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Design of heterothermic muscle in fish

Stephen L. Katz

Northwest Fisheries Sciences Center, National Marine Fisheries Services — NOAA, 2725 Montlake Boulevard E., Seattle, WA 98112, USA

View larger version (44K): [in a new window]   Fig. 1. (A) Structure of the myotomes in side or fillet view. This diagram shows three myotomes each separated by the removal of two intervening myotomes to demonstrate the nested nature of the cones. The silhouette of the fish indicates the orientation of the myotomes within the fillet. Each anterior-pointing cone is indicated with a white arrow and each posterior-pointing cone is indicated with a black arrow. (B) Diagram of the myotomes from a generic non-heterothermic fish in cross section, or steak view. The red, oxidative muscle is in a small wedge in close apposition to the skin along the mid-lateral line (indicated in orange). The remainder of the muscle consists of white, glycolytic fibers within the cones. Sectioning through the nested cones produces the concentric ring structure visible in this view (white arrows). (C) Diagram of the myotomes of a heterothermic yellowfin tuna (Thunnus albacares) in cross section, or steak view. This diagram shows the distribution of red muscle that is common to tunas, where there is an internal loin of red muscle fibers (in red) in addition to the superficial wedge of red fibers seen in other fish (orange). The location where the mid-lateral septum passes through this section is indicated with a white arrow.

View larger version (61K): [in a new window]   Fig. 2. (A) Dissection photograph of a yellowfin tuna (Thunnus albacares) showing the location and structure of the mid-lateral septum. The head is on the right and the tail on the left, and the dorsal half of the left fillet has been removed to reveal this view from above. As described by Westneat et al. (1993), the anterior oblique tendons run outwards and posteriorly and are composed of tendon precipitated around ribs. Four of them are highlighted in green. Posterior oblique tendons run inwards and posteriorly, and four of these are highlighted in yellow. Scale bar, 5 cm. (B) Dissection photograph of the posterior region of a yellowfin tuna (Thunnus albacares) with the skin removed to reveal the dwindling posterior muscle volume and the progressive replacement of muscle with tendon. These tendons form from myosepta, but progressing towards the peduncle (white arrow) they completely replace the muscle and form dense, twisting ropes of solid tendon. The yellow arrows indicate the long tendons from the subdermal sheath that originate in the myosepta but form mechanical connections to the skin, indicated by the tendons still attached to the skin after an attempt to peel them away. This also suggests a potential trajectory for forces generated in anterior myotomes (see text). The presence of a mechanical connection can be seen in the way the skin `tents up' when the tendon is pulled on with forceps in the lower, reflected flap of skin. Scale bar, 5 cm.

View larger version (28K): [in a new window]   Fig. 3. (A) Diagram of a yellowfin tuna (Thunnus albacares) in cross section or steak view indicating the structural components of the blood vessels that make up the specialized supply for the internal red muscle. The right half of the diagram is similar to Fig. 1C to show the muscle anatomy and allow comparison. In the left half, the muscle anatomy has been removed and the superimposed vascularity is displayed. Arterial vessels are in red and venous vessels are in blue. In yellowfin, the deep red muscle is supplied by large lateral vessels that lie close to the skin, at the margins of the superficial red muscle and the skin. In addition, there is a central rete composed of vessels attached to the posterior cardinal vein and dorsal aorta, from which vessels also enter the deep red muscle. (B) Diagram of the anatomy of a bluefin tuna (Thunnus thunnus) in steak view similar to that in A. Like the yellowfin tuna, the bluefin tuna has peripheral retia, but it lacks the central rete. Importantly, comparison of these figures shows that the vascularity of the deep red muscle is diverse among the heterothermic fish, even between these closely related tuna.

View larger version (24K): [in a new window]   Fig. 4. Bar graph summarizing values of peak stress and oscillatory power output from muscles tested in vitro. Shaded bars, red muscle; white bars, white muscle. (A) Values for peak stress (force/cross-sectional area) in kNm-2 for a variety of fish that cover a range of temperatures. (B) Power output in W kg-1 fish. Data are reported only for muscles tested at temperatures that were the same as the acclimation temperature of the intact fish and are given in parentheses next to the fish name. In those cases where more than one study reported values, the range of values is indicated with error bars. For comparison, a value for frog sartorius is provided. Fish species for which data were reported include Hawaiian seargent (Abudefduf abdominalis), saddle wrasse (Thalassoma duperrey), shorthorned sculpin (Myxocephalus scorpius), trout (Oncorhyncus mykiss), scup (Stenotomus chrysops), largemouth bass (Micropterus salmoides), yellowfin tuna (Thunnus albacares), bonito (Sarda chiliensis) and saithe (Pollachius virens). 1Johnson and Johnston, (1991b); 2Beddow and Johnston (1995); 3Johnson and Johnston, (1991a); 4Langfeld et al. (1989); 5Altringham et al. (1993); 6Coughlin et al. (1996b); 7Rome et al. (1999); 8Hammond et al. (1998); 9Stevens (1988); 10Katz et al. (2001); 11Altringham and Block (1996); 12Altringham and Johnston (1990); 13Johnson et al. (1994).

View larger version (28K): [in a new window]   Fig. 5. Results of in vitro measurements of power output from red muscle using the oscillatory work loop technique for the non-heterothermic bonito (Sarda chiliensis) (A,C) and the heterothermic yellowfin tuna (Thunnus albacares) (B,D). Data are from Altringham and Block (1996). (A,B) Power in Wkg-1 fish for four experimental temperatures, each tested over a range of cycle frequencies. (C,D) The data from A,B normalized by cycle frequency to estimate work per cycle. Normalization by cycle frequency separates the effect of temperature on the force-generating capacity of the muscle from the effect of temperature on the time constants of force development and decay. The results show that yellowfin and, except at the highest temperature bonitos as well, have a modest temperature-dependence in the maximum work per cycle they can generate at the different temperatures. The data also show that, when compared at the same temperatures and frequencies, the non-heterothermic red muscle performs at least as well as the heterothermic red muscle.

View larger version (33K): [in a new window]   Fig. 6. Comparison of red muscle strain calculated from videography using beam theory (filled circles) and from sonomicrometry (continuous lines) for a yellowfin tuna swimming at 2.5 fork lengths s-1 (FL s-1). The image on the right of the figure is an example overhead video image of a yellowfin tuna swimming in a water-tunnel treadmill. The dots on the lateral outline of the fish mark the locations of the digitized points used to calculate body bending and thickness, which are then used to calculate muscle strain using equation 1. The approximate locations of the sonomicrometers within superficial muscle are indicated by green dots superimposed on the image, and the location of the sonomicrometer within the deep red muscle is indicated with a red dot. The association between muscle strain data collected at these locations is indicated by arrows. (A) Muscle strain calculated at 0.5 FL for superficial red muscle located in close apposition to the skin. (B) Muscle strain calculated at 0.5 FL for deep red muscle located within the myotome. (C) Muscle strain calculated at 0.7 FL for superficial red muscle in close apposition to the skin. The width of the vertical green bar indicates the magnitude of the phase shift between video and sonomicrometry estimates of muscle strain in the deep red muscle. The phase shift was calculated as the difference in argument for the principal harmonic component of a Fourier transform of the two time series and, in this case, was approximately 0.1 of a complete strain cycle, a value very close to the phase difference in muscle strain for the superficial muscle in the two longitudinal locations.

View larger version (23K): [in a new window]   Fig. 7. Plot of the rate of oxygen consumption as a function of swimming speed for a selection of heterothermic and non-heterothermic species. Heterothermic tuna are indicated by red lines, and non-heterotherms are indicated by blue lines. The colored regions indicate broad distinctions between strategic differences in design. These performance characteristics are hard to measure experimentally and should not treated as quantitative measures of performance limits. The `effective' strategies have higher aerobic swimming speeds, but consume more O2 at any speed. The `efficient' strategies have lower aerobic swimming speeds, but consume less O2 at any speed than heterothermic fish. The broken green line indicates the top aerobic speed predicted by Korsmeyer et al. (1996) based on modeled estimates of tissue O2 delivery and consumption. Data are presented for sockeye salmon (Oncorhynchus nerka) (Brett and Glass, 1973), Atlantic mackerel (Scomber scombrus) (Lucas et al., 1993), yellowfin tuna (Thunnus albacares) (Dewar and Graham, 1994), skipjack (Katsuwonus pelamus) (Gooding et al., 1981) and Pacific albacore (Thunnus alalunga) (Graham et al., 1989).

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