Recently, global environmental temperature increase due to global warming and climate change are getting worse every year, and livestock cannot be free from the effects. Heat stress occurs when the net heat dissipation flowing from the body to its surrounding environment is less than the amount of heat energy produced by the body [1], and it causes serious losses in animal welfare and productivity. Heat stress reduces the feed intake, body weight, production efficiency and metabolic rate of animals [2,3]. In broilers, heat stress increased pale, soft and exudative meat, drip loss and lactate content in the muscle, whereas it reduced protein synthesis in the breast muscle, caused oxidative damage to skeletal muscle and had a harmful effect on meat color and pH value [4,5]. Heat stress not only caused a reduction in feed intake, body weight, dietary digestibility, dietary calcium, serum protein and calcium content but also caused reproductive problems, poor egg quality, impaired skeletal integrity, poor egg mass and poor egg production in laying hens [6,7]. Poor performance under heat stress is accompanied by not only drop in the growth performance but also increasing mortality of broilers [8].

The heat stress levels animals feel vary according to environmental factors, such as ambient temperature, relative humidity, solar radiation and wind speed, and animal management strategies, such as feed, water, environment modifications and handling changes. In addition, animal characteristics such as species, color, sex, age, temperament, previous exposure, body condition and current health could also affect the extent of heal stress [3,9]. Therefore, the heat stress from which animals suffer can be diagnosed accurately when a variety of measurement methods are combined to reflect animal-based criteria in addition to measuring environmental factors.

Ambient temperature is a crucial climatic factors that has a strong effect on maintaining the body temperature within the normothermic ranges in domestic fowls; therefore, their body temperature monitoring will provide useful information in regard to the intensity of thermal stressors on their thermoregulatory status [10,11]. The conventional methods directly measure the body temperature, and thus are associated with invasiveness, and being time consuming and labor-intensive. Therefore, conventional methods would potentially result in measurement errors. In response to these shortcomings, infrared thermal imaging technology offers a fast, highly precise, non-invasive, and non-contact method for measuring the skin surface temperature [12]. Furthermore, this technology enables to continuously collect the data during the stress period, which eliminates the confounding effects associated with frequent capturing of animal and sampling [13].

A strong correlation has been reported between body temperature and facial surface temperature (FST) in chicken [11]; therefore, the variations in environmental temperature could rapidly be manifested in skin surface temperature, which makes it an important parameter in monitoring the comfort or thermal stress of chickens using infrared thermography [14–16]. For skin temperature measurement using infrared thermography in poultry studies, bare areas such as the eye, comb and wattle, earlobes, or nose are the potential zones for detection of temperature differences as thermal stressor intensity changes. Herborn et al [13] identified temperature differences in the skin surface of hens as thermal intensity shifted from a mild to a more severe acute stress. However, to our knowledge less is known about the contributions of different facial surface sites of laying hens when exposed to thermally comfortable or stressful conditions. Therefore, this study was aimed at identifying the regional differences in the FST of laying hens through infrared thermography technology in response to the thermal variations in the environment.

One of the notable features of the FST is that it is highly affected by dynamic environmental temperature changes. The core temperature in hens is regulated within the range of about 40.6°C to 41.7°C [18] but in this experiment, 10.27°C was the maximum difference of the mean MFST between the ambient temperature group of 6°C and 32°C. In addition, the standard error of the mean (SEM) associated with MFST tended to be smaller with the elevation of ambient temperature; however, higher values for SEM were obtained as ambient temperature declined. For FST measurements, the maximum surface temperature is an important parameter to indirectly measure the core temperature of animals as it more closely resembles the core temperature (Table 1). MFST, the result of body heat exchange, does not rise above the core temperature if the homeostasis of warm-blooded animals is maintained. At the proper temperature (OT), MFST ranged from 38.58°C to 41.88°C, which is generally close to the body core temperature in hens. This association demonstrates that the FST measurements using the thermal imaging camera is a suitable method in reflecting normal body temperature in hens when the environmental temperature is appropriate. On the other hand, the MFST value of 45.41°C recorded at 12:00 h in HT-exposed hens substantially exceeded the normal core temperature range (40.6°C to 41.7°C), which could possibly be explained by the inefficient body heat dissipation in laying hens when kept in heat stress situations. The ambient temperature at this time interval (12:00) was 32°C, which was the highest among the values recorded during HT experiment. A study with laying hens revealed that when THI increased from 25 to 29, hens experienced critical heat stress as evidenced by reductions in feed consumption and egg production, and increase in mortality rate [19]. This might provide an indication that in the current experiment, HT-exposed hens at 12:00 experienced a stressful situation as the mean THI was 27.

Environmental temperature and relative humidity are the major factors that determine body surface heat exchange, and FST measurement using infrared thermography is believed to reflect the rapid changes in body surface temperature. However, it is not enough to consider only ambient temperature and humidity as determinants in order to more sensitively detect changes in FST of laying hens. This is indicated by the fact that FST was measured high even though ambient temperature was not high, such as LT at 12:00 h or OT at 15:00 to 21:00 h. Heat stress results from an imbalance in the homeostasis of the animals, and the level of heat stress that an animal experiences is related to three main factors: the weather conditions, animal characteristics, as well as management protocols used [3,9]. Temperature, humidity, wind speed and solar radiation are important weather components involved in the extent of heat stress as animal experiences [3]. Therefore, several equations have been developed to help summarize these factors into a single usable number [20]. In laying hens, additional parameters such as laying age, the performance of laying, laying time, feeding time, active time, the diurnal rhythm of core temperature as well as species, color, sex, age, temperament, previous exposure, body condition, current health [9] should be considered for animal susceptibility. In addition, since core body temperature (CBT) is the body temperature that the animal maintains for body homeostasis, CBT measurements in the future studies and comparison with the CBT value with the body surface temperature value can specifically support the effect on the sensitivity of the animal [21]. To this end, further studies should be carried out to identify a correlation between each factor for hens’ susceptibility and heat loss and production, and this effort will help detect more accurate and sensitive FST in laying hens.

Laying hen is a small animal, therefore, all regions of the face could easily be included in one photo, which results in MFST that incorporates the surface temperature values of the regions. However, infrared thermography can produce errors depending on the measurement distance or angle. Therefore, in order to minimize these errors, it is necessary to identify which facial region in the laying hen is the most reliable to record the highest distribution of MFST. Wattle surface temperature was the most stable part which showed the highest level of heat production at constant values under any thermal variations. However, the MFST values were frequently identified at around the eyes region in LT-exposed hens. Therefore, wattles and around the eyes could be the most reliable regions for FST measurement in laying hens. However, depending on the environmental temperature, wattles and around the eyes, around the eyes and wattles, wattles could be more reliable at optimal, low, and high temperatures, respectively.

In the present experiment, the poor correlation between MFST and THI and the coefficient of determination of the regression equation might be explained by the measurement method through infrared thermography. Since thermal images were measured manually by the attendant entering the experiment room at each measurement time, the laying hens could be affected by human access. In order to minimize interference due to human approach, the measurement distance of the thermal imaging camera was set at 1.5 m. In this experiment, however, the target subject for thermal image recording was the head of a small animal that is a very small area. Therefore, it is judged that the accurate temperature could not be sensitively detected because the size of the measurement object was small, and the distance was far. In actual farm situations, more accurate FST data will be obtained if the real-time automatic measurement systems could be installed at appropriate spots such as feed bins, water supply nipples, and egg laying boxes. In general, hens have a better ability to cope with low than high temperatures [18], and there is an increasing burden of long-term exposure to high temperatures in the summer, rather than the risk of exposure to low temperatures when managed in a henhouse. When the environmental temperature exceeds 30°C, the difficulty of body heat dissipation given to thick feathered hens increases, leading to high temperature stress. In this situation, the FST of laying hens has the advantage of being closer to the CBT [16] and being easier to access and measure than the surface temperature of other areas such as wings, legs, breast, and back.

Overall, body surface temperature measurements using infrared thermal imaging cameras can be applied to a large number of subjects in a short time, significantly reducing the time and effort acting as a burden on managers who measure body temperature, and there is also no stress on the livestock, which is the measurement target. The findings of this study enabled a better understanding of the temperature differences in the facial regions of hens in response to the ambient temperature fluctuations. Such data could be viewed as potential markers for identification of thermal stress intensity, and thus a useful way to improve the welfare of hens during the high-temperature periods.