Recibido: 15/03/2020 Aceptado: 15/12/2020
25
DOI: https://doi.org/10.52973/rcfcv-luz311.art3 Revista Cientica, FCV-LUZ / Vol. XXXI, N°1, 25 - 30, 2021
ABSTRACT
With the aim to assess the eect of short-term thermal stress
on physiological traits of ewes an experiment was designed.
Fourteen hair sheep ewes were selected during early reproductive
management and randomly segregated in two groups. Control
group (CG) with indoor conditions, and an experimental group (EG)
under continuous outdoor conditions without shadow accessing
during 14 days (d). Respiratory frequency (RF), rectal temperature
(RT) and infrared image temperatures were estimated. Traits were
measured for 8 d twice a d (9:00 am and 15:00 pm). Environmental
temperature and humidity were monitored, and temperature and
humidity index was estimated. All physiological and environmental
traits showed significantly variation by group and time of
measurement (P < 0.001). RT and RF were signicantly higher
for EG and during pm measurements. Environmental conditions
indicated thermal stress conditions for outdoor EG during the
afternoon was related ultimately with respiratory mechanism as the
main indicator of continuous thermal stress. Head infrared image
temperature was a good predictor of body temperature.
Key words: Heat stress; infrared thermography; respiratory
frequency; rectal temperature
RESUMEN
Con el objetivo de evaluar el efecto a corto plazo del estrés térmico
continuo sobre las variables siológicas en ovejas, se diseñó un
experimento. Catorce ovejas de pelo fueron seleccionadas durante
el manejo reproductivo temprano y aleatoriamente segregadas
en dos grupos. El grupo Control (CG) con condiciones de sombra
y el grupo experimental (EG) en condiciones de exterior sin
acceso a sombra durante 14 días (d). La frecuencia respiratoria
(FR), temperatura rectal (TR) y temperaturas infrarrojas fueron
estimadas. Las variables fueron medidas durante 8 d dos veces
por d (9:00 am and 15:00 pm). La temperatura y humedad
ambiental fue monitoreada y el indice de temperatura y humedad
fue estimada. Todas las variables mostraron variación signicativa
por grupo y tiempo de medición (P < 0,001). TR y RF fueron
signicativamente mayores en EG y durante las mediciones en
la tarde. Las condiciones ambientales sugieren que el estrés
térmico en condiciones exteriores durante la tarde se relaciona
más claramente con mecanismo de respiración como principal
indicador del estrés térmico a corto plazo. La temperatura infrarroja
de la cabeza fue un mejor predictor de temperatura corporal.
Palabras clave: Estrés térmico; frecuencia respiratoria; temperatura
rectal; termografía infrarroja
Physiological response to thermal stress in hair-sheep ewes during
subtropical summer
Indicadores siológicos de respuesta al estrés térmico en ovejas de pelo durante el verano
subtropical
Javier Alejandro Gómez-Guzmán
1
, José Fernando Vázquez-Armijo
2
, Javier Hernández-Meléndez
3
, Ana Laura Lara-Rivera
4
and Gaspar Manuel Parra-Bracamonte
1
*
1
Centro de Biotecnología Genómica, Instituto Politécnico Nacional. México.
2
Centro Universitario UAEM Temascaltepec, Universidad
Autónoma del Estado de México. México.
3
Facultad de Ingeniería y Ciencias, Universidad Autónoma de Tamaulipas. México.
4
Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León. México. *E-mail: gparra@ipn.mx.
Indicadores siológicos de respuesta / Gómez-Guzmán y col.____________________________________________________________
26
INTRODUCTION
Under the global warming scenario, different environments
suppose a threat for domestic livestock. Among all the stress
conditions, high temperatures are considered the most severe for
animal production [4]. Additionally, humidity, radiation, precipitation
and wind intensity aect livestock production. Specic weather
conditions in particular regions, specically the air temperature and
humidity have direct inuence on animal production [1, 23]. The
exposure to high temperatures produces signicant and drastic
changes on biological functions of sheep (Ovis aries), including
eciency in feed use, water metabolism and mineral equilibrium
alterations and important consequences in endocrine, metabolite
and blood physiology [15].
Animals have a variety of physiological mechanisms for
thermolysis, when these mechanisms are not enough to relieve
the eect of heat load, body temperature (BT) can rise to the point
where animal welfare is compromised [1]. BT is a good measure
of heat tolerance in animals, since it is the result of all processes
of heat gain and loss in the body. Changes in heart rate (HR),
respiratory frequency (RF) and rectal temperature (RT) are the
key parameters that indicate the mechanism of physiological
adaptation in small ruminants [24]. In environments with heat
stress (HS), RF is the rst thermoregulation mechanism used by
ruminants to help them maintain BT; the panting is a physiological
medium recognized as a response to increased environment heat
through a substantial increasing in RF [17].
Some studies has assessed the physiological effect of
temperature stress on sheep supporting the negative eect on
hypothalamus-pituitary-gonads axis [2,21]. Some of these eects
are related to the increasing in glucocorticoid level as a stress
response stimulating hypothalamus for somatostatin secretion
inhibiting growth hormone [11]; additionally, most productive losses
in sheep come from a variety of reproductive problems associated
thermic stress. In females it directly affects the presence and
duration of estrus, displaying low growth of the dominant follicle
and reduced concentrations of gonadotropin-releasing and
luteinizing hormones, reected in a lower estrogen synthesis [9].
The corporal temperature observed by dierent methods such as
rectal and thermographic infrared images and RF has been used as
indicators of short-term thermic stress in dierent reproductive and
growth stages in sheep [28], but not in early stage of pregnancy.
In Pelibuey ewes, the available research indicate that this breed
show more eective BT regulation under articial conditions of
environmental hyperthermia [20], less eects on progesterone
levels [16] and their embryo percentage apparently is less
influenced by artificial hyperthermia [27]. However all these
evidences have been assessed under articial conditions in climate
chamber-induced short term hyperthermia but not under natural
environment conditions.
The aim of the present study was to estimate the physiological
response during early reproductive management of ewes subjected
to continuous TS during late summer under exterior management
conditions in subtropical late summer, under the hypothesis that,
physiological traits of Pelibuey ewes were aected by continuous
TS during the studied period.
MATERIALS AND METHODS
The experiment was conducted during late summer at experimental
farm of Facultad de Ingeniería y Ciencias-Universidad Autónoma de
Tamaulipas, located in northeast Mexico (23°56’ N, 99°06’ W), at 190
meters above sea level. The climate was considered sub-tropical,
which is semi-arid and sub-humid, with summer rains and sporadic
winter rains. The average annual temperature is 23 °C with a total
annual rainfall of 800 millimeters (mm).
Fourteen hair sheep ewes (2-3 years old and 3-4 body condition
score) were treated with an intravaginal sponge impregnated with
20 milligrams (mg) of chronolone (Chronogest® CR, Intervet®
Productions SA, Igoville, France) [22] for 14 days (d). Twenty four
hours (h) before sponge withdrawal, 400 international units (IU)
of equine chorionic gonadotropin (eCG) (Folligon®, Intervet®,
Boxmeer, Holland) were applied. Ewes in estrus were mated by
natural mating around 24 h after the onset of estrus. After copula,
ewes were divided into two groups (n = 7). A control group (CG)
was managed in a conned system and were kept in roofed pens.
A second experimental group (EG) was maintained in a conned
system and were kept in unroofed pen from 7:00 am to 7:00 pm,
under continuous TS stimulus. Both groups had free access to
water and the same isocaloric and iso-protein diet.
The experiment was conducted during eight d of September,
measuring twice a d (9:00 am and 15:00 pm) physiological traits
of RT and RF; also, BT by infrared images (II), considering the
nose, eye, head, back, belly and hip. RT was estimated using
a digital thermometer (Neutek MT-201C, Citisalud S.A. de C.V.,
Mexico). RF, was estimated visually. The II were collected using a
Flir 2 camera (Willsonville, Oregon, USA) and processed with Flir
Tools software. Complementarily, environmental temperature and
humidity were monitored by a hygrothermometer Thermotracker
Higro (Culiacan, Sinaloa, México). Conguration of sensors and
processing of data will be completed using Thermotracker Pro 3.0
software. Temperature and humidity index (ITH) was computed
using the formula described by Mader [14] using the formula {ITH
= [0.8 × ambient temperature] + [(% relative humidity ÷ 100) ×
(ambient temperature − 14.4)] + 46.4}.
All statistical analysis were performed in SAS software ver. 9.0
(Statistical Analysis System, Cary, NC, USA). A mixed model for
repeated measures was tted using the MIXED procedure as:
YGTITH
ijki
ik
ijk1
bf
=+++
Where: Y: physiological and environmental response variables,
G= xed eect of i-the group (CG and EG), T= xed eect of j-th
time of measurement (am and pm), and the ITH as linear covariate
(only for physiological traits). The repeated eect of sheep-day
measured adjusted by a Compound Symmetry covariance
structure was considered given its best AIC and BIC statistics.
Least square means were estimated and compared by a t test
with a Tukey adjustment. Pearson correlation coecients were
computed for all variables using the CORR procedure.
RESULTS AND DISCUSSION
Least square means by group and time of measurement
comparison are showed in TABLE I. Both factors were important
for all physiological traits evaluated (P < 0.01). All temperature
estimates (rectal and infrared) were signicantly dierent among
_____________________________________________________________Revista Cientica, FCV-LUZ / Vol. XXXI, N°1, 25 - 30, 2021
27
groups (P < 0.001). Temperature indicators showed in general that
EG and pm measured ewes had the higher LSmeans. RT showed
averaged increasing values of 0.3 °C for EG compared to CG and
0.6°C during pm. Infrared temperature recording, showed the same
pattern or dierences, between experimental groups and time of
measurement; however, nose had sustained lower temperatures
than other corporal sites, with the highest temperatures recorded
in ewe back and hip (TABLE I). The most important observed
change was in RF; showing a signicantly increasing in EG ewes
maintained in outdoor conditions, speeding their respirations in
almost 30 %, and even more during pm measurements (44 %).
Dierences in environmental recorded traits prevalent during the
experiment in both, experimental groups and time of measurement
are presented in TABLE II. Prevalent conditions showed that
temperatures during morning measurement in CG were slightly higher
than those observed in EG (P < 0.001), with higher percentage of
humidity for animals maintained under outdoor conditions. However,
temperature conditions were consistently higher with almost 10
degrees of dierence for outdoor conditions with lower humidity,
producing signicantly higher ITH estimates (TABLE II).
Correlations among measured indicators are presented in TABLE III.
RT showed signicant but moderate and low correlations with infrared
temperature indicators in CG and signicant but low correlations in
EG. Interestingly, RF showed moderate to high correlations with
infrared temperatures in CG, and a signicant correlation (P < 0.001)
of 0.70 with ITH. Conversely, moderate correlations were observer in
EG among RF and all infrared temperatures, except with ITH showing
a slightly high correlation with ITH (P < 0.001). In both, CG and EG, all
infrared temperatures were highly correlated (r > 0.7). groups. Head
infrared temperature showed to be a reliable indicator given its high
correlation with all other infrared temperature indicators (r > 0.82).
Comfort zone of livestock it is defined as that area with a
temperature range, within which the animal can stay without the
need to activate its thermal self-regulation mechanisms [3]. The
neutral environmental temperature (ET) for sheep was 13 to 31 °C.
Therefore, in this study the ET during the morning was not sucient
for the sheep to be under thermal stress; however, in the EG during
most of the afternoon an upper dierence of 9,2 °C was observed
over the CG with shade availability. Those conditions kept EG ewes
in TS during the experiment.
Traits
Group Time
CG EG am pm
RT 39.34 ± 0.09 a 39.65 ± 0.08 b 39.19 ± 0.12 a 39.81 ± 0.10 b
RF 79.64 ± 2.65 a 108.26 ± 2.22 b 67.59 ± 4.77 a 120.32 ± 379 b
Eye 36.90 ± 0.32 a 38.70 ± 0.26 b 36.20 ± 0.53 a 39.40 ± 0.42 b
Nose 35.77 ± 0.27 a 37.36 ± 0.22 b 34.78 ± 0.48 a 38.34 ± 0.37 b
Head 36.14 ± 0.43 a 38.82 ± 0.37 b 35.50 ± 0.63 a 39.46 ± 0.51 b
Belly 36.25 ± 0.27 a 38.47 ± 0.22 b 35.83 ± 0.49 a 38.89 ± 0.38 b
Back 36.74 ± 0.63 a 41.06 ± 0.53 b 36.70 ± 1.06 a 41.11 ± 0.85 b
Hip 35.89 ± 0.69 a 41.14 ± 0.59 b 35.99 ± 1.11 a 41.04 ± 0.90 b
TABLE I
Eect of the group and the measurement time on physiological traits in hair
sheep ewes
RT: Rectal temperature, °C, RF: Respiratory frequency, times by minute. CG: Control group.
EG: Experimental group
Time Trait CG EG
am
Temperature °C 24.60 ± 0.27 a 22.99 ± 0.25 b
Humidity % 87.64 ± 0.97 a 95.06 ± 0.90 b
ITH 75.11 ± 0.26 a 73.06 ± 0.24 b
pm
Temperature °C 28.13 ± 0.18 a 37.32 ± 0.16 b
Humidity % 77.72 ± 0.57 a 49.24 ± 0.53 b
ITH 79.39 ± 0.18 a 87.33 ± 0.17 b
TABLE II
Dierences in meteorological parameters between morning and afternoon in both groups
sensors during the study
CG: Control group. EG: Experimental group
Indicadores siológicos de respuesta / Gómez-Guzmán y col.____________________________________________________________
28
Some indices have been developed to assess TS. The most
common empirical model of heat load is the ITH, which is a
combination of temperature and humidity eects in a single value
associated with the heat load level and has been used to assess
stress [23]. It is established that an ITH of 74 or less is considered
normal, 75 to 78 corresponds to an alert stage, 79 to 83 to a danger
stage and an ITH equal to or greater than 84 is an emergency
[14]. Under these parameters, outdoor EG ewes were borderline
a normal and under an ITH above normal and the shadow group
was close to being in alert stage. It is considered that due to the
decrease in humidity in the CG the temperature is greater and
that is enough for the ITH to increase in this group. It is known
that according to environmental principles, these variables are
inversely proportional [26]. However, the environmental conditions
(EC) during afternoon resulted in an ITH which might be dangerous
for ewes.
An increase in RT is considered a good indicator of TS in
animals. Signicant increases in RT associated to ITH during the
summer indicate that the animals were in conditions of thermal
stress [19]. The EC that were presented in this study allowed to
suggest that the increase in RT within both groups was directly
related to the increase in ET and ITH. In addition, under the
condition of the present study, the signicant increase in RT was
observed in the EG over the CG; this increase is due to the lack
of the body’s ability to maintain its thermal equilibrium [6]. Macías
et al. [12] reported that in non-lactating ewes the dierences in RT
increase over the course of the d, being smaller in the morning and
greater in the afternoon during the summer season. Similarly, in
the study by Silva et al. [26], signicant eects of higher RT values
were observed in the hottest h of the d which is consistent with
the present values observed in both groups during the afternoon.
In the other hand, regarding RF, the criteria for co-monitoring RF
as an indicator of stress range from < 61-80 breaths/minute (min)
for medium-high stress and 81-120 breaths/min for high stress
[25]. Under this criterion, in the present study the CG presented
medium high stress levels and the EG a high stress; the same
result can be observed by the time of measurement, since in the
morning ewes were in medium high stress and in the afternoon
at a high stress level. It is known that sheep that are exposed to
high ambient temperatures increase their eorts to dissipate body
heat, resulting in an increase in RF [7]. In the present study it
was observed that the increase in the ET and ITH during morning
and afternoon caused the ewes to present signicant increase
in the RF, which shows the importance of RF as a mechanism
of heat loss in small ruminants. Macías et al. [12] reported that
in non-lactating females dierences in RF increased during the
warmer h during the d due to the activation of mechanisms for
heat loss.
For the estimation of animal heat tolerance, RT and RF are
the best physiological variables. However, the assessment of
adaptability can be complemented with variables such as heart
rate and surface temperature [5]. It has also been observed
that thermographic evaluation surveys in sheep can adequately
assess temperature gradients and identify breeds that have
better heat tolerance [10]. Given to a high correlation between
environmental indices and sheep surface temperature, the
importance of establishing indicative values of thermal discomfort
to adopt measures to mitigate thermal stress and not compromise
the productive performance has been stated [23]. In the present
assessment, the temperature on the hair surface shows signicant
differences within both groups and time of measurement; this
agrees well to the results by Macias et al. [13] reporting lower
BT during the mornings and higher at noon. This is because the
variation in temperature in animals is inuenced by the oscillation
of the ambient temperature during the d [18]. In this study, higher
temperatures were obtained on the surface of the animal in the EG,
which was directly exposed to solar irradiation unlike the group that
had access to the shade in the hottest h of the d. Solar radiation
together with a high ambient temperature is considered to be an
important factor for the increase in the temperature of the animal
surface. This is due to vasodilation caused by blood capillaries,
which increase blood ow to the surface of the animal as a way of
RT RF Nose Eye Head Back Hips Belly ITH
RT 0.51*** 0.59*** 0.57*** 0.61*** 0.53*** 0.53*** 0.40** 0.29*
RF 0.42** 0.73*** 0.73*** 0.81*** 0.77*** 0.79*** 0.79*** 0.70***
Nose 0.27* 0.55*** 0.85*** 0.94*** 0.84*** 0.85*** 0.80*** 0.54***
Eye 0.36* 0.52*** 0.79*** 0.89*** 0.76*** 0.80*** 0.73*** 0.48***
Head 0.36* 0.54*** 0.82*** 0.92*** 0.91*** 0.92*** 0.88*** 0.54***
Back 0.41** 0.49*** 0.65*** 0.74*** 0.87*** 0.95*** 0.87*** 0.46**
Hips 0.39* 0.46** 0.70*** 0.80*** 0.88*** 0.89*** 0.89*** 0.51***
Belly 0.36* 0.60*** 0.79*** 0.79*** 0.84*** 0.79*** 0.82*** 0.56***
ITH 0.17 0.72*** 0.51*** 0.45** 0.48*** 0.43** 0.40* 0.48***
TABLE III
Pearson correlation coecient among studied physiological traits and ith environmental variable in two
assessed groups
Control group: Above diagonal, Experimental group: Below diagonal. RT: Rectal temperature, RF: Respiratory frequency,
ITH, Temperature and humidity index. *P < 0.05. ** P < 0.010. *** P < 0.001
_____________________________________________________________Revista Cientica, FCV-LUZ / Vol. XXXI, N°1, 25 - 30, 2021
29
heat dissipation [8]. In addition, it was observed that within the CG
the surface temperature was lower than the RT, which is consistent
with that reported by Piccione et al. [26]. Most importantly, the
present results showed that within the EG, the head temperature
showed a moderate correlation RF and ITH (r ≈ 0,50), maintaining
a high correlation with the other infrared temperature indicators,
which can serve as non-invasive means to detect the presence of
TS within the ock.
Although it was not possible to assess the punctual eect of
continuous TS on reproductive performance of the studied ewes,
the results suggest through the physiological traits that some
possible eects would be expected. Previous studies in Pelibuey
breed have assessed the eect of chamber-induced short term
hyperthermia on some reproductive traits. These available
research indicate that this breed show more eective BT regulation
under articial conditions of environmental hyperthermia [20], has
less eects on progesterone levels during gestational period [16]
and that its embryo development percentage apparently is less
inuenced by articial hyperthermia [27]. However since these
evidences have been assessed under articial conditions did not
allow to fully understand the magnitude of real environmental
hyperthermia on ewes performance.
CONCLUSIONS
Results showed that continuous environmental TS has important
eects on physiological traits of Pelibuey ewes during late summer.
The main effects of this continuous short-term TS are more
observed in RF and BT. Increasing the RF was the best mechanism
for heat removal for the ewes during the present study. It also
establishes the use of novel methods such as thermal infrared
imaging as non-invasive eective was of detection of TS. Finally,
the importance of roofed facilities to avoid heat loading in animals
was considered, since it was observed that the experimental group
presented TS conditions that could possibly damage its production
and reproduction.
ACKNOWLEDGEMENTS
Authors want to thank the Instituto Politécnico Nacional
(SIP20195038) and Universidad Autónoma del Estado de México
(4766/2019CIB) for the nancial support to this study. Fisrt author
acknowledges the scholarship granted by the Consejo Nacional
de Ciencia y Tecnología-CONACYT, Mexico.
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