See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/250067249

Temperature Measurements from Salmon Sharks, Lamna ditropis, in Alaskan

Waters

Article  in  Copeia · August 2001

DOI: 10.1643/0045-8511(2001)001[0794:TMFSSL]2.0.CO;2

CITATIONS READS

29 138

2 authors, including:

Kenneth J. Goldman
Captain's Toy Chest
48 PUBLICATIONS   2,858 CITATIONS   

SEE PROFILE

All content following this page was uploaded by Kenneth J. Goldman on 15 October 2014.

The user has requested enhancement of the downloaded file.

Copeia, 2001(3), pp. 794–796

Temperature Measurements from Salmon Sharks, Lamna ditropis,

in Alaskan Waters
SCOT D. ANDERSON AND KENNETH J. GOLDMAN

Salmon sharks, Lamna ditropis, occur only in the North Pacific Ocean. These large
sharks can grow to 250 cm total length and weigh 220 kg. They are endothermic,
and previous investigators reported red muscle temperatures of 8–11 C above am-
bient water temperature. We recorded red muscle temperatures up to 15.6 C above
ambient, along with additional muscle and organ temperatures.

S ALMON sharks, Lamna ditropis, occur in the

boreal and cool temperate coastal and oce-
anic waters of the North Pacific Ocean (Stras-
burg, 1958; Compagno, 1984). Adults of this
species represent a large apex fish predator in
the upper pelagic zone, yet recent summaries
indicate little is known about their biology and
life history (Nagasawa, 1998; Goldman and Hu-
man, 2001). Salmon sharks are grouped in the
family Lamnidae and, like all other family mem-
bers, possess vascular countercurrent heat ex-
changers known as retia mirabilia (Eschricht and
Müller, 1835a,b; Burne, 1923). The retia allow
the retention of metabolically produced heat,
resulting in tissue temperatures that are signif-
icantly above ambient (Carey and Teal, 1969;
Carey and Gibson, 1983; Carey et al., 1985).
Salmon sharks have retia located in the cranium
(orbital retia), musculature (lateral cutaneous re-
tia), and viscera (suprahepatic and kidney retia).
Although retia are responsible for greatly reduc-
ing heat loss via the gills (Carey et al., 1971;
Neill et al., 1976; Carey et al., 1981), the body
shape and size of these fishes also reduce heat
loss across the body surface (Graham, 1983;
Block and Finnerty, 1994).
The only previous measurements of salmon
shark body temperature, obtained via thermom-
eter probe from three relatively small (90–150
cm fork length, FL) specimens (Smith and
Rhodes, 1983), showed that deep muscle tem-
peratures were 8–11 C above sea surface tem-
perature (SST). We recorded 31 deep red mus-
cle, seven white (epaxial) muscle, 19 liver, 23
cloacal, and two stomach, spiral valve, heart,
eye, and brain temperature measurements from
31 salmon sharks caught in the Gulf of Alaska.
One spinal cord temperature and one kidney
rete temperature were also measured.
MATERIALS AND METHODS
Salmon sharks (n 5 31) were caught by hook
and line in the Gulf of Alaska (from 598599N,
1478479W to 598529N, 1498419W) during August
q 2001 by the American Society of Ichthyologists and Herpetologists
1996, August and September 1997, and May
2000. Water depths fished were generally under
120 m. Sharks were brought along side of the
vessel and quickly gaffed, euthanized by direct
brain destruction, and pulled on board.
Temperature measurements (total n 5 92)
were obtained in the following order: muscle,
liver, cloaca, stomach, spiral valve, heart, eye,
and brain (all within 35 min of capture). The
spinal cord and kidney rete temperatures were
measured last. Temperatures were measured
with a Fluke K/J 51 thermometer equipped with
a 20 cm thermistor tipped needle. To obtain
measurements from the deep red muscle, we
inserted the probe 12 cm deep at a 308 angle to
the origin of the dorsal fin. Once inserted, the
tip of the probe was moved around slightly to
find the highest temperature. White (epaxial)
muscle temperature measurements were ob-
tained by pulling the probe out to a depth 6 cm
below the body surface. To measure liver tem-
peratures, we inserted the probe 3–5 cm into
the organ through a small incision made ven-
trally between the pectoral fins. To measure clo-
acal temperatures, we inserted the probe 20 cm
and recorded temperatures when stable. Stom-
ach, spiral valve, and heart temperatures were
measured by inserting the probe tip several cen-
timeters into the organ. Eye temperatures were
measured at a depth of 5.5 cm, and brain tem-
peratures were taken 24 cm from the tip of the
snout at a depth of 7–8 cm. Spinal cord tem-
perature was obtained by inserting the probe 5
cm into the neural canal anterior to the first
dorsal fin, and the kidney rete temperature was
taken by inserting the probe into the center of
the rete. Sea surface temperatures were obtained
after each shark was processed. Statistical anal-
ysis consisted of comparing temperature mea-
surements to SST using paired t-tests.
RESULTS
All temperatures, except heart temperature,
were significantly elevated over SST (all tests ex-
 ANDERSON AND GOLDMAN—SALMON SHARK BODY TEMPERATURE 795

TABLE 1. MEAN, STANDARD DEVIATION, RANGE, AND SAMPLE SIZE FOR LENGTH AND BODY TEMPERATURE MEA-
SUREMENTS FROM SALMON SHARKS IN GULF OF ALASKA WATERS. Information on sea surface temperature and the
difference (Xd) between red muscle temperature and SST is also given.

Length (cm) Mean SD Range n

Precaudal 182.2 12.6 159.0–213.4 31

Fork 204.3 13.4 175.0–231.0 31
Total 226.0 14.9 201.0–261.7 31
Temperature (8C)
Red muscle 24.1 2.0 18.9–27.5 31
White muscle 18.6 2.1 15.7–21.0 7
Liver 23.0 2.7 15.2–26.9 19
Cloaca 23.0 1.4 18.7–25.9 23
Stomach 22.5 3.7 19.8–25.1 2
Spiral valve 26.7 0.7 26.2–27.2 2
Heart 9.3 0.2 9.1–9.4 2
Eye 21.1 2.4 19.4–22.8 2
Brain 18.4 1.3 17.4–19.3 2
Kidney rete 21.3 — — 1
Spinal cord 22.3 — — 1
Sea surface 13.3 1.5 8.6–15.4 31
Xd 10.8 2.4 6.3–15.6 31

cept heart, P , 0.001; heart, P . 0.5; Table 1).
Of the 17 sharks where temperatures were mea-
sured from deep red muscle, liver and cloaca,
58.8% of the highest temperatures were record-
ed in deep red muscle, 23.6% from the liver,
and the remaining 17.6% from the cloaca.
DISCUSSION
Smith and Rhodes (1983) recorded deep red
muscle temperatures in salmon sharks as high
as 19.0 C (mean 18.0 C, SD 5 1.73, n 5 3), and
up to 11.0 C above SST, which was 8.0 C. We
found deep red muscle temperatures as high as
27.5 C (mean 24.1 C), and up to 15.6 C degrees
above SST. It is highly unlikely that this differ-
ence is a result of SST differences, because the
lowest SST during our study was similar to that
of Smith and Rhodes (1983). Our red muscle
temperature data average 6.1 C higher than that
of Smith and Rhodes (1983) and are closer to
body core temperatures reported for free-swim-
ming white sharks, Carcharodon carcharias
(McCosker, 1987; Goldman, 1997; Lowe and
Goldman, 2001). It is not surprising that heart
temperature was not significantly elevated over
SST because the heart receives blood after heat
has been removed in the suprahepatic rete.
Previous body temperature measurements for
this species were taken within one minute after
being landed, but fight times were not reported
(Smith and Rhodes, 1983). The efficiency of
our fishing vessel crew in catching and quickly
hauling aboard these large sharks enabled us to
obtain temperature measurements after rela-
tively short fight times and soon after death. For
this reason, we suspect the core temperatures of
free-swimming salmon sharks (when measured
via telemetry) will be comparable to the highest
temperatures reported here. However, absence
of knowledge of the temperature at swimming
depth and the level of activity prior to capture
prevents accurate comparisons and statements
regarding thermoregulatory ability.
Elevated temperatures from multiple body
locations show that the different retia (orbital,
subcutaneous lateral, suprahepatic, and kid-
ney) are extremely effective at keeping the
body uniformly warm. Although there is strong
evidence that lamnid sharks thermoregulate
through physiological means (Carey et al.,
1981; Emery, 1985, 1986), the question of ho-
meothermy versus degree of thermoregulatory
ability (degree of independence of body tem-
perature from ambient temperature) or even
gigantothermy cannot be definitively answered
for any of these species. The relationship be-
tween body size, heat production, and heat loss
in these sharks may prove to be very important
when examining these questions. The use of
telemetry to obtain temperatures from (small
and large) free-swimming salmon sharks will
greatly aid in addressing that question and also
in determining their in vivo body core temper-
ature and its degree of elevation over ambient
temperatures.
 796 COPEIA, 2001, NO. 3
ACKNOWLEDGMENTS
We thank everyone at the Saltwater Safari
Company, Seward, Alaska, particularly Captain
B. Candopoulos, A. Condopoulos, M. Theriault,
and M. Thibault. Thanks to all of the customers
of the M/V LEGEND who caught the sharks for
their cooperation and genuine interest in our
research. We thank R. Brill, J. Graham, and D.
Bernal for their very helpful comments on ear-
lier versions of this manuscript. Special thanks
to C. M. Prier, J. Graham, and D. Bernal for
their assistance in the field. This paper is dedi-
cated to the memories of A. Molina and F. G.
Carey, friends and mentors.
LITERATURE CITED
BLOCK, B. A, AND J. R. FINNERTY. 1994. Endothermy
in fishes: a phylogenetic analysis of constraints, pre-
dispositions, and selection pressures. Environ. Biol.
Fish. 40:283–302.
BURNE, R. H. 1923. Some peculiarities of the blood
vascular system of the porbeagle shark, Lamna cor-
nubica. Philo. Trans. R. Soc. Lond. 212:209–257.
CAREY, F. G., AND Q. H. GIBSON. 1983. Heat and oxy-
gen exchange in the rete mirabile of the bluefin tuna,
Thunnus thynnus. Comp. Biochem. Physiol. 74A:
333–342.
———, AND J. M. TEAL. 1969. Mako and porbeagle:
warm-bodied sharks. Ibid. 28:199–204.
———, ———, J. W. KANWISHER, K. D. LAWSON, AND
J. S. BECKETT. 1971. Warm-bodied fish. Am. Zool.
11:137–145.
———, ———, AND ———. 1981. The visceral tem-
peratures of mackerel sharks (Lamnidae). Physiol.
Zool. 54:334–344.
———, J. G. CASEY, H. L. PRATT, D. URQUHART, AND
J. E. MCCOSKER. 1985. Temperature, heat produc-
tion, and heat exchange in lamnid sharks. So. Calif.
Acad. Sci., Mem. 9:92–108.
COMPAGNO, L. J. V. 1984. Sharks of the world. An an-
notated and illustrated catalogue of shark species
known to date. FAO species catalog. Vol. 4. Part 1.
Hexanchiformes to Lamniformes. U.N. Dev. Prog.,
FAO, Rome.
EMERY, S. H. 1985. Hematology and cardiac morphol-
ogy in the great white shark, Carcharodon carcharias.
So. Calif. Acad. Sci., Mem. 9:73–80.
———. 1986. Hematological comparisons of endo-
thermic vs. ectothermic elasmobranch fishes. Cop-
eia 1986:700–705.
ESCHRICHT, D. F., AND J. MÜLLER. 1835a. Über die ar-
teriösen and venösen Wundernetze an der Leber
und einen merkwürdigen Bau dieses Organes beim
View publication stats
Thunfische, Thynnus vulgaris. Physikal. Abhandl. d.
K Wissensch. Berlin, Germany.
———, AND ———. 1835b. Nachtrag zu der Abhan-
dlung der Herren Eschricht und Müller über die
Wundernetze an der Leber des Thunfisches: Über
die Wundernetze am Darmkanal des Squalus vulpes
L., Alopecias vulpes Nob. Physikal. Abhandl. d. K Wis-
sensch. Berlin, Germany.
GOLDMAN, K. J. 1997. Regulation of body temperature
in the white shark, Carcharodon carcharias. J. Comp.
Physiol. B Biol. Sci. 167:423–429.
———, AND B. HUMAN. 2001. Salmon shark, Lamna
ditropis. In: Sharks, rays and chimaeras: the status of
the chondrichthyan fishes. S. L. Fowler, M. Camhi,
G. Burgess, S. Fordham, and J. Musick (eds.).
IUCN/SSG Shark Specialist Group. IUCN, Gland,
Switzerland.
GRAHAM, J. B. 1983. Heat transfer, p. 248–279. In: Fish
Biomechanics. P. W. Webb and D. Weihs (eds.).
Praeger Publishing, New York.
LOWE, C. G., AND K. J. GOLDMAN. 2001. Thermal and
bioenergetics of elasmobranchs: bridging the gap.
In: The behavior and sensory biology of sharks and
rays: state of the art and future direction. T. C. Tri-
cas and S. H. Gruber (eds.). American Elasmo-
branch Society Symposium, Special Volume in Hon-
or of Dr. D. R. Nelson. Environ. Biol. Fish. 60:251–
266.
MCCOSKER J. E. 1987. The white shark, Carcharodon
carcharias, has a warm stomach. Copeia 1987:195–
197.
NAGASAWA, K. 1998. Predation by salmon sharks (Lam-
na ditropis) on Pacific salmon (Oncorhynchus spp.)
in the North Pacific Ocean. Bull. N. Pac. Anad. Fish
Comm. 1:419–433.
NEILL, W. H., R. K. CHANG, AND A. E. DIZON. 1976.
Magnitude and ecological implications of thermal
inertia in skipjack tuna, Katsuwonnus pelamis (Lin-
naeus). Environ. Biol. Fish. 1:61–80.
SMITH R. L., AND D. RHODES. 1983. Body temperature
of the salmon shark, Lamna ditropis. J. Mar. Biol.
Assn. U.K. 63:243–244.
STRASBURG D. W. 1958. Distribution, abundance, and
habits of pelagic sharks in the central Pacific
Ocean. U.S. Fish Wildl. Serv., Fish. Bull. 58:335–
361.
(SDA) P.O. BOX 390, INVERNESS, CALIFORNIA
94937; AND (KJG) COLLEGE OF WILLIAM AND
MARY, SCHOOL OF MARINE SCIENCE, VIRGINIA
INSTITUTE OF MARINE SCIENCE, P.O. BOX 1346,
GLOUCESTER POINT, VIRGINIA 23062. E-mail:
(KJG) keng@vims.edu. Send reprint requests
to KJG. Submitted: 29 Feb. 2000. Accepted:
23 Feb. 2001. Section editor: R. E. Gatten Jr.