Effect of Environmental Enrichment Within Cages on Production and Welfare in Laying HensABSTRACT
This study aims to compare the effects of conventional cage systems (CC) and environmentally enriched cage systems (EEC) (which include nest boxes, perches, and pecking stones) on the productivity and welfare of laying hens, also considering the responses of two genotypes - Hyline Brown (HB) and Isa Tinted (IT). A total of 280 hens were evaluated for production (egg production, cracked eggs, mortality), welfare (keel bone damage, feather score, health score, footpad dermatitis, body condition, beak and claw lengths), and stress (heterophile/lymphocyte ratio, tonic immobility). Hens in CC produced more eggs (p<0.01) but had a higher incidence of cracked eggs (p<0.001). Hens in CC exhibited more feather loss, comb and cloacal wounds, and footpad dermatitis (p<0.05), while EEC hens had more keel bone damage (p<0.01). HB hens had higher productivity (86.07% vs. 82.01%) and lower cracked egg rates (0.19% vs. 0.92%) compared to IT (p<0.01). IT hens had higher mortality and stress (p<0.001). Welfare indicators favored HB hens across all parameters, except footpad dermatitis (p<0.05). While EEC lowered egg production, the reduced cracked egg rate and better welfare outcomes, such as improved feather coverage and fewer injuries, suggest advantages. HB outperformed IT in productivity, stress tolerance, and welfare across both systems.
Keywords:
Egg production; laying hens; pecking stone; stress; welfare
INTRODUCTION
The welfare of laying hens has become a focal point in discussions on animal agriculture, driven by consumer demand for ethically produced food and a growing awareness of animal welfare issues (EFSA, 2023). A central aspect of these discussions is the housing systems used in laying hen production. Conventional cage systems, though efficient in terms of egg production and space utilization, are often criticized for restricting natural behaviors such as perching, dust bathing, and foraging (Majewski et al., 2024). In contrast, cage-free systems provide more space and resources, allowing hens to express these behaviors, potentially improving their welfare (EFSA 2023; Majewski et al., 2024). However, transitioning from conventional cages to cage-free systems presents significant challenges, including concerns about economic and environmental sustainability (Mench & Rodenburg, 2018). Cage systems are often favored for their lower energy use and carbon footprint, making them appealing to producers (Kheiralipour et al., 2024). This highlights the need for a balanced approach that considers both the economic and environmental benefits of cage systems and the welfare advantages of cage-free systems.
Conventional cage systems remain the predominant method for rearing laying hens globally (Weeks et al., 2016; Orihuela et al., 2019; Tainika & Şekeroğlu 2020). However, in recent years, enriched cage systems incorporating nesting areas and perches have emerged as an alternative, particularly in European countries (Tainika & Şekeroğlu 2020; Majewski et al., 2024). These systems partially meet hens’ natural behavioral needs (Orihuela et al., 2019), but still face issues with damaging behaviors such as feather pecking and cannibalism (Weeks et al., 2016; Van Staaveren et al., 2021). Feather pecking (FP) is a significant welfare concern, resulting in poor feather condition, skin damage, and even mortality, thereby posing a major challenge to the egg production industry (Nicol, 2019; Cronin & Glatz, 2020).
Pecking devices have been proposed as enrichment options to mitigate feather-pecking behavior in cage-reared birds (Campbell et al., 2019). Although various materials like hanging CDs, ropes, and toy balls are used (Campbell et al., 2019), there is limited published data on their effectiveness in commercial rearing farms (Zepp et al., 2018). Pecking stones in cage-free systems, however, have shown promise in directing pecking behavior and blunting beaks, potentially reducing the need for beak trimming (Iqbal et al., 2020). Their use in cage systems may prevent aggressive pecking behaviors that lead to injuries and feather pecking (Moroki & Tanaka, 2016). Thus, incorporating enrichments like pecking stones in cage systems may enhance welfare by facilitating natural behaviors.
While there is growing research on the welfare and productivity benefits of enriched cage systems, comprehensive studies comparing different genotypes in these systems are lacking. Genotype selection is crucial in laying hen breeding (Fernyhough et al., 2020; Rakonjac et al., 2021; Sharma et al., 2022), as different genotypes may respond differently to environmental conditions and management practices. Understanding genotype-specific responses to cage design can optimize housing environments, ensuring optimal welfare and productivity (Fernyhough et al., 2020; Özentürk & Yildiz 2021; Rakonjac et al., 2021; Sharma et al., 2022). Some genotypes may benefit more from additional space and enrichment features (Campbell et al., 2019; Ross et al., 2020), underscoring the importance of genotype-environment interactions in commercial egg production (Özentürk & Yildiz 2021; Sharma et al., 2022).
This study aims to comprehensively compare the effects of conventional cage systems with environmentally enriched cage systems-incorporating nest boxes, perches, and pecking stones-on the productivity and welfare of laying hens. The inclusion of pecking stones in enriched cage systems is a unique aspect of this study, designed to enhance natural pecking behavior, crucial for hen welfare. Various welfare and stress assessment methods, including feather scoring, keel bone damage assessment, footpad dermatitis evaluation, and stress level measurement were employed to evaluate the welfare implications of these housing systems. Additionally, this study focuses on two different laying hen genotypes, Hyline Brown and Isa Tinted, to understand how different genetic backgrounds might respond to these housing systems.
MATERIALS AND METHODS
Ethics Approval
The research was ethically approved by the Atatürk University Experimental Animals Local Ethics Committee (Protocol no: 35, dated 28.02.2022).
Animals and Housing
This study was conducted at the laying hen houses of the Poultry Unit of Atatürk University, Food and Livestock Research and Application Centre. A total of 280 laying hens, comprising equal numbers of brown layer Hyline Brown (HB) and white layer Isa Tinted (IT) hybrids hatched on the same day, were used. At 20 weeks of age, these hens were randomly assigned to cages, ensuring high uniformity based on live weight. The trial spanned from 24 weeks to 72 weeks of age.
The experimental design involved two different genotypes (IT and HB) and two cage arrangements: conventional cage (CC) and environmentally enriched cage (EEC). Each cage compartment measured 60 cm in depth, 62.5 cm in width, with a rear height of 46 cm and a front height of 51 cm. Each cage was equipped with a 62.5 cm feeder and two water nipple systems.
For the EEC, a nesting area enclosed on three sides (right, left, top) was created with a curtain tarpaulin within the existing cage. Additionally, wooden bars were placed transversely from the middle of the cage at a height of 10 cm for perch application. Each chicken was provided with a 15 cm long perch. Plastic boxes (10x6x6 cm) were mounted on the side wires of the cage at a height of 25 cm, containing pecking stones. These stones were commercially available mineral pecking stones containing Calcium, Magnesium, Sodium, other trace elements, oyster shell flour, carob flour shell, calcium carbonate, and other nutritional elements.
The experimental setup consisted of 56 cage compartments, 28 from each cage group (CC and EEC), with 14 cages housing IT hens and 14 cages housing HB hens in each group. Each cage housed 5 hens, providing a settlement area of 750 cm² per hen (Table 1).
The poultry house was ventilated through windows on the side walls, ventilation chimneys on the ceiling, and a 140 cm x 140 cm fan operating under negative pressure. The temperature was maintained between 16-24°C using sensors connected to the ventilation and heating systems. Lighting was provided by fluorescent lamps emitting white light, set to be bright for 16 hours a day. During the productive period, the hens were fed ad libitum with granule form feed: 1st Term egg feed at 21-45 weeks (2750 ME, 16.26% HP), 2nd Term egg feed at 46-60 weeks (2720 ME, 15.83% HP), and 3rd Term egg feed at 61-72 weeks (2720 ME, 15.65% CP).
Determination of Production Performances
Egg production (EP) and cracked egg (CE) data were recorded daily for each cage and calculated weekly. Mortality was also recorded daily, and mortality rates were calculated for each group. If a hen died, it was replaced by a similar hen from a reserve flock to maintain density uniformity within the cages (Özentürk & Yildiz 2021).
Determination of Welfare Parameters
Welfare parameters, including keel bone damage, feather score, health score, bumblefoot syndrome, body condition, and beak and nail lengths were evaluated in two randomly selected hens from each cage (112 hens in total) at 36, 54, and 72 weeks of age. All scoring was performed visually by the same person to ensure consistency.
Keel Bone Damage: Hens were positioned supine, and any curvature, deviation, or thickening of the keel bone was scored (Table 2) (Grafl et al., 2017; Petek & Çavuşoğlu 2021).
Description of the scoring scheme used for the assessment of keel bone damage and integument condition.
Feather Score: Feather scoring considered feather configuration in six body parts (neck, chest, back, wing, tail, and cloaca), both separately and as a total score. Scoring ranged from 0 to 3 (Table 3), with regional scores of 2 and above indicating significant feather damage (Tauson et al., 2005; Giersberg et al., 2017; Özentürk et al., 2023).
Health Score and Bumblefoot Syndrome: Body injuries, including those on the comb and cloaca, and the presence of bumblefoot were scored on a scale from 0 to 2, with a score of 2 indicating significant damage (Tauson et al., 2005; Grafl et al., 2017; Özentürk et al., 2023).
Body Condition: Evaluated by assessing the chest muscle width and spine bone protrusion, scored from 0 to 2, with a score of 0 indicating a good condition (Grafl et al., 2017).
Beak and Nail Lengths: Beak length was measured from the outer end of the nostril to the tip of the beak, while claw length was determined by measuring the four toes on both feet, with the average of eight measurements used to determine the average claw length (Dikmen et al., 2016; Iqbal et al., 2020).
Determination of Stress Level
Stress levels were evaluated using the heterophile/lymphocyte ratio (H/L) and tonic immobility (TI) parameters. These were examined in a total of 56 hens, with one hen selected from each cage, at the end of the experiment at 72 weeks of age.
Heterophile/Lymphocyte Ratio (H/L): The H/L ratio is commonly used as an indicator of stress in animals, with higher values typically reflecting greater physiological stress (Özentürk & Yildiz 2021). In this study, blood samples were taken from the vena cutanea ulnaris of a randomly selected hen from each cage. Smears were prepared, dried, and stained using the May-Grunwald-Giemsa method (Gross and Siegel 1983). The H/L ratio was calculated by counting 100 white blood cells under a light microscope at x100 magnification (Özentürk & Yildiz 2021).
Tonic Immobility (TI): Tonic immobility is a natural, reflexive state of immobility that occurs in many animal species and is often used to measure fear or stress. The duration of TI can offer insights into an animal’s stress response, with longer durations typically indicating higher levels of fear or stress. TI was tested by placing each hen in a supine position on a table and holding it in place for 10 seconds. If the hen remained motionless for at least 10 seconds, TI was considered induced, and the total duration was recorded up to a maximum of 600 seconds. If the hen moved within 10 seconds, the procedure was repeated up to four times (Konkol et al. 2020).
Statistical analysis
Data were analyzed using IBM® SPSS version 20. A General Linear Model (GLM) was used to analyze egg production across different age periods. The Chi-square test (X2) was employed to analyze mortality rates. Mann-Whitney U tests were used for pairwise comparisons of genotype and cage groups for feather scores, injuries, spinal bone damage, and body condition parameters. A 4-way comparison was performed using the Kruskal-Wallis test for interactions. The Shapiro-Wilk test was used to determine the normality of the data distribution. The effects of breed and cage group on the heterophile-lymphocyte ratio were analyzed using the GLM, and multiple comparisons were made using Duncan’s multiple comparison test.
RESULTS
The results of egg production and cracked egg rates are summarized in Table 4. Over the 24-72 week period, the brown layer HB hybrid had significantly higher egg productivity (86.07%) compared to the white layer IT hybrid (82.01%) (p<0.01). The cracked egg rate was also lower in the HB genotype (0.19%) versus the IT hybrid (0.92%) (p<0.01). Cage systems significantly affected egg production (p<0.01), with higher production in conventional cages, while a lower incidence of cracked eggs was noted in environmentally enriched cages (p<0.001). Weekly egg yield varied over time (p<0.001), increasing initially and then decreasing after approximately 36 weeks (Fig. 1).
Weekly egg production across different genotype × cage design combinations, highlighting interactions between genotype and cage design on egg production rates.
Table 5 shows mortality rates, with significantly higher mortality observed in the IT hybrid (p<0.001). No significant differences in mortality were found between cage systems (p>0.05). However, the interaction between cage design and genotype was significant (p<0.001), with the highest mortality rate found in the IT hybrid in conventional cages.
Feather and health scores, summarized in Table 6, showed significant differences between genotypes (p<0.05) in all parameters, except footpad dermatitis. The IT hybrid had lower welfare, indicated by longer beak and claw lengths. Hens in conventional cages experienced more feather loss, comb and cloacal wounds, footpad dermatitis, and longer beaks (p<0.05), while keel bone damage was more prevalent in environmentally enriched cages (p<0.01). Welfare parameters deteriorated over time, with the lowest scores observed at 72 weeks (p<0.01). Table 7 and Figures 2 and 3 detail feather and health scores across genotype x cage design groups, revealing significant differences in all parameters, except footpad dermatitis (p<0.01). In terms of total feather score, the least feather loss was observed in the HB hybrid grown under EEC conditions, and the highest feather loss was observed in the IT hybrid grown under CC conditions. Similarly, the most comb and cloaca injuries were observed in the IT hybrid grown in CC (p<0.01). Keel bone damage was mostly observed in hens raised under EEC conditions (p<0.01).
Feather scores in genotype × cage design groups, emphasizing genotype-environment interactions on feather condition under different cage systems.
Health scores in genotype × cage design groups, illustrating the impact of genotype and cage design on overall health, including keel bone damage and integument condition.
Table 8 presents H/L ratio and tonic immobility data at 72 weeks, indicating higher stress levels in the IT hybrid (p<0.01) with no significant differences between cage systems (p>0.05).
DISCUSSION
Contrary to the general assumption that enriched environments enhance production parameters, our study found that hens in conventional cages (CC) produced more eggs than those in environmentally enriched cages (EEC). This result aligns with studies by Tactacan et al., (2009) and Stojčić et al. (2012), but contrasts with findings where similar or higher egg production was reported in enriched systems (Dikmen et al., 2016; Onbaşılar et al., 2020). The variability in these results may be due to differences in breed and enrichment design. The reduced egg production in EEC in our study could be due to lower illumination in the nesting areas, as plastic curtains might have affected light stimulation, which is crucial for egg-laying cycles (England & Ruhnke, 2020). Additionally, increased activity and resource competition in enriched systems may lead to higher energy expenditure, impacting egg production. The HB hybrid outperformed the IT hybrid in egg production, likely due to genetic differences (Ketta et al., 2020). This is consistent with Kaba & Bozkurt, (2023), who found that brown layers have higher egg production and fewer broken eggs than white layers. However, other studies have not observed significant differences between hybrids (Onbaşılar et al., 2015; Özentürk & Yildiz, 2021), possibly due to variations in genetics, physiology, and behavior (Nelson et al., 2020). As expected, hen-day egg production changed throughout the laying period, consistent with previous research (Tactacan et al., 2009; Dikmen et al., 2016; Özentürk & Yildiz, 2021).
Our study also found a lower rate of cracked eggs in EEC, which contrasts with some studies reporting higher or similar rates in enriched systems (Onbaşılar et al., 2015; Dikmen et al., 2016; Onbaşılar et al., 2020). The lower cracked egg rate in EEC could be due to reduced risk of eggs being crushed by other hens, as hens prefer laying in closed nesting areas (Onbaşılar et al., 2015; Engel et al., 2019). This finding highlights a key advantage of EEC systems, where practical features such as nesting areas can reduce egg damage and enhance overall product quality, potentially minimizing economic losses for producers. While lower egg production in EEC systems may impact farm profitability and discourage adoption, the reduced rate of cracked eggs and improved welfare indicators could offset these productivity losses by enhancing egg quality and marketability. Scaling up enriched systems will require a cost-benefit analysis of infrastructure investments and long-term productivity outcomes, which should be addressed in future research. The IT hens had a higher rate of cracked eggs, consistent with other studies that found higher rates in white layer hybrids like Lohmann White (Onbaşılar et al., 2015).
High mortality rates negatively impact egg production sustainability. Extending hen lifespan can reduce resource demands and enhance sustainability (Fernyhough et al., 2020). Our study found no significant difference in mortality between CC and EEC, consistent with Tactacan et al. (2009), but contrary to studies showing a significant effect of rearing systems on mortality (Sherwin et al., 2010; Weeks et al., 2016). Mortality rates are influenced by various factors, including management practices and conditions during both rearing and laying periods. The higher mortality observed in the IT hybrid is linked to lower welfare and higher stress, indicated by greater feather loss and body wounds (Özentürk & Yildiz, 2021). Factors such as smaller body size, susceptibility to cloacal prolapse, and more aggressive behavior in the IT hybrid may contribute to increased mortality (Kozak et al., 2019; Özentürk & Yildiz, 2021). Additionally, the visibility of bleeding due to white feathers may increase aggressive pecking, further elevating mortality rates (Özentürk & Yildiz, 2021). Research indicates that flocks with longer beaks tend to experience higher cumulative mortality compared to those with trimmed beaks (Weeks et al., 2016). In our study, the lower mortality rate observed in the HB hybrid may be linked to their shorter beaks, which likely helped reduce injurious pecking incidents.
Environmental enrichment, which modifies the environment to support animals’ biological and psychological welfare, is a strategy to reduce FP (Zepp et al., 2018; Ross et al., 2020; Van Staaveren et al., 2021). Our findings indicate that hens raised in environmentally enriched cages (EEC) exhibited better feather condition, particularly in the neck and tail regions, suggesting a positive effect of enrichment. This aligns with previous studies that found improved feather condition in enriched systems (Onbaşılar et al., 2015; Blatchford et al., 2016; Onbaşılar et al., 2020). Feather loss, often resulting from feather pecking behavior (Nicol et al., 2013; Giersberg et al., 2017; Nicol, 2019; Cronin & Glatz, 2020; Sözcü et al., 2021; Baker et al., 2022), can be reduced by providing a nesting site in EEC, which offers hens a closed area and potentially reduces feather pecking. However, some studies reported more feather loss in EC (Dikmen et al., 2016) or similar feather loss in both cage systems (Tactacan et al., 2009; Sherwin et al., 2010). Unique to our study was the inclusion of pecking stones, which have been shown to reduce FP by encouraging foraging behavior and abrading the beak (Moroki & Tanaka, 2016; Zepp et al., 2018; Campbell et al., 2019; Iqbal et al., 2020; Sandilands et al., 2022). The shorter beak lengths observed in EEC support the abrasive effect of pecking stones. Pecking stones may also occupy hens’ time, potentially reducing stress and aggressive behavior (Liebers et al., 2019; Iqbal et al., 2020; Schreiter et al., 2020). This finding suggests that pecking stones are a cost-effective enhancement to enriched systems, improving welfare while potentially lowering veterinary expenses related to feather pecking injuries. By reducing feather pecking and encouraging natural foraging behavior, as demonstrated by shorter beak lengths observed in our study, pecking stones prove to be a valuable enrichment tool. Incorporating pecking stones in environmentally enriched cages (EEC) can provide practical benefits for producers, offering a welfare improvement without significantly increasing production costs.
Our study also found that the HB exhibited better feather and health scores compared to the IT, which had more feather loss and injuries. These differences may be related to genetic factors and feather pigmentation, as white-feathered birds like IT are generally more reactive (Kozak et al., 2019, 2016; Özentürk & Yildiz 2021; Özentürk et al., 2023). Genes determining feather pigmentation may influence pecking behavior (Bright, 2007; Nicol et al., 2013). Injuries may be more noticeable on white feathers, triggering more pecking (Özentürk & Yildiz 2021; Özentürk et al., 2023). Feather loss was most pronounced in the tail and cloaca regions, consistent with other studies (Bright, 2007; Giersberg et al., 2017; Saraiva et al., 2020). Integument scores showed that feather loss and injuries increased with age, peaking at 72 weeks, a trend supported by literature indicating that feather condition deteriorates over the laying period (Van Staaveren et al., 2021; Özentürk et al., 2023).
Our study found fewer comb and cloacal wounds in hens raised in EEC. Similar results were reported by Blatchford et al., (2016), who observed more comb wounds in CC compared to enriched cages (EC). However, other studies have reported mixed findings, with some showing no significant difference in skin and vent damage between CC and EC (Sherwin et al., 2010), or even more body wounds in EC (Dikmen et al., 2016). The presence of perches in enriched cages has been associated with increased cloacal injuries due to greater visibility and pecking risk (Lay Jr et al., 2011), particularly during laying periods. Most hens have a strong motivation to lay eggs in the nesting area of enriched cages (Engel et al., 2019; Bécot et al., 2023). The use of a closed nesting area in EEC may reduce these injuries by allowing hens to escape aggressive pecking (Lay Jr et al., 2011; Alm et al., 2016). Additionally, the pecking stones used in our study may have redirected pecking behavior, reducing aggression and wearing down the hens’ beaks, as evidenced by the shorter beak lengths observed in EEC-raised hens. This finding is supported by previous studies indicating that pecking stones can decrease skin lesions and injuries (Liebers et al., 2019; Schreiter et al., 2020). Regarding hybrid differences, our study found more severe cloacal and comb injuries in the IT compared to the HB. The smaller body size and cloacal structure of the IT hybrid (Onbaşılar et al., 2015; Özentürk & Yildiz, 2021) may contribute to higher prolapse incidence, especially in hens with high egg weights (Özentürk & Yildiz, 2020). Genetic differences between white and brown hybrids, including their activity levels and aggression, likely contribute to the observed variations in injury rates and health scores (Rozempolska-Rucińska et al., 2020; Özentürk et al., 2023).
Keel bone damage (KBD) is a significant welfare issue in laying hens, causing severe pain and negatively impacting welfare (Harlander-Matauschek et al., 2015; Arpášová et al., 2023). In this study, KBD was greater in EEC, likely due to pressure during perching, which can cause keel bone curvature or deviation (Hester, 2014; Malchow et al., 2022). Hester et al., (2013) found higher keel bone deviations in cages with perches. While perches can increase bone strength (Lay Jr et al., 2011) and reduce bone fractures (Hartcher & Jones, 2017), prolonged pressure while perching and potential crashes increase the risk of KBD (Lay Jr et al., 2011; Harlander-Matauschek et al., 2015; Hartcher & Jones, 2017). Blatchford et al., (2016) observed more keel abnormalities in hens at 72 weeks in EEC compared to CC, though some studies found no significant difference in keel fractures between the two systems (Sherwin et al., 2010; Onbaşılar et al., 2020). To reduce keel bone damage (KBD), future research should focus on alternative perch designs, such as using softer materials or flexible structures that distribute pressure more evenly across the keel bone. Adjustable perch heights could also help mitigate this issue. Additionally, training programs for producers should highlight optimal perch placement and spacing to minimize collisions and injuries. Tackling this issue is essential for encouraging the adoption of enriched housing systems while minimizing potential welfare trade-offs. Considering genotype-specific housing adjustments is another important strategy to reduce KBD. Our study also found higher KBD in the IT, consistent with studies indicating genotype differences in KBD (Habig et al., 2021; Sözcü et al., 2021). Perching behavior, influenced by genotype, can exacerbate KBD (Bist et al., 2023). Feather pecking is positively correlated with KBD, as it can lead to escape behaviors that increase collision risk (Nicol, 2019; Cronin & Glatz, 2020; Baker et al., 2022). The IT hybrid exhibited more feather loss and injuries, likely contributing to higher KBD due to increased escape behaviors. The age of the hens is also critical, as bone weakening from calcium mobilization for egg production increases fracture susceptibility (Rufener & Makagon, 2020). KBD damage was significantly greater at 56 and 72 weeks than at 36 weeks in our study, aligning with findings showing that the incidence of keel bone fractures increases during the ovulation period and stabilizes after 49 weeks (Toscano et al., 2018).
Hens raised in EEC exhibited less footpad dermatitis compared to those in CC, consistent with Blatchford et al., (2016), who reported fewer foot lesions in EC. Foot lesions often result from increased compressive loads on perches and wire floors (Weitzenbürger et al., 2006). Barnett et al., (2009) found that perches can improve foot health by reducing time spent on wire flooring (Barnett et al., 2009), and perching behavior supports musculoskeletal health, reducing footpad dermatitis (Bist et al., 2023). However, some studies have reported worse or similar foot lesions in EC compared to CC (Sherwin et al., 2010; Dikmen et al., 2016; Onbaşılar et al., 2020), suggesting that perch material, shape, and height may affect foot health. No significant difference in footpad dermatitis was found between hybrids in this study, although Sözcü et al., (2021) reported differences in foot lesions between hybrids in a cage-free system. This discrepancy may be due to genotype x rearing system interactions, as foot sole problems are more common in free-range systems (Heerkens et al., 2016).
Excessive claw length can be an issue for hens without access to nail trimming materials (Hester, 2014; Blatchford et al., 2016). In this study, both cage types had nail trimming materials, resulting in no significant difference in claw length between groups, consistent with Onbaşılar et al., (2020). However, some studies have reported longer claws in CC due to the absence of nail trimming equipment (Onbaşılar et al., 2015; Blatchford et al., 2016; Dikmen et al., 2016). The white layer IT hybrid had longer claw and beak lengths than the brown layer HB, aligning with literature findings (Onbaşılar et al., 2015). Differences in beak length may be attributed to variations in beak trimming time and methods during the chick period, while claw length variations between hybrids may be due to genetic differences in claw growth, compound hardness, or different use patterns of nail shortening equipment. Claw lengths also increased with age in all systems, as noted by Blatchford et al., (2016).
Leukocyte components, particularly the H/L ratio, are key indicators of chronic stress in poultry (Lentfer et al., 2015). Tonic Immobility (TI), a measure of fear in chickens, reflects welfare status in different housing conditions (Lentfer et al., 2015). Our study found no significant differences in TI and H/L ratios between the cage systems, aligning with Tactacan et al., (2009), who also reported similar stress levels in CC and EC systems (Tactacan et al., 2009). While perches, nesting areas, and pecking stones in EECs may reduce stress by fulfilling natural behaviors (Nicol 2015; Engel et al., 2019; Iqbal et al., 2020; Ross et al., 2020; Meuser et al., 2021; Bécot et al., 2023) , they can also introduce stress factors, such as bone damage from perches (Malchow et al., 2022; Bist et al., 2023).
In our findings, stress indicators like feather loss, comb injuries, and footpad dermatitis were more common in CC hens, while keel bone damage was higher in EEC hens. This suggests that different stress factors in each system might balance overall stress levels. Additionally, long-term adaptation to the cage environment might explain the lack of significant differences in stress.
The white layer IT hybrid exhibited higher stress levels compared to the brown layer HB, as indicated by TI and H/L ratio measurements. According to Clark et al., (2009), a heterophil percentage of 26% and a lymphocyte percentage of 66% are typical in chicken blood, while Gross and Siegel (1983) suggested that H/L ratios of 0.2, 0.5, and 0.8 correspond to mild, moderate, and severe stress, respectively. Based on these benchmarks, both hybrids in our study were exposed to mild to moderate stress. Other studies have also reported genotype-based differences in stress levels as measured by the H/L ratio (Peixoto et al., 2020; Özentürk & Yildiz 2021).
Fear, as a welfare indicator, shows behavioral and physiological variation across genotypes (Saraiva et al., 2020; Meuser et al., 2021), with specific differences in TI responses noted among breeds (Sözcü et al., 2021; Tiemann et al., 2023). These differences can be attributed to factors such as weight, behavioral needs, and environmental adaptability (Rozempolska-Rucińska et al., 2020; Özentürk & Yildiz 2021; Tiemann et al., 2023). Genetic selection and physiological, biochemical, and cellular changes also play a role in fear responses (Nelson et al., 2020; Meuser et al., 2021; Tiemann et al., 2023). For instance, quantitative trait loci linked to fear have been identified in white leghorns (Peixoto et al., 2020). Moreover, genotypic differences in homeostasis and adaptability suggest varying stress tolerance and sensitivity (Kozak et al., 2016). Our findings indicate that IT hybrids experienced higher stress, as evidenced by increased feather loss and body injuries, likely due to a heightened stress response in this genotype.
CONCLUSION
In conclusion, our study provides valuable insights into the effects of cage design and genotype on the welfare, stress, and productivity of laying hens. Comparing two cage systems and different hybrids, we offer important guidance on optimizing hen welfare and productivity. Although egg production was lower in EEC, the reduced rate of cracked eggs presents a market advantage. Welfare indicators showed that hens in EEC, enriched with perches, nesting areas, and pecking stones, had better feather coverage and fewer injuries, demonstrating the benefits of enriched environments in allowing natural behaviors that enhance welfare. The inclusion of pecking stones was particularly beneficial because they attracted foraging behavior and increased beak wear, which was associated with reduced feather pecking, resulting in less feather loss and fewer injuries. It has been determined that using pecking stones for enrichment purposes would be advantageous, and we recommend further research on their use in future studies. However, the higher rate of keel bone damage (KBD) in EEC suggests a need for caution, likely due to perch collisions. Stress levels showed no significant differences between rearing systems, indicating the need for further study on the impact of enrichment tools on stress. Based on our findings, we recommend producers to incorporate pecking stones as a practical solution for enhancing hen welfare, alongside careful management of perch design to minimize potential risks for KBD. Our findings contribute valuable empirical data on the effects of enriched environments on productivity and welfare, offering insights for improving poultry housing practices. Breed selection also significantly influenced outcomes, with HB showing higher egg production, lower cracked egg rates, and better welfare indicators than IT in both systems. HB’s greater stress tolerance and overall welfare make it a preferred choice. The laying period was shown to be crucial, as feather loss, KBD, and injuries increased over time, emphasizing the need for ongoing evaluation of welfare throughout the laying cycle. We suggest that producers pay attention to the effects of long-term housing conditions on welfare parameters and adjust their practices accordingly, ensuring optimal care and productivity across the hens’ lifespan.
ACKNOWLEDGEMENTS
We thank Atatürk University Scientific Research Projects Coordination Unit for providing a project grant to fund this study (TSA-2022-10594). We also thank Atatürk University Food and Livestock Application and Research Center for providing animal material and experimental area.
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FUNDING
This work was supported by Atatürk University Scientific Research Projects Coordination Unit. (Grant numbers [TSA-2022-10594]).
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DATA AVAILABILITY STATEMENT
The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.
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DISCLAIMER/PUBLISHER’S NOTE
The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.
The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.
