Thyroid hormone secretion rate and biological half-life (t12 ) of l -thyroxine-131I in the musk shrew (Suncus murinus)

GENERAL

AND

COMPARATIVE

Thyroid Hormone L-Thyroxine-

12, 536-540

ENDOCRINOLOGY

Secretion

(1969)

Rate and

1311 in the Musk

Biological

Shrew

(Suncus

Half-Life

(t,,,)

of

rnurir~us)~~~

G. L. DRYDEN Department

of

Biology,

Slippery Rock Pennsylvania

State 16057

College,

Slippery

Rock,

AND

T. R. BAUMAN,3 Departments

of Dairy

C. H. CONAWAY; Husbandry’s” Columbia,

Received

AND

and Zoology,’ Missouri 65201

September

R. R. ANDERSON5 University

of Mkwuri.

19, 1968

A mean thyroid hormone secretion rate (TSR) of 1.61 pg/lOOg body wt/day was determined for 26 Asian musk shrews (Suncus murinus) born and raised in captivity. Young females had statistically higher TSR’s (1.90 + 0.17 /rg) than old males but the biological significance of this is unknown. The mean TSR of the entire group is not excessive for mammals in this weight class (mean 32.2 g) and is actually less than that of the Missouri Valley mole. The mean tfjf of L-Ta in young males and females (15.19 + 0.98 hr) is significantly shorter than in old males (20.38 * 0.46 hr) when Tapazole is administered to prevent la11 recycling. An overall mean tl,? of 18.08 + 0.28 hr for 17 shrews does not indicate inordinate thyroid act,ivity when compared with the tlfl of laboratory rodents. These data indicate that the thyroid acbvity, and presumably, the overall metabolic rate of this tropically distributed insectivore species does not justify placing Sunczta mwin~ts in a metabolically peculiar category.

Because some species of shrews are among the smallest mammals and others consume relatively huge amounts of food, the shrews in general have been assumed to exhibit unusually high metabolic rates. This concept was supported by Morrison and Pearson (,1946), Pearson (1947, 1948) and Buckner i1963) who reported oxygen consumption rates of several species of temperate climate, North American shrews greater than would be predicted on the basis of their body size. Oxygen consump-

tion rates of various t’issue slices of Cryptotis pnrvcc (Redmond and Layne, 1958) and whole body heat production by several species of resting British shrews (Hawkins et al., 1960) suggest, however, that the metabolic rates of t,hese shrews (also temperatc climate species) are not higher than would be predicted for mammals of their weight class. More recent oxygen consumption determinations by Gebczynska and Gebczynski (1965) and Gebczynski (1965) for the same species studied by Haw.kins et al. disagree with the concept that these animals possess “standard” metabolic rates for their size and thus reopen the controversy. Gebczynski (1965) suggests that of their disadvantageous body hWaUSC weight : surf ace arca ratios and high-protein

‘This work is a contribution from the Missouri Agricultural Experiment Station Journal Series No. 5465. Approved by the Director. ’ Aided in part by a grant from U. S. Atomic Energy Commission, Contract AT (11-l) COO1758-5. 536

THYHOID

SECRETION

diets, the small shrews are indeed more metabolically active than are vegetarian rodents of comparable weight, as originally suggested by Morrison and Pearson (1946). Detailed physiological investigations of tropical shrews are unreported and, excepting a study of the thyroid hormone secretion rate (TSR) in a mole (Leach et nl., 1962), the endocrinological bask of metabolic activity of the insectivores has been ignored. Xumu mwim~s, a tropical soricid, has recently been adapted to captivity (Dryden, 196Sj and may become suitable for routine laboratory investigations. Since the insectivores are rcgardcd as the most primitive living Eutherians (Simpson, 1945) and determinations of metabolic rates in tropical shrews have not been reported, the TSR and biological half-life It ,,.‘) of L-thyroxine-‘“‘I in SMZCILSmwims are presented for comparison with other metabolic indices of temperate climate shrews and with the same indicts of more ad\-anced Eutherians. MATERIALS

AKD

METHODS

The shrews usc,d in this study were from thr CJniversity of Missouri captivr colony and wrrr maintained under 14 hr of artificial illumination at 25.5 k 1” for 2 wreks prior to TSR or t,/? determination. Thry mercl fed Gaines Meal and water nd Zihitum. Shrews brtwc,cn 40 and 90 days are arbitrarily classified as “young” xathrr than juvenile and those oldrr than 90 days as “old” Ante sexual “adulthood” is attaincld shortlyaftor leaving the nest, at about 4 wcek~, espe&lly 1~) females (Drydrn. 1969). Tht, 26 animals ranged in weight from 1%48 g with a mean of 32.2 g. The method of determining TSR was based on a modification of that, of Grosvcnor and Turner in which 0.5 mp of mcthitnazolc (1 (1958) methyl-2 mrrcaptoimidazolc~) was injected subc.utancouslp daily to block recycling of ?I from met,abolized thyroxine. The shrews were injected intrapcritoneally with 5 PC.3 of carrier-frcr Y in :I I-olumc of 0.5 ml and 48 hr was allowed for maximum uptake by thr thyroid. Estrrnal thrroid c*ounts were made under light, cthcr anesthesia b> pla&p thr thyroid area over a scintillation probe connt~ctcd to :I Picker analytical ratcmeter. Thyrosin? (L-T.,) injrctions were\ begun at 0.75 pg/ 100g h0d.y wt per da.v an d incrcxsed in incremc,nts of 0.25 &g/100 g body wt every other day. M+~thimzaole (Tapazole) was injected concomittantly with thyroxine. The thyrosinc dosage was

KATE

OF

MHlZE\VS

537

increased

every second day, after the thyroid made, until a dosage was reached that blockrd rtlease of thyroidal V. The inhibiting dose was recorded as the ent.imat.cd TSR. TSR values reported herein are the thyroxine cyuiralents of the animal’s rndogenous srcretion of both thyroxine and triiodothyroninc. Sincr the method is basrtl on c.ompletc inhibition of t,hyroidal lx11 release, the values must be in slight ~‘scess of the actual secrc,tion rate. For t, 2 of L-T, dctcrmination. each shrew was lightly anesthrtizrd with t,thcr and injected intracardiall>wit,11 1 $3 inppros. 0.04&0.05 pg) of thyroxine-““I. Initial whole body counts were made at 12-hr postinjrction with subsequent counts at approximately 24, 48, and 72 hr. T1,?‘s mere drkrmined in tht> same shrews with Tapszole 1 month after the control determinat,ions without Tapazole. Tapazole was injected subcutaneously daily at the level of 0.5 mg/lOOg bocl) wt for 2 days prior to thyroxine-‘“‘1 injection and until the last. rount was mad<~. Whole body caounts xere mndc by restraining ihc shrews in a commercial. I,lastic animal holder under a very sensitive Packard licluid scintillation whole hod, counter with 2 n gc~omctry (I,ow I,cvrl Radiation Laboratory, IJnivtGty of Missouri). Individual l,,Z’s wcrr culculatcd l)y ttw rlif~ttmd of least squares and plottc(l on scmilop lx,ljrr. Vkual inspection of the rc>rultant slol~ indirat,td c3ticntually a straight linr dcc.rciase in radioactivity from 12 through 72 hr. The thyroxine-‘“‘1 was supldied by .ibbott Laboratories, St. Louis. MO. nntl was guaranteed to he not less than 90%. L-T,. Differences in group means wcr(x nnalyzcyl statistically by Student’s t tcsl.

count was

RESCLTS

The mean rl‘SR for the cntire group of 26 shrews was 1.61 i- 0.072 pg L-T,/lOO g body &/day. Adult males averaged 1.53 -+ 0.068 pg L-T,/loO g body wt/day with a range of 1.25-2.0 pg. There was no statistically significant. difference between the mean TSR of old males and that of all young shren-s (I .7.i k 0.15 pg) which ranged frown I .O to 2.25 /~g. The mean TSR of young females (1.90 -t 0.17 ,lg), howhigher (p < .05) c’vcr, was statistically than that of old males even though all malts, as well as tbc young of bot,h sexes, had comparablr TSR’s (Table I ‘1 When Tapazolc was administered to prevent recycling of ‘“‘I from mctabolizcd thyroxine, the mean tllL’ of L-T, in 17

THYROID

SECRETION

shrews w,as 18.08 + 0.28 hr, ranging from 11.68 to 26.76 hr. This was significantly shorter (p < .OOl) than the mean tl,? of 25.73 4 0.21 hr in 21 shrews determined earlier in the absence of Tapazole. Under Tapazole treatment the mean tl,? of 20.38 -+ 0.46 hr in 10 old males was significantly (p < .Ol) longer than in 7 young males and females which had a mean tl,? of 15.19 & 0.98 hr. The t,,-‘s were quite variable in all shrews: (with Tapazole treatment) 14.89-26.76 hr for old males, 11.68-18.91 hr for young males, and 13.13-16.33 hr for young females. Mean t+‘s of young males and females were statistically comparable (Table 1) in in-treatment groups.

RATE

OF

SHREWS

539

mediate between 11.3 hr for adult female Mus (Anderson, unpublished data) and 19.5 hr for adult female Rattus (Grossie et al., 1965). Young Suncus exhibit significantly shorter t+‘s than do older shrews (15.19 hr vs. 20.38 hr) but this pattern is common in other species also. The t,,? of young Suncus, while shorter than that of adults (15.19 hr), is intermediate between that of very young Bos (14.88; Mixner and Lennon, 1959) and juvenile Procyon (19.68 hr; Bauman et al., 1965). These data on thyroid act’ivit’y in calltive Suncus do not directly refute the rcports of Morrison and Pearson (1946)) Pearson (1947, 1948), Gebczynska and DISCUSSION Gebczynski (1965), and others which indiThe thyroid secretion rates of Suncus cate highly elevated metabolic rates in nzurinus, as determined under the condi- small (SW Gebczynski, 1965 for weights of tions described, fail to indicate that this various species studied) wild-caught, temspecies exhibits an extraordinary metabo- perat,e climate shrews. Certainly the diminlism. The overall TSR of 1.61 ,ug/lOO g utive size of some species may place them body wt/day is below that of both Scalopus in a special metabolic category as Pearson (1.96 pg) and Didelphis (1.72 pg for adults (1948) suspected. Since our shrews were and 2.65 pg for juveniles) determined in accustomed to captivity it is possible t’hat the same laboratory under similar condi- the present findings might not necessarily tions (Leach et al., 1962; Bauman and reflect the metabolic activity of the same Turner, 1966). It is, however, higher than species under natural conditions. Our data that recorded for smaller (Mus and Per- do indicate, however, that these comparatively large, tropical shrews, born and omyscus) and larger (Rattus and Cnvia) rodents in the summer (see Bauman et al., raised in captivit,y, exhibit thyroidal (and presumably general metabolic) activity 1965). While young female Suncus have statis- more in lint with those of other non-soricid tically higher TSR’s t,han old males, the Euthcrians. Perhaps much of the existing biological significance of this is unclear un- diversity of opinion about the metabolic less it is an expression of the lesser body rates of the smaller species will be reconweight of the young females. No difference ciled as thcsc species are adapted to capin TSR due to sex or age was found in tivity and then investigated. When these the only other insectivore, Scalopus, for species are available, care still must be which data are available (Leach et al., t,aken to determine the met’abolic rates with minimal disturbance to the subject as 1962). The tl,? of L-T, in Suncus also support,s recognized by Hawkins et al. (1960). The the concept that thyroid activity in this effects of seasonal and daily activity speciesis not excessive although values ob- rhythms of t’emperate climate shrews on tained for young females indicate greater metabolic processesdiscussed by Gehczynthyroid activity than in old males, as do ski (1965) may also persist under controlled environmental conditions and must he TSR values of both groups. Assuming that a more realistic t,,? is obtained when Is11 considered, especially in short-duration dcis prevented from recycling by Tapazole, terminations. Until such drterminat.ions 18.08 + 0.28 hr for all Suncu,s is not an under carefully controlled conditions are made, we suggest that generalizations reunusually short, time. This value is inter-

F M,F

M M

SC?%

16 5 5 26

34.91 33.62 22.53 32.2

Mt%n body weight k)

SECRETION

1.25-2.0 1.0-2.25 1.25-2.25 1.0-2.25

R%ii Of (rg/lOO g body wt/day)

R.~TES

AND

1.53 1.60 1.90 1.61

I? 4 ‘r +

0.06P 0.230 0.1705 0.072

Me%i sEa (dlO0 g body wt/day)

BIOLOGICAL

12 4 5 21

1

22.17-38.38 23.43-29.35 21.06-24.54 21.06-38.38

R,&lkgiYf

Without

Tapasole

OF L-THYROXNZ~~~I

TABLE

No. of animals

HALF-LIFE

26.90 25.92 22.78 25.73

“Y*

(control)

IN

zk * + *

f

0.44 0.83 0.37 0.216

SE

YOUNG

(Y)

10 4 3 17

No. of animals

AND

With

MUSK

Range of t,/x hr

(0)

14.89-26.76 11.68-18.91 13.13-16.33 11.65-26.76

OLD

a SE = Standard error. b Differencesingroupmeans were analyzed by Student’s t test as follows: 1 vs. 3 significantly different at p < .Ol, 2 vs. 3 significantly 4 vs. 5 significantly different at. p < .05, 6 vs. 9 significantly different at p < 001, 7 vs. 8 significantly different at p < .Ol.

Y Y 0,Y

0

Age

% animals

L-THYROXINE

20.38 15.49 14.81 18.08

Mean

5 + + +_

0.46’ 1.00 0.6g8 0.2P

f SW h/z br

different at p < .OOl,

Tapaaole

SHREWS

2 + r

i2 3

:: 4

540

DRYDEN

garding the metabolic rates of the shrews as a taxonomic group be reserved to aw,ait furt,her investigative clarification. REFERESCES T. R., CLAYTON, F. W., ANU TURSER, C. W. (1965). The L-thyroxine stlcretion rate, L-triiodothyronine equivalent, and biological half-life (t& of L-thyroxinc-I’3’ in the raccoon (Procyor~ lotor). Gen. Comp. Endocrinol. 5, 261-266. BAUX~N, T. R., API’D TURSER, C. W. (1966). L-thyroxine secretion ratrs and L-triiodothyronine equivalents in thr opossum (Didelphis virginianus). Gen. Comp. Endocrinol. 6, 109-113. BUCKNER, C. H. (1963). Metabolism, food capacity and feeding behavior in four species of shrews. Can. J. Zool. 42, 259-279. DRYDEN, G. L. (1968). Growth and development of Sucus mwinus in captivity on Guam. J. Ma,tnm. 49, 51-62. DRYIXX, G. L. (1969). Reproduction in Suncu.~ mutitus. J. Reprod. Fertility (Suppl. No. 6) (in prrss). GEBCZYNSKA, Z., AND GEBCZYNSPI, M. (1965). Oxygen consumption in two species of watcrshrews. Acta Theriol. 10, 209-214. GEBCZYNSKI, M. (1965). Seasonal and age change in the metabolism and activity of Sorez arnnezls Linnaeus 1758. Acta I’hetiol. 10, 303-331. GROSSIE, J., HENDRICH, C. E., AND TURNER, C. W. (1965). Comparative methods for determining biological half-life (t& of L-thyroxine in norBAu.MAN,

ET

AL.

mal, thyroidectomizrd and methimazole treated female rats. Proc. Sot. ExptZ. Riol. Med. 120, 413-415. GROSVENOR, C. E., .~ND TURNER, C. W. (1958). Effect of lactation upon thyroid secretion rate in the rat. Proc. Sor. Exptl. Riol. Med. 99, 517519. HAWKINS, A. E., JEWELL, P. A., AND TOMLINRON, G. (1960). The mrtabolism of some British shrews. Proc. Zool. Sot. London 135, 99-103. L~ac~r, B. J., BAUMAS. T. R., AND TURNER, C. W. (1962). Thyroxine secretion rate of the Missouri Valley mole (Scalop7ra aquaticru). Proc. Snc. Exptl. Riol. Xed. 110, 681-682. MIXNER, J. P., AND LENNON. H. D., JR. (1959). Thyroxine secretion ratps in dairy cattle as calculated from plasma lrvels, turnover rates and volumes of distribution of thyroxine. Intern. Dairy Congr. Proc. 1, 20. MORRISON, P. R.. AND PEARSON, 0. P. (1946). The metabolism of a very small mammal. Science 104, 287-289. PEARHOS, 0. P. (1947). The rate of metabolism of some small mammals. Ecology 28, 127-145. PE.~RSON, 0. P. (1948). Metabolism of small mammals. with remarks on the lowrr limit of mammalian size. Scietbce 108, 44. REDMOND, J. R., AND ~,AYNE, J. x. (1958). 11 consideration of tho mct,abolic rates of some shrew tissues. Science 128, 1508-1509. SIMPSON. G. G. (1945). Principles of classification and a classificat,ion of mammals. BUZZ. Am. Museum Nat. Hist. 85, l-350.