The red muscle morphology of the thresher sharks (family Alopiidae)
1 Center for Marine Biotechnology and Biomedicine and Marine Biology
Research Division, Scripps Institution of Oceanography, University of
California, San Diego, La Jolla, CA 92093-0204, USA
2 Pfleger Institute of Environmental Research, Oceanside, CA 92054,
USA
3 Department of Biology, University of Massachusetts, Dartmouth, North
Dartmouth, MA 02747, USA
* Author for correspondence (e-mail: chugey{at}pier.org)
Accepted 24 September 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: Alopias, endothermy, red muscle, aerobic, temperature, retia, lamnid
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
There are three recognized thresher shark species (the common thresher,
A. vulpinus; the pelagic thresher, Alopias pelagicus
Nakamura 1935; and the bigeye thresher, Alopias superciliosus Lowe
1841) that comprise the family Alopiidae. The group is most readily
distinguished from other sharks by an unusually elongate upper caudal lobe
that is typically as long as the body itself
(Compagno, 1984). Despite the
many synapomorphic characters of the alopiid sharks (i.e. caudal fin
morphology, dermal denticles, chondrocranial similarities, dentition;
Gruber and Compagno, 1981
;
Compagno, 1990
), there is
little comparative information on the myotomal anatomy of this group, with
most of what is known coming from studies of a single species, A.
vulpinus (Bone and Chubb,
1983
; Bernal et al.,
2003
).
Although A. vulpinus has been recognized as having the RM
morphology consistent with that of endothermic species
(Bone and Chubb, 1983), it was
not until recently that in vivo body temperatures confirmed RM
endothermy in this species (Bernal and
Sepulveda, 2005
). Because the thresher sharks (Alopiidae) are not
considered to be the sister group to the endothermic lamnid sharks (Lamnidae;
Compagno, 1990
), the RM
morphology and endothermic capacity of A. vulpinus marks the third
group to have independently evolved the ability to warm its aerobic swimming
musculature (anterior and internal RM perfused by retia).
While the RM morphology of A. vulpinus has been documented
(Bone and Chubb, 1983;
Bernal et al., 2003
), it is not
known whether the myotomal framework that enables RM endothermy is an alopiid
synapomorphy (occurring also in A. superciliosus and A.
pelagicus) or an autapomorphic character state of A. vulpinus.
There are no morphological studies related to RM endothermy for either A.
superciliosus or A. pelagicus, and only two inconclusive muscle
temperature measurements exist for A. superciliosus
(Carey et al., 1971
). Because
previous works have established a strong correlation between RM position,
vascular specialization (i.e. retia) and RM endothermy, the present study
quantified the RM morphology of A. superciliosus and A.
pelagicus and compared the findings with those of A. vulpinus
(Bernal et al., 2003
). The
objective of this work was to determine whether A. superciliosus and
A. pelagicus possess the aerobic myotomal specializations that are
associated with RM endothermy in A. vulpinus, lamnid sharks and
tunas.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Specimen collection and identification
Due to the difficulty of acquiring whole A. superciliosus and
A. pelagicus (two relatively uncommon species in California waters)
and because both sharks are large, slow-growing species for which there is
concern over their current status of exploitation, three specimens of each
species were used to examine the RM morphology. The three A.
superciliosus were purchased whole from the California drift-gillnet
fishers operating out of San Diego, CA, USA. Two A. pelagicus were
obtained from Chesapeake Fish Co., San Diego, CA, USA (imported from Guaymas,
Mexico), and a third A. pelagicus (the largest specimen) was caught
by long line during fishing operations aboard the R/V David Starr
Jordan (National Marine Fisheries Service during an Eastern Tropical
Pacific shark census, 2004). Comparative data for A. vulpinus were
obtained from Bernal et al.
(2003).
Because the two A. pelagicus that were purchased from commercial
fishers were not intact (heads, tails and viscera discarded at sea) their
specific identification was verified with DNA sequence analysis of the
16s and 12s mitochondrial genes. For all three A.
pelagicus specimens, DNA extraction and sequencing protocols followed
Craig et al. (2004). Total
genomic DNA was isolated using the Qiagen DNeasy isolation kit, and polymerase
chain reaction (PCR) was used to amplify a 594-bp fragment of the 16s
gene and a 424-bp fragment of the 12s rDNA gene. Sequences were
aligned using ClustalX
((http://bips.u-strasbg.fr/fr/Documentation/ClustalX/)
and visually optimized using MacClade
(http://macclade.org);
percent sequence divergence was estimated in PAUP*4b10
(http://paup.csit.fsu.edu).
Results confirmed the A. pelagicus identification for the three
specimens and showed no genetic differences among them at the 16s
locus and no appreciable differences (0.2%) at the 12s locus. Both of
these genes in A. pelagicus showed a 4.5% and 6.6% difference from
A. superciliosus, as determined by comparisons with sequences
available on GenBank; accession no. AY830718
(Greig et al., 2005
).
Body size
For the two processed (i.e. missing the head and tail) pelagic threshers
and for the largest bigeye thresher (which was not weighed), morphometric
parameters were estimated using established fork length (FL) to total
length (TL) and TL vs body mass regressions. Pelagic
thresher alternate-length (insertion of first dorsal to insertion of second
dorsal) was converted to TL using data from the California Drift
Gillnet Fishery database (D. Holts, National Marine Fisheries Service,
unpublished), and TL-body mass relationships were determined using regressions
from Liu et al. (1999). The
body mass of the A. superciliosus specimen was determined using data
from Kohler et al. (1995
).
Body sectioning, RM quantification and three-dimensional reconstruction
Body sectioning and RM quantification were performed using methods similar
to those described in Bernal et al.
(2003). Briefly, sharks were
frozen whole, in a position that avoided any bending of the body, and
transverse sections (
3-4 cm thick) were cut along the entire length of
the shark using a large band saw. For all individuals that were intact,
observations were made on the presence of RM throughout the length of the
entire upper lobe of the caudal fin. The thickness of each slice was measured,
and high-resolution digital images (Canon, PowerShot A80) were taken of the
anterior surface. For every section, both total (i.e. complete surface) and RM
cross-sectional areas (cm2) were measured using the NIH Image J
software©. The longitudinal distribution of RM was determined
following the protocol of Bernal et al.
(2003
), which adjusted the RM
surface area (cm2) at 50% FL to a relative value of 1.0,
and this relative value was used as a reference point for all other positions
along the body. This relative RM surface area (i.e. normalized at 50%
FL) was estimated for each specimen at 5% FL increments, and
the mean (± S.E.M.) was calculated for each species (i.e.
A. superciliosus, N=3; A. pelagicus, N=3) in order to build
a RM distribution plot along the length of the body. The same procedure was
also used for the A. vulpinus (N=6) data obtained from
Bernal et al. (2003
). These
methods provide a relative RM estimate that enables the comparison of
different sized individuals as well as comparison with previously published
data on A. vulpinus and other species. For each section, RM volume
(cm3) was calculated from the product of RM surface area
(cm2 averaged from both the anterior and posterior sides) and slice
thickness (cm), and the RM mass determined using a density of 1.05 g
cm-3 (Bernal et al.,
2003
).
Three-dimensional reconstructions of the muscle morphology were created by using the high-resolution two-dimensional images of the body sections and by building a vector-based outline of the area of interest (e.g. whole body, visceral mass, spine and RM). Outlines were then skinned together using morphometric data for one specimen of each of the three species, and final images rendered using Strata 3D Pro (Strata, St George, UT, USA).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Both A. superciliosus and A. pelagicus were found to have
their RM located in a lateral/subcutaneous position, which contrasts the
medial arrangement of A. vulpinus
(Bone and Chubb, 1983;
Bernal et al., 2003
)
(Fig. 1). In addition, A.
superciliosus and A. pelagicus also exhibited similarities in
the transverse arrangement of the RM, whereby the RM was predominantly
distributed along the edges of the lateral myotomes in both the epaxial and
hypaxial musculature (Fig. 1,
insets). Although the RM formed a continuous subcutaneous layer around most of
the transverse body sections, it was most dense near the region of the
horizontal septum, and, in A. superciliosus, the RM was almost
exclusively positioned along the septum between 20 and 40% FL. The
epaxial and hypaxial distribution of the RM around the sides of A.
superciliosus and A. pelagicus differed from that documented for
A. vulpinus, which, over most of its body, only has RM positioned
epaxially (Fig. 1).
|
|
Other observations
For both A. superciliosus and A. pelagicus, the
transverse body sections were examined for the presence of vascular structures
that would possibly facilitate heat retention (i.e. retia). Detailed
observations of both the lateral and central circulation did not reveal the
presence of vascular modifications for either species. The observations did,
however, reveal the presence of a dominant central circulation (i.e. large
dorsal aorta and post cardinal vein) and a diminished lateral circulation.
This contrasts the circulation of A. vulpinus, which has a reduced
central circulation and dominant lateral blood supply
(Bone and Chubb, 1983;
Bernal et al., 2003
).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
RM quantity
Despite differences in RM position among the three thresher species, there
were no significant differences in the relative amount of RM present in each
(Table 1). This agrees with
previous studies that have found no apparent correlation between RM quantity
and endothermy in either lamnid sharks or tunas
(Graham et al., 1983;
Bernal et al., 2003
). Further,
it appears that among the sharks studied so far (including the three thresher
species), they all possess a relatively similar amount of RM (approximately
2-3% of body mass; Bernal et al.,
2003
; Table 1)
despite notable differences in swimming activity level, endothermic status,
body size and caudal propeller shape (i.e. lunate, heterocercal). Due to the
limited sample size used in this study, it is not possible to discern if there
are allometric scaling relationships for the relative amount of RM in both
A. superciliosus and A. pelagicus. However, previous work on
A. vulpinus, lamnids and other sharks has shown that there is a
proportional increase (isometric) in the relative amount of RM and body mass
(Bernal et al., 2003
), which
suggests that the relative RM amount in A. superciliosus and A.
pelagicus may also scale isometrically. This contrasts what has been
documented for active bony fishes, which have a somewhat higher and more
variable amount of RM (e.g. RM amount ranging from 4 to 13% in scombrids) that
scales allometrically (Graham et al.,
1983
). It is possible that the narrow and consistent range of
relative RM amount in sharks may reflect similarities in their physiology and
ecology. One common feature among sharks is the widespread use of the liver
for buoyancy regulation, a tactic that could decrease the need for additional
RM to produce forward thrust in the maintenance of hydrostatic equilibrium.
Further, perhaps the narrow range is correlated with a limited scope for
aerobic performance. Indeed, swimming tunnel studies on juvenile mako sharks
(Isurus oxyrinchus), lemon sharks (Negaprion brevirostris),
scalloped hammerheads (Sphyrna lewini) and leopard sharks
(Triakis semifasciata) have shown that they only perform over a
relatively narrow aerobic range (0.25-1.5 L s-1;
Graham et al., 1990
;
Lowe, 1996
;
Bushnell et al., 1989
;
Bernal et al., 2001b
;
Donley and Shadwick, 2003
;
Donley et al., 2004
; reviewed
by Carlson et al., 2004
) when
compared with active teleosts (Brett and
Glass, 1973
; Sepulveda et al., 2000,
2003
).
RM position
The transverse distribution of the RM in A. superciliosus and
A. pelagicus (i.e. lateral and above and below the horizontal septum)
is similar to that found in the blue shark (Prionace glauca) and the
leopard shark and parallels the myotomal arrangement of other ectothermic
sharks (Bernal et al., 2003;
Donley and Shadwick, 2003
).
This myotomal arrangement is the predominant character state of most bony
fishes and elasmobranches and is, however, distinct from that of their sister
taxon A. vulpinus and the lamnids
(Bone and Chubb, 1983
;
Carey et al., 1985
;
Bernal et al., 2003
). In A.
vulpinus, the RM is positioned only in the epaxial musculature until the
caudal peduncle, where it also begins to extend into the hypaxial region. This
transverse arrangement is also found in the lamnids and may be attributed to
several factors, which include the position of the lateral blood supply (which
is also above the horizontal septum) or possibly the orientation of the tendon
system that transmits force to the caudal propeller
(Carey et al., 1985
;
Bernal et al., 2003
; S.
Gemballa, P. Konstantinidis, J. M. Donley, C. A. Sepulveda and R. E. Shadwick,
submitted). In the present study, we also found the RM to extend to the tip of
the upper caudal lobe, a characteristic observed in all three thresher
species. This small band of RM may allow thresher sharks to increase the
maneuverability of the caudal fin while feeding
(Gubanov, 1972
;
Nakano et al., 2003
) or
possibly aid in controlling the dorso-ventral angle of the tail as it swings
through the water.
RM and regional endothermy
Previous works have speculated about the endothermic status of all three
thresher sharks (Carey et al.,
1971; Gruber and Compagno,
1981
; Bone and Chubb,
1983
; Block and Finnerty,
1994
; Weng and Block,
2004
). Recent field studies have shown that the RM of the common
thresher is warmer than ambient seawater temperature
(Bernal and Sepulveda, 2005
)
and that A. superciliosus has a large orbital rete, highly suggestive
of cranial endothermy (Block and Carey,
1985
; Weng and Block,
2004
). There are no RM temperature measurements for A.
pelagicus and only two inconclusive RM temperature measurements for
A. superciliosus (Carey et al.,
1971
). Although additional RM temperature data are warranted for
both A. superciliosus and A. pelagicus, it is clear that
these species lack a medial RM position, a feature shared by all of the known
RM endotherms (i.e. common thresher, lamnids and tunas). In addition, we did
not find any vascular heat exchangers in any of the transverse body sections
of A. superciliosus and A. pelagicus. Taken together, the
subcutaneous RM position and the lack of a vascular heat exchange system
almost certainly preclude them from maintaining an elevated RM temperature
because any heat generated by the RM would be lost to the surrounding water by
convection through the skin and via diffusion across the gills.
Regional endothermy and thresher shark natural history
While all three thresher species, at times, occupy similar depths and
habitats (Hanan et al., 1993);
latitudinal and depth-distribution data suggest that A. vulpinus,
with its warm RM, and A. superciliosus, which is probably a cranial
endotherm (Weng and Block,
2004
), inhabit cooler waters than A. pelagicus, a species
predominantly found in tropical and subtropical waters
(Compagno, 1998
;
Liu et al., 1999
). A.
vulpinus has been shown to have the greatest overall latitudinal
distribution, ranging in the eastern Pacific from 58°N to 55°S
(Compagno, 2001
). Although the
latitudinal distribution of A. superciliosus is not as extensive as
that of A. vulpinus (approximately 35°N to 35°S;
Ivanov, 1986
;
Compagno, 2001
), the
temperature minima experienced may exceed those of the other threshers when
considering the deep waters it has been shown to inhabit. Satellite tagging
and acoustic telemetry studies have shown that A. superciliosus
spends much of the daylight hours at depth in waters between 6 and 12°C
(Nakano et al., 2003
;
Weng and Block, 2004
). Similar
archival tagging data for A. vulpinus also show this species to
frequent waters below the thermocline, but the amount of time spent at depth
and the range of temperatures encountered (9-17°C; D. Cartamil,
unpublished) are less extreme than those of A. superciliosus. Future
studies that further characterize the vertical and horizontal movements of
these two sharks may begin to elucidate which form of regional endothermy
(i.e. RM, eye and brain) better enables the threshers to exploit colder
environments (i.e. high latitude and greater depth). However, because there
are no movement studies on A. pelagicus, currently it is not possible
to fully assess habitat partitioning and possible niche expansion in this
group.
Thresher shark phylogeny
The phylogenetic relationship of the thresher sharks has been examined
using both morphological and molecular techniques
(Maisey, 1985;
Compagno, 1990
;
Eitner, 1995
;
Martin and Naylor, 1997
;
Naylor et al., 1997
). Using
morphological characters, Compagno
(1990
) hypothesized that the
three thresher species comprise a monophyletic family (Alopiidae) in the Order
Lamniformes. This hypothesis is based on several alopiid synapomorphies, which
include pectoral fin structure and origin, fin placement, size and morphology,
caudal fin morphology and vertebral count, chondrocranial morphology and
mouth, teeth and jaw similarities
(Compagno, 1990
). Compagno
(1990
) further hypothesized
that A. vulpinus is the ancestral sister taxon to A.
pelagicus and A. superciliosus. This hypothesis is also
supported by the molecular-based analysis of Eitner
(1995
); however, in the Eitner
(1995
) study, there was also
evidence suggesting a fourth alopiid species. Other hypotheses based on
molecular data fail to provide a monophyletic origin for the threshers; this,
however, has been primarily attributed to long branch lengths and short
internodes, which can decrease species resolution
(Martin and Naylor, 1997
;
Morrissey et al., 1997
;
Naylor et al., 1997
). Because
of the strong morphological hypothesis presented by Compagno
(1990
), Martin and Naylor
(1997
) and Naylor et al.
(1997
) forced monophyly for
the alopiids and place the Cetorhinidae (basking shark) as the sister group to
the Lamnidae (the lamnids are the only other lamnoid group documented with an
internal and anterior RM arrangement). If the Compagno
(1990
) hypothesis is used in
the present study, the presence of an internal and anterior RM arrangement in
A. vulpinus suggests that this character state is an autapomorphic
trait of A. vulpinus and cannot be used alone to distinguish the
relatedness of the alopiids.
Conclusions
This study compared RM position and quantity in the three species of
thresher sharks (family Alopiidae) and has shown that A. vulpinus is
the only alopiid to possess the aerobic specializations (medial and more
anterior RM position) that facilitate RM endothermy. Neither A.
superciliosus nor A. pelagicus have their RM in this body
position. Rather, RM in these species occurs along the lateral edges of the
myotomes, near the skin, and extends more posteriorly, a pattern typical of
species lacking the capacity for RM endothermy.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bernal, D. and Sepulveda, C. A. (2005). Evidence for temperature elevation in the aerobic swimming musculature of the common thresher shark, Alopias vulpinus. Copeia 2005,163 -168.
Bernal, D., Dickson, K. A., Shadwick, R. E. and Graham, J. B. (2001a). Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas. Comp. Biochem. Physiol. 129A,695 -726.
Bernal, D., Sepulveda, C. and Graham, J. B.
(2001b). Water-tunnel studies of heat balance in swimming mako
sharks. J. Exp. Biol.
204,4043
-4054.
Bernal, D., Sepulveda, C. A., Mathieu-Costello, O. and Graham,
J. B. (2003). Comparative studies of high performance
swimming in sharks. I. Red muscle morphometrics, vascularization and
ultrastructure. J. Exp. Biol.
206,2831
-2843.
Block, B. A. and Carey, F. G. (1985). Warm brain and eye temperatures in sharks. J. Comp. Physiol. B 156,229 -236.[Medline]
Block, B. A. and Finnerty, J. R. (1994). Endothermy in fishes: a phylogenetic analysis of constraints, predispositions, and selection pressures. Env. Biol. Fish. 40,283 -302.[CrossRef]
Bone, Q. and Chubb, A. D. (1983). The retial system of the locomotor muscle in the thresher shark. J. Mar. Biol. Assoc. U.K. 63,239 -241.
Brett, J. R. and Glass, N. R. (1973). Metabolic rates and critical swimming speeds of sockeye salmon, Oncorhynchus nerka, in relation to size and temperature. J. Fish. Res. Board Can. 30,379 -387.
Bushnell, P. G., Lutz, P. L. and Gruber, S. H. (1989). The metabolic rate of an active, tropical elasmobranch, the lemon shark (Negaprion brevirostris). Exp. Biol. 48,279 -283.[Medline]
Carey, F. G (1973). Fishes with warm bodies. Sci. Am. 228,35 -44.
Carey, F. G. and Teal, J. M. (1966). Heat
conservation in tuna fish muscle. Proc. Natl. Acad. Sci.
USA 56,1464
-1469.
Carey, F. G., Teal, J. M., Kanwisher, J. W. and Lawson, K. D. (1971). Warm bodied fish. Am. Zool. 11,135 -145.
Carey, F. G., Casey, J. G., Pratt, H. L., Urquhart, D. and McCosker, J. E. (1985). Temperature, heat production and heat exchange in lamnid sharks. Mem. S. Calif. Acad. Sci. 9, 92-108.
Carlson, J. K., Goldman, K. J. and Lowe, C. G. (2004). Metabolism, energetic demand and endothermy. In The Biology of Sharks and their Relatives (ed. J. Musick, J. Carrier and M. Heithaus), pp. 203-219. New York: CRC Press.
Compagno, L. J. V. (1984). Sharks of the World. Part 1. Hexanchiformes to Lamniformes. FAO Fisheries Synopsis 125 4:1 -249.
Compagno, L. J. V. (1990). Relationship of the megamouth shark, Megachasma pelagios (Lanmiformes: Megachasmidae), with comments on its feeding habits. In Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of Fisheries. NOAA Technical Report NMFS 90 (ed. H. L. Pratt, S. H. Gruber and T. Taniuchi), pp. 357-379. Washington DC: NOAA.
Compagno, L. J. V. (1998). Alopiidae. Thresher sharks. In FAO Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific (ed. K. E. Carpenter and V. H. Niem), pp. 1269-1273. Rome: FAO.
Compagno, L. J. V. (2001). Sharks of the World. Bullhead, mackeral and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO Species Catalogue 2, 78-88.
Craig, M. T., Hastings, P. A. and Pondella II, D. J. (2004). Speciation in the Central American Seaway: the importance of taxon sampling in the identification of trans-isthmian species pairs. J. Biogeo. 31,1085 -1091.[CrossRef]
Dickson, K. A. and Graham, J. B. (2004). Evolution and consequences of endothermy in fishes. Physiol. Biochem. Zool. 77,998 -1018.[CrossRef][Medline]
Donley, J. M. and Shadwick, R. E. (2003).
Steady swimming muscle dynamics in the leopard shark Triakis semifasciata.J. Exp. Biol. 206,1117
-1126.
Donley, J. M., Sepulveda, C. A., Konstantinidis, P., Gemballa, S. and Shadwick, R. E. (2004). Convergent evolution in mechanical design of lamnid sharks and tunas. Nature 429, 61-65.[CrossRef][Medline]
Donley, J. M., Sepulveda, C. A., Konstantinidis, P., Gemballa,
S. and Shadwick, R. E. (2005). Patterns of red muscle
strain/activation and body kinematics during steady swimming in a lamnid
shark, the shortfin mako (Isurus oxyrinchus) J. Exp.
Biol. 208,2377
-2387.
Eitner, B. J. (1995). Systematics of the genus Alopias (Lamniformes: Alopiidae) with evidence for the existence of an unrecognized species. Copeia 1995,562 -571.
Graham, J. B., Koehrn, F. J. and Dickson, K. A. (1983). Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy. Can. J. Zool. 61,2087 -2096.
Graham, J. B., Dewar, H., Lai, N. C., Lowell, W. R. and Arce, S. M. (1990). Aspects of shark swimming performance determined using a large water tunnel. J. Exp. Biol. 151,175 -192.
Greig, T. W., Moore, M. K., Woodley, C. M. and Quattro, J. M. (2005). Mitochondrial gene sequences useful for species identification of commercially regulated Atlantic ocean sharks. Fish. Bull. 103,516 -523.
Gruber, S. H. and Compagno, L. J. V. (1981). Taxonomic status and biology of the bigeye thresher, Alopias superciliosus. Fish. Bull. 79,617 -640.
Gubanov, Y. P. (1972). On the biology of the thresher shark, Alopias vulpinus (Bonnaterre), in the northwest Indian Ocean. J. Ichthyol. 12,591 -600.
Hanan, D. A., Holts, D. B. and Coan, A. L., Jr (1993). The California drift gill net fishery for sharks and swordfish, 1981-82 through 1990-91. Fish Bull. 175, 89-95.
Ivanov, O. A. (1986). On the distribution of the bigeye thresher shark, Alopias superciliosus, in the Pacific Ocean. J. Ichthyol. 26,121 -122.
Kohler, N. E., Casey, J. G. and Turner, P. A. (1995). Length-weight relationships for 13 species of sharks from the western North Atlantic. Fish. Bull. 93,412 -418.
Liu, K. M., Chen, C. T., Liao, T. H. and Joung, S. J. (1999). Age, growth, and reproduction of the pelagic thresher shark, Alopias pelagicus in the Northwestern Pacific. Copeia 1999,68 -74.
Lowe, C. G. (1996). Kinematics and critical
swimming speeds of juvenile scalloped hammerhead sharks. J. Exp.
Biol. 199,2605
-2610.
Maisey, J. G. (1985). Relationships of the megamouth shark, Megachasma. Copeia 1985,228 -231.
Martin, A. P. and Naylor, G. J. P. (1997). Independent origins of filter-feeding in megamouth and basking sharks (order Lamniformes) inferred from phylogenetic analysis of cytochrome b gene sequences. In Biology of the Megamouth Shark (ed. K. Yano, J. F. Morrissey, Y. Yabumoto and K. Nakaya), pp.39 -50. Tokyo: Tokai University Press.
Morrissey, J. F., Dunn, K. A. and Mule, F. (1997). The phylogenetic position of Megachasma pelagios inferred from mtDNA sequence data. In Biology of the Megamouth Shark (ed. K. Yano, J. F. Morrissey, Y. Yabumoto and K. Nakaya), pp. 33-37. Tokyo: Tokai University Press.
Nakano, H., Matsunaga, H., Okamoto, H. and Okazaki, M. (2003). Acoustic tracking of bigeye thresher shark Alopias superciliosus in the Eastern Pacific Ocean. Mar. Ecol. Prog. Ser. 265,255 -261.
Naylor, G. J. P., Martin, A. P., Mattison, E. G. and Brown, W. M. (1997). Interrelationships of lamniform sharks: testing phylogenetic hypotheses with sequence data. In Molecular Systematics of Fishes (ed. T. D. Kocher and C. A. Stepien), pp.199 -218. San Diego: Academic Press.
Sepulveda, C. A. and Dickson, K. A. (2000). Maximum sustainable speeds and cost of swimming in juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). J. Exp. Biol. 203,3089 -3101.[Abstract]
Sepulveda, C. A., Dickson, K. A. and Graham, J. B.
(2003). Swimming performance studies on the eastern Pacific
bonito Sarda chiliensis, a close relative of the tunas (family
Scombridae). I. Energetics. J. Exp. Biol.
206,2739
-2748.
Weng, K. C. and Block, B. A. (2004). Diel vertical migration of the bigeye thresher shark (Alopias superciliosus), a species possessing orbital retia mirabilia. Fish Bull. 102,221 -229.
Related articles in JEB: