HEAT STRESS EFFECTS ON FETAL DEVELOPMENT DURING LATE GESTATION IN THE EWE 1,2. University of Illinois, Urbana, 61801
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1 HEAT STRESS EFFECTS ON FETAL DEVELOPMENT DURING LATE GESTATION IN THE EWE 1,2 D. E. Brown, P. C. Harrison, F. C. Hinds, J. A. Lewis and M. H. Wallace University of Illinois, Urbana, SUMMARY Forty-eight crossbred ewes were subjected to heat stress of short or long duration during the last third of gestation in a completely randomized design to determine the effects of maternal heat stress on lamb birth weight, lamb conformation and subsequent preweaning growth rate. s were spring range pasture, confinement on slotted floors in a heated room maintained between 28 to 38 C or in a slotted floor barn with feed intake equal to the feed intake of the 38 C housed ewes. Treatment exposure averaged 25 and 53 days for short and long duration, respectively. Lamb birth weights of heated, range and restricted fed ewes were 3.18, 4.57 and 4.16 kg, respectively. After adjustment for sex and multiple birth effects, birth weight of lambs from hot environment ewes were smaller (P<.01) for both durations of treatment. Lamb birth weights from heated ewes were smaller than those of lambs from restricted fed ewes (P<.05). Relative kidney and liver weights were greater in lambs from heated ewes (P<.05). Relative muscle weights and relative linear equivalent bone lengths were not different among ewe treatments. Lambs from heated ewes had 30 and 56-day weights similar to those of lambs from range and restricted fed ewe groups. Small Iambs resulting from maternal heat stress of 25 or 53 days duration are proportional dwarfs and occur independently of ewe level of nutrition. Department of Animal Science. 2Studies were conducted at the Dixon Springs Agricultural Center, Simpson, IL. The cooperation of Drs. M. E. Mansfield and D. Drori is gratefully appreciated. (Key Words: Sheep, Heat Stress, Pregnancy, Dwarfism.) INTRODUCTION Stress from high environmental temperature has been shown to lower fertilization rate and increase embryonic mortality in ewes (Dutt et al., 1959; Vincent and Ulberg, 1965; Thwaites, 1967). Impaired fetal development is a consequence of thermal challenge during the second and/or final third of gestation (Yeates, 1956; Alexander and Williams, 1971; Shelton, 1964a,b). Heat-induced fetal dwarfing has been characterized as proportional by Yeates (1958), but disproportional by Alexander and Williams (1971), who defined a proportional dwarf as a small birth-weight lamb with organ weights and bone lengths similar to the relative linear equivalent values of control lambs. Disproportional dwarfs (Alexander and Williams, 1971) were characterized as consistently larger in relative head components, body length, kidneys and adrenals and having relatively smaller liver, thyroids and biceps femoris muscle. Alexander and Williams (1971) also found that the degree of dwarfing was further influenced by level of nutrition. Shelton and Huston (1968), however, found no alleviation of dwarfing by increasing the dietary protein intake of heat stressed, pregnant ewes. A consequence of estrus induction methods developed over the last fifteen years is the sheep industry's goal to produce lambs throughout the year. Widespread implementation of this goal will bring the previously observed problem of fetal dwarfing to national attention. Thus, it is the purpose of this investigation to determine under controlled conditions if heatinduced fetal dwarfing can be produced independent of season in a period of time shorter than the last third of pregnancy, to determine if 442 JOURNAL OF ANIMAL SCIENCE, Vol. 44, No. 3,1977
2 FETAL RETARDATION IN SHEEP 443 dwarf lambs are disproportional and finally to determine the extent of dwarfing independent of ewe feed intake. EXPERIMENTAL PROCEDURE Mature Targhee x Suffolk crossbred ewes having 4.4 to 4.7 cm fleeces were range bred from October 28 to November 3 and from November 20 to December 23 to Targhee rams. The ewes were checked for pregnancy by sonar analysis on February 28, 1975 using the procedure described by Lindahl et al. (1975) modified with a 35.5 cm intrarectal transducer probe containing a 1.25 cm diameter crystal. Fortyeight ewes determined pregnant were randomly allocated in groups of 16 to range (R), restricted feeding in a slotted-floor barn (RF) or on slotted floors in a hot-room (H) treatment on February 28. Range (R) ewes were with a conventionally managed pregnant ewe flock on pasture. The H treatment consisted of two adjacent temperature controlled rooms. Each room contained two 1.2 m x 2.4 m slotted-floor pens to each of which four ewes were allocated. Average daily maximum and night minimum temperatures were 38 and 28 C and 38 and 32 C, respectively, in the two hot rooms. Relative humidity varied from 40 to 60%. The 16 RF ewes were allocated to four 1.2 m x 2.4 m pens in an open-sided, slotted-floor barn. They were fed daily a ground ration of 75% hay, 22% corn, 3% soybean meal equal in quantity to the H ewes previous day consumption. Rectal temperatures of all ewes in RF and H treatments were recorded weekly for 8 weeks between 8:30 and 10:00 am using a YSI tele-thermometer and thermistor probe at a depth of 6 centimeters. Heated ewes, when possible, were removed to a conventional lambing barn within 2 days of parturition, RF ewes lambed in their slotted floor pens and range ewes were checked daily for newborn lambs. At lambing, birth weight, ewe condition (fat, good, poor) and lamb condition (dead, weak, average, strong) were recorded. Randomly selected lambs from each treatment were necropsied within 6 hr after lambing and frozen intact for subsequent tissue and bone measurements. All ewes with remaining Iambs were managed as a single flock on mixed grass-legume pastures. Lambs were weighed at 30 and 56 days postpartum. Data were analyzed by multiple linear regression analysis of variance. The model accounted for the effects of duration of treatment, lamb sex and type of birth. R ESU LTS Rectal temperatures were significantly ele- TABLE 1. SPRING LAMBING PERFORMANCE OF EWES MAINTAINED IN THREE ENVIRONMENTAL CONDITIONS DURING THE LAST THIRD OF PREGNANCY Item Range control Restricted feed Hot room No. ewes preg. Ewe condition a Ewe disposition b Lamb % -- live c Lamb % -- total Avg birth wt - live, kg Avg birth wt - total, kg Lamb condition d ** "* ** ** al = Fat, 2 = Good, 3 = Poor. bl = Wild, 2 = Calm. CLambs + pregnant ewes 100. do = Dead, 1 = Weak, 2 = Avg, 3 = Strong. *P<.05 after removal of sex and multiple birth effects. **P<.O1 after removal of sex and multiple birth effects.
3 444 BROWN ET AL. vated (P<.05) in H ewes from week 2 through week 8 of treatment. Maximum rectal temperature elevation occurred after 3 weeks in the hot environment. At 3 weeks mean rectal temperatures were C and C for H and RF ewes, respectively. Lambing occurred in two distinct intervals following the initiation of treatments: between 19 and 32 days ( days) and between 44 and 66 days ( days). No effect of treatment duration on ewe condition or disposition or on live lambs born, lamb condition or lamb birth weight was found. Thus, data were pooled across duration of treatment and are summarized in table 1. The heated ewes produced fewer live lambs than RF or R ewes (P<.01). Mean birth weight of all lambs (live and dead) from H ewes was.9 and 1.4 kg less, resuectively, than all lambs from RF and R ewes, (P<.01). Live lamb birth weight of H ewes was similarly reduced (P<.01), with no interaction between birth weight and live vs dead lambs. Lambs at birth were weaker in H than in either R or RF ewe groups (P<.01). Relative organ and muscle weights and relative bone lengths (expressed as a proportion of the "linear equivalence" of birth weight, Lyne and Verhagen, 1957) of randomly selected lambs are presented in table 2. Of organs weighed, only the kidneys and liver of H lambs were larger (P<.0$) than the average of those of RF and R lambs, while the relative heart and liver weights of RF lambs were smaller (P<.05) than those of R lambs. There was a trend for all other organ weights to be a larger proportion of body mass in H treatment lambs. The linear equivalent bone lengths did not differ among treatments (table 2). Thirty-day lamb weights, 56-day lamb weights and percentage of lambs surviving at 30 and 56 days did not differ among treatments (table 3). Discussion Dwarfing. The reduced weight of lambs born to heat-stressed ewes during the entire last third of pregnancy agrees with the results of Yeates (1958), Goode (1964), Shelton (1964a,b) and Alexander and Williams (1971). However, the TABLE 2. RELATIVE ORGAN WEIGHTS AND BONE LENGTHS OF LAMBS FROM CONTROL, RESTRICTED FED AND HEAT STRESSED EWES Item Control c Restricted feed d Heated 9 Heart a (9) * Kidney (6) (5) (5)* Liver (6) (5)* (5)* Thyroid (6) (8) Spleen (5) (5) (5) Adrenal (5) (5) Extensor Semitendenosis Gastrocnemius Head length b Head width Humerus Radius-ulna Metacarpal II Femur Tibia-tibia Metatarsals (5) aorgans and muscles: tissue wt (g) + birth' weight (kg). bbone dimensions: length (em) + linear equivalent birth wt (kg -3 ). CMean +- SEM, n = 10 unless in parentheses. dmean + SEM, n = 6 unless in parentheses. emean + SEM, n = 10 unless in parentheses. *P<.05 after regression on sex and number of lambs per ewe.
4 FETAL RETARDATION IN SHEEP 445 TABLE 3. THIRTY AND 56 DAY WEIGHTS OF LAMBS FROM EWES MAINTAINED IN DIFFERENT ENVIRONMENTS DURING GESTATION Day of age Range Restricted feed Hot room ab (20) (23) (5) (18) (22) (5) amean +- SEM, kilograms. bno significant differences in lamb weights exist between treatments within age after regression on sex and number of lambs per ewe. fact that birth weights were reduced equally when the ewes were heat stressed for mean periods of 25 or 53 days indicates that dwarfing can occur with maternal heat stress during only the last month of pregnancy. A direct consequence of this finding is that late summer lambing in many parts of the United States appears susceptible to fetal dwarfing. No distinction between true stillbirths and lambs which died from lambing in close quarters of the slotted floor pens was possible. The significant reduction in lambs born alive is thus not comparable to the reduction in number of Iambs surviving 5 days postpartum from heatstressed ewes observed by Shelton (1964b). However, it appears that small H Iambs left with their dams on spring pasture overcome the deficit in birth weight within 30 days after parturition and have 56-day weaning weights similar to spring born lambs from non-heat stressed ewes. Factors Affecting Dwarfing. Ewes housed at prevailing spring temperatures with feed intake restricted to that of heat stressed ewes produced Iambs similar in weight to lambs of range ewes. Thus, the reduced birth weight of lambs from heat-stressed ewes occurred independent of the level of feed consumed. Lowered plane of nutrition may lead to reduced birth weights and be additive with heat stress in reducing birth weights only with very severe feed restriction, as observed in ewes fed one half of that consumed by heat-stressed ewes (Alexander and Williams, 1971). Data from the present experiment demonstrate that effective thermal environment alone will depress fetal growth. It remains to be determined if feed restriction of heat-stressed ewes would cause an additional depression of lamb birth weights. Alteration of gestation length by heat stress could also be an important factor affecting lamb birth weight as suggested by Shelton and Huston (1968). However, Yeates (1953) reported full term pregnancies of ewes kept in hot rooms for either the last 2/3 or 1/3 of pregnancy. Dwarfing has also occurred when all Iambs were deliver by Caesarian section between days 142 and 146 (Alexander and Williams, 1971). Yeates (1956) found that 7 hr per day of 41 C 60% RH was required to produce dwarfs in Romney Marsh ewes, while 45 C 60% RH was required to produce dwarfism in Peppin strain Merino ewes. Alexander and Williams (1971) found that 9 hr at 44.4 C and 15 hr at prevailing air temperature (highest mean daily minimum temperature was 23 C) was insufficient to reduce birth weight of Merino sheep, but that 9 hr at 44.4 C and 15 hr at 32.2 C resulted in birth-weight reductions of 1.0 to 1.5 kilograms). Shelton (1964b), however, reported that 10 hr per day of 38 C to 40 C and prevailing night temperatures was sufficient to reduce birth weights in Rambouillet crossbred ewes. Thus, results to date suggest that nutrition, ewe breed, and effective environmental temperature may all contribute to retardation of fetal lamb growth during heat stress of the pregnant ewe, but their exact roles arc not known. Type of Dwarfing. Since relative linear proportions of long bones were similar for lambs from heat stressed and control ewes, the present experiment suggests that intrauterine growth retardation rather than disproportional fetal dwarfing results from late gestation heat stress. Alexander and Williams (1971), following the procedure of Lyne and Verhagen (1957), reported that heat-dwarfed lambs were not proportional miniatures after linear measurements were expressed relative to the linear equivalence of birth weight (wtl/3). They
5 446 BROWN ET AL. found that relative head length and width, body length and relative kidney and adrenal weights were all disproportionately large, while relative weights of liver, thyroid and biceps femoris were all disproportionately small in heat-induced dwarf lambs. These data are in contrast to those of the present experiment. Twins were included in their statistical analysis without correction for multiple births and may have introduced bias in the t-rest employed. However, in the present study, after statistical correction for sex and number of lambs per ewe, only relative kidney and liver size were increased in lambs of heat-stressed ewes. Since fetal body temperature increases during maternal heat stress (Morishima et al., 1975) the observed simultaneous enlargement of kidney and liver could be the result of increased fetal metabolic activity during maternal heat stress. Heat does not appear to cause dwarfism through maternal hypothyroidism since thyroxine administration has failed to alleviate dwarfism (Shelton, 1965; Alexander and Williams, 1971). Suppression of placental development, however, may be a factor as dwarf fetuses have reduced cotyledonary mass (Alexander and Williams, 1971) and birth weights have been reduced by Alexander (1964) through surgical reduction of cotyledon numbers. Decreased uterine blood flow during heat stress has been hypothesized to be a potential cause of dwarfing by Leduc (1972) and Shelton (1964b). Roman-Ponce et al. (1976) have recently reported reduced mid-uterine artery blood flow in response to heat stress in nonpregnant ovariectomized ewes. Brown et al. (1976) also reported decreased uterine blood flow during heat stress in pregnant rabbits. LITERATURE CITED Alexander, G Studies on the placenta of the sheep (Ovis aries L.): effect of surgical reduction in the number of caruncles. J. Repro& Fertil. 7:307. Alexander, G. and D. Williams Heat stress and development of the conceptus in domestic sheep. J. Agr. Sci., Cambridge 76: 53. Brown, D. E., P. C. Harrison, F. C. Hinds, J. M. Lewis, M. H. Wallace and L. A. Cogburn Thermal effects on fetal growth and blood flow. J. Anim. Sci. 42:1340. (Abstr.). Dutt, R. H., E. F. Ellington and W. W. Carlton Fertilization rate and early embryo survival in sheared and unsbeared ewes following exposure to elevated air temperatures. J. Anita. Sci. 18:1308. Goode, L Effects of summer confinement upon ewe productivity. J. Anita. Sci. 23:906. (Abstr.). Leduc, B The effect of hyperventilation on maternal placenta/ blood flow in pregnant rabbits. J. Physiol. (Lond.) 225:339. Lindahl, I. L., J. P. Totsch, P. A. Martin and P. J. Dziuk Early diagnosis of pregnancy in sows by ultrasonic amplitude-depth analysis. J. Anita. Sci. 40: 220. Lyne, A. G. and A. M. W. Verhagen Growth of the marsupial Trichosurus vulpecula and a comparison with some higher animals. Growth 21:167. Morishima, H. O., B. Glaser, W. H. Niemann and L. S. James Increased uterine activity and fetal deterioration during maternal hyperthermia. Amer. J. Obstet. and Gynecol. 121 : 531. Roman-Ponce, H., D. Caton, D. H. Barton, W. W. Thatcher and C. J. Wilcox Thermal stress effects on uterine blood flow. J. Anita. Sci. 43: 301. (Abstr.). Shelton, M. 1964a. Relation of birth weight to death losses and certain reproductive characteristics of fall-born lambs. J. Anita. Sci. 23: 355. Shelton, M. 1964b. Relation of environmental temperature during gestation to birth weight and mortality of lambs. J. Anim. Sci. 23:360. Shelton, M Effect of heat stress and thyroxine implants during gestation on lambing performance and wool production. J. Anita. Sci. 24:288. Shdton, M. and J. E. Huston Effects of high temperature stress during gestation on certain aspects of reproduction in the ewe. J. Anita. Sci. 27:153. Thwaites, C. J Embryo mortality in the heat stressed ewe. I. The influence of breed. J. Reprod. Fertil. 14: 5. Vincent, C. K. and L. C. Ulberg Survival of sheep embryos exposed to high temperature. J. Anita. Sci. 24:931 (Abstr.). Yeates, N. T. M The effect of high air temperature on reproduction in the ewe. J. Agr. Sci., Cambridge 43 : 199. Yeates, N. T. M The effect of high air temperature on pregnancy and birth weight in Merino sheep. Australian J. Agr. Res. 7:435. Yeates, N. T. M Foetal dwarfism in sheep-an effect of high atmospheric temperature during gestation. J. Agr. Sci. Cambridge 51: 84.
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