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J. Anim. Sci. 2006. 84:1093-1101
© 2006 American Society of Animal Science

ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION

Maintenance of body temperature in the neonatal lamb: Effects of breed, birth weight, and litter size1

C. M. Dwyer2 and C. A. Morgan

Sustainable Livestock Systems Group, SAC, West Mains Road, Edinburgh, EH9 3JG, UK


   Abstract
Top
 Abstract
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
To survive, the newborn lamb must be able to maintain body temperature and to stand and move to the udder to suck colostrum to fuel heat production. The objective of this study was to investigate whether neonatal lambs showing slow behavioral progress to standing and sucking also have an impaired ability to maintain body temperature. The time taken to stand and suck after birth, rectal temperatures, and blood samples were collected from 115 newborn single, twin, and triplet lambs of 2 breeds, Scottish Blackface and Suffolk, which are known to show variations in their neonatal behavioral progress. Blood samples were assayed for thyroid hormones, known to be involved in heat production, and cortisol, which plays a role in tissue maturation before birth. In addition, colostrum samples were collected from the 56 ewes that gave birth to the lambs, and assayed for protein, fat, and vitamin contents. Heavy lambs (more than 1 SD above the breed mean), Blackface lambs, and singleton or twin lambs were quicker to stand and suck from their mothers than lightweight (more than 1 SD below the breed mean), Suffolk, or triplet lambs. Low birth weight lambs also had lower rectal temperatures than heavier lambs (P < 0.01), as did Suffolk compared with Blackface lambs (P < 0.001). Lambs that were slow to suck after birth had lower rectal temperatures than quick lambs, and this difference persisted for at least 3 d after birth. Within breed, heavy lambs had greater plasma triiodothyronine and thyroxine immediately after birth than light lambs. Blackface lambs had greater plasma triiodothyronine and thyroxine than Suffolk lambs but tended to have less cortisol. Colostrum produced by Blackface ewes had a greater fat content than that of Suffolk ewes (P < 0.001). Thus, lambs that are behaviorally slow at birth are also less able to maintain their body temperature after birth. Although part of their lower body temperature might be attributable to behavioral influences on thermoregulation, the data also suggest that physiological differences exist between these animals. These differences may be related to different degrees of maturity at birth.

Key Words: behavior • breed • neonate • sheep • temperature


   INTRODUCTION
Top
 Abstract
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The worldwide rate of mortality in newborn lambs is in excess of 15% of lambs born and represents a challenge to sheep production and welfare. The ability to survive is crucially dependent on the response of the lamb to the thermal (climatic) environment into which it is born. Lambs are born, often into cold or wet conditions, with low fat cover and have a high surface area to BW ratio, which exacerbates heat loss (Alexander, 1970Go; Stephenson et al., 2001Go). There is a high energy demand to maintain body temperature, and this must be supplied by efficient metabolism of brown adipose tissue (BAT) and by showing the appropriate standing and sucking responses to obtain milk. Temperature control at birth is dependent mainly on heat production by oxidation of fat from BAT by a process under the control of triiodothyronine (T3; Dauncey, 1990Go). Triiodothyronine is produced from thyroxine (T4) in BAT by the enzme 5'-monodeiodinase, the activity of which increases in the last month of pregnancy. Tissue maturation in the fetus is controlled by the increased production of cortisol toward the end of pregnancy (Fowden et al., 1998Go; Mellor, 1988Go). The development of neonatal behavior and thermoregulatory ability may thus be related to relative maturity at birth. Lambs that are slow to stand and suck after birth have greater mortality (Dwyer et al., 2001Go), and lambs with low rectal temperatures are more likely to fail to reach the udder (Slee and Springbett, 1986Go). Further, damage to the fetal central nervous system during delivery causes impaired sucking and locomotor activity in lambs (Haughey, 1980Go) and impairs thermoregulation in the neonate (Eales and Small, 1980Go; Bellows and Lammoglia, 2000Go). Therefore, it seems that neonatal behavior, specifically success in finding the udder and obtaining colostrum, is intimately associated with the ability to thermoregulate. In this study we investigated whether lambs showing slow neonatal behavioral progress also have an impaired ability to maintain body temperature.


   MATERIALS AND METHODS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Animals

Data were collected from the purebred offspring of 56 ewes [33 Blackface (BF) and 23 Suffolk (S)] over 2 years. Thirteen ewes contributed lamb records in both years. The ewes produced 115 lambs alive at birth (BF: 16 singles, 40 twins, and 13 triplets; S: 11 singles, 20 twins, and 14 triplets). Lambs were sired by 1 of 10 rams (4 BF and 6 S).

Ewes were estrous-synchronized using progesterone vaginal sponges (Veramix; Upjohn Ltd, Crawley, UK) and artificially inseminated with fresh semen. At approximately midgestation, the ewes were brought indoors into large straw-bedded pens (7 x 7 m) in groups of approximately 10 ewes and given access to hay and fresh drinking water ad libitum. Concentrates (locally milled ewe nuts; 218 g of CP per kg of DM) were provided from wk 14 of gestation, at a ration of 300 g·ewe–1·d–1 (S) or 200 g·ewe–1·d–1 (BF). The rations were doubled every 2 wk until wk 18 of gestation and then maintained at this level. The ewes were vaccinated with a clostridial vaccine (Covexin-8, Mallinckrodt, Middle-sex, UK) in wk 17.

In the weeks immediately before parturition, the ewes were habituated to the presence of observers in the central walkways between pens. Approximately 3 d before the expected parturition dates (parturition occurs on average at d 145 of gestation), the ewes were kept under 24-h video surveillance. In addition, at least 1 observer was present at all times once lambing had begun. As far as possible, the ewes were allowed to give birth to and care for their lambs unaided. However, lambing assistance (n = 30 lambs) was given if the ewe had failed to progress through a time schedule of events; that is, 1 h after the appearance of fluids but no appearance of parts of the lamb, and/or 2 h after parts of the lamb were seen at the vulva with no other obvious progress being made. In all cases, intervention was kept to a minimum and mainly involved correcting lamb presentation before the ewe continued the birth process unaided. Once the lamb had been born, it was allowed 3 h to achieve a successful sucking unaided. Lambs that had not sucked after this time were assisted to suck.

Lamb weight, crown-rump (CR) length, and sex were recorded within 24 h of birth. Lambs were marked with the identity number of their mothers and also for birth order using paint brands. The ewes remained in the lambing pens until 3 d after birth, when they and their lambs were moved outside to pasture. The lambs were born and maintained throughout at ambient temperature (mean temperature at birth = 7.4°C; range = –2 to 18°C).

Data Recording

The time of birth, the overt length of labor (calculated from the appearance of fluids until birth of the last lamb), the interval between littermates in multiple litters, and the degree of assistance required were recorded for all ewes and lambs. Birthing difficulty was assessed on a score of 1 to 3, with 1 indicating no assistance required, 2 indicating that presentation only was corrected or minor assistance was given, and 3 indicating that the lamb was delivered manually. Lamb presentation at delivery was also recorded whenever possible. A correct presentation was recorded when the lamb was presented forefeet first with the nose lying along the forelegs. Any other presentation at birth (head first with 1 or both forelegs retracted, head back, 2 lambs together, backwards, or breech) was recorded.

Behavior. Data on lamb behavioral latencies were collected on handheld Psion Workabout computers during the 2 h after the birth of each lamb using Observer data recording software (Noldus Information Technology, Wageningen, The Netherlands; Noldus et al., 2000Go). The time from birth to successful standing (standing on all 4 extended legs for more than 5 s) and successful sucking (teat held in mouth, lamb still and in parallel-inverse position with tail wagging for at least 5 s, confirmed by palpation of the abdomen at 2 h) was recorded.

Physiology. Between 30 and 50 min (mean = 45 min) after birth, the lamb was caught and a 2-mL blood sample was taken by jugular venipuncture into heparinized vacutainers. Rectal temperature was also recorded at this time using digital probes (Digital thermometers, Boots, Nottingham, UK). To minimize the disruption to ewe and lamb bonding, all samples were collected within the home pen of the animal, which allowed the ewe to continue to interact with the lamb during sampling, and all samples were collected within 2 min of entering the pen. The blood sampling and temperature recording procedures were repeated at 24 and 72 h after birth. Blood samples were stored on ice until centrifugation (20 min, 1,000 x g). The resultant plasma was separated and stored at –80°C until assayed for cortisol, T3, and T4 concentrations. At 2 h after birth, a 15-mL sample of colostrum was taken from each ewe. Five milliliters was frozen at –20°C for subsequent analysis of immunoglobulin G, vitamin A, and vitamin E contents. The remaining 10 mL was stored in a tube with preservative (8 mg of Bronopol, Broad-Spectrum Microtabs II, D&F Control Systems Inc., Dublin, CA) at 4°C until protein and fat contents were determined.

Assay Procedures

Cortisol. Samples for cortisol analysis were extracted from 100 µL of plasma with diethyl ether, and the concentrations were measured using RIA of the extracted steroid, as previously described (Duncan et al., 1990Go). Single samples were extracted and then assayed in duplicate. The intra- and interassay CV were 9.1 and 10.2% respectively, and the minimum detectable level of the assay was 0.23 ng·mL–1.

Thyroid Hormones. Concentrations of thyroid hormones were determined using a solid phase, competitive chemiluminescent enzyme immunoassay system [Immulite, Diagnostic Products Corporation (DPC), California]. Concentrations were determined using kits, controls, monoclonal mouse antibodies, and reagents supplied by DPC. The intra- and interassay CV were 7.6 and 8.6% for T3 and 8.9 and 10.8% for T4. The minimum detectable levels of the assays were 0.29 and 3.9 nmol/L for T3 and T4, respectively.

Vitamin Content of Colostrum. Colostrum was de-proteinized with ethanol, and the vitamins were extracted into hexane (Hoehler et al., 1998Go). The resulting hexane extracts were analyzed by HPLC (Kontron 400, Kontron Instruments, Watford, UK) with programmed fluorescence detection and by reference to internal and external standards (Williams, 1985Go). The mobile phase was 1% ethanol in hexane at a flow rate of 2 mL/min isocratic using a Waters Spherisorb Silica 250 x 4.6-mm column with integral guard (Waters Ltd., Elstree, Herts., UK.

Protein and Fat Contents of Colostrum. Ewe colostrum samples were diluted with water, and the protein and fat contents were determined by near-infrared reflectance using a Milkoscan 50 (Foss, Hillerød, Denmark). The instrument was first calibrated using bovine milk samples and a number of sheep samples analyzed by a modified Kjeldahl nitrogen method [protein: BS1741, part 5, section 5.2 (1996)Go] and a modified Rose Gottlieb method [fat: BSEN IS01211 (2001)Go].

Statistical Analysis

As lamb breeds differed markedly in their birth weights (BF = 3.96 ± 0.08 kg; S = 4.93 ± 0.20 kg), within breed lamb weights were divided into light weight lambs (>1 SD below the breed mean; n = 20), medium weight lambs (weighing within 1 SD of the breed mean; n = 77), and heavy weight lambs (>1 SD greater than the breed mean; n = 16). This weight code was used in subsequent analysis of birth weight on the data that were not normally distributed. The effect of birth weight on normally distributed neonatal physiological variables (thyroid hormones) was assessed by regression within breed. The behavioral data, lamb rectal temperatures, and plasma cortisol concentrations were not normally distributed in the neonatal lambs. The behavioral and cortisol data could be normalized by natural logarithm transformations, but the temperature data could not be normalized. Total cortisol over the first 3 d of life was calculated as the area under the curve by integration. This variable was not normally distributed and could not be normalized by transformation. Therefore, the nonparametric Kruskal-Wallis test in Minitab (Release 12.1; Minitab Inc., State College, PA) was used to investigate temperature and total cortisol. The effect of time on cortisol concentrations in lamb plasma was determined by Wilcoxon matched-pairs analysis.

To investigate the relationship between lamb behavior and rectal temperature, lambs were divided into groups based on the time taken for them to stand and suck, and the group was used as a factor in the analysis. For other lamb behavioral and physiological variables, the effects of birth difficulty, birth weight, litter size, lamb sex, lamb breed, and ewe parity and age were fitted as fixed effects to the model using the REML procedure (Patterson and Thompson, 1971Go) in Genstat 7.0 (Lawes Agricultural Trust, Rothamsted Experimental Station, UK), after checking for interactions among the variables. The potentially confounding effects of birth weight and litter size were addressed by fitting birth weight as a covariate and running the model twice by alternating the order of the explanatory variables. Year and ewe identity were fitted as random factors in the analysis, as ewes produced more than 1 lamb in the data set. This test procedure approximated to an ANOVA when the data were balanced but was capable of also handling unbalanced data. It was deemed the most appropriate test for these data, as they were unbalanced with respect to most of the fixed effects. For categorical data (birth difficulty score and sucking failure), significant differences were determined by {chi}2 tests.


   RESULTS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
There were no significant effects of lamb sex or ewe age and parity on the data; thus these factors will not be discussed further.

Breed Effects

Gestation length (P < 0.001), lamb birth weight (P < 0.001), and lamb CR length (P = 0.007) were affected by breed (Table 1Go). Blackface lambs were born following a gestation of approximately 1.5 d less than S lambs, and were lighter and shorter than S lambs. Blackface lambs required less assistance at delivery than S lambs (respectively 14.7 and 43.5%, {chi}2 = 11.71, df = 1, P < 0.001) and were less likely to be incorrectly presented at birth (21.1 and 41.3% respectively, {chi}2 = 7.50, df = 1, P = 0.006). Suffolk lambs were slower than BF lambs to stand (P < 0.001) and suck (P < 0.001; Table 1Go). Additionally, a greater proportion of S lambs failed to suck during the recording period (sucking failure: S = 57.1%, BF = 2.9%, {chi}2 = 42.94, df = 1, P < 0.001).


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  		Table 1. The effects of breed and litter size on gestation length, lamb weights and neonatal lamb behavior1
 
There was no relationship between ambient temperature at birth and lamb rectal temperature over the first 3 d of life (Spearmans rank order correlation = 0.002, P = 0.985), nor was there any relationship between assistance given with delivery and rectal temperature (Kruskal Wallis H = 1.76, df = 2, P = 0.415). Blackface lambs had greater body temperatures than S lambs throughout the first 3 d of life (P < 0.001; Table 2Go).


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  		Table 2. The effects of breed and litter size on lamb rectal temperatures (in °C) measured over the first 3 d of life1
 
Plasma cortisol concentrations were high in newborn lambs and declined with age over the first 3 d of life (Wilcoxon matched pairs, t = 271, n = 88, P < 0.001; Figure 1Go). There was no significant effect of lamb breed at any sampling time after delivery. However, the total amount of cortisol in S plasma over the first 3 d of life (calculated as the area under the curve) tended to be greater than in BF lambs (plasma cortisol (ng/mL: medians with interquartile ranges): BF = 193.7 (151.3 – 267.9), S = 253.2 (164.1 – 331.7), Kruskal Wallis H = 3.64, df = 1, P = 0.057).


Figure 1
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  		Figure 1. The effect of lamb age on plasma cortisol concentrations for Blackface (solid symbols and solid lines) and Suffolk lambs (open symbols and broken lines) over the first 3 d of life. Values are medians with inter-quartile ranges. Plasma cortisol declined with increasing lamb age (P < 0.001) and tended to be greater in Suffolk lambs compared with Blackface over the first 3 d of life (P = 0.057).

 
There was a significant effect of lamb breed on both thyroid hormones (Table 3Go). Throughout the recording period BF lambs had greater circulating concentrations of both T3 and T4 than S lambs. The ratio of T3/T4 was equal in both breeds immediately after birth and at 72 h, but tended to be greater in Suffolk lambs 24 h after birth (mean ratio: BF = 0.046, S = 0.050, SED = 0.002, Wald = 3.27, df = 1, P = 0.07).


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  		Table 3. The effect of lamb breed on plasma T3 and T4 (nmol/L) over the first 3 d of life1
 
Blackface ewes had a greater concentration of fat (P < 0.001) but not of protein (P = 0.271) in their colostrum than S ewes (Table 4Go). There were no significant effects of breed on the immunoglobulin G content of the colostrum (P = 0.15), but as might be expected from the greater fat content, BF colostrum had a greater concentration of vitamin E (P = 0.021) and tended to have greater vitamin A concentration (P = 0.079) than S colostrum.


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  		Table 4. The effects of breed and litter size on colostrum content of ewes1
 
Litter Size Effects

Gestation length (P = 0.017), lamb birth weight (P < 0.001), and lamb CR length (P < 0.001) were affected by litter size (Table 1Go). Triplet pregnancies were shorter than singleton or twin pregnancies. Lamb birth weight and CR length declined with each increase in lamb number in the litter. There were no effects of litter size on assistance at delivery ({chi}2 = 4.26, df = 2, P = 0.119) or lamb presentation ({chi}2 = 1.60, df = 2, P = 0.449). There was an effect of litter size (Table 1Go) on lamb neonatal behaviors that was not attributable to birth weight. Triplet lambs were slower to suck than single and twin lambs (P = 0.007), and both triplet and single lambs were slower to stand than twin lambs (P < 0.001). Triplet lambs had lower temperatures than single or twin lambs immediately after birth (P = 0.007) and at 24 h of age (P = 0.007) but not by 72 h (P = 0.972; Table 2Go).

There were no significant effects of litter size on plasma cortisol concentrations (Wald = 2.84, df = 2, P = 0.242). In addition, there were no significant effects of litter size on the thyroid hormones that were not accounted for by birth weight (T3: Wald = 2.32, df = 2, P = 0.313; T4: Wald = 2.03, df = 2, P = 0.362). Ewes had increasing amounts of fat content in their colostrum with each increase in litter size (P = 0.008; Table 4Go). Litter size also had an impact on protein content with triplet-bearing ewes producing colostrum with a reduced protein content compared with single- or twin-bearing ewes (P = 0.005). Colostrum of twin-bearing ewes had a greater vitamin E content than other litter sizes (P = 0.021), but there was no effect on vitamin A content (P = 0.534).

Birth Weight Effects

Heavy lambs were quicker to suck than light lambs (P = 0.047; Table 5Go), although there was no effect on time to stand (P = 0.33). Lamb birth weight relative to the breed mean had a significant impact on lamb rectal temperature (Figure 2Go); light lambs had lower temperatures than heavier lambs at 1 h (P = 0.045), 24 h (P = 0.001), and 72 h after birth (P = 0.016). Heavy lambs tended to be more likely to need assistance at delivery than light lambs (percentage of lambs requiring assistance: light = 20.0%, medium = 23.7%, heavy = 50.0%, {chi}2 = 5.24, df = 2, P = 0.073).


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  		Table 5. Relationship between lamb birth weight and neonatal behavioral progress to standing and sucking1
 

Figure 2
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  		Figure 2. The relationship between lamb birth weight and rectal temperature recorded within 1 h, at 24, and at 72 h after birth. Values are medians with upper inter-quartile ranges. Light lambs (weighing more than 1 SD less than the breed mean; n = 20) had significantly lower temperatures than heavy lambs (weighing more than 1 SD greater than the breed mean; n = 16) at < 1 h after birth (P = 0.045), at 24 h after birth (P = 0.001), and at 72 h after birth (P = 0.016). a,bBars with different letters are significantly different.

 
There were no effects of birth weight on plasma cortisol concentrations (Wald = 0.70, d.f. = 1, P = 0.402). However, lambs that had been assisted at delivery had greater plasma cortisol than unassisted lambs at both 24 and 72 h after birth [plasma cortisol (ng/mL; mean values with 95% confidence intervals): 24 h—unassisted lambs = 40.8 (31.7–52.5); partly assisted lambs = 37.3 (29.0 – 48.0); assisted lambs = 74.8 (58.1 – 96.4), Wald = 10.47, df = 2, P = 0.005; 72 h—unassisted lambs = 17.8 (12.9 – 24.7), partly assisted lambs = 29.2 (21.1 – 40.4), assisted lambs = 40.0 (28.9 – 55.3), Wald = 9.21, df = 2, P = 0.01)].

Plasma T3 was significantly related to birth weight, in both breeds of lamb, for the first 24 h of life but not thereafter (Table 6Go). In the BF breed, birth weight had an effect on plasma T4 immediately after birth only (P = 0.001), whereas, for S lambs, plasma T4 was related to birthweight for the first 24 h of life (P = 0.017), and there was still a tendency for birth weight to influence T4 72 h after birth (P = 0.076; Table 6Go).


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  		Table 6. Correlation of lamb birth weight with T3 and T4 concentrations in plasma from Blackface and Suffolk lambs collected over the first 3 d of life1
 
Relationship Between Lamb Behavior and Rectal Temperature

Lambs that were slow to stand had lower rectal temperatures within 1 h of birth (P < 0.001) and at 24 h after birth (P = 0.045) than lambs that stood quickly (Figure 3aGo). This relationship had disappeared by 72 h after birth (P = 0.08). Lambs that were slow to suck, or failed to suck successfully within the recording period and needed assistance to suck also had lower temperatures than lambs that were quick to suck after birth over the first 3 d of life (P = 0.027; Figure 3bGo).


Figure 3
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  		Figure 3. The relationship between lamb rectal temperatures and behavioral progress after birth. (a) Median time to stand after birth (with upper interquartile ranges); groups are lambs that stood within 15 min of birth (n = 52); lambs that stood between 15 and 30 min after birth (n = 40); lambs that stood between 30 and 60 min after birth (n = 8); and lambs that stood more than 1 h after birth (n = 9). Differences are significant at < 1 h after birth (P < 0.001) and 24 h after birth (P = 0.045) but not at 72 h (P = 0.08). (b) Median time to suck after birth (with upper interquartile ranges); groups are lambs that sucked within 30 min of birth (n = 19); lambs that sucked between 30 and 60 min after birth (n = 36); lambs that sucked between 1 and 2 h after birth (n = 20); and lambs that took longer than 2 h or required assistance to suck (n = 31). Differences are significant at < 1 h after birth (P = 0.002), 24 h after birth (P = 0.005), and 72 h after birth (P = 0.027). a,bBars with different letters are significantly different.

 

   DISCUSSION
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
This experiment has confirmed our previous observations of differences between BF and S breeds in neonatal behavior (Dwyer and Lawrence, 2000Go; Dwyer, 2003Go). The data also demonstrate that the BF lambs, in addition to standing and sucking quickly, have greater rectal temperatures than S lambs, and greater plasma T3 and T4 over the first 3 d of life. Plasma cortisol tends to be greater in S lambs compared with BF. Our data also support previous observations (Dwyer, 2003Go) that low birth weight lambs within breed show slower behavioral progress after birth. In addition, this experiment has shown that lightweight lambs have lower body temperatures over the first days of life, and have less T3 and T4 at birth than heavier lambs. Triplet lambs were slower to stand and suck at birth than other litter sizes as seen previously (Dwyer, 2003Go), and this effect was in addition to their lower birth weight. Triplet lambs also had lower temperatures over the first days of life, but there were no influences of litter size on neonatal concentrations of cortisol or T3 and T4. The data therefore suggest that lamb thermoregulatory ability at birth can be influenced by genetic factors (lamb breed) and by environmental factors (such as prenatal nutrition and litter size) influencing birth weight. In both cases, lambs that are behaviorally slow at birth also have difficulty maintaining their body temperature.

Lambs are known to maintain body temperatures greater than those of adult ewes for the first month of life (Symonds et al., 1989Go; Clarke et al., 1997Go; Bird et al., 2001Go) and with a blunted nocturnal rhythm compared with ewes (Faurie et al., 2004Go). Lambs have a high metabolic turnover immediately after birth, which may increase body temperature (Symonds et al., 1995Go). Behavioral competence and body temperature appear to be linked; lambs with a low rectal temperature are more likely to fail to reach the udder after birth than those with normal temperatures (Slee and Springbett, 1986Go). Thus, behavioral mechanisms may operate to prevent falls in temperature. Standing rapidly after birth helps to reduce convective heat loss of the wet lamb to the ground, and sucking bouts or feeding raise body temperature (Bird et al., 2001Go). Thus the rapid behavioral progress of the BF lambs compared with S lambs and of the heavier lambs compared with low birth weight lambs seen in the current study will have contributed directly to their greater temperatures. In addition, neonatal huddling with other lambs or sleeping close to the ewe could prevent falls in core temperature. Our previous data demonstrate that BF lambs and ewes maintain closer spatial relationships than S lambs and ewes (Dwyer and Lawrence, 2000Go), suggesting that this may be an additional mechanism by which BF lambs are able to maintain greater temperatures than S lambs.

Breed differences in ability to maintain body temperature at birth and genetic variation in this trait within breed have been observed before (Sykes et al., 1976Go; Slee and Springbett, 1986Go; Slee et al., 1991Go). Blackface lambs are smaller than S lambs and would be expected to lose heat more quickly and to be energetically disadvantaged. However, BF lambs were more successful at maintaining body temperature than S lambs, at least over the first 3 d of life. This indicates that the BF were either more efficient at conserving heat through better coat or tissue insulation or were more efficient at producing heat than S lambs, or both. Differences in coat insulation at birth are small immediately after delivery when the lambs are wet with birth fluids (Sykes et al., 1976Go), which is when the first breed difference in body temperature was recorded in the current study. Thereafter BF lambs have a thicker birth coat than S lambs, and phenotypic correlations with coat depth and cold resistance have been reported in BF lambs (Stott and Slee, 1987Go). However, Slee (1978)Go demonstrated a breed difference in cold resistance in clipped lambs, suggesting that birth coat is at most only a contributory factor to breed differences in thermoregulation. With respect to the degree of tissue insulation, Sykes et al. (1976)Go concluded that differences between breeds would be too small to account for the large differences in temperature regulation. Thus it is likely that the differences in ability to maintain body temperature between the BF and S breeds seen here, in addition to behavioral mechanisms mentioned previously, were a result of differences in the rate of development of cold thermogenesis after birth (Sykes et al., 1976Go).

Cold thermogenesis in the newborn lamb occurs largely in BAT, which can rapidly generate heat by nonshivering thermogenesis (Stephenson et al., 2001Go). The prenatal development and subsequent neonatal responses of BAT are influenced by the thyroid hormones, particularly through actions on BAT iodothyronine 5' monodeiodinase (which converts T4 to T3) and mitochondrial uncoupling protein (UCP1; reviewed by Polk, 1988Go). The greater concentrations of plasma T3 and T4 seen in BF lambs suggest that both their thyroid and BAT was more active than in S lambs and thus cold thermogenesis was more efficient in BF lambs. Symonds et al. (1989)Go showed that lambs with low plasma T3 concentrations (below 1.73 nmol/L) relied more on shivering thermogenesis in response to cold exposure than lambs with greater concentrations of T3 (>2.06 nmol/L), which had a greater contribution from non-shivering thermogenesis. The minimum plasma T3 concentrations recorded here in both breeds of lamb were considerably greater than 2.06 nmol/L; thus it is likely that nonshivering thermogenesis predominated. The ratio of T3/T4 in the plasma was similar for both breeds except at 24 h old, when it tended to be greater in S lambs. Thus, a behavioral delay and reduced thermogenesis in S lambs appear to contribute to their lower rectal temperatures during the neonatal period in comparison with BF lambs.

Cortisol is an important regulator of fetal maturation and increases the production of T3 in the fetus in preparation for the increase in metabolic rate and thermogenesis that occurs at birth (reviewed by Liggins, 1994Go). Brown adipose tissue UCP1 is increased in the fetal lamb by infusion of cortisol (Mostyn et al., 2003Go), which also increases fetal T3. Given the greater concentration of thyroid hormones in BF lambs in the current study, it was surprising that greater plasma cortisol concentration was measured in the neonatal S lambs compared with BF lambs. It is possible that this represents a delay in neonatal maturity in the S lambs, and a more frequent sampling regimen might have shown a difference in the rate of decline of plasma cortisol concentration over the first days of neonatal life. Whether this breed difference is also present in the fetus or whether BF fetal lambs have greater plasma cortisol concentrations than S fetuses requires further investigation.

The lesser ability of low birth weight and triplet lambs to maintain body temperature after birth can be at least partly attributed to their small body size and therefore greater relative surface area for heat loss. In addition they were slower to stand and suck so were less able to make use of behavioral strategies to maintain body temperature. Low birth weight lambs will have experienced some degree of undernutrition in utero (for example, through being part of a triplet litter), and fetal adipose tissue development is known to be sensitive to fetal nutrition (Budge et al., 2003Go). Fetuses subjected to low nutrition in late gestation have less adipose tissue and reduced abundance of UCP1 mRNA in that tissue (Budge et al., 2004Go). In the current study, plasma concentrations of plasma T3 and T4 were reduced at birth in low birth weight lambs in comparison with heavier lambs as has been shown before (Cabello and Levieux, 1981Go; Wrutniak et al., 1990Go). This suggests that these animals were also compromised in their ability to produce heat by nonshivering thermogenesis immediately after birth.

The supply of nutrients in colostrum is important for the production of heat by the lamb as neonatal reserves are rapidly exhausted. The supply to the lamb will be the product of colostrum composition and yield and lamb sucking behavior and ingestion. Colostrum yield was not measured in the present experiment, but our previous (unpublished) data have shown that the yield for the 2 breeds is similar. Likewise, other studies suggest that, although differences are apparent between meat- and milk-type sheep (Pattinson and Thomas, 2004Go), there are no breed differences in colostrum yield between breeds of a similar type (Snowder and Glimp, 1991Go; Pattinson and Thomas, 2004Go). However, the fat content of the colostrum of BF ewes was greater than that in the S and thus, once the lambs had obtained the colostrum, the BF lambs would have had a greater nutrient supply for thermoregulation. This may have contributed to their greater body temperature at 24 h after birth. In addition, the increase in litter size also resulted in increased fat content of colostrum as has been shown before (Snowder and Glimp, 1991Go), although protein content was reduced in triplet-bearing ewes. This increase in fat content may have partly compensated larger litter sizes for their reduced intake of colostrum.

In conclusion, our data show that lambs that are active at birth (BF lambs and heavier lambs) are better able to maintain their body temperature than slower lambs (S lambs and light weight lambs). This may be partly attributable to behavioral means of thermoregulation, but BF and heavier lambs also have greater plasma concentrations of T3 and T4, suggesting they are better able to generate heat, and a better colostral nutrient supply to fuel thermoregulation. These differences may suggest a causal relationship, where physiological development underpins behavioral competency, or be related to different degrees of maturity at birth. Further investigation of neonatal lamb BAT to assess activity of 5' deiodinase and UCP would help to determine the relationships of genotype, litter size, and birth weight with thermoregulatory ability.


   Footnotes
 
1 This study was supported by the Scottish Executive Environment and Rural Affairs Department. We thank the following: N. Scott and M. Ramsay for the animal husbandry; S. Robson, M. Farish, J. Donbavand, J. Chirnside, and H. Pickup for technical assistance at lambing time; A. Thain for cortisol assays, S. Gorrie for thyroid hormone assays, J. Rooke and M. Ewen for analysis of vitamin contents and immunoglobulin G; E. Brechany and J. Dunsmuir at the Hannah Research Institute for the colostrum analysis; and C. Theobald and I. Nevison for statistical advice. Back

2 Corresponding author: Cathy.Dwyer{at}sac.ac.uk

Received for publication July 14, 2005. Accepted for publication November 30, 2005.


   LITERATURE CITED
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 


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