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 musculature. 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 temperature 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 effectively 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 appears as heat (Webb, 1975). Heat production 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). Increased velocity can what we term passive thermoregulation. cause increased hdy surface heat loss Investigation into biochemical solutions by to or (iliat t lemat ical relat ionsh i 1) genera t ed for- tunas acute chronic temperature tunas by Sharp and Vlyinen, 1978). Later challenges have yet to be initiated. we will discuss whether this increased c:onvective-entianced surtace conductance (Strunk, 1973) could coinpensate fir in- FIELD EVIDEN(:E FOK TUNA THF.KMOKE(;Ul.ATION creased heat prodiiction in tunas. (:an field evidence he used 10 demon- 'The effectiveness of countercarrent heat strate theririoregulatory abilities of' tuna? exchangers are dependent upon length of 11' so, what types? l'resumably, if' Th's were the channels. velocity of' the fluids within relativelv constant and independent of'I.,, t 11 e channels, and t he t liernial trims 1 er considerable ther.inoi-egulatory ability chiiracteristic.s of' tlie tluids and the rtian- could be assumed (Bligh and Johnson, ne1 walls (Mirchell ;itid blvcrs, ISSXj. Be- 1973). cause the ett'ectivencss of tuna's vascula1 Figure 1 summarizes the existing field coiit~tcrciir~i.etitsystem is inversely related observations concerning the abilities of to I)lood flow, increases in cardiac output, tunas to del'end a relatively fixed Th. hr- requiwd by increases in swim velocity, rett and Hester (1964) determined the could decrease ttie hcat exchanger's eft&- following linear least squares regression tiveness so that increased heat production relationships between muscle teinpera- c~iildbe dissipated without appreciably in- t ures and sea -si1 r f ace tern pera t u res for creasing T,. (hi-ey and Teal (1969) ob- skipjack and yellow fin tunas : served that violent struggles of fish caught on hook and line do indeed reduce, rather I.,,= .O.X1 T, + 7.47 (yellowfin tuna) and than increase, 'Ih of large Iduefin tuna. Th = 0.58 T, 1- 16.39 (skipjack tuna). 2 .?2 A. E. DIZONAND R. W. BRILL

40r -- surface temperature from 7” to 30°C. SKIPJACK TUNA The greatest T, observed was 21.5”C in areas of 7.3”C surface-water temperature. At least for skipjack tuna, the regression BLUEFIN TUNA relationship presented by Barrett and Hester (1964) is confounded’by additional d//’information from Carey and Teal (1969) YELLOWFIN TUNA and Stevens and Fry (1971). The former / observed excess muscle temperatures W / / below (Fig. 1, open bar) and the latter, 0 u)3 / above (Fig. 1, solid bars) values predicted I 0 by Barrett and Hester (1964). The excess Wn red muscle temperatures observed by Ste- vens and Fry (1971) are almost double those observed by Barrett and Hester ,L--’ 0 5 IO 15 20 25 30 35 (1964) although the fish were taken from SEA-SURFACE TEMPERATURE L’C ) areas with the same surface-water temperatures; thus it appears that body temper- FIG. 1. Linear regression of red muscle tempera- atures of tunas, at least skipjack, are quite ture (T,) on sea-surface temperature for skipjack and labile. yellowfin tunas (SJ and YF, respectively, from Barrett Nevertheless, as a result of their own and Hester, 1964) and bluefin tuna (BF, from Carey and Teal, 1969). Solid bars are ranges of red muscle and Barrett and Hester’s (1964) observa- temperatures from skipjack tuna (from Stevens and tions, Carey and Teal (1969) concluded Fry, 1971 -right-hand bar from 9 fish averaging 73.5 that bluefin tuna were more adept at tem- cm FL, left-hand bar from 20 fish averaging 44.5 cm perature control than skipjack or yellowfin FL). Open bar is range of red muscle temperatures tunas. Stevens and Fry (1971) concluded from skipjack tuna (from Carey and Teal, 1969). that skipjack tuna could also maintain a fixed Tb in waters of 25” to 34°C. Carey and Teal (1969, p. 212) implied that a The results were significantly different in physiological thermoregulatory mecha- slope and level. Over the range tested, size nism might be employed by the bluefin was an unimportant determinant of body tuna: “Modifications of the rete under the temperature in yellowfin tuna. However, fish’s (bluefin tuna) control maintain tem- larger skipjack tuna tended to be slightly peratures at a constant level.” Stevens and warmer: Fry (1971) simply state that skipjack tuna Tb= 0.59 T, -t 0.015 L -t 8.63 regulate muscle temperature; they do not suggest a mechanism. where L = fork length, mm. However, does this field data justify the The slopes were significantly different conclusion that tunas control their muscle from unity, therefore fish from cooler wat- temperatures? We do not think so. Evi- ers tended to have greater T,’s, a first indi- dence from just captured fish is difficult to cation of a thermoregulatory response. interpret because: By the test of “slope,” (Fig. 1) bluefin 1) The fish have experienced an un- tuna are quite adept at temperature regu- known thermal history. The open ocean is lation (Carey and Teal, 1969): a heterothermal environment. Very cool water is available at depths easily reached Tb = 0.25 T, + 24.94. by tunas because all but the largest species Bluefin tuna apparently maintain greater lack swim bladders, or have swim bladders independence of Th from T, and are also which are reduced in size or atrophied relatively warmer than either skipjack or (Godsil and Byers, 1944; Gibbs and Col- yellowfin tunas (at least at the center of lette, 1971). Dizon et d. (1978) show that their ambient temperature range. Their extensive vertical migrations (surface to Th’s varied only 5°C over a range of sea- 273 m) are continuous features of the day- THERMOREGULATIONIN TUNAS 2 53 light activity pattern of skipjack tuna (70 cally advanced bluefin tuna group, 4, Kish- cm), in areas where T, ranged from 25°C inouye, 1923; Godsil and Byers, 1944; at the surface to less than 12°C at 270 m Gibbs and Collette, 1967.) depth. Because all tunas possess a degree Transmitters were placed on 14 bluefin of thermal inertia, their characteristic Th tuna. Because several fish exhibited muscle would be a function of the sequence of and stomach temperatures that were inde- ambient temperatures experienced prior pendent of T,’s, Carey and Lawson (1973) to capture, and not just the sea-surface concluded that bluefin tuna can ther- temperature used by Barrett and Hester moregulate in the mammalian sense (;.e., (1964), Carey and Teal (1969), and Stevens maintain relatively constant body temper- and Fry (1971). Looking for thermoreg- atures even though subjected to prolonged ulatory ability by relating Thto T, is mean- changes in T,) by altering the effectiveness ingful only if T, has been constant long of their vascular heat exchange system. enough for the fish to reach thermal steady There is, however, an alternate expla- state (Neill and Stevens 1974; Neill et al., nation. Using a purely empirical approach, 1976). This time period is size-related, and Neill and Stevens (1974) successfully is thus especially important for larger tuna. mathematically modeled the bluefin tuna 2) As described earlier, there is a fun- telemetry data assuming a constant rate of damental relationship between activity and heat dissipation and heat production (Fig. heat production, but field evidence is con- 2 ) . N o p h y siologica I therm ore g u I a tor y tradictory on the effect of activity on Tb. mechanisms dependent upon T, were Carey and Teal (1966) show that “lively” postulated, and yet the model could ex- bigeye tuna (Thunnus ohms) have higher plain the observed muscle and stomach body temperatures than “weak’ ones. Also, temperature stability observed by Carey Stevens and Fry (1 97 1) unequivocally and Lawson (1973). demonstrate that skipjack tuna T,’s in- Although the Neil1 and Stevens’ (1 974) crease by one-third when strenuously analysis does not prove or disprove the exercised, but Carey and Teal (1 969) show possibility that bluefin tuna are capable of that hook-and-line caught fish have lower rapid physiological thermoregulation, muscle temperatures than trap-caught thermal inertia (passive thermoregulation) ones. Even though hook-and-line fish pre- of these large tunas may well have ac- sumably have fought harder and longer counted for the observed stability of Tb. than trap-caught fish, they are cooler. 3) Perhaps, fish measured at different LABORATORY EVIDENCE FOR TUNA surface-water temperatures, in widely di- THERMOREGULATION vergent geographical areas, are members of different stocks (Sharp, 1978).T, differ- To differentiate between behavioral, ences might result from acclimation pro- passive, or physiological thermoregulation cesses spanning days to generations (Hazel requires an experiment that monitors ac- and Prosser, 1974). tivity levels at constant Ta for long periods To alleviate uncertainties outlined of time. We designed equipment to control above, Carey and Lawson (1973) proposed T, precisely in a tank sufficiently large to an experiment involving long-term moni- accommodate small yellowfin and skipjack toring of I-,,in response to controlled tunas, which are routinely maintained in changes in T,. They designed a field ex- captivity at the Kewalo Research Facility in periment using the naturally occurring Honolulu (Nakamura, 1972). To monitor heterothermal conditions around NOVA muscle temperature, we employed a small, Scotia, the northernmost range of giant ultrasonic transmitter (Fig. 3; Kochelle and bluefin tuna. Ultrasonic transmitters were <:outant, 1974). A photocell system moni- used to simultaneously monitor stomach or tored activity, and IT2,was generally main- muscle temperature and water tempera- tainet! within 0.0.5”(: in the annular- ture. (Heat exchangers also service the vis- shaped test tank (6.1 in m;Ljor diam X 5.3 in ceral structures of‘ the inore phylogeneti- minor diam x 0.6 in deep, Fig. 3). 2 54 A, E. DIZONAND R. W. BRILL

O' I& ' 1200 ' 1400 ' I& 1800 2doo 2200 ' 2400 ' 0200 0400 ' 0600 0800 1000 1200 2511.1

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FIG. 2. Actual Tb (x) and modeled Tb (0) of two logical thermoregulation is used in constructing the free-swimming bluefin tuna (Carey and Lawson. model, yet the fir is remarkably gtmd. Panel A shows 1973) encountering abrupt changes in T, (*) (from muscle temperatures trom bluefin tuna No. 8, B and Neil1 and Stevens, 1974). No assumption of physio- C show temperatures from bluefin tuna No. 14.

Nine skipjack tuna (SJ 1-9) were indi- photocells into swim speed. vidually subjected to consecutive temper- Does a simple plot of ?'h versus -r,reveal ature treatments: 4-8 hr at 25"C, 12 hr at if yellowfin and skipjack tunas are coni- 20"C, 12 hi- at 30°C. 12 hr at 2OoC, and pensating for increasing T, by reducing 12 hr at 25°C (Table 1). Six yellowfin tuna T,, as bluefin tuna seem to do (Carey and (YF 1-6) were subjected to consecutive Teal, 1969; Careyet ai., 197l)?That is, are 12-hr temperature treatments: 25", 20", the slopes of the regression of' Tt, on Ta 30"C, 20"C, and 25°C (7'able 2). Six other significantly different f.roin one? No such yellowfin tuna (YF 6- 12) were subjected to compensations occurred (Fig. 4); 'T, was an altered sequence of 12-hr temperature independent of. T,. The regression re- treatments: 25", SO", and 25°C (Table 2). lationships are: To eliminate any effects of thermal inertia. 1-h = 2.12 + 0.95 T, (yellowfin tuna) we analyzed only data collected aftei -I.,) stabilized following ambient temperature -rh = 3.14 + 0.97 -I., (skipjack tuna) changes. Some sets of data are incomplete Th is clearly highly dependent on T, and beCdUse the fish died prematurely or be- skipjack tuna are warmer than yellowfin cause it would not swim complete laps tuna. At 25"C, ttic fish in our experiment5 which are required for the logic equipment are 15°C cooler than those measured by to translate position inhrmation from the Barrett and Hester (1964) (27.7"C com- THERMOREGULATIONIN TUNAS 255

TRANSMITTER

THERMISTOR PROBE

FlG. 3. Schematic diagram of the annular test tank delivered to and removed from the swim channel system and of deployment of temperature-sensitive through countercurrent perforated pipes, so that ultrasonic transmitter on a yellowfin tuna. Seawater is longitudinal temperature gradients do not develop. pared to 26.2"C for the yellowfin tuna term acclimatory adjustments of the fish and 30.9"C compared to 27.2"C for caught by Barrett and Hester (1964). skipjack tuna), probably reHecting the The T, of skipjack tuna exceed those.of higher states of activity prior to capture of yellowfin tuna (Tables 1 and 2), but we do the wild fish. The differences in slope (0.98 not know whether this is due to activity dif- IJ.\. 0.81 and 0.95 us. 0.58, respectively) are ferences or heat exchanger efficiency dif- perhaps due either to the unknown past ferences. To resolve this, heat production thermal and activity histories, or to long- (Fig. 5, estimated by the following proce- A. E. DIZON AND K. w.BRILL.

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Cd = drag coefficient (dimensionless), a 35r- --Itemperature, velocity, and length dependent empirical constant equal to:

- C c= 10 RL-0.5 Y d- (2) - 30 W U3 where t KL nW = p.V.L./.-' (3) RL = Reynoldsnumber Iw = seawater viscosity (poise), a tem- W perature-dependent property. d 25 ul Brill (1979) estimated standard meta- 3 I bolic rate (SMR) for skipjack tuna as: 0 wn p - 1 53 W0.S63 2- . (4) where 20 P, = SMK (watts), W = weight (Kg). oL-___- IWe hope this is similar for yellowfin tuna. 0 20 25 30 TEST TEMPERATURE ('C ) Heat production within the muscle of the fish is assumed to be approximately FIG. 4. Linear regressbn of red muscle tempera- equal to Pl (the input metabolic power) ture (Tb)on ambient temperature (T,). Relationships are: Tb= 2.12 f 0.95 T, (yellowfin tuna) and Tb= 3.14 + 0.97 T. (skipjack tuna). The dotted line is Tb = T.. 6r----. - - - a dures, see also Webb, 1975; Sharp and A Francis, 1976; Sharp and Vlymen, 1978; 5B A

Ware, 1978; and Wu and Yates, 1978) was I ul used as a covariate because it accounts for c swim velocity, fish size, and the tempera- YELLOWFIN TUNA ture-dependent properties (viscosity and A A density) of seawater.

P, = (o.5-p.v~.s-cd.107).,--1 (1) where P, = input metabolic power to the swimming muscles (watts) 77 = muscle efficiency, in this instance I- the efficiency of- converting chem- ulw ical energy into propulsive power (dimensionless), -0.2 (Brown and I Muir, 1970; Webb, 1975). Note, the caudal fin is assumed to be 100% efficient; p = seawater density jg/cm) a tcmpera- 20 25 30 ture-dependent parameter; TEST TEMPERATURE ('C) V = swim velocity (cm/sec); S = surface area, which is approxi- FIG. 5. Estimated heat production (based on swim mately equal to 0.4 Lz where L is speed, muscle efficiency, and standard metabolic rate) at each test temperature. The lines are drawn fork length in centimeters (Webb, through the median heat production estimates. 0- 1975); skipjack tuna, A-yellowfin tuna. THERMOREGULATIONIN TUNAS 15Il minus the output power dissipated as In contrast to yellowfin tuna, skip-jack thrust, plus P, (the SMK), tuna exhibited great variability in whole body thermal conductance ovei- the three H,, = (1 - a)P, + 1'2 (5) test temperatures (Fig. 6). SJ 1, 2, 5, and 9 It thus appears (Fig. 5). that although showed a significant increase in K during the T, values of skipjack tuna are above the 30°C test treatment. For the othei tish. those of' yellowfin tuna, heat production in large changes in K were the only coninion- yellowfin tuna is generally higher. For both ality. In some rases, the alteration in T, fish, heat production increases with Ta. was appropriate. decreasing in the f'ace of Yet, here we have a contradiction. Fig- increasing I', and the heat load imposed ure 4 indicates no thermoregulatory abil- by faster- swiiiiniing; in othei, cases ic was ity, TXt-emains virtually constant over the not. However. the significance of' these 10" range of test temperatures. Hecause data are that alterations in swim speed, and heat production also increases at 30°C consequently, heat production were not (especially in yellowfin tuna, Fig. 5), heat accompanied by expected changes in I', dissipation 1-ate per degree of driving gra- (Tables 1 and 2). even though heat pro- dient must be greater at higher test tem- duction is inexorably linked to swim speed. peratures. The abilitv to maintain a con- Clearly, some mechanism intervenes to stant TXa1 various levels of heat production alter the pattern of heat loss, heat genera- suggests that heat dissipation per degree of tion, or both. driving gradient is variable, and possibly In our experiment, the changes in K controllable. were appropriate for therinoi-egiilation in Mammalian physiologists (Kleiber, six of the eight yellowfir] tuna but in only a 1972) often employ an index of' whole- few of the skipjack tuna. Exceptions were body thermal conductance to quantify not unexpected, because we are dealing thermoregulatory ability: with very small temperature changes within the thermal zones of tolerance for both species. We have also stressed these where fish by confinement, and by application of HI, = steady state heat loss (TI, is not the telemetry device. Under these condi- changing, therefore HL,= HP) tions, appropriate thei-rnoi-egulatory re- (watts), and sponses may have been impossible for K = whole body thermal conductance some of' the fish, or simply not necessary. (wattsPC). When a tuna is forced to swim at greater Whole body thermal conductance (K) in- speeds (and hence has higher internal heat cludes thermal conditions wit.hin the ani- production) in water temperatures close to mal and the environment (Tracy, 1972). its upper lethal temperature, thermo- Comparisons will be made only between regulation is more critical. We increased temperature treatments, not fish; we are swim speed in 23 skipjack tuna by inci-eas- concerned only with how K changes with ing their density which demands laster T, and not its absolute value. For this rea- swimming in ordei- to maintain hydrostatic son, absolute values of heat production are equilibrium. 'These fish have no swim Idad- less important and the use of K isjustified. der. Only three survived long enough to Yellowfin tuna seem the most adept at give meaningful data after force-feeding thermal regulation (Fig. 6). YF 1-5 arid YF the plastic-coated weights and attaching 8 seem to have controlled their heat dissi- the ultrasonic transmitter. Data were col- pation rate appropriately; K was greatest lected for 12 hi. at 25°C and subsequently at 30°C (close to upper preferred ambient 12 hr at 30°C (Talde 3).SJ I responded to temperature, 32"C, Sharp, 1978), re- the increase in ambient temperature by duced at 25°C. and reduced still further reducing both swim speed and muscle teni- at 20°C in some fish. YF 6 and 7 show no perature (Table 3), perhaps a behavioral apparent pattern, T, and K were uncor- thermoregulatory response. Because of related. the weights. SJ 2 and 3 apparently could 260 A. E. DIZONAND K. W. BRILL

YELLOWFIN TUNA

TEST TEMPERATURE ('C )

FIG. 6. The effect of ambient temperature on whole values of K based upon the 95% confidence limits of body thermal conductance (K). K was determined by mean swim speed and T,. Note: The K values for SJ 4 dividing estimated heat production by excess muscle and 5 are based upon T, of white muscle. temperature (T,J. Vertical lines represent extreme not reduce speed significantly, but T, de- an appropriate manner to reduce T, at creased nonetheless. Mean T, for SJ 3 at high ambient temperatures. But is a con- 30°C was 40% less than at 25"C, and we clusion of physiological thermoregulation estimated that heat dissipation rate in- appropriate? As suggested in the intro- creased 38%. This occurred with no change duction, several processes could serve to in swim velocity. stabilize or alter T, when a fish is con- fronted with changes in T, or increased POSSIBLE THERMOREGULATORY MECHANISMS metabolic heat production. As swim speed increases, increased heat Our data show that T, can change di- production may be dissipated at a lower T, rectly, inversely, or independently of swim because increased blood flow through the velocity and heat production (Tables 1, 2, countercurrent heat exchangers may re- and 3), consequently whole body thermal duce their effectiveness (Mitchell and conductance (K) changes quite dramati- Myers, 1968), thus allowing more heat to cally (Fig. 6). In addition, yellowfin tuna be dissipated via the gills. In addition, in- and weighted skipjack tuna seem to alter creased heat production may be more ef- their whole body thermal conductance in fectively dissipated at the body surface due THERMOREGULATIONIN TUNAS 26 I

'rAB1.F. 3. Crund mwn .\uiim .\peed.\ uud T,'s (9547, confidence limits) for .skipjack tuna weighted with PLmtic-coated lecui to 2ncreu.w .swim .\heed.

____ - ~~~ .. ~~___-~ Fork Weight Test temperatures (C) length Weight carried (cm) (g) (g) 25" 30" -__ ~.~~ . _~ ~ _ . ~ Skipjurk luiic~I 42.4 1,262 67.5 Swim speed (cmhec) 933221.31 89.18t 1.10 Temperature excess ("C) 2.7920.05 2.58+-0.04 Estimated heat production (watts) 3.62 3.30 K (wattsPC) 1.30+-0.05 1.2820.07 Shiplark funo 2 '44.7 1,405 86.7 Swim speed (cm/sec) 87.05r 1.50 84.445 1.81 Temperature excess ("C) 3.1550.06 2.28-cO.08 Estimated heat production (watts) 3.54 3.20 K (wattsPC) 1. I21t0.05 1.4620.08 Skippck tunn 3 41.6 1,174 211.5 Swim speed (cmhec) 96.27r 1.21 95.8820.83 Temperature excess ("C) 4.9620.21 2.9520.05 Estimated heat production (watts) 3.62 3.48 K (wattsPC) 0.73+0.05 1.18-cO.03 to enhancement of surface conduction due moregulatory mechanisms, T, obtains ab- to faster water velocity over the body surd levels at the sustainable speed of 4 (Tracy, 1972; Strunk, 1973; Erskine and lengthshec, even if the heat exchanger is Spotila, 1977; and Brill et al., 1978). Both only 25% efficient (;.e., 75% of the esti- processes must occur, but they cannot be mated heat production is dissipated via the the sole explanation for our data because gills). Clearly, in a real tuna, some mecha- we show T, and swim speed bear no fixed nism must intervene to increase thermal relationship. conductivity as swim speed increases, and Furthermore, the effectiveness of the this mechanism must have a greater dy- heat conservation system must drastically namic range than convective-enhanced decrease with increasing swim speed. A surface conduction or the reduction in ef- significant T, is generated at slow speeds fectiveness of the heat exchanger due to but the subsequent cubic increases in heat faster blood flow through its vessels. For production are effectively dissipated at these reasons and the lack of any predicta- reasonable temperature driving gradients. ble relationship between swim speed and Enhanced surface conduction due to water body temperature, we feel tunas are capa- velocity increases will not compensate for ble of some degree of physiological ther- the increased heat production caused by moregulation. faster swimming. If no physiological ther- There are two situations arising for moregulatory mechanisms are assumed to tunas in which changes in heat dissipation be operating, T, will rise approximately as rate per degree of driving gradient would the square of swini speed, since heat probe beneficial; 1) T, may be increased or duction rate is roughly proportional to decreased when ambient temperatures VZ."and surface conduction is propor- approach lethal limits and 2) increased tional to V0.5 (Sharp and Vlymen, 1978). heat production, brought on by fast Figure 7 is the T, velocity relationships of a swimming, must be effectively dissipated to hypothetical, non-thermoregulating yel- prevent generation of lethal muscle tem- lowfin tuna (the same size as YF 5); the in- peratures. We hypothesize that these two dependent variable in this mathematical exigencies may be met by physiological model (created by Sharp and Vlymen, 1978) processes involving changes in circulatory is swim speed, no changes in internal ther- patterns that alter the effectiveness of the mal conductivity or gill heat loss are as- heat exchangers or changes in the relative sumed. In the absence of any effective ther- contributions of the red and white muscle 45, (Kishinouyc. 1923: (;odsil and Hycrs, 1944), t hcrctorts heat gencixted aei-ob- callv t)y this niuscle is nor retained hut clis- sipatrd in thc sainc niiinner as non- thei.moconser.viIig fish, via the gills arid body surfac:r (Stevens and Sutterliri, 1976; Eiskine arid Spotil;r. 1977). We suspect that the contribution of red muscle fibets to propulsion may be limited to slow swim speeds. Control of the relative contribution of' the red and white muscle fibers to propulsion may also serve in tine control 01' T, in response to changing Ta.At high ambienl ternperatures white muscle, which con- tributes significantly less to the temperature hurden of the fish, may be used to a greater extent than red. Alternatively, circulatory modifications within the heat exchangers mav alter their effectiveness as thermal barriers. In fish, changes in watel temperature and activity significantly affect cardiovascular dynamics by altering FIG. 7. Predicted excess red muscle temperature (T,) of a nonthermoi-egulating tuna similar in size to the concentrations of. circulating catechol- YF 5 (66.4 crn Fi., 6.035 g body weight) as a function amines (Kandall, 1970; Stevens Pt ai., 1972; of swim speed. Calculation of T. is based on a model Watters and Smith, 1973). Stevens Pt al. of convective-enhanced surface conductance (Sharp (1974) show that the arterial vessels of the and Vlymen, 1978). The 100% function requires that all metabolic heat be dissipated at the body surface; central heat exchanger have thick muscu- the other two functions assume 504 and 254 of the lar walls, although apparently not inner- estimated heat production is dissipated through the vated. However, circulating catechola- body surface. The latter presumahlv represent situa- mines could modify circulatory patterns tions where the heat exchangers allow a greater pro- within the central and lateral heat exchangers portion of' metabolic heat to be disslpated via the gills. The open dot is the measured mean swim speed and and thereby alter their effectiveness. 77 mean T. of YF 5 at 25". I he latter mechanism may be more irn- portant in skipjack and yellowfin tunas, be- fiber systems to propulsion. cause the lateral cutaneous vessels, which The second exigency, prevention of supply blood to the white muscle and overheating, presents no conceptual prob- bypass the heat exchangers, are much lem. However, the notion that white mus- smaller than the dorsal aorta and postcar- cle fibers are only used at high, unsustain- dinal vein (Godsil and Byers, 1944), al- able swim speeds (only used anaerobically) though the cutaneous vessels may be must be discarded. White muscle fibers of highly distensible. 111 the other Tliunnu~ skipjack tuna have the enzymatic capacity spp., these vessels are well developed. to function aerobically (Hochachka et nl., 1978), and become active at velocities SUMMARY below maximum sustainable swim speed (Brill and Dizon, unpublished data). Other Tunas are thermoconserving fish that fish have been shown to use their white sometimes adjust their T, in an appropri- muscle fibers at sustainable speeds (Pritch- ate manner-lower in warm waters, higher ard rf nl., 1971; Bone, 1975; Bone et a/., in cool. Yet, investigators do not agree 1978). White muscle fibers of tunas are whether tunas can regulate T,, or even the supplied by circulatory pathways that biological advantage of having a T,. Three bypass the vascular heat exchangers thermoregulatory options are theoretically 7rHEKMOREGUl.ATION IN TUNAS 263 open to tunas: 1) Behavioral thermoregu- necessary power. As speeds increase, tem- lation, 2) passive thermoregulation, and 3) perature could be kept within acceptable physiological thermoregulation, in which limits by proportionally grading more heat dissipation rates per degree of driving white muscle fibers into activity. White gradient can be controlled. muscle has been shown to have significant Maximum muscle temperatures of re- aerobic capacity and to become active at cently landed skipjack and yellowfin tunas sustainable swim speeds. In addition, cir- suggested that as T, increased, ‘rh slightly culatory pattern alterations within the heat decreased. Is this physiological tempera- exchangers may serve to reduce their ef- ture regulation or the result of interaction fectiveness or to shunt proportionally of the effects of thermal inertia and past more blood around the heat exchangers. temperature and activity history? Thus, tunas have the capacity to control Telemetry measurements from large, T,’s by behavioral means, such as seeking free-swimming bluefin tuna have been more favorable environments or altering used to build a case for rapid physiological swim speeds to change heat production. In thermoregulation; subsequent analysis of addition, passive thermoregulation is pos- the same data demonstrated that the ther- sible due to significant thermal inertia. mal inertia characteristic (passive thermo- Thermal sequestering of the muscle by the regulation) of tunas is sufficient to explain vascular heat exchangers allows tunas to the observed temperature constancy. develop a significant T, and to maintain a To differentiate between the three temperature constancy extending from forms of thermoregulation, we devised an minutes to several hours depending upon experiment to monitor Thand swim speed size. Physiological thermoregulatory mech- and maintain T, for a time sufficiently long anisms seem indicated because of the labile so that only steady state Th’s were used for and independent nature of T, and accom- analysis. Yellowfin and skipjack tunas modation of very high heat production demonstrated alterations in swim speed during fast sustainable swim speeds. These that were not accompanied by expected adaptations, as well as acclimatory pro- changes in T,. Clearly, skipjack and yel- cesses, provide tunas with potent ther- lowfin tunas are not prisoners of their own moregulatory mechanisms for dealing with thermoconserving mechanisms. Most of their thermally heterogeneous habitats. the yellowfin tuna and about half of the skipjack tuna showed appropriate thermal REFERENCES conductance changes (K)-conductance rates rose with increasing T,. Skipjack tuna Barrett, 1. and F. J. Hester. 1964. Body temperature forced to swim fast at temperatures close to of yellowfin and skipjack tunas in relation to sea their upper lethal temperature, were able surface temperature. Nature (London) 203:96-97. Blackburn, M. 1965. Oceanography and ecology of to reduce T, without reducing swim speed. tunas. In H. 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