1. Introduction
The changes to animal feeding management and environmental conditions arising from global warming can increase animal stress levels greatly and affect animal behavioral welfare, which can lead to the loss of farm animals and food crises [
1]. Probiotics are widely known to improve behavioral welfare and productivity in farm animals, while simultaneously lowering animal stress under poultry feeding management and environmental conditions [
2,
3]. A probiotic composed of
B. subtillus,
S. galilaeus, and
Sphingobacteriaceae has been reported to improve egg production, egg quality, and broiler production, while reducing odor [
4,
5].
Probiotics and digital livestock systems have been introduced as sustainable livestock strategies to help combat climate change [
1,
6]. Such technologies can improve livestock production, as well as farm income through enhanced animal health, behavior, and welfare while reducing environmental issues due to climate change [
7,
8].
In some previous studies, digital livestock systems were reported for improving egg production, egg quality, and animal behavioral welfare through increased nutrient digestibility, as well as balanced blood parameters, immune function, cecal microbiota, and short-chain fatty acids in laying hens and swine [
6,
9]. The digital poultry system is an innovative animal-feeding and -management model that can meet the constraints of climate change by using remote control, sensing, and precision livestock technology for animal movements and management and environmental conditions such as temperature, humidity, ventilation, and smell [
10,
11]. It is expected to reduce the time and labor necessary for feeding management involving water and feed intake, weight, litter, and dead chicks, while boosting animal health and facilitating business management [
12,
13]. Owing to these benefits, researchers in many countries have studied diverse application methods to increase the production, behaviors, and welfare of broiler chickens using digital poultry systems [
1,
10,
14].
The health of broiler chickens depends primarily on animal management and environmental condition control. As factory-intensive conventional livestock systems have fallen behind in terms of automation and insufficient labor, the overall control of poultry houses has been unsatisfactory. Moreover, a poor environment has negative effects on the animal behavioral welfare, which results in increased animal stress and impaired welfare, leading to reduced poultry production [
15,
16,
17].
Until recently, little has been reported in the literature about the biological mechanism of the combination of a probiotics and a digital poultry system for improving animal behavioral welfare such as drinking, eating, locomotion, grooming, resting, and also foot pads, hock burns, plumage, and gait scores, in addition to growth performance such as body weight, feed intake, and the feed conversion ratio of broiler chickens [
6,
9,
10,
18].
However, based on the previously studied biological mechanism for improving the productivity and behavioral welfare of farm animals, applying the combination of a probiotics and a digital poultry system may have a positive effect on the growth performance and behavioral welfare of broiler chickens. Therefore, the study hypothesized that the application of this combined system will improve behavioral welfare and growth performance in broiler chickens. The aim of this study was to identify the biological mechanisms for improving immune functions, cecal microbiota balance, animal behavioral welfare, and growth performance in broiler chickens by using the combination of a probiotics and a digital poultry system.
4. Discussion
Renewed interest in the application effects of a digital poultry system along with probiotics has gained global attention in recent years owing to the convergence of livestock and ICT tools as sustainable livestock farming strategies in response to climate change [
1,
2,
9,
11]. The main goal of this study was to identify the biological mechanisms of the growth performances, behaviors, and welfare of broiler chickens reared by the combination of a probiotic and a digital poultry system. The research findings highlight a new fact that the growth performances of broiler chickens could be improved by the combination of a probiotics and a digital poultry system compared to the conventional poultry system (
Table 2). The results of this study are partially in line with the authors’ previous report, wherein improved egg production was observed for laying hens that were not fed probiotics and housed in a digital poultry system converged with ICT [
9,
14], along with improved growth performances of broiler chickens housed in a digital poultry system without being fed probiotics [
27], and enhanced swine production when raised under a combination of a probiotics and a digital livestock system compared to the conventional system [
6,
9,
10]. These observations support our results, but studies on the growth performances of broiler chickens reared under the combined system have not been reported yet. Since the combination of a probiotics and a digital poultry system helped improve the growth performance of broiler chickens, it can be considered as a molecular mechanism related to animal biomarkers through balanced immune organ indexes, such as the spleen, thymus, and bursa of Fabricius, as well as the serum IgG, corticosterone, H/L ratio, and cecal bacteria [
3,
9,
14,
27] (
Table 3,
Table 4 and
Table 5). The fact that the corticosterone level was highest in the CON group may be attributable to physiological changes in the broiler chickens due to insufficient basic animal management techniques, such as environmental temperature, humidity, ventilation, and maintenance of dietary intake and water supply [
4,
5,
9,
14,
15]. In particular, compared to the digital poultry system groups, the animal caretaker’s frequent entry into the livestock barn and interference with animal management to observe the condition of the livestock, such as animal feeding management and animal care, would have acted as major stress factors [
8,
9,
12,
15,
16,
17]. In the CON group, when the water supply stopped suddenly, the ventilation fans stopped working so that the environmental abnormalities caused abnormal animal movements, which we observed directly and took action on. Meanwhile, the digital poultry system groups used automation technology combining big data and ICT tools to identify the housing environment and animal status without time and space constraints, allowing real-time monitoring to quickly implement appropriate measures so as to ensure comfortable animal welfare. With these improvements, it can be seen that the corticosterone levels were lower compared to those of the CON group [
8,
15,
16,
17]. The digital poultry system group used automation technology combining big data and ICT tools to identify the housing environment and animal status without time and space constraints, allowing real-time monitoring via remote control using mobile phones to quickly implement appropriate measures so as to ensure comfortable animal welfare. With these improvements, it can be seen that it affects the improvement of biomarkers, the development of immune organs, the level of antibodies and corticosterone, etc. [
8,
15,
16,
17]. The digital poultry system group used automatic technology to monitor the housing environment, feeding management, and animal movement in real-time, such that appropriate actions can be taken when problems arise (see above). Therefore, by increasing the dietary intake and nutrient digestibility (not determined here [
8]), the development of immune cells is stimulated while the serum IgG, corticosterone, H/L ratio, and cecal bacteria become balanced as the biomarkers are maintained (
Table 3,
Table 4 and
Table 5). By maintaining the balance of biomarkers and promoting animal welfare, it is expected that the growth performance could be improved [
1,
6,
8,
9,
10,
11,
12]. On the other hand, probiotics that can replace antibiotics in poultry feed are known to compete with other gut bacteria for nutrients, induce the production of antibacterial substances, and improve the growth performances of birds by increasing their immune functions, nutrient digestibility, intestinal morphologies, and microbiota [
3,
14,
27,
28]. The significantly higher growth performance of broiler chickens in the DPS500 group could be due to the interaction of the combination of a probiotics and a digital poultry system. All these are related to the effects of probiotics.
The study results indicate that the combined system can suppress animal stressors by stimulating immune functions in broiler chickens. In addition, one of the most-important roles of probiotics is to stimulate immunity against invading pathogenic bacteria; they are known to improve the appropriate microbial environment of the digestive tract and host animal immunity [
3,
29,
30]. Animals raised under good animal feeding and environmental management practices using ICT show lower stress levels, which ultimately improves animal production [
1,
16,
31]. The fact that the combination of a probiotics and a digital poultry system improves animal biomarkers, such as the development of immune organs, the levels of serum IgG and corticosterone, the H/L ratio, and the control of cecal bacteria, is consistent with the results of previous reports and digital poultry systems fused with ICT [
14,
27]. It is clear how the probiotics exert their effect. The digital poultry system uses automatic technology to monitor the housing environment, feeding management, and animal movement in real-time, such that appropriate actions can be taken when problems arise (see above). Therefore, by increasing the dietary intake and nutrient digestibility (not determined here [
8]), the development of immune cells is stimulated while the serum IgG, corticosterone, H/L ratio, and cecal bacteria balance as biomarkers are maintained (
Table 3,
Table 4 and
Table 5). By maintaining the balance of biomarkers and promoting animal welfare, it is expected that the growth performance could be improved [
1,
6,
8,
9,
10,
11,
12].
These results found with respect to broiler chickens may be attributable to the use of smartphones through sensing platforms, automatic animal feeding management, and environmental management via central control through cloud computing systems [
1,
7,
10]. It can be observed that probiotics stimulate the development and growth of immune cells in conventional poultry systems based on the fact that the CON500 group had better immune function than the CON group, even though there was no difference between the DPCS and CON500 groups. Probiotics are well known to enhance the development and growth of immune cells by feed intake stimulation in the digestive tract (
Table 2), as well as increase the absorption and utilization rates of nutrients (not determined) [
3,
6].
Our results suggest that the intestinal microbiota balance was well maintained in broilers raised under a combination of a probiotics and a digital poultry system. The gut microbiota are directly related to the growth performance and health of animals. In general, the number and structural composition of gut microbiota play important roles in the absorption of nutrients and health in the host animals [
32]. There were no differences between the DPCS and CON500 groups in terms of the cecal
Lactobacilli,
E. coli, and total aerobic bacterial balance, but the DPCS and CON500 group showed more balanced results than the CON group. The digital poultry system maintains gut microbiota balance compared to the CON group (
Table 5). The gut microbiota are closely related to the health of the host and are greatly influenced by diet, animal management, and environment [
2,
3,
4,
6,
27,
28,
29]. Animals raised in the digital poultry system may have achieved maintenance of gut microbiota via a reduced number of harmful bacteria and an increased number of beneficial bacteria in the cecum because of their increased nutrient digestibility and good environmental management through digital technologies (remote control and sensing technologies), which can help control these factors well. The balanced gut microbiota of livestock can have positive effects on the survival and growth of these animals, such as improved immune functions and body weight gain [
1,
8,
28,
29]. These research findings could be a beneficial effect of the combination of a probiotics and a digital poultry system and may be due to the biological function of the probiotics and the automated animal feeding and environmental management from the digital poultry system. The benefits are believed to be derived from the stimulated immune functions (
Table 3 and
Table 4) and activated nutrient metabolisms (not determined) in the digestive tracts of animals housed under a combination of a probiotics and a digital poultry system [
6]. The results are also in line with the authors’ previous reports [
6,
14,
27]. The use of either probiotics or raising animals alone under a digital poultry system without the use of a probiotics is known to maintain balanced cecal microflora, but few results have been reported in the literature for broiler chickens so far [
6]. Furthermore, the result that the cecal microbiota balance of broiler chickens reared in the ICT convergence smart system was maintained supports this result [
27]. Probiotics are a class of beneficial microbiota that influence host responses by regulating appropriate gut microbiota. In broiler chickens, the cecal environment can be influenced by the ingestion of probiotics that prevent gut colonization by harmful bacteria [
3,
30,
31]. The growth performances of broilers reared under the conventional poultry systems were lower than those of broilers reared under a combination of probiotics and digital poultry systems, and the CON group showed lower values than CON500 (
Table 2). Even though the control group in the experiment was not exposed to specific stress factors, the fact that the microbial balance and immune functions in the cecum were worse than those of the other treatment groups can be seen as a synergistic effect of the combination of probiotics and the digital poultry system (
Table 3,
Table 4 and
Table 5).
Lactobacillus sp. is known to maintain antibacterial activity and bacterial balance, in addition to maintaining the natural stability of the intestinal microflora against biological changes caused by various environmental conditions [
2,
3]. In the conventional poultry system, poor animal health, such as decreased nutrient digestibility, as well as lower immune function due to insufficient management of the housing environment and animal feeding by the animal caretaker, may have disturbed the stability of the intestinal microbial ecosystem and perturbed homeostasis, causing the decrease in growth performance [
2,
3,
28,
30]. The digital poultry system utilizes mobile phones and sensing technology to proactively monitor animal movements and environmental conditions to solve problems related to animal production in real-time, thereby increasing nutrient digestibility and improving the immune system development and biomarker balance in the animals. This may have contributed to increasing the growth performance by maintaining homeostasis [
1,
6,
9,
10,
11]. The results of the present study show that probiotics improve immune functions while relieving stress by maintaining microflora balance and inhibiting the growth of harmful bacteria in the cecum. In particular,
Lactobacillus is known to maintain antibacterial activity and bacterial balance, in addition to maintaining the natural stability of gut microbiota against biological changes caused by various types of animal stress. Specific measures were established to frequently observe the farm environment and chicken movements directly in the CON groups, monitor the digital poultry system groups via remote control in real-time to solve problems, and collect information on the behavioral patterns and health conditions of the animals. During the experiments, if the environmental conditions changed or problems were noted in terms of floor moisture and ammonia because of the water supply or bedding, the animal caretaker directly entered the cage and operated the supplied equipment or replaced the bedding to solve the problem. When lesions or inflammation of the foot pads were identified, the wounds were treated with disinfectant to help recovery (see above). In stressful environments such as poor health of the animals, heat and cold, digestive disorders, reduced nutrient availability, and reduced immune function [
3,
14,
15], stabilization of the intestinal microbial ecosystem is disturbed and homeostasis is broken, resulting in reduced growth performances of the animals [
14,
29,
32]. It is probably for this reason that the growth performances of broiler chickens housed under the conventional poultry system were lower than those housed under the combination of a probiotics and a digital poultry system (
Table 2), with the CON group showing lower values than the CON500 group. The digital poultry system, a convergence technology of ICT and livestock farming, is known to lower animal stress. In particular, it reduces animal stress by appropriately maintaining the factors related to growth performance, increases nutrient digestibility, and enhances the development of immune organs via preemptively monitoring animal movements and environmental conditions using mobile phones and sensing technology [
6,
33].
The study results showed that the combination of a probiotics and a digital poultry system can improve animal behavioral parameters, such as drinking, eating, locomotion (moving), grooming, and resting (lying down) as well as animal welfare indexes, such as the foot pads, knee burns, plumage, and gait, compared to the conventional poultry system (
Table 6 and
Table 7). Despite maintaining appropriate animal stocking density during the experiment, there were significant differences in the foot pads, knee burns, plumage, and gait between the CON and the other groups. The reason for this is that the CON group had an inadequate environment, feeding management, and animal management; on the other hand, the digital poultry system groups allowed the collection and utilization of standardized data using a digital system combining big data and ICT, through which we were able to identify abnormal entities in real-time via remote control and implement specific measures. Broiler chickens are often raised on flat floors, and bedding containing sawdust is provided to create an environment where the livestock can feel comfortable. In the process of raising livestock, the amount of manure discharge increases, and the moisture content of the floor increases gradually. Physical abnormalities, such as dermatitis on the soles of the foot pads and feather pulling, can easily occur in animals that come into direct contact with wet floors. This may have affected the foot pads, knee burns, plumage, and gait scores in the CON group. The digital poultry system operates in a self-driving manner using an automatic litter spreader according to input information previously set by the manager. By monitoring the condition of the bedding and animal in real-time, specific measures can be implemented, which can improve animal welfare and comfort. As the digital poultry system groups had better environment and animal management than the CON groups, there were fewer lesions on the soles of the foot pads of the broiler chickens, and the other parameters (knee burn, plumage, gait) were also observed to be superior. The authors’ previous study on an ICT-converged digital poultry system improving egg production by maintaining good animal behavioral welfare in laying hens also supports these findings [
9,
14]. In their previous studies, the authors reported that animal behavioral welfare indicators, such as drinking, eating, locomotion (moving), grooming, and resting (lying down), appearance, feather conditions, body conditions, and the health of birds reared in an ICT-converged digital poultry system in the absence of probiotics were improved compared to those under the conventional livestock system [
6,
9,
34]; however, the results of research on animal behavioral welfare under the combination of a probiotics and a digital poultry system with converged ICT in broiler chickens are not well known. The improved animal behavioral welfare observed in this study may be attributed to the superior retention of biomarkers that maintain animal activity, including immune function and cecal microflora, through controlled animal feeding management and environmental stress factors via a remote system (
Table 4 and
Table 5) [
6,
9,
33,
34]. Factory-intensive conventional livestock systems increase animal stress due to various reasons including poor environmental conditions (hot and cold), health deterioration due to careless animal management, digestive disorders, low nutrient availability, and a decreased immune function [
6,
35], which threatens animal behavioral welfare and carbon neutrality. Factory-intensive livestock systems threaten carbon neutrality by increasing odor and methane generation due to poor feeding environments and livestock management systems. The digital livestock system including poultry, which uses ICT convergence with farm animals, can realize carbon neutrality in the livestock industry by establishing a low-carbon livestock management system. The digital livestock system can help realize carbon neutrality through the development of methane-reducing feed with the simultaneous establishment of a low-carbon livestock management system [
6,
9,
11].
An ICT-converged digital poultry system using AI, big data, cloud computing, IOT, ML, and multimodal sensor technologies can guarantee greater amounts of free animal rights by reducing stress, which is related to animal behavioral welfare [
1,
6,
7,
9,
10,
11]. It could reduce animal stress by using remote control and real-time monitoring of the behavioral welfare, care, and movements of broiler chickens. They can observe animal feeding, the barn environment (temperature, humidity, ventilation), and the health management of individuals by remote control and sensing technology through the use of the Internet and mobile phones [
14,
17,
27]. To meet the consumption demands of animal-based foods to solve the growing food procurement problems of humans, existing breeding programs and animal feeding practices focused on high livestock production and economic productivity have influenced not only the health and behavioral welfare of broiler chickens, but also other farm animals. These can lead to several stressors that affect animal wellbeing [
15,
16,
17]. Probiotics can inhibit colonization by harmful bacteria and help activate beneficial bacteria in the gut. In particular, balanced cecal microbiota in the digestive tracts of poultry through the use of probiotics can help improve animal behavioral welfare by maintaining microbial homeostasis [
3,
6,
36,
37]; as seen from
Table 6, the fact that the CON500, DPCS, and DPS500 groups had better animal behavioral welfare scores and body condition scores than the CON group supports this reason. Intensive animal feeding management practices for poultry may cause stress and adversely affect animal behavioral welfare, which are important problems related to economic losses in broiler farms, but the use of probiotics in poultry can improve livestock production by maintaining good animal behavioral welfare [
3,
38,
39,
40]. The main result of this study was that, in the conventional poultry system of raising chickens, the farmers must adhere to good production practices, which include providing the chickens with good ambient conditions, adequate stocking density (greater than 10 chickens per square meter), the availability of food and water, and sufficient living space, to meet the welfare conditions. The difference here compared to the digital poultry system is that, with the conventional poultry system, a person takes care of everything, while in the digital system, all work is handled almost automatically. Therefore, it can be considered that the control group was exposed to numerous stress-causing factors (environment, animal feeding management, animal movement, etc.), so that the production and immunological parameters were significantly worse than those of chickens raised under the digital poultry system.