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.2009 Feb;212(Pt 4):461-70.
doi: 10.1242/jeb.022814.

Evidence for cranial endothermy in the opah (Lampris guttatus)

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Evidence for cranial endothermy in the opah (Lampris guttatus)

Rosa M Runcie et al. J Exp Biol.2009 Feb.

Abstract

Cranial endothermy evolved independently in lamnid sharks, billfishes and tunas, and is thought to minimize the effects of ambient temperature change on both vision and neural function during deep dives. The opah, Lampris guttatus, is a large epipelagic-mesopelagic predator that makes repeated dives into cool waters to forage. To determine if L. guttatus exhibits cranial endothermy, we measured cranial temperatures in live, decked fish and identified potential sources of heat and mechanisms to conserve heat. In 40 opah (95.1+/-7.6 cm fork length), the temperature of the tissue behind the eye was elevated by a mean (+/-s.e.m.) of 2.1+/-0.3 degrees C and a maximum of 6.3 degrees C above myotomal muscle temperature (T(m)), used as a proxy for ambient temperature. Cranial temperature varied significantly with T(m) and temperature elevation was greater at lower T(m). The proximal region of the paired lateral rectus extraocular muscle appears to be the primary source of heat. This muscle is the largest extraocular muscle, is adjacent to the optic nerve and brain and is separated from the brain only by a thin layer of bone. The proximal lateral rectus muscle is darker red in color and has a higher citrate synthase activity, indicating a higher capacity for aerobic heat production, than all other extraocular muscles. Furthermore, this muscle has a layer of fat insulating it from the gill cavity and is perfused by a network of arteries and veins that forms a putative counter-current heat exchanger. Taken together, these results support the hypothesis that the opah can maintain elevated cranial temperatures.

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Figures

Fig. 1.
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=0.632×muscle temperature+8.90 (R=0.81,P<0.05) and for the dead opah is cranial temperature=0.741×muscle temperature+4.29 (R=0.73,P<0.05). The broken line represents isothermal conditions (cranial temperature=muscle temperature).
Fig. 2.
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.
Fig. 3.
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.
Fig. 4.
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.
Fig. 5.
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.
Fig. 6.
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 temperatureversus 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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References

    1. Alexander, R. L. (1998). Blood supply to the eyes and brain of lamniform sharks (Lamniformes). Zool. Soc. Lond. 245, 363-369.
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