First published online January 30, 2009
Journal of Experimental Biology 212, 461-470 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.022814
Evidence for cranial endothermy in the opah (Lampris guttatus)
Rosa M. Runcie1,*,
Heidi Dewar2,
Donald R. Hawn3,
Lawrence R. Frank4 and
Kathryn A. Dickson1,
1 Department of Biological Science, California State University Fullerton,
Fullerton, CA 92834, USA
2 NOAA Fisheries, Southwest Fisheries Science Center, 8604 La Jolla Shores
Drive, La Jolla, CA 92037, USA
3 Joint Institute for Marine and Atmospheric Research, University of
Hawaii/Ecosystems and Oceanography Division, NOAA Fisheries, 2570 Dole Street,
Honolulu, HI 96822, USA
4 Center for Scientific Computation in Imaging and Center for Functional
Magnetic Resonance Imaging, University of California, San Diego, La Jolla, CA
92093, USA
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Fig. 1. Cranial temperature as a function of deep, fast-twitch, glycolytic myotomal
muscle temperature, used as a proxy for ambient water temperature, in 40 opah
that were alive when decked by long-line gear (solid squares) and in 81 dead
opah (open squares). The best-fit regression for the live opah is cranial
temperature=0.632xmuscle temperature+8.90 (R=0.81,
P<0.05) and for the dead opah is cranial
temperature=0.741xmuscle temperature+4.29 (R=0.73,
P<0.05). The broken line represents isothermal conditions (cranial
temperature=muscle temperature).
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Fig. 2. (A) Photograph of the six extraocular muscles in opah, viewed from the back
of the left eye. Proximal and distal regions of the lateral rectus (PLRM and
DLRM), medial rectus (MRM), superior rectus (SRM), inferior rectus (IRM),
superior oblique (SOM) and inferior oblique (IOM) are labeled. (B) A schematic
representation of the arterial circulation from the carotid artery to the
lateral rectus (LRM), SRM, MRM and IRM, based on gross dissections.
Illustration is based on Fig. 2A.
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Fig. 3. Magnetic resonance image (MRI) of the cranial region of the opah and
resulting 3-D reconstructions using image segmentation. (A) MRI coronal
section, approximately midway through eyes showing the position of the
extraocular muscles relative to the eye, skull, brain, adipose tissue and gill
cavity. (B) Transverse view and (C) coronal view 3-D models created from
segmentation of the MRI data showing the relative positions of the extraocular
muscles, insulating fat, and brain. In the 3-D models, only the right eye is
shown. Lateral rectus (LRM), medial rectus (MRM), superior oblique (SOM) and
superior rectus (SRM) extraocular muscles are labeled.
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Fig. 4. Transmission electron micrographs (TEMs) of transverse sections of the
proximal portion of the lateral rectus extraocular muscle. (A) An entire
extraocular muscle fiber filled with myofibrils. n=nucleus of adjacent muscle
fibers. (B) Higher magnification of a portion of a proximal lateral rectus
muscle fiber showing the regular array of thick and thin filaments within the
myofibrils (mf). mt=subsarcolemmal mitochondria.
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Fig. 5. (A. and B) Light micrographs of transverse sections through the putative
counter-current heat exchanger perfusing the proximal portion of the lateral
rectus extraocular muscle (PLRM) showing arteries (a) surrounded by veins (v).
Inside most blood vessels are darkly stained nucleated red blood cells. In (B)
almost the entire width of the heat exchanger located on the medial surface of
the PLRM is shown, illustrating the network of adjacent arteries (a) and veins
(v). In this opah, the entire rete had a maximum width of 1 mm, with up to 12
adjacent blood vessels and a maximum of 86 adjacent blood vessels along its
length of 9 mm. (C) Section of the lateral rectus extraocular muscle (LRM)
approximately midway between its origin and insertion, showing the arteries
(a), surrounded by veins (v), that penetrate the muscle medio-laterally,
separated from other artery–vein groups by muscle fibers (m). These
blood vessels are continuous with those that make up the counter-current heat
exchanger. Scale bars are 100 µm.
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Fig. 6. Cranial temperature as a function of deep myotomal muscle temperature in
the live opah from Fig. 1 (red
solid squares and red line). Also plotted are cranial temperature
versus ambient temperature data for other fish species known to be
cranial endotherms: solid black line, shortfin mako shark
(Block and Carey, 1985 ); broken
line, giant ( 200–450 kg) Atlantic bluefin tuna
(Linthicum and Carey, 1972);
diamonds, billfish species – blue marlin (open), white marlin (black
filled) and spearfish (gray filled) (Block,
1991); open circles, tuna species – small Atlantic bluefin,
albacore, bigeye, little tunny (Linthicum
and Carey, 1972), skipjack
(Stevens and Fry, 1971), black
skipjack (Schaefer, 1984),
frigate tuna (Schaefer, 1985);
and filled circles, slender tuna
(Sepulveda et al., 2007). The
dotted black line represents isothermal conditions (cranial temperature=water
temperature).
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© The Company of Biologists Ltd 2009
