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Thermoregulation in Tunas ANDREW E. DIZON KICHARD W. BRILL

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Thermoregulation in Tunas ANDREW E. DIZON KICHARD W. BRILL AMER.ZOOI ... lY:249-269 (1979). Thermoregulation in Tunas ANDREWE. DIZON Southwest FwhQrzec Center Honolulu l,aborutoiy, Nntzonul Mmznc Fuhcrze\ Scnlu e, NOAA, Honolulu, H(iisuu 96812 AND KICHARDW. BRILL. Dejmrtmtnt of Physiology, Uniiwsity (fHauviii, Honolulu, Huuiuii 96822 SYNOPSIS.Because tunas possess countercurrent vascular pathways serving the tt-unk mus- culature. metabolic heat is retained, and muscle temperatures can considerably exceed that of the surrounding water (+I" to +21°C). And because tunas have thls excess. it is reasonable to suppose they have some means of controlling its magnitude. Tuna5 must contend with two rxigencies which can perturb Idytemperature: changes in watei tem- perature and, in contrast to non-thermoconservmg fish, changes in activity. 80th can be met by adaptive change in excess muscle temperature. I1 this could be accomplished in the absence of changes in environmental temperature or activiry level. this would constitute physiological thermoregulation. It excess muscle temperature cannot be altered sufficiently to acceptable levels, more favorablr environmental temperatures must be sought or activity levels changed. We would consider this behavioral thermoregulatlon. High sustained swim speeds, characteristic of the continuously swimming tunas, require special consideration. Heat production is proportional to approximately the cube of swim speed. In order to maintain a slight temperature excess at basal swim speeds (1-2 lengths/ sec), and yet not overheat during sustained high speed swimming (>4 lengthshec), niecha- nisms are required to conserve heat under the forme1 conditions and to dissipate it effec- tively under the latter. In this report, we review published observations other investigators have interpreted as physiological thermoregulation in tunas. desrribe recent tindings in our laboratory. and suggest some possible thermoregulatory mechanisms. INTRODUCTI<)N taxonomically distinguishes the 13 species of. ti-ue tunas (tribe Thunnini) froril other Tunas cannot be strictly classified as nieinbei-s of the family Scoinbridae. r.g., either poikilothei-ms 01- horneotherms. the bonitos , seer fishes . and in ac ke re I s They are "thermocoriserving" fish which (Klawe, 1977; <;ollette, 1978). All true can maintain muscle temperat tires (Tb) tunas have heat exchangers and all get hot several degrees above ambient The (Carey ct al., 197 1). There arc seven thermocoriserving mechanism, the coun- species within the genus Thiinnii.\. thrw iii rei-current rete in the vasculai- system Euthynnu.\, two in Auxi.\, arid one monotypic serving the trunk musculature (reviewed genus. Kcit.\ 11 zt ron UY. As ;I dul t s, the Th u n n UA recently by Stevens anti Neil], 1978), spp. md I\'nt.ciizi~~in~i.\pclnini.\ a1.e pelagic fish . .~~ ~~ ~~~~ ~~~ ~~~~~ . that are disti-ibuted inore or less continu- We thank W. W. Reynolds lor organizing and in- ously across the oceans: the other viting us to this symposiunr. Page charges for publi- cation of this papei. and air fare for travel to this occur more than a few hundred in symposium, were supported bv National Science land (Hlackburn, 1965). Foundation Grant #PCM 78-0.5691 to W. W. Because of the counteix-urrent rete, Reynolds. We also wish to thank J. M.Rochelle and C. metabolic heat is retained and niirsclc tem- C. Chutant for gener-ously providing the ultrasonic to above transmitters used lor monitoring body temperature peratures range from I" 21°C of ti-eeswimming skipjack and yellowhn tunas and G. ambient (Bari-ett and Hestel.. 1964; (:arev (:. Whittow for reviewing this manuscript. et ul., 1971; Stevens and Fry, 1971; 249 2.50 A. E. D~ZONAND K. W. BKII.I Graham, 1975; Dizon ut id., 1978; Stevens are mobile and live in ;I heterothermal en- and Neill, 1978). Because tuniis are fast, vironment. Their mnges, except forbluefin continuous swimmers, and are the most tu nil (Thu II mc.\ thy tt tt ic,\ ) , ;ire n arix~wIy cii-- highly adapted members of their fknily cti msci-ibed by tempera ture. HI ue f in tuna for life in the resource-poor pelagic oceans ha\.e been observed in waters where sur- (Magnuson, 1973, 1978), elevated ml.lscle f:.'ice teiriperatures range f'rom 6" to 30°C temperatures have been hypothesixd t(J ((bey ;ind .I'cal, 1960; Sh;iip, 197.8) tlut increase muscle power (Carey Pt a/.. l!47 I), comniet-cia1 concentrations occur betwren maximum swim speed ((;raharn, 1 975), 14" and 2 1°C (1.aevastu and Rosa, 1963). thermal inertia (Neill and Stevens, 1974; Like bluefin tuna, all)acore (T. c~/alnrcgu) Neil1 ut nl., 1976), maximum sustained are considered ;I temperate species and are swim speed (George and Stevens, 1978). found in fishable concentrations between and muscle efficiency, if., getting more 16" and. .19"~~(Laui~sand Lynn, 1977). kilometers per calorie. Stevens and Neil1 Tropical yellow fin tuna (T. ulhrtctm\ ) are (1978) have outlined the ai-guments sug- fished between 23" and 32°C (Sharp, 1978) gested above. and skipjack tuna (Knhuroonus pulurnis ), the Aside from the fact of warm-bodiedness, other so-called tropical tuna, are fished investigators do not agree on why tunas between 19' and 23°C but observed be- maintain an excess muscle temperature tween 17" and 28°C (Laevastu and Rosa, (T,, where: T, = Th - T,) or if they can 1963). Little is known about the other less control T, in response to thermoregula- conimercially important species. If these tory needs. For the purpose of this essay, data. based on sea-su r face temperatures, we will assume that it is ot. significant re He ct act u a I t e m p e r at u re p r e fe r e n ce , benefit to maintain muscle temperatures tunas can behaviorally thermoregulate. above ambient. We will, however, establish Because tunas are thermoconserving that 1) control of T, is demonstrable in at fish, they have a behavioral thermoreg- least 2 of the I3 species of tunas, 2) because ulatory option not open to other teleosts. of the fast sustained swim speeds in tunas, They can presumably alter heat produc- control is theoretically necessary, and 3) tion simply by altering their activity levels. physiological control'is possible. Approximately 80% of the free energy lib- erated by the propulsive musculature ap- pears as heat (Webb, 1975). Heat produc- tion is related to approximately the cube of THERMOREGULATORY OPTIONS FOR TUNAS swim velocity (a fundamental relationship; see collected papers in Wu ut al., 1975). Tb Before proceeding, we wish to clarify is a function of heat production and heat how we conceptualize the process of ther- dissipation. Alterations of Tbby changes of moregulation in tunas; we intend it to do activity-related heat production would no more than facilitate subsequent discus- represent the second type of behavioral sion. We define thermoregulatory options thermoregulation. open to tunas as follows: Pussizv thermoregulution Behavioral thermoregulation Here, we include any process that tends We subdivide behavioral thermoregula- to stabilize Tband which requires no CNS tion into two types: a) by environmental intervention : selection (Reynolds, 1977), and b) by con- a) Water temperature-related and swim trol of activity-dependeot heat production. velocity-related heat production. Temper- The first subdivision is open to all fish liv- ature changes affect the viscosity and den- ing in heterothermal environments. We sity of seawater and therefore alter the know tunas have sensors to perceive am- energetic requirements of a swimming bient temperature changes (Dizon et al., animal (Ware, 1978). Also, as velocity in- 1974, 1976; Steffel et al., 1976), and they creases, the coefficient of drag decreases sliglitly; soine cnvigy is saved hc.r.cb (CVcI)I), I 'I/? \ r ologrc 111 thrt Ill0 I l'g /Il(l t1on 1Yi.5). Altliougti thc eflecth of' trvnpcm- turc, swim speed, viscosity. and tiensitv are Here. we wish io be niorc rrstiictivc in soiiiewhat conipensiitory in teriiis of drag our definition. j\ctivity-iiidepericlent (I.P., physiological) tliermoi.egiilation requires itid, tliiis, hciit production, thcii- ef'fects that the <:NS has the iibility to alter tlie callriot be ignoi-cd ;ind must bc taken into el'l'ectivcness ol' the ttiei.mocoiisei.ving xxoiint in iinv ticit pi'odiict ioii-dissil,ation models. Otherwise these ellects, in concert rnec.hanisins. Presu mat )ly, t hcsc changes witti others, could be rc~sponsibletor-ol)- ;II e mediated bv a tliermoi.egiilatorv cvriter served thermoi egulat orv hility of' t uniis. honiologou~to that in ttie anterioi. f'orc- I))'I'hcrnial inertia. 'I'herinal inertiii may brain of' birds arid inaiiiinals (Crawshah, explain the observed statility of muscle 1 97i; Kluger, 1978). f'i-ool of' physiologi- mid stoniach ternperat ures in the giant cal thei.moi-egiilation will I)<,alterations in TXindependent of' 01 opposite to activiiy- t)lueflll tull;l (<:m.ey rt d.,I97 I ; (hey ant1 1.awson. I 973). 1k;iuse of the couniercur- related changes in heat production, when rent hcat exchangers posse passive thc~i-moi.egularoi~~eflects are dis- heat is exchanged with the ctnvironrnent at counted. he reiilainder ot the essq will deal with this topic. ;i ~iiuchreduced tate when cornpared with ot her siniilar-sized teleosts (Neill and Ste- Although our definition of physiological vens, 1974). 7'hei.cli)re, T,, can lag signifi- thei.mor-c.gulatioll 1ocuses OJI CNS-me- cantly behind at)riipl changes in T,. Neil1 diated ctwnges in heat dissipation, l)io- and his colleagues (Neill and Stevens, cheniical control of heat production may 1974; Neil1 rt d., 1976) have quantified exist. However, oui- data only allows us to these ef'fects. distinguish behavioral t'roni physiological c)Swim velocity-related heat dissipation. thcriiioi-egulation, not physiological from LJnder specified circunistances swim speed Oiocheinical. In addition, use of' basic hy- changes alter surface heat dissipation rate drodynamic pririciples allows us to distin- (Tiacy, 1972; Erskine and Spotil;t, 1977; guish physiological tliermoregulation 1 rom Brill rt nl., 1978).
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