Thermoregulatory responses of ewes to winter shearing in mid- or late-pregnancy

Abstract

Shearing ewes during mid or late gestation can improve lamb birth weight and vigor. The aim was to compare the thermoregulation and metabolic responses of ewes shorn in mid versus late gestation during winter. Sixty-seven Merino ewes were allocated to four experimental groups according to the stage of gestation in which they were shorn (Day 87 or Day 117) and whether ewes were shorn or not (shorn or non-shorn ewes; Sh or NSh). Rectal (RT), tympanic (TT), and maximum corneal temperature were recorded, and blood triiodothyronine and β-hydroxybutyrate concentrations were determined. Heat loss indexes were calculated using TT and MCT temperatures. RT was higher in NSh than Sh ewes (P < 0.0001). After shearing, RT remained stable in NSh ewes but decreased in Sh ewes (P < 0.001). The TT heat loss index was higher in NSh ewes (P < 0.0001), and declined post shearing in Sh ewes (P < 0.0001), indicating increased peripheral vasoconstriction. Shearing triggered acute thermogenesis as indicated by increased blood triiodothyronine and β-hydroxybutyrate concentrations in Sh than NSh ewes (P = 0.001 and P = 0.03, respectively). Shearing pregnant ewes during winter triggered significant thermoregulatory responses that were insufficient to maintain core body temperature. The responses were energetically demanding, as indicated by increased β-hydroxybutyrate and triiodothyronine concentrations.

Introduction

Shearing is an essential practice in most sheep production systems and is traditionally performed yearly for wool harvesting. However, because shearing triggers significant physiological changes, it should be strategically aligned with the breeding cycle (see review:¹. For example, shearing ewes during mid or late gestation is a practice widely used by farmers due to its positive impact on lamb birth weight and vigor^2–4. Notably, some studies found that newborn lambs born to ewes shorn during mid-pregnancy exhibit greater birth weight and vitality than those born to ewes shorn during late gestation^5,6. Moreover, ewes produce more milk^7,8, which may also explain the higher growth rate of lambs⁹ and, in some studies, higher weaning weight^7,8. Conversely, as there is a sudden increase in maintenance energy requirements for thermogenesis, coupled with the physical and handling stress of the procedure, a negative energy balance can trigger rapid mobilization of fatty acids and subsequent ketogenesis, increasing the risk of toxemia when ewes are shorn, particularly during late gestation¹⁰. Therefore, mid-pregnancy shearing offers more productive benefits while minimizing health and welfare risks for the ewes than late-gestation shearing. However, to the best of our knowledge, there is a lack of studies comparing ewes’ thermoregulatory responses to winter shearing at different stages of gestation. Understanding this aspect would provide valuable guidance for farmers in determining the optimal timing for shearing, particularly concerning cold stress and welfare.

In subtropical and temperate regions, gestation -and consequently shearing pregnant ewes- coincides with winter. Fleece removal, combined with exposure to cold temperatures, causes pregnant ewes to experience significant cold stress, triggering thermoregulatory responses. However, these responses may be insufficient to maintain core body temperature due to the substantial increase in heat loss following shearing^11,12. To counteract heat loss and enhance endogenous heat production, shorn ewes undergo physiological and metabolic adaptations that help prevent significant declines in core body temperature. Shearing induces intense peripheral vasoconstriction to reduce heat dissipation⁹. Additionally, prepartum shearing increases blood concentrations of thyroxine (T4), triiodothyronine (T3), and cortisol^2,13,14. These endocrine changes support thermogenesis by stimulating tissue oxygen consumption and catabolic pathways, such as lipolysis¹⁰. Following shearing, elevated blood concentrations of non-esterified fatty acids¹⁵ and β-hydroxybutyrate³ indicated increased mobilization of body fat reserves and high rates of fat breakdown. Well-fed shorn ewes also exhibit increased food intake¹⁶, contributing to heat production through digestion-related catabolic processes.

In the final third of gestation, ewes experience increased energy demands due to the rapid growth of the fetus and mammary glands^17,18. Consequently, fat reserve mobilization intensifies during this stage, affecting the ewe’s body condition¹⁹. At the same time, voluntary herbage intake declines as the expanding uterus exerts pressure on the rumen²⁰. Although ewes have a higher metabolic rate in late gestation than in earlier stages²¹, we hypothesized that their ability to regulate their temperature and metabolism in response to winter shearing is reduced compared to ewes shorn in mid-gestation. Therefore, the aim of this study was to compare the thermoregulation and metabolic responses of ewes shorn in mid versus late gestation.

Methods

All the procedures were approved by the Comisión de Ética en el Uso de Animales (CEUA) of the Universidad de la República, Uruguay (protocols 1210/21 and 1592/22) and were in accordance with national guidelines and regulations.

Location, general management, and experimental design

The study was performed in Campo Experimental N°1 of the Facultad de Veterinaria, Universidad de la República (34.35 S, 55.60 W). Overall, 67 multiparous Australian Merino ewes (3–4 years old) were used in the study. All of them were shorn for the last time approximately 9 months before. During the natural breeding season (March–April, autumn in the Southern Hemisphere), estrus was synchronized in two groups of ewes with a 30-day interval. Half of the ewes were inseminated in March, while the remaining half were in April. This strategy was implemented to have ewes in mid- and late pregnancy simultaneously.

Estrus was synchronized with two intramuscular injections of a synthetic prostaglandin analog separated by 7 days (160 µg/dose Delprostenate, Glandinex, Universal Lab., Montevideo, Uruguay). Estrus was detected twice daily using vasectomized rams painted on the chest. Transcervical artificial insemination (AI) was performed with fresh semen from two Merino rams, whose breeding soundness evaluation was conducted in February, and a seminal evaluation was conducted 45 days before each AI. Forty-five days after each AI, pregnancy was diagnosed with a transrectal ultrasound scan using a MyLab One Vet ultrasonic device (Esaote, Genova, Italy) equipped with a linear probe (8 MHz) coupled to a PVC tube extension probe to allow the manipulation, and only ewes carrying a single fetus were selected for this experiment. At the time of pregnancy diagnosis, ewes weighed 45.2 ± 0.5 kg (mean ± SEM) and had a body condition score of 2.9 ± 0.03 (scale 1 to 5). During the study, ewes remained in a single group, with other ewes from the same flock that did not enter the study, grazing on natural pastures (winter measurement of pasture availability: 373 DM/ewe).

Four days before shearing, ewes were allocated to four experimental groups in a 2 × 2 factorial arrangement. The main factors were the stage of gestation in which ewes were shorn (day 85–90 vs. day 115–120 of the gestation; D87 vs. D117) and if ewes were shorn or not (shorn vs. non-shorn ewes; Sh vs. NSh). Therefore, the four treatments were D87Sh (n = 22), D87NSh (n = 12), D117Sh (n = 21) and D117NSh (n = 12). Ewes were weighed, and body condition scores were recorded the day before shearing. Ewe body weights were 47.3 ± 0.9 kg, 45.8 ± 1.2 kg, 43.6 ± 0.9 kg, and 42.7 ± 0.5 kg, and body condition was 2.8 ± 0.1, 2.9 ± 0.1, 3.0 ± 0.1, and 2.9 ± 0.1 for ewes in D87Sh, D87NSh, D117Sh, and D117NSh, respectively.

Shearing procedures

All Sh ewes were shorn on July 20 (mid-winter in the Southern Hemisphere; Day 0) with the Tally-Hi procedure, beginning at 08:00 h. Tally Hi is performed with the animal untied and is the most commonly used shearing method in Uruguay (https://www.engraw.com.uy/docs/good-animal-husbandry-practices.pdf). The non-shorn ewes were handled similarly, being moved to the pen close to the shearing shed. Shearing was performed using a high comb (Heiniger Blizzard, Swiss), leaving a fleece stubble length of 8 mm.

Body temperatures

Rectal and tympanic temperatures (RT and TT, respectively) were recorded before shearing (between 6:00 and 7:30 h) and then at 4, 24, 48, and 72 h after shearing using standard thermometers (Joytech Healthcare Co, Hangzhou, China and Braun Thermoscan 5, Mexico, Mexico, respectively). The maximum corneal temperature (MCT) in the iris region was recorded at 4, 24, 48, and 72 h after shearing, according to Corrales-Hlinka et al.¹². Thermal images were recorded by the same person with a digital infrared camera (FLIR E8, Estonia; infrared resolution photos: 320 × 240; object range of temperature: −20 to + 250 °C; accuracy ± 2.0%; field of view: 45° x 34°) at a distance of 0.5 m from the animal. The reflected air temperature was recorded in situ for each measurement using a homemade Lambert radiator using aluminum foil^12,22. The camera was calibrated to environmental and reflective air temperatures and to the atmospheric relative humidity, setting the emissivity to 0.98, as previously described for sheep^12,22. The ellipse function tool was applied to the ocular surface, including the central cornea¹², and FLIR Tools software (FLIR Systems, Wilsonville, OR) was used for post-capture radiometric analysis. This allowed adjustment of emissivity- and reflected-temperature parameters and the calculation of the maximum temperature within the user-defined elliptical region of interest.

Heat loss indexes

Two heat loss indexes (HLI) were calculated according to the formula proposed by Amaral-Silva et al.²³:

One of the heat indexes used the TT (HLI-TT) and the other MCT (HLI-MCT) as the surface temperatures. These indices range from 0 to 1, where 0 indicates maximum vasoconstriction and 1 indicates maximum vasodilatation. The HLI-TT was calculated for data collected on Day 0 and at 4, 24, 48, and 72 h after shearing, while the HLI-MCT was calculated for data recorded at 4, 24, 48, and 72 h after shearing, as MCT was first recorded 4 h after shearing.

Collection of blood samples, T3, and β-hydroxybutyrate measurements

Blood was collected by jugular venipuncture on Days − 3, -2, -1, and 4 h pre-shearing and Days 1, 2, 3, and 23 post-shearing. Samples were allowed to clot, centrifuged, and the serum was separated and stored at -20 °C until hormonal measurement. The β-hydroxybutyrate concentration was measured in the samples collected on Days − 1 and 3, using a handheld meter (Optium Xceed; Abbott Laboratories), according to Ha et al.²⁴. Immediately after blood collection, a drop of blood was placed on the reactive strip indicated for the device, which gave the digital results in about 10 s. The apparatus was calibrated according to the manufacturer’s recommendations.

Samples for T3 were collected in tubes without anticoagulant, and all samples were measured using a commercial solid-phase radioimmunoassay kit (T3-RIA-CT; DiaSource, Belgium). The analytical sensitivity of the assay was 0.163 nmol/L. The intra-assay coefficients of variation were 13.1% and 8.3% for low and high controls, respectively. The inter-assay coefficients of variation were 14.2% and 12.5% for low and high controls, respectively.

Environmental conditions

Air temperature, humidity, wind speed, and rainfall were recorded using a Vantage Vue weather station (Davis Instruments, USA) every 1 h from Day − 3 to Day 3. Rainfall was not observed during the experiment. Environmental temperature, humidity, and wind speed are presented in Fig. 1A and B, and 1C, respectively.

Fig. 1.

Mean values of air temperature, humidity, and wind speed. The arrow indicates the moment at which ewes were shorn.

Statistical analysis

The normal distribution of the data was confirmed using the Shapiro-Wilk test. All the data were analyzed using mixed models (mixed proc in SAS; platform: SAS OnDemand for Academics), including the shearing treatment (Sh vs. NSh), the stage of gestation (D87 vs. D117), time, and the two-way and three-way interactions as main effects. When data were collected at multiple time points before shearing, a mean value was calculated and used as the pre-shearing value (BSh) for statistical analysis. In the RT, TT, and T3 data, BSh values were included as covariates to assess ewes’ ability to respond to shearing regardless of their initial status. Time was included as a repeated measure. The autoregressive covariance structure was included to account for the separation between measurements. Posthoc comparisons were made with the pdiff function of SAS. Data are presented as LS mean ± SEM. Differences were considered significant when P ≤ 0.05 and as tendencies when 0.05 < P ≤ 0.1.

Results

Body temperatures

The RT, TT, and MCT varied with shearing, and significant interactions between shearing and time were observed in RT and TT (Table 1). The RT and MCT also varied over time, and the TT tended to vary (Table 1). Rectal temperature was greater in NSh than Sh ewes (P < 0.0001), varied with time (P = 0.05), and there was an interaction between shearing treatments and time (P = 0.039) (Table 1). While RT remained stable in NSh ewes along the study, it varied in Sh ewes, reaching values lower than NSh at 24 h, 48 h, and 72 h after shearing (P < 0.001 for all). Data are presented in the pooled form because there was no effect of gestational stage (Fig. 2A).

Table 1.

Effect of shearing (Sh =shorn and Nsh = unshorn) at day 87 of gestation (D87) or day 117 (D117) on ewe rectal (RT), tympanic (TT), and maximum corneal (MCT) temperature (°C) and heat loss index calculated using TT (HLI-TT) or MCT (HLI-MCT).

	Treatments				P
	Sh	NSh	D87	D117	Sh/NSh	GS	ti	Sh*GS	Sh*ti	GS*ti	Sh*GS*ti
RT (°C)	39.2 ± 0.03	39.5 ± 0.04	39.3 ± 0.04	39.4 ± 0.04	< 0.0001	ns	0.05	ns	0.039	ns	ns
TT (°C)	35.8 ± 0.07	36.7 ± 0.09	36.2 ± 0.08	36.3 ± 0.08	< 0.0001	ns	0.053	ns	0.0003	ns	ns
MCT (°C)	37.2 ± 0.1	37.7 ± 0.1	37.5 ± 0.1	37.4 ± 0.1	0.0008	ns	0.0005	ns	ns	ns	ns
HLI-TT	0.86 ± 0.00	0.89 ± 0.00	0.87 ± 0.00	0.88 ± 0.00	< 0.0001	ns	< 0.0001	ns	0.053	ns	ns
HLI-MCT	0.926 ± 0.004	0.932 ± 0.004	0.931 ± 0.003	0.927 ± 0.003	ns	ns	< 0.0001	ns	0.052	ns	ns

Data are presented as LS mean ± SEM, and P values indicate the main effects of the factors included in the model (being shorn or not – Sh/NSh, stage of the gestation - GS, time -ti, and the two-way and three-way interactions).

Fig. 2.

(A) Rectal temperature, (B) Tympanic temperature, and (C) Maximum corneal temperature in shorn (red squares) or non-shorn ewes (blue line, open circles) in ewes shorn on days 87 or 117 of gestation (indicated by the dotted arrows). The bars included in (A) and (B) correspond to recordings done before shearing (BSh) that were included as covariates. †: < P ≤ 0.1; ***: P < 0.001.

Similarly, TT was greater in NSh than Sh ewes (P < 0.0001), tended to vary with time (P = 0.053), and there was an interaction between shearing treatments and time (P = 0.0003) (Table 1). Tympanic temperature tended to be lower in Sh than NSh ewes 4 h after shearing (P = 0.1) and was lower at 24 h, 48 h, and 72 h (P < 0.001 for all) (Fig. 2B). Neither the gestation stage nor any interaction affected the MCT, which was greater in NSh than Sh ewes (P = 0.0008; Table 1). It varied over time (P = 0.0005), independent of the treatments (Fig. 2C). As gestation stage did not influence TT or MCT, data are presented in the pooled form in Fig. 2B and C.

Heat loss indexes

The HLI-TT was greater in NSh than Sh ewes (P < 0.0001), with no effects of the gestation stage (Table 1), and there was a tendency toward an interaction between being shorn and time (P = 0.053), with no other significant interactions (Fig. 3A). The HLI-MCT varied only with time (P < 0.0001) and tended to have an interaction between being shorn and time (P = 0.052) (Table 1; Fig. 3B).

Fig. 3.

Heat loss indexes calculated based on (A) Tympanic temperature (HLI-TT) or (B) Maximum corneal temperature (HLI-MCT) of ewes shorn on days 87 or 117 of the gestation (indicated by the dotted arrows). Data are presented pooled, as there was no effect of gestational stage. In Figure A, there was a greater index in non-shorn than in shorn ewes (P < 0.0001).

T3 concentrations

Triiodothyronine concentration was greater in Sh than in NSh ewes (1.17 ± 0.02 nmol/L vs. 1.07 ± 0.02 nmol/L; P = 0.001) and tended to be greater in D87 than D117 (1.15 ± 0.02 nmol/L vs. 1.09 ± 0.02 nmol/L; P = 0.057). There was an interaction between shearing and gestational period (P = 0.026) (Table 2). While NShD87 had greater T3 concentration than NShD117, ShD87 did not differ from ShD117. Triiodothyronine concentration did not differ between ShD87 and NShD87, it was greater in Sh117 than NShD117 (P < 0.0001).

Table 2.

Effect of shearing (Sh =shorn and Nsh = unshorn) at day 87 of gestation (D87) or day 117 (D117) on triiodothyronine (T3) and β-hydroxybutyrate (BOB) concentration.

	Time	Treatments				P			Interactions
		ShD87	NShD87	ShD117	NShD117	Sh/NSh	GS	ti	ShxGS	Shxti	GSxti	ShxGSxti
T3 (nmol/L)	Pre	1.23 ± 0.06	1.28 ± 0.08	1.21 ± 0.06	1.22 ± 0.08	0.001	0.057	0.0001	0.026	0.009	ns	ns
	4 h	1.06 ± 0.06	0.99 ± 0.09	1.05 ± 0.06	0.84 ± 0.08
	24 h	1.25 ± 0.06	1.12 ± 0.08	1.20 ± 0.06	0.98 ± 0.08
	48 h	1.17 ± 0.06	1.31 ± 0.08	1.19 ± 0.06	1.22 ± 0.08
	72 h	1.28 ± 0.06	1.18 ± 0.08	1.20 ± 0.06	0.94 ± 0.08
	23 d	1.02 ± 0.06	0.92 ± 0.08	1.20 ± 0.06	0.85 ± 0.08
BOB (nmol/L)	Pre	0.33 ± 0.07c	0.33 ± 0.07c	0.58 ± 0.07b	0.55 ± 0.07b	0.03	< 0.0001	0.002	0.10	0.0002	0.054	0.02
	72 h	0.42 ± 0.07bc	0.33 ± 0.07c	0.96 ± 0.07a	0.51 ± 0.07bc

Data are presented as LS mean ± SEM. P values indicate the main effects of shearing (Sh/NSh), gestational stage (GS), time (ti), and their interactions. T3: As there was no three-way interaction, the effects of significant main factors are mentioned in the text. BOB: Different letters indicate P ≤ 0.05.

Lastly, while there was an interaction between being shorn and time (P = 0.009) (Table 2), there was no interaction between gestational stage and time, and no three-way interaction. Triiodothyronine concentration tended to be greater in Sh than NSh ewes 4 h after shearing (P = 0.056) and was greater 24 h, 72 h, and 23 d after shearing (P = 0.02, P = 0.01, and P = 0.002, respectively).

β-hydroxybutyrate concentrations

The β-hydroxybutyrate concentration was greater in Sh than NSh ewes (0.57 ± 0.04 mmol/L vs. 0.43 ± 0.04 mmol/L; P = 0.03), in D117 than D87 ewes (0.65 ± 0.04 mmol/L vs. 0.35 ± 0.04 mmol/L, P < 0.0001), and 72 h after shearing than 24 h before shearing (0.55 ± 0.04 mmol/L vs. 0.45 ± 0.04 mmol/L, P = 0.002). There was a tendency for an interaction between being shorn and the stage of gestation (P = 0.1), and between the stage of gestation and time (P = 0.054). There was a significant interaction between being shorn or not and time (P = 0.0002): although there was no difference before shearing in β-hydroxybutyrate concentration (0.43 ± 0.05 mmol/L vs. 0.44 ± 0.05 mmol/L for Sh and NSh ewes), 72 h after shearing it was greater in Sh than NSh ewes (0.69 ± 0.05 mmol/L vs. 0.42 ± 0.05 mmol/L; P = 0.0003).

There was also a three-way interaction among being shorn or not, gestational stage, and time (P = 0.02). Before shearing, D117 ewes had greater concentrations than D87 ewes (P < 0.05) (Table 2). Furthermore, 72 h after shearing, D117Sh ewes still had greater concentrations than D87Sh, D87NSh, and D117NSh ewes (P < 0.05), with no differences between these three groups (Table 2).

Discussion

This study investigated the short-term thermoregulatory response of ewes to winter shearing at mid- or late gestation. Due to the synchronization of pregnancies, mid- and late-gestation ewes were subjected to the same environmental conditions. While this study primarily assessed short-term responses, the effect of shearing can persist, carrying associated metabolic and energetic costs. Following shearing, pregnant ewes activate a range of thermoregulatory mechanisms to prevent excessive decreases in core temperature. Fleece removal significantly increases heat loss with the lower critical temperature of shorn sheep, with an 8 mm fleece 8 mm fleece stubble being 28 °C²⁵. In this study, pregnant ewes were exposed to a strong cold challenge after winter shearing, with environmental temperatures averaging 10 °C, reaching a minimum of 2.6 °C, and accompanied by light wind. The heat loss index based on TT declined for at least 72 h post-shearing, indicating increased peripheral vasoconstriction as an acute strategy to minimize heat loss. Additionally, shearing likely triggered acute thermogenesis, as indicated by higher concentrations of T3 and β-hydroxybutyrate in Sh than NSh ewes. Elevated β-hydroxybutyrate concentrations suggest increased lipolysis^10,26, a process closely linked to body heat production²⁷. Likewise, higher T3 concentrations are associated with an increased metabolic rate²⁸. Despite the activation of thermoregulatory mechanisms, shorn pregnant ewes were probably unable to fully maintain their core temperature, as evidenced by a decline in RT during the first few days after shearing.

The physiological responses to shearing are energetically costly and include increased T3 secretion, reduced peripheral blood perfusion, and increased β-hydroxybutyrate concentration, indicating increased lipolysis. Despite these adaptive responses, Sh ewes may not have fully maintained core body temperature, as reflected by the decrease in RT, highlighting the substantial metabolic demands imposed by shearing. Moreover, this acute metabolic reprioritization may limit the ewes’ ability to sustain thermoregulatory responses throughout the remainder of gestation. As lipid reserves are depleted, and pasture availability and quality can be insufficient to meet the energy demands of even non-shorn ewes²⁹, their capacity to cope with prolonged cold exposure is further compromised.

Three days after shearing, ewes in late gestation had greater β-hydroxybutyrate concentrations than those shorn during mid-gestation. However, this difference appears to be primarily linked to the gestational stage, as previously reported in sheep³⁰. In the current study late gestation ewes showed elevated β-hydroxybutyrate concentrations prior to shearing compared with those in mid-gestation. Most short-term responses to shearing were similar between mid- and late-gestation ewes, suggesting that the timing of shearing within gestation may have a limited impact on their immediate welfare and health. However, shearing ewes during mid-gestation may yield more pronounced positive productive outcomes than late gestation, as it influences placental development and function, fetal growth, and lamb weight and vigor^3,5,6. Since mid- and late gestation typically occur during winter in subtropical and temperate regions, earlier shearing during pregnancy results in a more extended period of cold exposure before lambing. Although the later stages of gestation would align with late winter or early spring, ewes shorn earlier remain exposed to harsh environmental conditions for an extended period. Therefore, long-term studies are needed to assess the overall physiological costs of shearing across different gestational stages, particularly in relation to prolonged cold exposure.

Overall, the results of this study suggest that shearing pregnant ewes triggers thermoregulatory responses that are insufficient to maintain ewe rectal temperature. The responses were similar regardless of whether shearing occurred in mid or late gestation and were energetically demanding, as indicated by increased β-hydroxybutyrate and T3 concentrations. These findings suggest farmers should carefully plan and exercise caution when shearing pregnant ewes in winter. However, the optimal timing of shearing should be determined by factors beyond animal welfare alone.

Author contributions

RU designed the study, performed the statistical analysis, and drafted the manuscript and the final submitted version. LPS organized the fieldwork, collected data at the field, organized data, reviewed the manuscript, and approved the submitted version. KN organized the fieldwork, collected data at the field, organized data, reviewed the manuscript, and approved the submitted version. LCP organized the fieldwork, collected data at the field, organized data, reviewed the manuscript, and approved the submitted version. AFM discussed the original design, interpreted data, reviewed the manuscript, and approved the submitted version.

Data availability

Data are available from the corresponding author upon reasonable request.

Declarations

Competing interests

The authors declare no competing interests.