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First published online October 21, 2004
Journal of Experimental Biology 207, 4015-4024 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01267

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Tuna comparative physiology

Jeffrey B. Graham^1,* and Kathryn A. Dickson²

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 Department of Biological Science, California State University Fullerton, Fullerton, CA 92834-6850, USA

View larger version (14K): [in a new window]   Fig. 1. Morphological phylogeny of the Family Scombridae showing its two subfamilies, Gasterochismatinae and Scombrinae, the latter composed of four Tribes. The bonitos (Tribe Sardini) and tunas (Thunnini) are sister groups. Letter abbreviations for the five tuna genera: Al, Allothunnus; A, Auxis; E, Euthynnus; K, Katsuwonus; T, Thunnus. Modified from Collette et al. (2001); Graham and Dickson (2000).

View larger version (27K): [in a new window]   Fig. 2. (A) Cretaceous–Pleistocene (C–Pl) time scale showing relative cooling in benthic ocean temperature based on stable oxygen isotope ratios. Warmest times were late Paleocene (Pa), while coolest were Pleistocene. Numbers in circles mark the approximate timing of five major paleoceanographic events: (1) Central American land bridge formation (3 mya); (2) beginning of thermohaline circulation (22 mya); (3) closure of the Tethys seaway (25 mya); (4) Antarctic glaciation and polar cooling (30 mya); (5) Northward tectonic drift of Australia (36 mya). Data summarized from Macdougall (1996); Fordyce and de Muizon (2001); Graham and Dickson (2004). Other Tertiary epochs abbreviated on the left axis are: Eocene, E; Oligocene, O; Miocene, M; Pliocene, P. (B) Phylogeny for the Sardini and Thunnini based on the earliest known occurrences of fossil remains (orange circles) of two extant Sardini genera (G, Gymnosarda; S, Sarda) and extant tuna genera (A, Auxis; E/K, Euthynnus or Katsuwonus; T, Thunnus). (Note that Thunnus fossils extend from the late Paleocene to the Pliocene.) The extinct Paleothunnus (P) is considered to be closely related to the tuna–bonito common ancestor. Data from Bannikov (1985); Carroll (1988); Monsch (2000; personal communication). Bonito genera abbreviations: S and G, as above; C, Cybiosarda; O, Orcynopsis. Tuna abbreviations as in Fig. 1; the two Thunnus subgenera (Neothunnus and Thunnus), each with four species, are indicated. (Note: terminal lines indicate number of extant species in each tuna genus.)

View larger version (30K): [in a new window]   Fig. 3. Data from Barkley et al. (1978); Brill (1994); Dagorn et al. (2000); Schaefer and Fuller (2002) rendered into a three-dimensional depiction of the vertical distribution of three tuna species in relation to ocean temperature (black isotherms) and O2 depth profiles (thick blue lines) in the vicinity of 160° W longitude of the equatorial Pacific Ocean. The back panel shows sea surface temperature (SST) isotherms in relation to latitude. Vertical panels show temperature and O2 at depth and the occurrence of each species (shaded areas). Skipjack of <4 kg move freely between the surface and 200 m but do not enter water at <18°C or with less than 3.5 ml O2 l-1 (dark blue line). Larger skipjack have the same low temperature and O2 limits but are also restricted by warm temperatures: 4–9 kg skipjack are restricted to <26°C whereas >9 kg skipjack are confined to 18–22°C. Yellowfin extend from the surface to depths greater than 400 m but have the same O2 limit as skipjack. Bigeye are found at greater depths than the other two species and have an O2 limit of 1.0 ml O2 l-1 (light blue line).

View larger version (34K): [in a new window]   Fig. 4. Pre-dawn to daylight acoustic track record of a South Pacific (Polynesia) bigeye tuna, showing its deep diving in pursuit of the downward migrating deep scattering layer (DSL). Reproduced with permission from Dagorn et al. (2000).

View larger version (79K): [in a new window]   Fig. 5. Factors affecting thunniform swimming biomechanics. (A) Contrasts of the more fusiform body shape of the striped bonito, Sarda orientalis (top), with the black skipjack's (Euthynnus lineatus) increased anterior vertical thickness (from Graham, 1975). (B) Three-dimensional perspective for Sarda (S) and Euthynnus (E) of similar size showing structural features of a single myotome. The hatched area is the only aspect of the myotome that would be visible in a skinned fish. Myotomes have anterior pointing arms (APA) and cones (APC) and posterior pointing cones (PPC) and connect to the vertebral column via the anterior (AOT) and posterior oblique tendons (POT) within the horizontal septum. Lines on the surface of APCs show how AOTs wrap around the APCs for force transfer. The tuna has thicker, longer APCs and an anterior-medial red muscle (RM) mass (stippling). In the bonito, with laterally placed RM, the AOT is longer than in the tuna. As the bonito POT extends posteriorly to insert on vertebrae, it makes a greater angle of incidence with the vertebrae than in tuna. Also illustrated for Euthynnus are its left-side lateral artery (la) and vein (lv) and its central rete (cr). Reproduced from Graham and Dickson (2000).

View larger version (59K): [in a new window]   Fig. 6. (A) Dorsal view photograph of the horizontal septum (i.e. vertebrae level) of a 62.7 cm fork length (FL) Sarda orientalis (S) and a 75.4 cm FL Euthynnus affinis (E). Yellow lines mark an anterior oblique tendon (AOT) extending from a vertebra out to the inter-tendon length (ITL), the segment of the posterior oblique tendon (POT) that parallels the backbone and spans one or two adjacent AOTs. The AOTs act as slings to support the POT (see Westneat and Wainwright, 2001), and the POT segment that inserts onto posterior vertebrae. The greater POT angles in Sarda reflect its lateral red muscle (RM) position. (B) Maximum lateral displacement (as percentage of fish total length, % TL) at each vertebral joint as a function of relative position along the body for Sarda chiliensis (turquoise squares) and kawakawa tuna (Euthynnus affinis; red circles). Modified from Dowis et al. (2003); tuna data from Donley and Dickson (2000).

View larger version (18K): [in a new window]   Fig. 7. Cladogram for Sarda and the five tuna genera (abbreviations as above) reflecting differences in the position and the relative quantity (as illustrated in near mid-body transverse sections) of RM (deep red), and the phyletic trend for greater emphasis on lateral vascular supply [arteries (red), veins (blue)] and retia (red and blue lines) for RM. See text for detail.