Infrared thermography as a non-invasive method for the evaluation of heat stress in pigs kept in pens free of cages in the maternity

Infrared thermography as a non-invasive method for the evaluation of heat stress in pigs kept in pens free of cages in the maternity

Computers and Electronics in Agriculture 157 (2019) 403–409 Contents lists available at ScienceDirect Computers and Electronics in Agriculture journ...

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Computers and Electronics in Agriculture 157 (2019) 403–409

Contents lists available at ScienceDirect

Computers and Electronics in Agriculture journal homepage: www.elsevier.com/locate/compag

Original papers

Infrared thermography as a non-invasive method for the evaluation of heat stress in pigs kept in pens free of cages in the maternity Gisele Dela Riccia, Késia Oliveira da Silva-Mirandab, Cristiane Gonçalves Tittoa, a b

T



Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Av. Duque de Caxias Norte, 225, Pirassununga, SP, Brazil Escola Superior de Agricultura Luiz de Queiróz, Universidade de São Paulo, Av. Pádua Dias, 11, Piracicaba, SP, Brazil

A R T I C LE I N FO

A B S T R A C T

Keywords: Autumn Cortisol Images Summer Tropical

Infrared thermography is a non-invasive method of body surface temperature analysis in pigs. This study aimed to evaluate the body surface temperature of sows and piglets kept in individual pens free of cages with or without cooling system with the use of infrared thermography. The study was conducted during the summer and autumn in Pirassununga, Brazil. Twenty-six sows during lactating phase and 281 piglets until 21 days-old were evaluated in two treatments: cooled pens with fans and water sprinklers on the roof and non-cooled pens. Both areas had ceramic roof tiles. Thermographic images were collected at intervals of seven days in the morning and afternoon in sows and randomly in five piglets per litter, and salivary cortisol were collected only on sows. The thermographic images were analyzed using the software IRSoft Version 3.6 Testo. Every three days respiratory rate and rectal temperatures were collected from sows and five piglets per litter. It was included fixed effect of treatment, period of the day, seasons and their interactions, besides the correlations of Pearson. In summer and autumn, the hottest surface area of sows was the mammary gland and the coldest the vaginal. For the piglets, the hottest area in the summer was the head and the coldest the snout. Summer presented the highest surface temperatures of the sugarcane bagasse bed, concrete floor and roof. No correlations were found between air temperature of and facilities. The respiratory rate presented moderate correlation with the back and with the snout of the sows. Rectal temperatures were higher in summer and in the afternoon, but it was similar between treatments. Although the cooling system had reduced the air temperature of the pens free of cage, it was not enough to reduce body superficial temperatures of the sows and piglets during lactating phase. Nevertheless, the use of infrared thermography allows to identify the hottest and coldest surface body areas of pigs and can be a tool to assess pig facilities and animal welfare.

1. Introduction Pigs have a certain difficulty in adapting to high temperature environments due to their high metabolism, poorly developed thermoregulatory system, thick subcutaneous adipose tissue layer and keratinization of their sweat glands, which impair the loss of heat by sweating (Justino et al., 2014). During heat stress in intensive farming, there is increased excretion of cortisol (Hao et al., 2014), causing alterations in metabolism, with important negative consequences on the behavior and welfare (Silanikove, 2000). Modifications of the environment can improve the quality of life of the animals, satisfying their behavioral and physiological needs (Bracke et al., 2006). The use of cage-free pens for the sows assists in thermoregulation, with the possibility of changing posture and choosing a more comfortable area. However, in hot regions, there is still a need for



thermal conditioning, such as the insertion of fans and water sprinklers, which can reduce the ambient temperature in pig confinement (Dela Ricci et al., 2018). To evaluate the level of comfort and welfare of animals in confinement systems, practical and easy to apply technologies are being used. Infrared thermography emerges as a non-invasive technique (Tattersall, 2016), which allows accurate analyzes of the body temperature of the pigs (Caldara, 2014), obtaining important thermal responses (Phillips and Heath, 2001), without exposing the animal to radiation (Hoogmoed and Snyder, 2002). It can also monitor the metabolic activity of the individuals through the superficial temperature, with qualitative and quantitative evaluations of the heat flow (Eddy et al., 2001), in addition to early diagnosis of diseases (Schaefer et al., 2002). Recently, the use of infrared thermography in experimental pig

Corresponding author. E-mail address: [email protected] (C.G. Titto).

https://doi.org/10.1016/j.compag.2019.01.017 Received 5 August 2018; Received in revised form 6 January 2019; Accepted 12 January 2019 0168-1699/ © 2019 Elsevier B.V. All rights reserved.

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was performed at a seven-day interval. Each sow was allowed to chew a braided cotton rope for 5–10 min. To obtain the required saliva (1 ml), the cotton rope was pressed and the saliva samples were stored in the Salivette® and centrifuged (Fanem Modelo Excelsa II, 206BL) at 3500 rpm for 30 min for cleaning, and immediately after the supernatants were sent for laboratory analysis for the determination of cortisol by the electrochemiluminescence method (Escribano et al., 2012). The respiratory rate and rectal temperature from all sows and five piglets at rest randomly selected from the litter were evaluated three times a week. Respiratory rate was obtained by direct visual observation and counting of the movements of the flanks of the sows and piglets for 1 min, with the help of a digital chronometer, named respiratory movements per minute (mov·min−1). Rectal temperature was collected by a digital thermometer. Infrared thermographic camera (Thermal imager TESTO 875®, Lenzkirch, Alemanha) with emissivity coefficient of 0.98 was used to obtain images for all body of sows and three piglets per litter at a sevenday interval. The evaluation was performed with dry animals and images could be obtained in different positions such: right lateral decubitus, left lateral decubitus, sitting or standing position. The distance used between the thermographic camera for recording the data was between 1 and 1.5 m in the shade. In each image seven point areas were measured for piglets and nine for sows: Dorsal, Ventral, Leg, Paw, Head, Snout and Ocular for the piglets with the addition of the Mammary Gland and Vaginal for the sows (Fig. 1). The temperatures of the roof, the bed of sugarcane bagasse and the concrete floor were also measured using the thermographic camera (Thermal imager TESTO 875®, Lenzkirch, Germany), on a distance of 1–1.5 m for recording the data (Fig. 2). Morning data was obtained from 6:00 to 12:00 and afternoon data was obtained from 13:00 to 18:00.

farms has been widely used, such as castration of piglets and environmental enrichment at weaning among others (Pérez-Pedraza et al., 2018; Pulido-Rodriguéz, 2017; Yañez-Pizaña et al., 2019). Considering the importance of the evaluation of methods that can bring thermal comfort and that can measure the quality of life in a practical and non-invasive way to the pigs, this study was elaborated with the objective of evaluating changes in the body surface temperature of sows kept in individual pens free of cages and their litter, with the infrared camera, in a cooled environment, seeking to indicate sustainable methods for improving the welfare of pigs in the lactating phase. 2. Material and methodology 2.1. Environment and animals The study was conducted at the maternity facilities of the Swine Sector of the City Hall, at the University of São Paulo, Fernando Costa Campus, in Pirassununga, state of São Paulo. The site is at an altitude of 340 m, south latitude of 21° 80′00″ and longitude west of 47° 25′42″, Cwa climate with average annual minimum temperatures of 13 and maximum of 31 °C, according to Koppen (2011), with north-south orientation. The experiment was carried out in the summer and autumn seasons of 2016. The present study was approved by the Ethics Committee on the Use of Animals - CEUA No. 3758260116 of the Faculdade de Zootecnia e Engenharia de Alimentos of the University of São Paulo. The system used was semi-confined in individual pens for sows and litter 1.80 m wide, 4.20 m long, without cages, cemented floor with sugarcane bagasse bed, anti-crushing grid 3.20 m in length, bite nipple drinkers for sows and piglets and concrete feeder trough for piglets and for sows. It has a creep area with radiated lamp for heating the piglets (maintained until weaning 24 h a day), separated from the pens by a wall of 1.65 m of height that allows access only of the infants from an opening in the wall of 0.5 m of height and 0.3 of width. Each pen has two hanging chains used as environmental enrichment for both ages (sows and piglets). The installation has ceiling height of 2.70 m with ceramic roof tiles. Facilities were divided into cooled and non-cooled area. In the cooled area there were ventilators (Ventisol, Brazil) of 60 cm, three propellers, power 1/5CV - 147 W; and maximum 1200 rpm. One ventilator was used for each two sows and their respective litters at 1.80 m from the floor, fixed on the wall, and one sprinkler for water irrigation on the roof (TRAPP - DY-1013, Brazil) was fixed on the wall so that the water was reaching the entire roof for every three pens. The treatments were 7 m distant from each other, and a plastic sheeting was fixed between then (3.5 m way) to separate the environments, preventing circulation of air from the fans for the non-cooled treatment. The meteorological parameters: air temperature and relative humidity were recorded in the experimental pens using a data logger (Onset HOBO® TEMP/RH/2 ext channels) every 15 min, installed in the center of the pens at a height of 1.5 m from the ground to avoid. Twenty-six sows and 281 piglets were studied (154 females and 127 males), weaned at twenty-one days. The animals were vaccinated, underwent routine procedures such as Australian mossing, tooth wearing, tail cutting and castration of male piglets on the second day after birth. Sows and piglets received diet twice a day, at 7 h and 15 h. Sows were fed daily with 7 kg and for piglets the daily quantity was increased gradually when they start eating from 200 g to 500 g until weaning.

2.3. Statistical analysis The data of infrared thermographic temperature, rectal temperature and cortisol were analyzed with fixed effects of treatment (cooled and non-cooled), season of the year (summer and autumn), period of the day (morning and afternoon) and their interactions. The comparisons of the means were performed by the F and t test (PDIFF) using the GLM procedure of SAS Software. Copyright© version 9.3. To correlate the data of infrared thermography, surface temperature and cortisol, the Pearson correlation coefficient was used. The probability level of 5% was chosen as the limit for statistical significance for all tests. From 5 to 7% of probability data was considered as a tendency. 3. Results 3.1. Ambient and facilities Air temperatures were higher in non-cooled pens in the afternoon and in the summer (P < 0.05) and relative humidity was higher in the summer in cooled pens compared to non-cooled ones (P < 0.05) (Table 1). The season influenced the bed surface, concrete and roof infrared thermographic temperatures (P < 0.05), with higher summer averages compared to autumn. However, periods (morning and afternoon) and treatments (cooled and non-cooled) influenced only the roof temperature, with higher temperatures in the afternoon and in the non-cooled environment (Table 2). Correlation were not found between the air temperature and the sugarcane bagasse bed, the concrete floor and the roof (P > 0.05). However, negative correlation were observed for relative humidity and sugarcane bagasse bed (r = −0.273; P < 0.05) and concrete floor (r = −0.302; P < 0.05).

2.2. Physiological analysis of sows and piglets All data was always collected in the pens where the animals were housed, with no need for manual restraint or relocation, starting on day two after birth, at two distinct times (7:00 and 13:00) until 21st day of piglets’ life. Saliva collection for determination of salivary cortisol of the sows 404

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Fig. 1. Demonstration of body areas where images were recorded using the thermographic camera in sows (M1 to M9) and piglets (L1 to L7).

while in the cooled environment it was observed 40.8 mov·min−1 (P < 0.05). Summer showed higher averages (59.2 mov·min−1) in relation to autumn (43.3 mov·min−1) (P < 0.05). The respiratory rate presented moderate correlation (P < 0.05) with the back (r = 0.312) and with the snout (r = 0.350). In relation to the facilities, positive correlations were found with the bed (r = 0.272; P > 0.05), concrete (r = 0.165; P > 0.05), roof (r = 0.487; P < 0.05) and with the internal temperature of the environment (r = 0.353; P < 0.05). Sows rectal temperature was higher in the afternoon (38.3 °C) in relation to the morning (37.9 °C) and in summer (38.4 °C) compared to autumn (37.8 °C). The non-cooled and cooled environment presented the same rectal temperature of 38.1 °C (P > 0.05). Cortisol had a higher mean in the afternoon (1.94 μg·dL−1) than in the morning (1.84 μg·dL−1) (P > 0.05) and in summer (2.0 μg·dL−1) compared to autumn (1.78 µg·dL−1) (P > 0.05). The ambient with the highest mean cortisol concentration was the non-cooled with 2.25 μg·dL−1 compared to the cooled area 1.54 µg·dL−1 (P > 0.05). Cortisol did not showed correlations with the ambient temperature or infrared thermography temperatures (P > 0.05; Table 5).

3.2. Sows The seasons influenced the body surface temperatures of the sow (P < 0.01), whereas the treatments (cooled and non-cooled) and the periods of the day did not (P > 0.05; Table 3). In summer and autumn, the warmest body surface area of the sows was the mammary gland with 35.9 °C and 34.9 °C (P < 0.01), respectively. The cooler body surface area, both in summer and autumn, was the vaginal, with 30.7 °C and 30.1 °C, respectively (P > 0.05; Table 3). Positive and significant correlations were found in relation to sugarcane bagasse bed and superficial temperatures of the dorsal, ventral, mammary gland, leg, head and ocular. In relation to the concrete floor, positive correlations (P < 0.05) were observed in relation to the dorsal, ventral, mammary gland, leg, paw, snout, head and ocular regions (Table 3). The surface temperatures of the dorsal, ventral, leg, paw and vaginal areas presented a positive correlation with the surface temperature of the roof (P < 0.05; Table 4). The respiratory rate of the sows was higher in the afternoon (54.6 mov·min−1) in relation to the morning (47.9 mov·min−1) (P < 0.05). The non-cooled environment presented 61.7 mov·min−1 405

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Fig. 2. Demonstration of the areas of the maternity pens where data were obtained using the thermographic camera. T1: roof without sprinkles (non-cooled), T2: roof with sprinkles (cooled), C1: bed of sugarcane bagasse, C2: concrete floor.

influenced the respiratory rate (64.7 mov·min−1; P > 0.05). Rectal temperature (38.2 °C) did not differ between treatments, periods or season (P > 0.05). The respiratory rate and the rectal temperature of the piglets did not presented significant correlations with the sugarcane bagasse bed, concrete floor or roof.

3.3. Piglets The seasons and periods of the day influenced body surface temperatures of the piglets (P < 0.05), while the treatments did not presented significance. The season of the year influenced the body surface temperatures of the belly and leg (P < 0.05; Table 6). In the summer, the highest surface temperature was found for the head area (36.7 °C) and in the autumn the temperatures of the dorsal, the ventral and the head were similar (35.1 °C) (P < 0.06). The coldest temperature found in summer and autumn was from the snout area (P > 0.05; Table 6). The body surface temperature showed a positive correlation (P < 0.05) with the surface temperature of the bed, instead the leg area (P > 0.05). The concrete floor showed positive correlations for all body surface temperatures evaluated (P < 0.05) while the roof presented positive correlation only with the leg (P < 0.05; Table 7). The period of the day influenced (P < 0.05) the respiratory rate of piglets, with higher averages in the afternoon (70.9 mov·min−1) in relation to the morning (58.5 mov·min−1). The season with the highest respiratory frequencies was summer (68.9 mov·min−1) compared to autumn (60.4 mov·min−1) (P < 0.05). The treatment did not

4. Discussion Pig production is considered one of the most intensive forms of animal production in Brazil, characterized by restricted space movement of sows and interaction between animals, causing important changes in the behavior and comfort of the pigs (Van Putten, 1989). However, advances in genetics, nutrition, animal husbandry and consumer pressure for better quality of life promoted the adoption of ethical production practices by improving quality of life and performance (Harvey and Hubbard, 2013), highlighting the European Union (EU) in determining protective measures, with laws approved in different areas of production (Molento, 2005). The breeding of pigs in cages causes frustration by preventing natural social behavior, since pigs are gregarious animals with a defined hierarchy (Duncan and Fraser, 1997). The absence of cages from

Table 1 Air temperature (T °C) and relative humidity (RH %) of cooled and non-cooled pens. Pens

Summer

Autumn

6–12 h

Cooled Non-cooled

13–18 h

6–12 h

13–18 h

T °C

RH %

T °C

RH %

T °C

RH %

T °C

RH %

23.3bB 25.6bA

79.0aA 67.4cB

26.2aB 29.2aA

86.7aA 66.0cB

21.0bA 21.8cA

84.9aA 80.6aA

22.9bA 23.4cA

84.8aA 74.8bA

Means followed by different small letter differ in line and capital letter in column for air temperature or relative humidity differ by t test (P < 0.05). 406

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Table 2 Infrared thermographic temperature of the sugarcane bagasse bed (bed), concrete floor (floor) and ceramic tiles roof (roof) of the maternity cage-free pens. Area

Bed Floor Roof

Hour

Environment

Season

Morning

Afternoon

P

Non-cooled

Cooled

P

Summer

Autumn

P

26.2 ± 0.51 25.0 ± 0.66 29.5 ± 0.86

27.3 ± 0,54 26.3 ± 0,73 35.7 ± 0,83

0.14 0.20 0.01

26.6 ± 0.52 25.2 ± 0.69 38.3 ± 0.83

26.9 ± 0.53 26.1 ± 0.71 27.0 ± 0.86

0.67 0.38 0.01

27.8 ± 0.53 27.5 ± 0.71 36.6 ± 0.74

25.7 ± 0.52 23.8 ± 0.69 28.6 ± 0.94

0.05 0.03 0.01

Table 3 Body surface temperatures by infrared thermography of sows in the lactating phase during summer and autumn. Body areas

Season

Pr > |t|

Summer Dorsal Ventral Leg Paw Head Mammary Gland Snout Vaginal Ocular

33.8 35.2 34.9 34.5 34.6 35.9 34.5 30.7 35.6

± ± ± ± ± ± ± ± ±

Table 6 Body surface temperatures by infrared thermography of piglets in the lactating phase kept in cage-free pens. Parameters

Autumn 0.35 0.32 0.36 0.34 0.34 0.31 0.30 1.85 0.37

31.2 33.3 32.7 32.6 32.7 34.9 32.7 30.1 33.8

± ± ± ± ± ± ± ± ±

Dorsal Ventral Mammary Gland Leg Paw Snout Head Vaginal Ocular

Pr > |t|

Summer 0.36 0.32 0.35 0.33 0.36 0.30 0.33 1.75 0.43

0.01 0.01 0.01 0.01 0.02 0.03 0.01 0.59 0.03

Dorsal Ventral Leg Paw Head Snout Ocular

Sugarcane bagasse bed

Concrete floor

0.623* 0.548* 0.637* 0.583* 0.509* 0.485 0.357* 0.379 0.411*

0.694* 0.667* 0.536* 0.728* 0.632* 0.522* 0.570* 0.492 0.665*

36.3 36.5 36.6 34.9 36.7 34.8 36.0

± ± ± ± ± ± ±

Autumn 0.30 0.28 0.23 0.32 0.29 0.41 0.39

35.1 35.1 34.9 33.7 35.1 33.3 34.7

± ± ± ± ± ± ±

0.33 0.31 0.26 0.35 0.32 0.46 0.48

0.06 0.01 0.01 0.11 0.06 0.07 0.41

Table 7 Correlations between body surface temperatures of piglets kept in cage-free pens and surface temperature of the facilities by infrared thermography camera.

Table 4 Correlations between body surface temperatures of sows kept in cage-free pens and surface temperature of facilities by infrared thermography. Surface temperature

Season

Ceramic tiles roof 0.441* 0.390* 0.226 0.411* 0.445* 0.262 0.335 0.082* 0.457

Surface temperature

Sugarcane bagasse bed

Concrete floor

Ceramic tiles roof

Dorsal Ventral Leg Paw Snow Head Ocular

0.478* 0.307 0.548* 0.393* 0.458* 0.492* 0.522*

0.506* 0.621* 0.767* 0.562* 0.564* 0.663* 0.415*

0.281 0.292 0.430* 0.256 0.289 0.288 0.231

* P < 0.05.

non-cooled environment due to higher ambient temperature and in the summer season. However, even with differences in their numerical values, the results found did not present significant physiological differences. Changes in cortisol concentration occur due to reactions to stressors and environmental challenges (Koeppen and Stanton, 2009). However, small variations, such as those found in this study, in cortisol concentrations present important peculiarities since significant differences were observed in sows' ocular temperature, demonstrating that when hypothalamic-pituitaryadrenal axis activation occurs, cortisol levels increase with changes of the blood flow, which causes variations in the production of heat, which can be analyzed by means of the ocular thermography (Church et al., 2009). The ocular temperature of sows and piglets were higher in the summer, as well as the rectal temperatures for sows. According to Schmidt et al. (2013) ocular temperature is related to body temperature due to its proximity to the brain. The values of ocular infrared temperature can be a significant indicator of body temperature, as well as a

* P < 0.05.

lactating sows allows the expression of part of their innate behaviors, such as bed exploration, exercise, interactions with their litter, maintaining social contact and playful behavior (D’Eath and Turner, 2009) and also allows the sows to remain in positions like lateral and ventral decubitus, with greater comfort, besides bigger interactions with piglets during the feeding. In addition, it is easy to control individual animal feeding, with different feed systems available as a creep area (Bench, 2013). The inability to present innate behaviors increases the cortisol of sows housed in cells (Broom and Fraser, 2007) and in a heat environment (Barb, 1990). In this study, cortisol concentrations of sows were higher in the afternoon and a likely explanation may be related to glucocorticoid hormone concentrations being higher in the daytime (heat stress) and reduced overnight in pigs (Janssens et al., 1995; Hillmann et al., 2008). Also, higher levels of cortisol were found in the

Table 5 Correlations between physiological parameters of sows and surface temperatures of facilities by infrared thermography. Physiological parameters Respiratory rate (mov·min Cortisol (µg·dL−1) Rectal temperature (°C)

−1

)

Sugarcane bagasse bed

Concrete floor

Ceramic tiles roof

0.272 −0.035 0.204

0.165 −0.089 0.076

0.487* 0.173 0.229

* P < 0.05. 407

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In relation to the facilities, the roof is not of the recommended height for adequate ventilation for lactating pigs, even if constructed of ceramic tiles. According to Furtado et al. (2003) ceramic tiles offer better comfort when compared to cement tile, for example. The surface temperature of the roof, in this study, showed difference between time of day, season and environment, demonstrating the importance of the coverage for the thermal comfort of sows and piglets. In animal confinement facilities, the roof has a primary function in determining thermal changes, especially in tropical regions (Turnpenny et al., 2000). Thus, the heat flow through the roofs is the main reason for the discomfort inside the rural facilities (Rosa, 1984). According to Abreu et al. (2001), since the thermal energy of the upper surface of the tile is transmitted to the lower surface of the tile raising the internal temperature of the installation, especially in the hours of greater ambient temperature, demonstrating the importance of the use of ventilators and sprinklers. Inside facilities, the incident radiation heat load is due to the roof absorption and this effect can be altered by the choice of material used, as well as increasing the distance between the floor and the roof (Suehrcke et al., 2008). Thus, in tropical regions, mechanisms have been used to decrease the total heat gain of the tiles, contributing to generate a cooling effect for the animal breeding facilities (Faghih and Bahadori, 2010). The use of ventilators and sprinklers increases the thermal and behavioral comfort of pigs, because it allows, in addition reducing ambient temperatures, than sows can present natural and important behavior, such as exploring and playfulness, with emphasis on heat loss through conduction (Barb, 1990; D’Eath and Turner, 2009).

suitable method to estimate the physiological condition of stress in confined pigs (Weschenfelder et al., 2013), and it becomes a practical and important substitute for invasive measurement methodologies (Johnson et al., 2011; Brown-Brand et al., 2013; Pulido-Rodriguéz, 2017). According to Weschenfelder et al. (2013) the ocular infrared temperature is an important indicator of body temperature and a useful method to evaluate the physiological condition of stress in pigs, constituting a substitute for invasive methods of analysis (Johnson et al., 2011; Brown-Brand et al., 2013). The temperature of the head and the snout of the sows presented as an important mechanism of measurement of heat. According to Schmidt et al. (2013) the eyes and behind the ears (in the head) are reliable points for measuring body surface temperature through the technique of thermography. Furthermore, in heat stress situations, the circulatory transfer to the skin is expanded by dilating the arterioles of the cutaneous vascular beds and by opening the arteriovenous anastomoses in the limbs, ears and snout, increasing the peripheral blood flow causing heat loss to the environment from the superficial skin (Romanovsky, 2014). Evaluating physiological parameters of pigs in comfort (22 °C) and thermal stress (32 °C), Manno (2006) found values of body surface temperatures 9.5% higher in animals under heat stress compared to pigs submitted to thermal comfort. The dorsal temperature of sows and piglets were higher in the summer season, in the afternoon and in the non-cooled environment. Due to exposure to higher temperatures in the non-cooled environment, these were responsible for the increase in the dorsal temperature when compared to the cooled ones, mainly due to the presence of water and ventilation that allow greater heat exchange. According to Silva and Silva (2009) the higher body surface temperatures are due to the increase in peripheral blood circulation used as a way to dissipate body heat. The piglets still remained in idleness, frequently crammed and inside the creep area, which can also increase the dorsal temperature of these animals. The dorsal surface temperature is considered a good measure to describe the environment in which the animal is housed (Collier et al., 2006; Stewart et al., 2008; Weschenfelder et al., 2013). The superficial temperature of the mammary gland was the highest found from the all body. Corroborating with this result, Kotrbacek and Nau (1985) indicated in their study that postpartum sows have hotter surface areas in the mammary gland, where in the last days of gestation of pigs, particularly after delivery, the temperature of the skin on the mammary gland represented the hottest area of the body surface, with temperatures of 39 °C on the first day of lactation and in other periods the temperature remained between 37 and 38 °C. According to BrownBrand et al. (2013) thermographic images are used to assess thermal comfort and body surface temperatures and are considerably affected by ambient temperature. The rectal temperature of sows was higher in the afternoon, in the summer season and in the non-cooled environment, following a consistency since these conditions showed higher ambient temperatures due to the time, the season and the absence of indoor cooling. In this study, piglets had exclusive access to a creep area to protect against the cold, which may have influenced the heating and the presentation of nearby rectal temperatures in both treatments and during the day and seasons. According to Silva (2008) physiological parameters such as rectal temperature, respiratory rate and skin temperature are directly influenced by the time of day, since in the afternoon the air temperature is often higher in this period in relation to morning hours, leading to an increase in these physiological variables important for analysis of heat stress. Animals commonly have a rectal variation that is minimal in the morning and maximum in the afternoon, making the air temperature in the afternoon responsible for the high rectal temperature of pigs in the tropics (Hillmann et al., 2008). The rectal temperature is considered as an adequate parameter to estimate the effect of the ambient temperature on the animals (Sellier et al., 2014), instead of being an invasive measure.

5. Conclusion Although the cooling system had reduced the air temperature of the pens free of cage, it was not enough to reduce body superficial temperatures of the sows and piglets during lactating phase. Nevertheless, the use of infrared thermography allows to identify the hottest and coldest surface body areas of pigs and can be a tool to assess pig facilities and animal welfare. Acknowledgements This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) Finance Code 001. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.compag.2018.12.053. References Abreu, P.G., Abreu, V.M.N., Dalla Costa, O.A., 2001. Maternity hut covering evaluation in outdoor pig production system, summer data. Rev. Bras. Zootec. 30, 1728–1734. Barb, C.R., 1990. Opioid modulation of LH secretion by pig pituitary cells in vitro. J. Reprod. Fertilit 90, 213–219. Bench, C.J., 2013. Group gestation sow housing with individual feeding – II: how space allowance group size and composition, and flooring affect sow welfare. Livest. Sci. 152, 218–227. Bracke, M.B.M., Zonderland, J.J., Lenskens, P., Schouten, W.G.P., Vermeer, H., Spoolder, H.A.M., Hendriks, H.J.M., Hopster, H., 2006. Formalized review of environmental enrichment for pigs in relation to political 12 decision making. Appl. Anim. Behav. Sci. 98, 165–182. Broom, D.M., Fraser, A.F. (Eds.), 2007. Domestic Animal Behaviour and Welfare, vol. 4 CABI Publishing, Wallingford. Brown-Brand, T., Eigenber, R., Purswell, J., 2013. Using thermal imaging as a method of investigating thermal thresholds in finishing pigs. Biosyst. Eng. 114, 327–333. Caldara, F.R., 2014. Piglets’ surface temperature change at different weights at birth. Asian-Australas. J. Anim. Sci. 27, 431–438. Collier, R.J., Dahl, G.E., Vanbaale, M.J., 2006. Major advances associated with environmental effects on dairy cattle. J. Dairy Sci. 89, 1244–1253. Church, J.S., Cook, N.J., Schaefer, A.L., 2009. Recent applications of infrared

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Computers and Electronics in Agriculture 157 (2019) 403–409

G.D. Ricci et al.

Pérez-Pedraza, E., Mota-Rojas, D., González-Lozano, M., Guerrero-Legarreta, I., MartínezBurnes, J., Mora-Medina, P., Cruz-Monterrosa, R., Ramírez-Necoechea, R., 2018. Infrared thermography and metabolic changes in castrated piglets due to the effects of age and the number of incisions in the testicles. Am. J. Anim. Vet. Sci. 13, 104–114. Pulido-Rodriguéz, L.F., 2017. Infrared thermography of the ocular surfasse as stress indicator for piglets postweaning. Pesq. Vet. Bras. 37, 453–458. Phillips, P.K., Heath, J.E., 2001. An infrared thermographic study of surface temperature in the euthermic woodchucks (Marmota monax). Comp. Biochem. Physiol. Part A, Physiol. 129, 557–562. Romanovsky, A.A., 2014. Skin temperature: its role in thermoregulation. Acta Physiol. (Oxf.) 210, 498–507. Rosa, Y.B.C.J., 1984. Influência de três materiais de cobertura no índice de conforto térmico em condições de verão, para Viçosa – MG. Editora UFV, Viçosa. Sellier, N., Guettier, E., Staub, C., 2014. A review of methods to measure animal body temperature in precision farming. Am. J. Agric. Sci. Technol. 2, 74–99. Schaefer, A.L., Matthews, L.R., Cook, N.J., Webster, J., Scott, S.L., 2002. Novel non-invasive measures of animal welfare. Animal Welfare and Behaviour. Science Solution, Joint NAWAC/ISAE Conference, Hamilton, New Zealand. Schmidt, M., Hoffmann, G., Ammon, C., Schön, P., Manteuffel, C., Amon, T., 2013. Application of infrared thermography on lactating sows. Livest. Mach. 68, 228–231. Silanikove, N., 2000. Effects of heat stress on the welfare of extensively managed domestic ruminants. Livest. Prod. Sci. 67, 1–18. Silva, I.J.O., 2008. Effect of housing system on the behavior and welfare for pregnant sows. Rev. Bras. Zoot. 37, 1319–1329. Silva, J.P., Silva, L.P.G., 2009. Estudo e avaliação do consumidor de carne suína “in natura” e industrializada na microrregião de Guarabira-PR. Agropec. Cient. SemiÁrido 05, 57–61. Stewart, M., Stafford, K.J., Dowling, S.K., Schaefer, A.L., Webster, J.R., 2008. Eye temperature and heart rate variability of calves disbudded with or without local anesthetic. Physiol. Behav. 93, 789–797. Suehrcke, H., Peterson, E.L., Selby, N., 2008. Effect of roof solar reflectance on the building heat gain in a hot climate. Energy Build. 40, 2224–2235. Tattersall, G.J., 2016. Infrared thermography: a non-invasive window into thermal physiology. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 202, 78–98. Turnpenny, J.R., Wathes, C.M., Clark, J.A., Mcarthur, A.J., 2000. Thermal balance of livestock. 2. Applications of a parsimonious model. Agric. For. Meteor. 101, 29–52. Van Putten, G., 1989. The pig: a model for discussing animal behaviour and welfare. Appl. Anim. Behav. Sci. 22, 115–128. Weschenfelder, A.V., Saucier, L., Maldague, X., Rocha, L.M., Shaefer, A.L., Faucitan, O.L., 2013. Use of infrared ocular thermography to assess physiological conditions of pigs prior to slaughter and predict pork quality variation. Meat Sci. 3, 616–620. Yañez-Pizaña, A., Mota-Rojas, D., Ramírez-Necoechea, R., Castillo, M., Santiago, P., Mora-Medina, P., González, M., 2019. Application of infrared thermography to assess the effect of different types of environmental enrichment on the ocular, auricular pavilion and nose area surface skin temperatures of weaned piglets. Comput. Electron. Agric. 156, 33–42.

thermography for animal welfare and veterinary research: everything from chicks to elephants. In: InfraMation, Proceedings, pp. 215–244. D’Eath, R.B., Turner, S.P., 2009. The natural behaviour of the pig. In: Marchant-Forde, J.N. (Ed.), The Welfare of Pigs. Springer, Dordrecht, pp. 13–45. Dela Ricci, G., Berto, D.A., Dalla Costa, O.A., Teixeira, R.S., Tonon, E., Titto, C.G., 2018. Specific climatization of swine maternity: ethological evaluation of lactating females. Braz. J. Hyg. Anim. Sanity 2, 12–15. Duncan, I.J.H., Fraser, D., 1997. Understanding animal welfare. In: Appleby, M.C., Hughes, B.O. (Eds.), Anim. Welf., vol. 3, pp. 19–31. Eddy, A.L., Hoogmed, V.L.M., Snyder, J.R., 2001. The role of termography in the management of equine lameness. Vet. J. 162, 172–181. Escribano, D., Fuentes-Rubiano, M., Cerón, J.J., 2012. Validation of an automated chemiluminescent immunoassay for salivary cortisol measurements in pigs. J. Vet. Diagn. Invest. 24, 918–923. Faghih, A.K., Bahadori, M.N., 2010. Three dimensional numerical investigation of air flow over domed roofs. J. W. Engin. Ind. Aerod. 98, 161–168. Furtado, D.A., Nascimento, J.W.B., Azevedo, P.V., 2003. Análise do conforto ambiental em galpões avícolas utilizando telhas de barro e suas associações no agreste paraibano. Rev. Braz. Sci. Av. 5, 107. Hao, Y., Feng, Y., Yang, P., Feng, J., Lin, H., Gu, X., 2014. Nutritional and physiological responses of finishing pigs exposed to a permanent heat exposure during three weeks. Arch. Anim. Nut. 68, 296–308. Harvey, D., Hubbard, C., 2013. Reconsidering the political economy of farm animal welfare: an anatomy of market failure. Food Pol. 38, 105–114. Hillmann, E., Schrader, L., Mayer, C., Gigax, L., 2008. Effects of weight, temperature and behaviour on the circadian rhythm of salivary cortisol in growing pigs. Anim. Cons. 8, 405–409. Hoogmoed, L.M., Snyder, J.R., 2002. Use of infrared thermography to detect injections and palmar digital neurectomy in horses. Vet. J. 164, 129–141. Janssens, C.J., Helmond, F.A., Wiegant, V.M., 1995. The effect of chronic stress on plasma cortisol concentrations in cyclic female pigs depends on the time of day. Domest. Anim. Endocrinol. 12, 167–177. Johnson, S.R., Rao, S., Hussey, S.B., Morley, P.S., Traub-Dargatz, J.L., 2011. Thermographic eye temperature as an index to body temperature in ponies. J. Eq. Vet. Sci. 31, 63–66. Justino, E., Nääs, I.A., Carvalho, T.M.R., Neves, D.P., Salgado, D.D’A., 2014. The impact of evaporative cooling on the thermoregulation and sensible heat loss of sows during farrowing. Eng. Agric. 34, 1050–1061. Koeppen, B.M., Stanton, B.A., 2009. Berne y Levy: Fisiologia, vol. 3 Elsevier Mosby, Barcelona. Koppen, 2011. Clima dos Municípios Paulistas. < http://www.cpa.unicamp.br/outrasinformacoes/clima-dos-municipios-paulistas.html > . Kotrbacek, V., Nau, H.R., 1985. The changes in skin temperatures of periparturient sows. Act. Vet. 54, 35–40. Manno, M.C., 2006. Effects of ambient temperature on the performance of pigs from 30 to 60 kg. Rev. Bras. Zoot. 35, 471–477. Molento, C.F.M., 2005. Bem-estar e produção animal: aspectos econômicos – revisão. Arch. Vet. Sci. 10, 1–11.

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