The development of thermoregulation in two species of woodrats, Neotoma lepida and Neotoma albigula

Corn I, I b m h e m .

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THE DEVELOPMENT OF THERMOREGULATION IN TWO SPECIES OF WOODRATS, NEOTOMA LEPIDA AND NEOTOMA ALBIGULA ORLANDO A. SCHWARTZ* AND VERNON C. BLEICHt Department of Biology, California Slate University, Long Beach, CA 90840, U.S.A.

(Received 13 October 1975) Abstract---I. Con|parativc thermoregulatory development was studied in two species of woodrats, Neotoma lepida and Ncotoma all~i,qula. These species experienced a similar temperature loss when exposed to' low ambient temperatures during the pro-weaning period. 2. Assuming identical physiological systems and temperature loss as it relates to physical mass, N. atbitlukt would be expected to have a lower cooling rate than N. lepida, because N. alhi,qula is larger in mass at comparable ages. 3. The results of this experiment ~how the reverse to be true, and this suggests that N. h,pida develops thermoregulatory capabilities faster than does N. all~itjuht. This is presumptive evidence that N. albioMa, which develops more rapidly, expends proportionately less energy for thermoregulation and more for growth during the pre-weaning period than does N. 1~Tdda.

I NTRODUC'I'iON A l t h o u g h the classes Ayes a n d M a m m a l i a generally are c o n s i d e r e d to be h o m e o t h e r m i c , s o m e y o u n g birds a n d m a m m a l s d e m o n s t r a t e physiological characteristics typical o f p o i k i l o t h e r m i c animals. T h o s e y o u n g birds and m a m m a l s generally are hatched o r b o r n in an altricial c o n d i t i o n , being nearly n a k e d o r h a v i n g p o o r l y d e v e l o p e d p l u m a g e o r pelage. Such a n i m a l s are d e p e n d e n t u p o n their p a r e n t s for b o t h their supply o f food and for b o d y heat. P o i k i l o t h e r m y in the y o u n g of birds a n d m a m m a l s serves to parcel energy into m o r e rapid g r o w t h r a t h e r t h a n into the m a i n t e n a n c e o f b o d y t e m p e r a t u r e in altricial species ( B a r t h o l o m e w . 1968). S c h w a r t z & Bleich (1975) studied the r e p r o d u c t i o n a n d g r o w t h o f the coastal form of the desert w o o d r a t , Neotoma lepida intermedia, a.nd the w h i t e - t h r o a t e d w o o d r a t , Neotoma albiyula ven,sta, f r o m s o u t h e r n California. O u r g r o w t h study indicated that N. albigula d e v e l o p s relatively m o r e rapidly t h a n d o e s N. lepida in the following characters: ,weight, b o d y length, h i n d f o o t length, a n d in earlier a g e o f eye o p e n ing, a u d i t o r y c a n a l o p e n i n g , d e v e l o p m e n t o f sexual m a t u r i t y , d e v e l o p m e n t of adult sexual d i m o r p h i s m , a n d a p p e a r a n c e in traps. Neotoma albigula w e i g h e d significantly m o r e (P < 0.05) at all a g e s f r o m birth to 101 days. At 101 d a y s o f age, m a l e and female N. lepida a t t a i n e d 67.0 a n d 7 0 . 3 ~ o f the a d u l t b o d y weight, respectively, w h e r e a s m a l e a n d female N. albigula a t t a i n e d 85.1 a n d 87.2%, W h e n p r e l i m i n a r y results o f the g r o w t h study suggested that N. albiqula d e v e l o p e d relatively m o r e rapidly t h a n did N. lepida, the following experi m e n t was a t t e m p t e d to d e t e r m i n e a physiological basis for the difference in g r o w t h patterns. * Present address: The Museum of Natural History, University of Kansas, Lawrence, KS 66045, U.S.A. t Present address: California Department of Fish and Game, Box 1741, Hemet, CA 92343, U.S.A. 211

TIlE STUDY AREAS All N. lepida used in this study were born to pregnant females captured at the U.S. Naval Weapons Annex, Fallbrook, San Diego Coumy. CA. The climate there is mild, wilh warm. dry summers and mild winters IBleich. 1973: • Schwartz, t974). A! the Annex. desert woodrats were abundant in the Coastal Sage Scrub community, particularly in areas supporting a dense growth of the prickly pear cactus, Optmtia occidentalis. Shelter materials and food are abundant throughout the year. and woodrats build houses out of cactus joints. The study area from which all N. alhigttla w e r e obtained was the Carrizo Creek area of eastern San Diego County, CA. This area is characterized by hot, dry summers and harsh winters (Rainey, 1965; Schwartz, 1974). At Carrizo Creek, white-throated woodrats inhabit dense stands of mesquite (Prosopis jul~lora var. Torrcyaml). Mesquite shrubs generally grow in stands widely separated from each other. White-throated woodrats inhabit burrows constructed at the bases of larger mesquite plants and rely on mesquite for much of their food (Brown, I968; Schwartz, 1974). The number of shelter sites is limited, and food is abundant during the spring when leaves and beans appear on the mesquite. Neotoma albigula used in this stud), were born to pregnant females captured at Carrizo Creek, or were born to females bred in the laboratory. but which were originally captured at that locality. /MATERIALS AND METHODS The ability of the animals to maintain their body temperature when subjected to cold'stress was measured on alternate days, beginning at 3 days of age. After 23 days of age, the size and activity of the young made further investigation impossible. Six N. lepida and seven N. albigula were used in this experiment. Litters were housed in a temperature-controlled laboratory (range 22-24~C} throughout the study. Prior to subjecting individuals to !ow ambient temperatures, a Yellow Springs Instrument Co. telethermometer fitted with an air probe was used to measure the nest temperature, ambient temperature (laboratory), and temperature of the refrigerated constant temperature chamber. Body temperatures of the young woodrats were measured with a quick-reading Sehultheis mer-

212

()RI.ANIX) A. ~'tIWARTZ AND VI:rt.NON

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cury thernlolllcler its the}' ~A'cr¢ from the nest, :tnd again after 15 rain in the cold chamber. Deep body temperan~res were approximated by placing the tip of the thcrnlometcr on the Inid-verdr;!l sttrfacc of the animal's body so thai the entire thermometer tip was encircled (McM;tnus, 19711. Readings gcncndly stabilized in less than 30 see. To minimi/e Ilucltmtions of temperature within the cold ch,mfl~er, it 25 I. container t~f water v,-as placed in the chvmber, alld a weighted 5|. beaker was phtced in Ihe water. "l'he beaker wits floored with two layers of cardbo~trd for inst,hllion, a n d a screen top was fitted to prevent the escape t~f older animals. Temperature in the c h a m b e r averaged 7.6 (" (range 6.9 8.(~, ). After exposure to the lowered tcnlpcrilttlrcs alld prior to their return to the nest, young woodrats tip to nine days of :age were warmed for scvcr, I minulcs with an infra-red htmp to help elevate their body tcrnperatttrus. In this manner, the shock to the mother of having a cold offspring phtced in the nest was minhnizcd. After exposure, all woodrats were weighed to the ne;tresl ().1 g.

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Nest t e m p e r a t u r e s t a k e n before r e m o v a l o f y o u n g from the nest w e r e s i g n i l i c a n t l y w a r m e r {P < 0.011 for N . alhi~l,ht ( X = 31.0, S.E. = 0.20, N = 33) t h a n for N . h,pi&s (j~r = 28.6, S.E. ~- 0.27, N ~ 22). T h i s differe n c e w a s a t t r i b u t e d , subjectively, to the t e n d e n c y o f N . a l h i q u h t to h u i l d b e t t e r n e s t s from t h e c o t t o n b a t ting s u p p l i e d in the l a b o n t t o r y . A l i n e a r regression line was used to c h a r a c t e r i z e p r e - e x p o s u r c b o d y t e m p e r a t t u - e (7]), a n d a polyn o m i a l r e g r e s s i o n e q u a t i o n to the t h i r d p o w e r w a s used to lit lines to p o s t - e x p o s u r e b o d y t e m p e r a t u r e d a t a ('/~,) as a f t m c t i o n o f a g e (Fig. I). T e m p e r a t u r e loss w a s c a l c u l a t e d by s u b t r a c t i n g p o s t - e x p o s u r e t e m p e r a t u r e s from p r o - e x p o s u r e t c m p e r a t t t r e ( 7 ] - 7~), a n d a simihtr p o l y n o n a i a l regression was used to fit c u r v e s to t h e s e net t e m p e r a t u r e loss data as a f u n c t i o n o f a g e (Fig. 2). W h e n p l o t t e d its a f u n c t i o n o f age, t e m p e r a t u r e loss w a s s i m i l a r for tx~th species. T o b e t t e r illustrate t h e t h e r m o r e g t d a t o r y differences o f t h e t w o species, i n s t a n t a n e o u s c o o l i n g r a t e s ( I C R )

19

2t

23

Fig. 2. (Ti -- 7"2) its a function of age in N. /epida and N. alhigula. w e r e c a l c u l a t e d for b o t h species for ealch e x p e r i m e n t a l r u n u s i n g the f o l l o w i n g f o r m u l a : I C R = In(T2 -- " ~ ) -

R 1"2'qU 1.'l'H

17

Age in clays

I n ( T I -- T~)/t

w h e r e (hi) is t h e n a t u n d l o g a r i t h m , (T,) is the p o s t - e x p o s u r e b o d y t e m p e r a t u r e , (T,) is the p r e - e x p o s u r e b o d y t e m p e r a t u r e , (T0 is t h e a m b i e n t t e m p e r a t u r e o f the c o l d c h a m b e r , a n d (t) is t h e l e n g t h o f e x p o s u r e in the c o l d c h a m b e r (t = 0.25 hr). T h i s f o r m u l a w a s d e r i v e d by s o l v i n g t h e f o l l o w i n g e q u a t i o n ( K l e i b e r , 1972): (dT/dt) = r(Th -

T3

for t h e r a t e c o n s t a n t . T h e I C R ' s as a f u n c t i o n o f w e i g h t w e r e p l o t t e d for b o t h species u s i n g a p o l y n o m i a l r e g r e s s i o n (Fig. 3). T h e s e c u r v e s w e r e c o m p a r e d statistically u s i n g t h e c o v a r i a n c e t e c h n i q u e d e scribed by S c h w a r t z & Bleieh (1975), a n d f o u n d to b e s i g n i f i c a n t l y different in s l o p e a n d i n t e r c e p t Weight, 0 --

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30

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Fig. i. Pre-exposure temperature (T0 and post-exposure temperature (T2) as a function of age in N. lepida a n d N. alb~mla. Equations are as follows: T~ for lepida, Y-- 0.124X + 33.g31: "Ft for albigula Y = 0.05IX + 35.I52. T_, for h,pMa. Y = 22.665 + 0.958X -- 0.0178X 2 + 1.175 x 10-4.V3; Tz tbr albi~juk,; !,'= 21.877 + 1.227X -0.0259.Y 2 -- 1.0514 × 10-*X s.

-I.B

Fig. 3. Instantaneous cooling rate (ICR) as a function of body weight in N. lepida a n d N. albigula. Equations are as follows: for lepida, Y = - 8 . 5 0 3 + 0.852X -0.0297X 2 + 3.564 x 10-4XS: for albigula, Y-~ --3,334 + 0.123X - 0.001lgX 2 + 2.066 × IO-~X ~.

TIle dcvclol-~lnent of Ihcrmorcgill:.lliorl ill v,oodrzlln

(P < 0.01). When ICR's were plotted as a function of surfitce areu inot illustrated}, it resuh similar to Fig. 3 was obtairlcd. Surfltce area was considered Io bc proportional to weight to the two-thirds power. DISCU,~,.~',.!;0 N Brown & Lee (1969) postulated thal in closely related animals of difl;:rent sizes, three Ihctors are important in their eft~'ct on heat loss: 11) bod~ starl'ace. which varies with the two-thirds power of wci~,ht in animals of the same shapc: (21 insulation: {3) evaporation of water from the skin and respiratory surl'accs. In our study, development of pelage was simihtr in both species and is thus u n i m p o r t a n t in causing a difference in tenaperuture loss. EviqSorative loss was considered to be minimal at the cold c h a m b e r temperature and is not considered signilicant in this study. This leaves the ditlbrencc in surlhce area as the primary avenue for heat loss, N c o t o m a l¢'pida and N. alhi~itdtt showed similar temperature losses when exposed to low ambient temperatures, Assuming identical physiological systems and physical mass as they relate to the instantaneous cooling rate. o n e would expect the smaller animal iN, h,phla) to have a higher cooling ntte than the larger animal (N, alb(quhO. Smaller animals have a higher surface a r e a / v o l u m e ratio, a n d thcretbre a relatively greater surface area for heat loss. T h e reverse of this result was obtained in o u r experiment. Ncotomct alhi~3ula cooled at a higher ratc than did N. lepida through the pre-weaning period. T h e results of this experiment suggest' that the differences in homeot h e n n y in yotmg N. h'pida and N. albiqtda are tied to the development of physiological systems, and that these systems develop more rapidly in h7;M, than in albiguka. In N. lepida, more rapid ontogeny o f thernmreguhtlion is coupled with a more prolonged period of morphological development, and in N. alb¢cdula it slower ontogeny o f thermoregulafion is coupled with a more rapid morphological development. N e o t o m a lepida probably expends more energy for endogenous heal production and less for morphological development than does N. alhi,qtda. Schwartz & Bleich (1975) have suggested that a m o r e rapid growth rate in N. albiqula is part of a reproductive and growth strategy to adapt it to a harsh desert environment, Parturition in N. albiffttla at Carrizo Creek begins at the same time as the appearance of semisucculent leaves and beans of the mesquite in late March. and then ceases prior to the onset o f summer heat in mid-June. An accelerated development would be necessary for young to achieve near adult size prior to the onset of summer heat, In contrast, N. lepida inhabits a more moderate climate with food and moisture resources available

throughout much of the year. Most breeding occurs from N o v e m b e r to April, and growth is slower. An additional adaptive advantage of more rapid growth in N. albigtda may be related to the dispersal pattern of this species. Stands of large mesquite appear to be the most desirable shelter-sites for the white-throated woodrat. T h e larger mcsquitc arc located in disjunct stands which are frequently widely

separated, A dispersing juvenile may be required to

213

travel over a comparatively long distance i,~ seeking a desirable shelter-site. M o r e rapid n~orphologieal dcvclopnlClll COtlJtl bc all a d v a n | a g e 1o il woodrat the.it was required to seek out i~ shelter-site in un environmeat becoming more stressful with Ihc Ollsel of SUlYImer heat. Similm' she|ter-sile and environmental prcsstu'es do not .:tl'Jpe:.tr to allL'ct coastal N. lt7~itht. The rest,Its of this st0dy suggest the lollowing consequences o f difl;ering growth rates in mammalian iili: histories. If a species achieves more rapid growth by partitioning more energy into growth than into heat -prodttction. increased time and energy h)l" n]a|Cl'llal c;.ne ;Alltt/or il]cFcilscd h~sulatioll arc is required to inailltain its body tenll-)erltture above that provided by its intrinsic l'~hysiological systems. This hypothesis is SUl~ported 133' the observation that N. all~iquhl built better nests and maintained higher.nest temper:~tures in the laboratory, Also. N. a. t'emtsta is one of the few burrowing woodrats, whereas most species build above ground nests. The w o o d r a t nest serves the p,'inmrv functions of protection from predators and from environmental extremes, but in the case of N. a. I't'ltllSttt lnily also serve to betlcr insulate the young during develo[maent. Development from an altricial condition in m a m mals appears to be a complex function of available environnaental resources, intrinsic physiological systcms. energy Sl'~enl iri maternal care. aim the insulative protection of lhc young.

Ackmm'h,d.qeluentx -We would tike to thatak Dr. C. W. Hill. California State University. Long Beach, lbr advice in design and execution of this research, and Drs. K. B. Arlnitage und R. S. Hofl'maml. University of Kansas, for itssisl;.tn¢c ill prcpilrZllion t)l' the nl;.tntlsCril3t.

REI:F.I~ENCES BAI,ITIIOLOMI:WG. A. (1968) Body temperature and energy metabolisn~t. In /ltlimal ]:unction: Pritwiples and Ath~ptathms. (Ediled by GomxgN M. S.). pp. 290 354. MacMilkm, New York. BLrw~s V. C. (t973) Ecology of rodents at the United States Naval Weapons Station Seal Beach. Fallbrook Annex. San Diego County. Californim Master's Thesis. California State Univ.. Long Beach. BROWN J, H. (1968) Adaptation to cnvironmentfil temperature in two species of woodrats. Ncotoma cirterc'a and N. alhiytda, l~[i.sc. PuhL Alux. Zool.. Utliv. Michi[lml I35. 1-48. BROWN J. H. & LH! A. K. (1969) Bergmann's rule and climatic adaptation in woodrats (Neotoma). Ecohttiott 52, 792--792. Kt.Hm-g M. 11972) A new Newton's law of cooling? Sciem'e. N.E 179. 1283-1285. McMANuS J..I. (1971) Early postnatal growth and developrnent of temperature regulation in the Mongolian gerbil. Meriones tUl~.jtffcukttus, d. Manlmal..52, 782-792. RAINLW D. G. {1965) Observations on the dislribution and ecology of the white-throated wood rat in Calitbrnia. Bull So, Cali[: Accld. Sci. 64, 27-42. SCHWAt~TZ O. A. It974) Comparative growth in two species ofwoodrats. Master's thesis. California State Univ.. Long Beach. SCHWARTZ O. A. & BLHOt V. C. (1975) Comparative growth in two species of woodrats. Neotoma lepida intermedia and Nt'otOnRl albiqula rem&sra, d. Mammal 56, 653-666,