle p
,Euthynnus affinis;,Katsuwonus pelamis);kawakawa triangle pskipjack
solid symbols are ectothermic scombrids ( mackerel,circle pchub
Scomber japonicus, and Pacific bonito, Sarda chi-diamond peastern
liensis). SMR values were estimated from the Y-intercepts of log oxygen
consumption versus swimming velocity curves for scombrid fishes in
swimming tunnels (Dewar and Graham 1994a; Sepulveda and Dickson
2000; Sepulveda et al. 2003).
abolic processes within tissues not specifically modified for
thermogenesis (i.e., the viscera and RM), there need not be an
energetic cost of endothermy other than the Q
10
effect on me-
tabolism in the endothermic tissues. However, in tunas, SMR
is higher than it is in related ectothermic fishes (Table 2; Fig.
3). The difference in SMR is larger than what would be pre-
dicted on the basis of only the Q
10
effect on the metabolic rate
of the endothermic tissue(s), implying that the high SMR is
not simply a result of thermal effects on tissue metabolism.
Much less is known about the swimming energetics of sharks,
but the limited data available (Table 2) indicate that the shortfin
mako has a higher SMR and higher metabolic rate while swim-
ming than has been measured in ectothermic sharks (reviewed
in Bernal et al. 2001a; Table 2).
In Figure 3, we compare SMR values from studies in which
the oxygen consumption rate ( o
2
) of tunas and ectothermic
˙
V
scombrids of similar size were measured in the same variable-
speed swimming tunnels at a range of speeds, and SMR was
calculated by extrapolating log o
2
versus swimming speed
˙
V
curves to zero speed. In tunas, SMR has also been measured
in tunas treated with a neuromuscular blocking agent, and the
values obtained are very similar to those estimated for the same
species by extrapolation (Brill 1979, 1987; Dewar and Graham
1994a; Sepulveda et al. 2003), but there are no comparable data
for ectothermic scombrids. The SMR at 24⬚C is higher in yel-
lowfin, skipjack, and kawakawa tunas than in similar-sized ec-
tothermic eastern Pacific bonito and chub mackerel (Dewar
and Graham 1994a; Sepulveda and Dickson 2000; Sepulveda
et al. 2003). The difference in SMR between the juvenile chub
mackerel and kawakawa and yellowfin tunas of similar size is
more than fivefold, and the SMR of the yellowfin tuna is ap-
proximately twice that of the bonito (Fig. 3). These large dif-
ferences cannot be explained by the Q
10
effect because RM
temperatures were elevated at most only 2⬚–3⬚C above water
temperature in the tunas (Dewar et al. 1994; Sepulveda and
Dickson 2000).
The SMR of the bonito is closer to that of similar-sized tunas
than is the mackerel SMR (Fig. 3), suggesting that it may be
intermediate between that of mackerels and tunas. This finding
would support the hypothesis that an elevated SMR was a pre-
cursor to the evolution of endothermy. However, at comparable
sizes, the SMRs of other active ectothermic fishes, such as
salmon and yellowtail, are similar to that of the bonito (re-
viewed in Sepulveda et al. 2003). Furthermore, if the bonito
SMR is added to a compilation of data for SMR versus fish
mass in tunas, mackerels, and other active teleosts (Fig. 1 of
Korsmeyer and Dewar 2001), the bonito and mackerel points
fall on a line parallel to, but lower than, that for the tunas.
Thus, among the scombrid fishes that have been studied, only
the tunas have unusually high SMR values.
Why Do Tunas Have Such High SMRs? High SMRs in tunas
could be a consequence of endothermy or a result of the high
aerobic capacity and aerobic performance of tunas, indepen-
dent of endothermy. Bushnell and Brill (1991) argued thattunas
have a high aerobic scope to allow them to simultaneously
perform several activities—swimming, recovering from anaer-
obic bursts, food processing, growth, and reproduction—all of
which require aerobic metabolism and are not necessarily as-
sociated with endothermy. The high SMR of tunas would then
be a consequence of the need to maintain the structural and
functional characteristics, such as a large heart, large respiratory
surface, large intestinal surface area for digestion and absorp-
tion, and fast-glycolytic muscle with a higher aerobic capacity,
that are necessary to achieve a high aerobic scope and maxi-
mum metabolic rate (Bushnell and Brill 1991; Korsmeyer et al.
1996; Korsmeyer and Dewar 2001). Tunas are known to have
high somatic and gonadal growth rates (reviewed in Brill 1996),
as well as rapid somatic growth as juveniles (Dickson et al.
2000), but how much this contributes to a high SMR is
unknown.
To test whether high osmoregulatory costs are associated with
the large and thin gill surface in tunas, Brill et al. (2001) mea-
sured Na
⫹
K
⫹
ATPase activities in the gills and intestine of yel-
lowfin and skipjack tunas as a way to quantify the maximum
cost of osmoregulation. Surprisingly, they found that enzyme
activities (per g tissue or per mg protein) were not significantly
higher in the tunas compared with ectothermic fishes. Fur-
thermore, maximum rates of oxygen consumption for osmo-
regulation, calculated from total Na
⫹
K
⫹
ATPase activity in gill
and intestine, accounted for only 9% and 13% of SMR in 1-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1011
kg skipjack and yellowfin tunas, respectively (Brill et al. 2001).
Those percentages are lower than values measured for tilapia
in the same study and are within the range of estimated os-
moregulation costs for other ectothermic fishes. Brill et al.
(2001) also noted that cardiac energy demand in tunas is 2%–
10% of SMR, similar to the proportion in salmonids. Prelim-
inary data show that digestive enzyme activities of albacore,
yellowfin, and skipjack tunas do not differ significantly from
those in chub mackerel and eastern Pacific bonito (D. Neu-
mann, P. McIntosh-Gihbsson, and K. Dickson, unpublished
observations). Thus, comparisons of enzymatic activities of gill
and visceral tissues do not indicate why SMR is so high in
tunas.
If a high SMR (and concomitant greater heat production
rate) evolved independently of endothermy, then a higher SMR
may represent a “preadaptation” for endothermy. This idea is
supported by the suggestion that the SMR of the bonito is
intermediate relative to SMR of the chub mackerel and tunas,
but that remains to be substantiated in comparisons of similar-
sized mackerel, bonito, and tuna. If the bonito is intermediate
between mackerels and tunas, then other aerobic capacity in-
dicators in the bonito should be higher than in mackerels but
lower than in tunas. This pattern is found for gill surface area
(Gray 1954; Muir and Hughes 1969; Hughes 1970) and RM
myoglobin concentration (reviewed in Dickson 1996) but not
for RM mitochondrial density (Mathieu-Costello et al. 1992;
Moyes et al. 1992; C. Porcu, S. Karl, and K. Dickson, unpub-
lished observations), blood hemoglobin concentration, RM, or
heart citrate synthase activities, or the relative mass of the heart,
caecal mass, liver, kidney, RM or fast-glycolytic myotomal mus-
cle (reviewed in Dickson 1996; Freund 1999; Graham and Dick-
son 2000).
At this time, we do not know whether the high SMR in tunas
is a consequence of endothermy or was a precursor to endo-
thermy or whether endothermy evolved before or after
anterior-medial RM. Mapping the characters of high SMR, en-
dothermy, anterior-medial RM, and thunniform locomotion
onto the scombrid phylogeny shows that all four co-occur after
the divergence of the tunas and bonitos (Fig. 1; Dowis et al.
2003; Sepulveda et al. 2003). More extensive studies of the
different tuna species and other bonitos are needed to deter-
mine what sequence of character state changes occurred so that
we can test specific hypotheses about the evolution of endo-
thermy in this group.
Summary
This article summarizes recent work on fish endothermy and
focuses on phylogenetically based comparisons of endothermic
fishes with their ectothermic relatives to identify characteristics
specifically associated with the evolution of endothermy. Dur-
ing the past decade, a great deal has been learned about swim-
ming performance in tunas and their relatives, takingadvantage
of the few laboratories in which these species can be held in
captivity. Maximal sustainable speeds, standard metabolic rates,
and energetics, kinematics, and muscle function during sus-
tainable swimming have been quantified in tunas and closely
related ectothermic species (mackerels and bonitos). Efforts
have also been directed at understanding the convergent char-
acteristics of lamnid sharks and tunas. Advances in tagging
technologies have begun to provide a detailed understanding
of how endothermic fishes utilize their environment, allowing
better integration of laboratory and field studies. Similar ar-
chival and acoustic tagging studies of related ectothermic spe-
cies will be needed for comparative studies.
We have focused on assessing the evidence for two hypoth-
eses to explain the convergent evolution of fish endothermy.
The niche expansion hypothesis is supported by several lines
of evidence but remains difficult to test unequivocally. Inter-
specific comparisons of tunas and their ectothermic sister taxa,
as well as more limited comparisons of lamnid sharks and active
ectothermic sharks, do not support the hypothesis that RM
endothermy enhances sustainable swimming performance. Al-
though the data are limited, maximum sustainable swimming
speeds, net cost of transport, and many indices of RM aerobic
capacity are similar in related endothermic and ectothermic
fishes. A benefit of RM endothermy may be an increase in
endurance at the speeds at which these fishes typical swim, but
endurance has not been measured in any endothermic fish
species. Standard metabolic rates are greater in endothermic
species compared with related ectothermic species, indicating
that endothermy is associated with significant energetic costs.
The best explanation for high SMRs in endothermic fishes is
that they result from maintenance of the adaptations needed
for the high aerobic capacities that support the many energet-
ically expensive processes that these large, continuously swim-
ming pelagic fishes must accomplish simultaneously. Therefore,
high SMRs may not be a direct consequence of endothermy.
Although significant advances have been made in the study
of endothermic fishes, many questions remain, and additional
work is needed to understand more completely why and how
endothermy evolved. Future studies of tunas with tissue tem-
peratures elevated at least 5⬚C above water temperature and of
tropical bonitos, as well as further investigations of other en-
dothermic fish groups, are needed. We also need better con-
sensus on the phylogenetic relationships among the groupsthat
include endothermic species, based on characters independent
of those related to endothermy, with which to trace the evo-
lutionary sequence of changes that led to endothermy. Although
modern molecular systematics methods have been applied to
these groups, there are many unresolved relationships, even for
the family Scombridae, which has been studied extensively (re-
viewed in Collette et al. 2001).
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1012 K. A. Dickson and J. B. Graham
Note Added in Proof
Bernal and Sepulveda (2005) measured red myotomal muscle
temperatures that were elevated above sea surface temperature
by up to 5.4⬚C ( of C) in the com-mean ⳲSEM 2.33⬚Ⳳ0.30⬚
mon thresher shark, Alopias vulpinus, captured by hook and
line and by longline. These data provide evidence for RM en-
dothermy in this species.
Acknowledgments
This article is based on a talk presented by K.A.D. at the Sixth
International Congress of Comparative Physiology and Bio-
chemistry at Mt. Buller, Australia. We thank Peter Frappell and
Pat Butler, the organizers of the symposium on Evolution and
Advantages of Endothermy, for the invitation to participate,
meeting participants for stimulating discussions, and California
State University Fullerton for financial support to attend the
meeting. Discussions with D. Bernal, H. Dewar, J. Donley, H.
Fierstine, K. Monsch, R. Shadwick, and C. Sepulveda contrib-
uted to the development of some of the ideas presented. We
thank K. Monsch for making unpublished data and manu-
scripts available and K. Monsch, H. Fierstine, and two anon-
ymous reviewers for their comments on earlier drafts of the
article.
Literature Cited
Alexander R.L. 1995. Evidence of a counter-current heat-
exchanger in the ray Mobula tarapacana (Chondrichthyes:
Elasmobranchii: Batoidea: Myliobatiformes). J Zool (Lond)
237:377–384.
———. 1996. Evidence of brain-warming in the mobulid rays,
Mobula tarapacana and Manta birostris (Chondrichthyes:
Elasmobranchii: Batoidea: Myliobatiformes). Zool J Linn Soc
118:151–164.
Altringham J.D. and B.A. Block. 1997. Why do tuna maintain
elevated slow muscle temperatures? power output of muscle
isolated from endothermic and ectothermic fish. J Exp Biol
200:2617–2627.
Altringham J.D. and R.E. Shadwick. 2001. Swimming and mus-
cle function. Pp. 313–344 in B.A. Block and E.D. Stevens,
eds. Tuna: Physiology, Ecology, and Evolution. Vol. 19. Fish
Physiology. Academic Press, San Diego, Calif.
Alvarado Bremer J.R., I. Naseri, and B. Ely. 1997. Orthodox
and unorthodox phylogenetic relationships among tunas re-
vealed by the nucleotide sequence analysis of the mitochon-
drial DNA control region. J Fish Biol 50:540–554.
Applegate S.P. and L. Espinosa-Arrubarrena. 1996. The fossil
history of Carcharodon and its possible ancestor, Cretolamna:
a study in tooth identification. Pp. 19–36 in A.P. Klimley
and D.G. Ainley, eds. Great White Sharks: The Biology of
Carcharodon carcharias. Academic Press, San Diego, Calif.
Ballantyne J.S., M.E. Chamberlin, and T.D. Singer. 1992. Ox-
idative metabolism in thermogenic tissues of the swordfish
and mako shark. J Exp Zool 261:110–114.
Bannikov A.F. 1985. Iskopaemye Skumbrievye SSSR (Fossil
Scombrids of the USSR). Nauka, Moscow.
Barkley R.A., W.H. Neill, and R.M. Gooding. 1978. Skipjack
tuna, Katsuwonus pelamis, habitat based on temperature and
oxygen requirements. Fish Bull US 76:653–662.
Barron J.A. and J.G. Baldauf. 1989. Tertiary cooling steps and
paleoproductivity as reflected by diatoms and biosiliceous
sediments. Pp. 341–354 in G.H. Berger, V.S. Smetacek, and
G. Wefer, eds. Productivity of the Oceans: Present and Past.
Wiley, New York.
Bennett A.F. and J.A. Ruben. 1979. Endothermy and activity
in vertebrates. Science 206:649–654.
Berger W. 1981. Paleoceanography: the deep sea record. Pp.
1437–1519 in C.C. Emiliani, ed. The Oceanic Lithosphere.
Vol. 7. The Sea. Wiley, New York.
Berger W.H., C.B. Lange, and G. Wefer. 2002. Upwelling history
of the Benguela-Namibia system: a synthesis of leg 175 re-
sults. Pp. 1–103 in G. Wefer, W.H. Berger, and C. Richter,
eds. Proceedings of the Ocean Drilling Program: Scientific
Results 175. Publication Ser vices Department, Ocean Drilling
Program Science Operator, Texas A&M University, College
Station. Available at http://www-odp.tamu.edu/publications/
175_SR/synth/synth.htm.
Berger W.H. and G. Wefer. 1996. Expeditions into the past:
paleoceanographic studies in the South Atlantic. Pp. 363–
410 in G. Wefer, W.H. Berger, G. Siedler, and D.J. Webb,
eds. The South Atlantic: Present and Past Circulation.
Springer, Berlin.
Berggren W.A. and D.R. Prothero. 1992. Eocene-Oligocene cli-
matic and biotic evolution: an overview. Pp. 1–28 in W.A.
Berggren and D.R. Prothero, eds. Eocene-Oligocene Climatic
and Biotic Evolution. Princeton University Press, Princeton,
N.J.
Bernal D., K.A. Dickson, R.E. Shadwick, and J.B. Graham.
2001a. Analysis of the evolutionary convergence for high
performance swimming in lamnid sharks and tunas. Comp
Biochem Physiol 129A:695–726.
Bernal D., C. Sepulveda, and J.B. Graham. 2001b. Water-tunnel
studies of heat balance in swimming mako sharks. J Exp Biol
204:4043–4054.
Bernal D., C. Sepulveda, O. Mathieu-Costello, and J.B. Graham.
2003a. Comparative studies of high performance swimming
in sharks. I. Red muscle morphometrics, vascularization,and
ultrastructure. J Exp Biol 206:2831–2843.
Bernal D. and C.A. Sepulveda. 2005. Evidence for temperature
elevation in the aerobic swimming musculature of the com-
mon thresher shark, Alopias vulpinus. Copeia (in press).
Bernal D., D. Smith, G. Lopez, D. Weitz, T. Grimminger, K.
Dickson, and J.B. Graham. 2003b. Comparative studies of
high performance swimming in sharks. II. Metabolic bio-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1013
chemistry of locomotor and myocardial muscle in endo-
thermic and ectothermic sharks. J Exp Biol 206:2845–2857.
Berta A. and P.J. Adam. 2001. Evolutionary biology of pinni-
peds. Pp. 235–260 in J. Mazin and V. de Buffre´ nil, eds. Sec-
ondary Adaptation of Tetrapods to Life in Water. Pfeil,
Munich.
Bice K.L. and J. Marotzke. 2001. Numerical evidence against a
reversed thermohaline circulation in the warm Paleocene/
Eocene ocean. J Geophys Res 106:11529–11542.
Blank J.M., J.M. Morrissette, P.S. Davie, and B.A. Block. 2002.
Effects of temperature, epinephrine and Ca
2⫹
on the hearts
of yellowfin tuna (Thunnus albacares). J Exp Biol 205:1881–
1888.
Blank J.M., J.M. Morrissette, A.M. Landeira-Fernandez, S.B.
Blackwell, T.D. Williams, and B.A. Block. 2003. In situ car-
diac performance of Pacific bluefin tuna hearts in response
to acute temperature change. J Exp Biol 207:881–890.
———. 2004. In situ cardiac performance of Pacific bluefin
tuna hearts in response to acute temperature change. J Exp
Biol 207:881–890.
Block B.A. 1986. Structure of the brain and eye heater tissue
in marlins, sailfish, and spearfishes. J Morphol 190:169–189.
———. 1987a. Billfish brain and eye heater: a new look at
nonshivering heat production. News Physiol Sci 2:208–213.
———. 1987b. Strategies for regulating brain and eye tem-
peratures: a thermogenic tissue in fish. Pp. 401–420 in P.
Dejours, L. Bolis, C.R. Taylor, and E.R. Weibel, eds. Com-
parative Physiology: Life in the Water and on Land. Liviana,
Padova.
———. 1990. Physiology and ecology of brain and eye heaters
in billfishes. Pp. 123–136 in R.H. Stroud, ed. Planning the
Future of Billfishes. National Coalition for Marine Preser-
vation, Savannah, Ga.
———. 1991. Endothermy in fish: thermogenesis, ecology, and
evolution. Pp. 269–311 in P.W. Hochachka and T.P. Momm-
sen, eds. Biochemistry and Molecular Biology of Fishes. Vol.
1. Elsevier, New York.
———. 1994. Thermogenesis in muscle. Annu Rev Physiol 56:
535–577.
Block B.A., D. Booth, and F.G. Carey.1992. Direct measurement
of swimming speeds and depth of blue marlin. J Exp Biol
166:267–284.
Block B.A. and F.G. Carey. 1985. Warm brain and eye tem-
peratures in sharks. J Comp Physiol B 156:229–236.
Block B.A., H. Dewar, S.B. Blackwell, T.D. Williams, E.D.
Prince, C.J. Farwell, A. Boustany, et al. 2001. Migratory
movements, depth preferences, and thermal biology of At-
lantic bluefin tuna. Science 293:1310–1314.
Block B.A. and J.R. Finnerty. 1994. Endothermic strategies in
fishes: a phylogenetic analysis of constraints, predispositions,
and selection pressures. Environ Biol Fishes 40:283–302.
Block B., J.R. Finnerty, A.F.R. Stewart, and J. Kidd. 1993. Evo-
lution of endothermy in fish: mapping physiological traits
on a molecular phylogeny. Science 260:210–214.
Block B.A. and E.D. Stevens, eds. 2001. Tuna: Physiology, Ecol-
ogy, and Evolution. Vol. 19. Fish Physiology. Academic Press,
San Diego, Calif.
Bone Q. and A.D. Chubb. 1983. The retial system of the lo-
comotor muscle in the thresher shark. J Mar Biol Assoc UK
63:239–241.
Boustany A.M., S.F. Davis, P. Pyle, S.D. Anderson, B.J. LeBoeuf,
and B.A. Block. 2002. Expanded niche for white sharks. Na-
ture 415:35–36.
Brill R., M. Lutcavage, G. Metzger, P. Bushnell, M. Arendt, J.
Lucy, C. Watson, and D. Foley. 2002. Horizontal and vertical
movements of juvenile bluefin tuna (Thunnus thynnus), in
relation to oceanographic conditions of the western North
Atlantic, determined with ultrasonic telemetry. Fish Bull US
100:155–167.
Brill R.W. 1978. Temperature effects on speeds of muscle con-
traction and stasis metabolic rate. Pp. 277–283 in G.D. Sharp
and A.E. Dizon, eds. The Physiological Ecology of Tunas.
Academic Press, New York.
———. 1979. The effect of body size on the standard metabolic
rate of skipjack tuna, Katsuwonus pelamis. Fish Bull US 77:
494–498.
———. 1987. On the standard metabolic rates of tropicaltunas,
including the effect of body size and acute temperature
change. Fish Bull US 85:25–36.
———. 1994. A review of temperature and oxygen tolerance
studies of tunas pertinent to fisheries oceanography, move-
ment models and stock assessments. Fish Oceanogr 3:204–
216.
———. 1996. Selective advantages conferred by the high per-
formance physiology of tunas, billfishes, and dolphin fish.
Comp Biochem Physiol 113A:3–15.
Brill R.W., B.A. Block, C.H. Boggs, K.A. Bigelow, E.V. Freund,
and D.J. Marcinek. 1999. Horizontal movements and depth
distribution of large adult yellowfin tuna, Thunnus albacares,
near the Hawaiian Islands, recorded using ultrasonic telem-
etry: implications for the physiological ecology of pelagic
fishes. Mar Biol 133:395–408.
Brill R.W. and P.G. Bushnell. 2001. The cardiovascular system
of tunas. Pp. 79–120 in B.A. Block and E.D. Stevens, eds.
Tuna: Physiology, Ecology, and Evolution. Vol. 19. Fish Phys-
iology. Academic Press, San Diego, Calif.
Brill R.W., H. Dewar, and J B. Graham. 1994. Basic concepts
relevant to heat transfer in fishes, and their use in measuring
the physiological thermoregulatory abilities of tunas. Environ
Biol Fishes 40:109–124.
Brill R.W., Y. Swimmer, C. Taxboel, K. Cousins, and T. Lowe.
2001. Gill and intestinal Na
⫹
-K
⫹
ATPase activity, and esti-
mated maximal osmoregulatory costs, in three high-energy-
demand teleosts: yellowfin tuna (Thunnus albacares), skip-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1014 K. A. Dickson and J. B. Graham
jack tuna (Katsuwonus pelamis), and dolphin fish
(Coryphaena hippurus). Mar Biol 138:935–944.
Bushnell P.G. and R.W. Brill. 1991. Responses of swimming
skipjack (Katsuwonus pelamis) and yellowfin (Thunnus al-
bacares) tunas to acute hypoxia, and a model for their car-
diorespiratory function. Physiol Zool 64:787–811.
Bushnell P.G., D.R. Jones, and A.P. Farrell. 1992. The arterial
system. Pp. 89–139 in W. Hoar and D. Randall, eds. Fish
Physiology. Vol. 12. Pt. A. The Cardiovascular System. Ac-
ademic Press, New York.
Carey F.G. 1982. A brain heater in the swordfish. Science 216:
1327–1329.
———. 1990. Further acoustic telemetry observations of
swordfish. Pp. 103–131 in R.H. Stroud, ed. Planning the
Future of Billfishes. National Coalition for Marine Preser-
vation, Savannah, Ga.
Carey F.G., J.G. Casey, H.L. Pratt, D. Urquhart, and J.E.
McCosker. 1985. Temperature, heat production and heat
exchange in lamnid sharks. Mem South Calif Acad Sci 9:92–
108.
Carey F.G., J.W. Kanwisher, O. Brazier, G. Gabrielson, J.G.
Casey, and H.L. Pratt, Jr. 1982. Temperature and activities
of a white shark, Carcharodon carcharias. Copeia 1982:254–
260.
Carey F.G, J.W. Kanwisher, and E.D. Stevens. 1984. Bluefin tuna
warm their viscera during digestion. J Exp Biol 109:1–20.
Carey F.G. and K.D. Lawson. 1973. Temperature regulation in
free-swimming bluefin tuna. Comp Biochem Physiol 44A:
375–392.
Carey F.G. and J.V. Scharold. 1990. Movements of blue sharks
(Prionace glauca) in depth and course. Mar Biol 106:329–
342.
Carey F.G. and J.M. Teal. 1966. Heat conservation in tuna fish
muscle. Proc Natl Acad Sci USA 56:1464–1469.
———. 1969a. Mako and porbeagle: warm-bodied sharks.
Comp Biochem Physiol 28A:199–204.
———. 1969b. Regulation of body temperature by the bluefin
tuna. Comp Biochem Physiol 28A:205–213.
Carey F.G., J.M. Teal, and J.W. Kanwisher. 1981. The visceral
temperatures of mackerel sharks (Lamnidae). Physiol Zool
54:334–344.
Carey F.G., J.M. Teal, J.W. Kanwisher, K.D. Lawson, and K.S.
Beckett. 1971. Warm-bodied fish. Am Zool 11:137–145.
Carpenter K.E., B.B. Collette, and J.L. Russo. 1995. Unstable
and stable classifications of scombroid fishes. Bull Mar Sci
56:379–405.
Carroll R.L. 1988. Vertebrate Paleontology and Evolution. Free-
man, New York.
———. 1997. Patterns and Processes of Vertebrate Evolution.
Cambridge University Press, Cambridge.
Chow S. and H. Kishino. 1995. Phylogenetic relationships be-
tween tuna species of the genus Thunnus (Scomdridae: Tel-
eostei): inconsistent implications from morphology, nuclear
and mitochondrial genomes. J Mol Evol 41:741–748.
Collette B.B. 1978. Adaptations and systematics of the mack-
erels and tunas. Pp. 7–39 in G.D. Sharp and A.E. Dizon, eds.
The Physiological Ecology of Tunas. Academic Press, New
York.
Collette B.B. and L.N. Chao. 1975. Systematics and morphology
of the bonitos (Sarda) and their relatives (Scombridae, Sar-
dini). Fish Bull US 73:516–625.
Collette B.B. and C.L. Nauen. 1983. Scombrids of the world:
an annotated and illustrated catalogue of tunas, mackerels,
bonitos, and related species known to date. FAO Species
Catalog. Vol. 2. Food and Agriculture Organization of the
United Nations, Rome.
Collette B.B., C. Reeb, and B.A. Block. 2001. Systematics of the
tunas and mackerels (Scombridae). Pp. 1–33 in B.A. Block
and E.D. Stevens, eds. Tuna: Physiology, Ecology, and Evo-
lution. Vol. 19. Fish Physiology. Academic Press, San Diego,
Calif.
Compagno L.J.V. 1984. Sharks of the world: an annotated and
illustrated catalogue of shark species known to date. FAO
Species Catalog. Vol. 4. Food and Agriculture Organization
of the United Nations, Rome.
Crompton A.W., C.R. Taylor, and J.A. Jagger. 1978. Evolution
of homeothermy in mammals. Nature 272:333–336.
Dagorn L., P. Bach, and E. Josse. 2000. Movement patterns of
large bigeye tuna (Thunnus obesus) in the open ocean, de-
termined using ultrasonic telemetry. Mar Biol 136:361–371.
Dewar H. and J.B. Graham. 1994a. Studies of tropical tuna
swimming performance in a large water tunnel. I. Energetics.
J Exp Biol 192:13–31.
———. 1994b. Studies of tropical tuna swimming performance
in a large water tunnel. III. Kinematics. J Exp Biol 192:45–
59.
Dewar H., J.B. Graham, and R.W. Brill. 1994. Studies of tropical
tuna swimming performance in a large water tunnel. II. Ther-
moregulation. J Exp Biol 192:33–44.
Dickson K.A. 1994. Tunas as small as 207 mm fork length can
elevate muscle temperatures significantly above ambient wa-
ter temperature. J Exp Biol 190:79–93.
———. 1995. Unique adaptations of the metabolic biochem-
istry of tunas and billfishes for life in the pelagic environ-
ment. Environ Biol Fishes 42:65–97.
———. 1996. Locomotor muscle of high-performance fishes:
what do comparisons of tunas with ectothermic sister taxa
reveal? Comp Biochem Physiol 113A:39–49.
Dickson K.A., J.M. Donley, C. Sepulveda, and L. Bhoopat. 2002.
Effects of temperature on sustained swimming performance
and swimming kinematics of the chub mackerel Scomber
japonicus. J Exp Biol 205:969–980.
Dickson K.A., M.O. Gregorio, S.J. Gruber, K.L. Loefler, M. Tran,
and C. Terrell. 1993. Biochemical indices of aerobic and an-
aerobic capacity in muscle tissues of California elasmobranch
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1015
fishes differing in typical activity level. Mar Biol 117:185–
193.
Dickson K.A., N.M. Johnson, J.M. Donley, J.A. Hoskinson,
M.W. Hansen, and J. D’Souza Tessier. 2000. Ontogenetic
changes in characteristics required for endothermy in ju-
venile black skipjack tuna (Euthynnus lineatus). J Exp Biol
203:3077–3087.
Dineley D.L and S.J. Metcalf. 1999. Fossil Fishes of Great Brit-
ain. Geological Conservation Review Series 16. Joint Nature
Conservation Committee, Peterborough.
Dizon A.E. and R.W. Brill. 1979. Thermoregulation in yellowfin
tuna, Thunnus albacares. Physiol Zool 52:581–593.
Donley J.M. and K.A. Dickson. 2000. Swimming kinematics of
juvenile kawakawa tuna, Euthynnus affinis, and chub mack-
erel, Scomber japonicus. J Exp Biol 203:3103–3116.
Donley J.M., C.A. Sepulveda, P. Konstantinidis, S. Gemballa,
and R.E. Shadwick. 2004. Convergent evolution in mechan-
ical design of lamnid sharks and tunas. Nature 429:61–65.
Donley J.M. and R.E. Shadwick. 2003. Steady swimming muscle
dynamics in the leopard shark Triakis semifasciata. J Exp Biol
206:1117–1126.
Dowis H., C.A. Sepulveda, J.B. Graham, and K.A. Dickson.
2003. Swimming performance studies on the eastern Pacific
bonito (Sarda chiliensis), a close relative of the tunas (family
Scombridae). II. Kinematics. J Exp Biol 206:2749–2758.
Ellerby D.J., J.D. Altringham, T. Williams, and B.A. Block. 2000.
Slow muscle function of Pacific bonito, Sarda chiliensis, dur-
ing steady swimming. J Exp Biol 203:2001–2013.
Fierstine H.L. 1990. A paleontological review of three billfish
families (Istiophoridae, Xiphiidae, and Xiphiorhynchidae).
Pp. 11–19 in R.H. Stroud, ed. Planning the Future of Bill-
fishes. National Coalition for Marine Preservation, Savannah,
Ga.
———. 2001. Analysis and new records of billfish (Teleostei:
Perciformes: Istiophoridae) from the Yorktown Formation,
early Pliocene of eastern North Carolina at Lee Creek Mine.
Pp. 21–69 in C.E. Ray and D.J. Bohaska, eds. Geology and
Paleontology of the Lee Creek Mine, North Carolina. III.
Smithsonian Contributions to Paleobiology 90. Smithsonian
Institution, Washington, D.C.
Fierstine H.L. and K.A. Monsch. 2002. Redescription and phy-
logenetic relationships of the family Blochiidae (Perciformes:
Scombroidei), middle Eocene, Monte Bolca, Italy. Miscel-
lanea Paleontologica, Studi e Ricerche sui Giacimenti Terziari
di Bolca, Museo Civico Storia Nat Verona 9:121–163.
Fierstine H.L. and V. Walters. 1968. Studies in locomotion and
anatomy of scombroid fishes. Mem South Calif Acad Sci 6:
1–31.
Finnerty J.R. and B.A. Block. 1995. Evolution of cytochrome
b in the Scombroidei (Teleostei): molecular insights into bill-
fish (Istiophoridae and Xiphiidae) relationships. Fish Bull
US 93:78–96.
Fordyce R.E. 1992. Cetacean evolution and Eocene/Oligocene
environments. Pp. 368–381 in W.A. Berggren and D.R.
Prothero, eds. Eocene-Oligocene Climatic and Biotic Evo-
lution. Princeton University Press, Princeton, N.J.
Fordyce R.E. and C. de Muizon. 2001. Evolutionary history of
the cetaceans: a review. Pp. 169–233 in J. Mazin and V. de
Buffre´nil, eds. Secondary Adaptation of Tetrapods to Life in
Water. Pfeil, Munich.
Franck J.P.C., J. Morrissette, J.E. Keen, R.L. Londraville, M.
Beamsley, and B.A. Block. 1998. Cloning and characterization
of fiber type-specific ryanodine receptor isoforms in skeletal
muscles of fish. Am J Physiol 275:C401–C415.
Freund E.V. 1999. Comparisons of Metabolic and Cardiac Per-
formance in Scombrid Fishes: Insights into the Evolution of
Endothermy. Ph.D. thesis. Stanford University, Stanford,
Calif.
Fudge D.S. and E.D. Stevens. 1996. The visceral retia mirabilia
of tuna and sharks: an annotated translation and discussion
of the Eschricht & Mu¨ller 1835 paper and related papers.
Guelph Ichthyol Rev 4:1–54.
Funakoshi S., K. Wada, and T. Suzuki. 1985. Development of
the rete mirabile with growth and muscle temperature in
young bluefin tuna. Bull Jpn Soc Sci Fish 51:1971–1975.
Goldman K.J. 1997. Regulation of body temperature in the
white shark, Carcharodon carcharias. J Comp Physiol 167:
423–429.
Gooding R.M., W.H. Neill, and A.E. Dizon. 1981. Respiration
rates and low-oxygen tolerance limits in skipjack tuna, Kat-
suwonus pelamis. Fish Bull US 79:31–48.
Graham J.B. 1973. Heat exchange in the black skipjack, and
the blood-gas relationship of warm-bodied fishes. Proc Natl
Acad Sci USA 70:1964–1967.
———. 1975. Heat exchange in the yellowfin tuna, Thunnus
albacares, and skipjack tuna, Katsuwonus pelamis, and the
adaptive significance of elevated body temperatures in scom-
brid fishes. Fish Bull US 73:219–229.
Graham J.B. and K.A. Dickson. 1981. Physiological thermo-
regulation in the albacore Thunnus alalunga. Physiol Zool
54:470–486.
———. 2000. The evolution of thunniform locomotion and
heat conservation in scombrid fishes: new insights based on
the morphology of Allothunnus fallai. Zool J Linn Soc 129:
419–466.
———. 2001. Laboratory investigations of tuna specializations
for endothermy. Pp. 121–165 in B.A. Block and E.D. Stevens,
eds. Tuna: Physiology, Ecology, and Evolution. Vol. 19. Fish
Physiology. Academic Press, San Diego, Calif.
Graham J.B. and D.R. Diener. 1978. Comparative morphology
of the central heat exchangers in the skipjacks Katsuwonus
and Euthynnus. Pp. 113–133 in G.D. Sharp and A.E. Dizon,
eds. The Physiological Ecology of Tunas. Academic Press,
New York.
Graham J.B., F.J. Koehrn, and K.A. Dickson. 1983. Distribution
and relative proportions of red muscle in scombrid fishes:
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1016 K. A. Dickson and J. B. Graham
consequences of body size and relationships to locomotion
and endothermy. Can J Zool 61:2087–2096.
Gray I.E. 1954. Comparative study of the gill area of marine
fishes. Biol Bull 107:219–225.
Gunn J. and B.A. Block. 2001. Advances in acoustic, archival,
and satellite tagging of tunas. Pp. 167–224 in B.A. Block and
E.D. Stevens, eds. Tuna: Physiology, Ecology, and Evolution.
Vol. 19. Fish Physiology. Academic Press, San Diego, Calif.
Holland K.N., R.W. Brill, R.K.C. Chang, J.R. Sibert, and D.A.
Fournier. 1992. Physiological and behavioral thermoregula-
tion in bigeye tuna (Thunnus obesus). Nature 358:410–412.
Hughes G.M. 1970. Morphological measurements on the gills
of fishes in relation to their respiratory function. Folia Mor-
phol 18:78–95.
Johnston I.A. and R. Brill. 1984. Thermal dependence of con-
tractile properties of single skinned muscle fibers from Ant-
arctic and various warm water marine fishes including skip-
jack tuna (Katsuwonus pelamis) and kawakawa (Euthynnus
affinis). J Comp Physiol B 155:63–70.
Joseph J., W. Klawe, and P. Murphy. 1988. Tuna and Billfish:
Fish without a Country. Inter-American Tropical Tuna Com-
mission, La Jolla, Calif.
Katz S.L. 2002. Design of heterothermic muscle in fish. J Exp
Biol 205:2251–2266.
Katz S.L., D.A. Syme, and R.E. Shadwick. 2001. Enhanced
power in yellowfin tuna. Nature 410:770–771.
Kieffer J.D., D. Alsop, and C.M. Wood. 1998. A respirometric
analysis of fuel use during aerobic swimming at different
temperatures in rainbow trout (Oncorhynchus mykiss). J Exp
Biol 201:3123–3133.
Kishinouye K. 1923. Contributions to the comparative study
of the so-called scombroid fishes. J Coll Agric Tokyo Imp
Univ 8:293–475.
Knower T., R.E. Shadwick, S.L. Katz, J.B. Graham, and C.S.
Wardle. 1999. Red muscle activation patterns in yellowfin
(Thunnus albacares) and skipjack (Katsuwonus pelamis) tunas
during steady swimming. J Exp Biol 202:2127–2138.
Korsmeyer K.E. and R.W. Brill. 2002. Active regulation of brain
temperature in yellowfin tuna. Theor Physiol 45:352.
Korsmeyer K.E. and H. Dewar. 2001. Tuna metabolism and
energetics. Pp. 35–78 in B.A. Block and E.D. Stevens, eds.
Tuna: Physiology, Ecology, and Evolution. Vol. 19. Fish Phys-
iology. Academic Press, San Diego, Calif.
Korsmeyer K.E., H. Dewar, N.C. Lai, and J.B. Graham. 1996.
The aerobic capacity of tunas: adaptation for multiple met-
abolic demands. Comp Biochem Physiol 113A:17–24.
Korsmeyer K.E., N.C. Lai, R.E. Shadwick, and J.B. Graham.
1997. Heart rate and stroke volume contributions to cardiac
output in swimming yellowfin: responses to exercise and
temperature. J Exp Biol 200:1975–1986.
Landini W. and L. Sorbini. 1996. Ecological and trophic rela-
tionships of Eocene of Monte Bolca (Pesciara) fish fauna.
Pp. 105–112 in A. Cherchi, ed. Autecology of Selected Fossil
Organisms: Achievements and Problems. Bollettino della So-
cieta` Paleontologica Italiana. Spec. Vol. 3. Mucchi, Modena.
Laurs R.M. and R.J. Lynn. 1993. North Pacific albacore ecology
and oceanography. NOAA Tech Rep 105:69–87.
Laurs R.M., H.S.H. Yuen, and J.H. Johnson. 1977. Small-scale
movements of albacore, Thunnus alalunga, in relation to
ocean features as indicated by ultrasonic tracking and ocean-
ographic sampling. Fish Bull US 75:347–357.
Lear C.H., H. Elderfield, and P.A. Wilson. 2000. Cenozoic deep-
sea temperatures and global ice volumes from Mg/Ca in
benthic foraminiferal calcite. Science 287:269–272.
Lindsey C.C. 1978. Form, function, and locomotory habits in
fish. Pp. 1–13 in W. Hoar and D. Randall, eds. Fish Physi-
ology. Vol. 7. Academic Press, New York.
Linthicum D.S. and F.G. Carey. 1972. Regulation of brain and
eye temperatures by the bluefin tuna. Comp Biochem Physiol
43A:425–433.
Lowe T.E., R.W. Brill, and K.L. Cousins. 2000. Blood oxygen–
binding characteristics of bigeye tuna (Thunnus obesus), a
high-energy-demand teleost that is tolerant of low ambient
oxygen. Mar Biol 136:1087–1098.
Lydeard C. and K.J. Roe. 1997. The phylogenetic utility of the
mitochondrial cytochrome b gene for inferring relationships
among Actinopterygian fishes. Pp. 285–303 in T.D. Kocher
and C. Stepien, eds. Molecular Systematics of Fishes. Aca-
demic Press, San Diego, Calif.
Macdougall J.D. 1996. A Short History of Planet Earth, Moun-
tains, Mammals, Fire, and Ice. Wiley, New York.
Magnuson J.J. 1973. Comparative study of adaptations for con-
tinuous swimming and hydrostatic equilibrium of scombroid
and xiphoid fishes. Fish Bull US 71:337–356.
———. 1978. Locomotion by scombrid fishes. Pp. 239–313 in
W. Hoar and D. Randall, eds. Fish Physiology. Vol. 7. Aca-
demic Press, New York.
Marcinek D.J., S.B. Blackwell, H. Dewar, E.V. Freund, C. Far-
well, D. Dau, A.C. Seitz, and B.A. Block. 2001a. Depth and
muscle temperature of Pacific bluefin tuna examined with
acoustic and pop-up satellite archival tags. Mar Biol 138:
869–885.
Marcinek D.J., J. Bonaventura, J.B. Wittenberg, and B.A. Block.
2001b. Oxygen affinity and amino acid sequence of myoglo-
bins from endothermic and ectothermic fish. Am J Physiol
280:R1123–R1133.
Martin A.P. 1996. Systematics of the Lamnidae and the origi-
nation time of Carcharodon carcharias inferred from the
comparative analysis of mitochondrial DNA sequences. Pp.
49–53 in A.P. Klimley and D.G. Ainley, eds. Great White
Sharks: The Biology of Carcharodon carcharias. Academic
Press, San Diego, Calif.
Martin A.P., G.J.P. Naylor, and S.R. Palumbi. 1992. Rates of
mitochondrial DNA evolution in sharks are slow compared
with mammals. Nature 357:153–155.
Mathieu-Costello O., P.J. Agey, and R.B. Logemann. 1992. Cap-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Evolution and Consequences of Endothermy in Fishes 1017
illary-fiber geometrical relationships in tuna red muscle. Can
J Zool 70:1218–1229.
McNab B.K. 1978. The evolution of homeothermy in the phy-
logeny of mammals. Am Nat 112:1–21.
Monsch K.A. 2000a. A new fossil bonito (Sardini, Teleostei)
from the Eocene of England and the Caucasus, and evolution
of tail region characters of its recent relatives. Paleontol Res
4:75–80.
———. 2000b. The Phylogeny of the Scombroid Fishes. Ph.D.
thesis. University of Bristol.
Moore J.A. 1998. Possible Nervous Innervation and Charac-
terization of the Blood Vessels of the Counter-Current Heat
Exchangers in Three Species of Tuna. M.S. thesis. California
State University, Fullerton.
Morrissette J.M., J.P.G. Franck, and B.A. Block. 2003. Char-
acterization of ryanodine receptor and Ca
2⫹
-ATPase isoforms
in the thermogenic heater organ of blue marlin (Makaira
nigricans). J Exp Biol 206:805–812.
Moyes C.D., O. Mathieu-Costello, R.W. Brill, and P.W. Ho-
chachka. 1992. Mitochondrial metabolism of cardiac and
skeletal muscles from a fast, Katsuwonus pelamis, and slow,
Cyprinus carpio, fish. Can J Zool 70:1246–1253.
Muir B.S. and G.M. Hughes. 1969. Gill dimensions for three
species of tunny. J Exp Biol 51:271–285.
Musyl M.K., R.W. Brill, C.H. Boggs, D.S. Curran, T.K. Kazama,
and M.P. Seki. 2003. Vertical movements of bigeye tuna
(Thunnus obesus) associated with islands, buoys, and sea-
mounts near the main Hawaiian Islands from archival tag-
ging data. Fish Oceanogr 12:152–169.
Nakamura I. and K. Mori. 1966. Morphological study on the
slender tuna Allothunnus fallai Serventy obtained from the
Tasman Sea. Rep Nankai Reg Fish Res Lab 23:67–83.
Naylor G.J.P., A.P. Martin, E.G. Mattison, and W.M. Brown.
1997. Interrelationships of lamniform sharks: testing phy-
logenetic hypotheses with sequence data. Pp. 199–218 in T.D.
Kocher and C. Stepien, eds. Molecular Systematics of Fishes.
Academic Press, San Diego, Calif.
Neill W.H., R.K.C. Chang, and A.E. Dizon. 1976. Magnitude
and ecological implications of thermal inertia in skipjack
tuna. Environ Biol Fishes 1:61–80.
Patterson C. 1993. Osteichthyes: Teleostei. Pp. 621–656 in M.J.
Benton, ed. The Fossil Record 2. Chapman & Hall, London.
Purdy R.W. 1996. Paleoecology of fossil white sharks. Pp. 67–
78 in A.P. Klimley and D.G. Ainley, eds. Great White Sharks:
The Biology of Carcharodon carcharias. Academic Press, San
Diego, Calif.
Rhodes D. and R. Smith. 1983. Body temperature of the salmon
shark, Lamna ditropis. J Mar Biol Assoc UK 63:243–244.
Rome L.C., P.T. Loughna, and G. Goldspink. 1984. Muscle fiber
recruitment as a function of swim speed and muscle tem-
perature in carp. Am J Physiol 247:R272–R279.
Schaefer K.M. 1984. Swimming performance, body tempera-
tures and gastric evacuation times of the black skipjack Eu-
thynnus lineatus. Copeia 1984:1000–1005.
———. 1985. Body temperatures in troll caught frigate tuna,
Auxis thazard. Copeia 1985:231–233.
Schaefer K.M. and D.W. Fuller. 2002. Movements, behavior,
and habitat selection of bigeye tuna (Thunnus obesus)inthe
eastern equatorial Pacific, ascertained through archival tags.
Fish Bull US 100:765–788.
Sepulveda C. and K.A. Dickson. 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.
Sepulveda C.A., K.A. Dickson, and J.B. Graham. 2003. Swim-
ming performance studies on the eastern Pacific bonito
(Sarda chiliensis), a close relative of the tunas (Family Scom-
bridae). I. Energetics. J Exp Biol 206:2739–2748.
Sharp G.D. 2001. Tuna oceanography: an applied science. Pp.
345–389 in B.A. Block and E.D. Stevens, eds. Tuna: Physi-
ology, Ecology, and Evolution. Vol. 19. Fish Physiology. Ac-
ademic Press, San Diego, Calif.
Sharp G.D. and W.J. Vlymen. 1978. The relation between heat
generation, conservation, and the swimming energetics of
tunas. Pp. 213–232 in G.D. Sharp and A.E. Dizon, eds. The
Physiological Ecology of Tunas. Academic Press, New York.
Sisson J.E. and B.D. Sidell. 1987. Effect of thermal acclimation
on muscle fiber recruitment of swimming striped bass (Mo-
rone saxatilis). Physiol Zool 60:310–320.
Smith A.G., D.G. Smith, and B. M. Funnell. 1994. Atlas of
Mesozoic and Cenozoic Coastlines. Cambridge University
Press, Cambridge.
Stevens E.D. and F.G. Carey. 1981. One why of the warmth of
warm-bodied fish. Am J Physiol 240:R151–R155.
Stevens E.D. and F.E.J. Fry. 1971. Brain and muscle tempera-
tures in ocean caught and captive skipjack tuna. Comp
Biochem Physiol 38A:203–211.
Stevens E.D., H.M. Lam, and J. Kendall. 1974. Vascular anatomy
of the counter-current heat exchanger of skipjack tuna. J Exp
Biol 61:145–153.
Stevens E.D. and J.M. McLeese. 1984. Why bluefin tuna have
warm tummies: temperature effect on trypsin and chymo-
trypsin. Am J Physiol 246:R487–R494.
Stevens E.D. and W.H. Neill. 1978. Body temperature relations
of tunas, especially skipjack. Pp. 316–356 in W. Hoar and
D. Randall, eds. Fish Physiology. Vol. 7. Academic Press, New
York.
Swimmer Y., R.W. Brill, L. Mailloux, and C. Moyes. 2001. Car-
diac biochemistry in three species of tuna with widely di-
vergent temperature tolerances. Am Zool 41:1602.
Syme D.A. and R.E. Shadwick. 2002. Effects of longitudinal
body position and swimming speed on mechanical power of
deep red muscle from skipjack tuna (Katsuwonus pelamis).
J Exp Biol 205:189–200.
Tubbesing V.A. and B.A. Block. 2000. Orbital rete and red mus-
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1018 K. A. Dickson and J. B. Graham
cle vein anatomy indicate a high degree of endothermy in
the brain and eye of the salmon shark. Acta Zool 81:49–56.
Tullis A., B.A. Block, and B.D. Sidell. 1991. Activities of key
metabolic enzymes in the heater organs of scombroid fishes.
J Exp Biol 161:383–403.
Videler J.J. 1993. Fish Swimming. Chapman & Hall, London.
Wardle C.S., J.J. Videler, T. Arimoto, J.M. Franco, and P. He.
1989. The muscle twitch and the maximum swimming speed
of giant bluefin tuna, Thunnus thynnus L. J Fish Biol 35:128–
137.
Webb P.W. and R.S. Keyes. 1982. Swimming kinematics of
sharks. Fish Bull US 80:803–812.
Weng K.C. and B.A. Block. 2004. Diel vertical migration of the
bigeye thresher shark (Alopias superciliosus), a species pos-
sessing orbital retia mirabilia. Fish Bull US 102:221–229.
Westneat M.W., W. Hoese, C.A. Pell, and S.A. Wainwright.
1993. The horizontal septum: mechanisms of force transfer
in locomotion of scombrid fishes (Scombridae, Perciformes).
J Morphol 217:183–204.
Westneat M.W. and S.A. Wainwright. 2001. Mechanical design
for swimming: muscle, tendon, and bone. Pp. 271–311 in
B.A. Block and E.D. Stevens, eds. Tuna: Physiology, Ecology,
and Evolution. Vol. 19. Fish Physiology. Academic Press, San
Diego, Calif.
Wolf N.G., P.R. Swift, and F.G. Carey. 1988. Swimming muscle
helps warm the brain of lamnid sharks. J Comp Physiol 157B:
709–715.
This content downloaded from 137.110.039.062 on March 20, 2018 19:01:12 PM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
