How does the presence of excreta affect the behavior of laying hens on scratch pads?

How does the presence of excreta affect the behavior of laying hens on scratch pads? Abstract Enriched cages for laying hens provide scratch pads for foraging on the wire mesh floors. Apart from foraging on scratch pads, hens also defecate on these pads, causing them to become soiled with excreta. This study was conducted to determine the relative preference of laying hens for foraging on clean (C) scratch pads or scratch pads soiled with excreta (E), and to study the behaviors performed by hens on such pads. A total of 288 laying hens was housed in 16 enriched cages (18 hens/cage), each divided into 2 compartments. On a daily basis, half of the scratch pads (one in each compartment) were removed and cleaned, while the other half were cleaned and then covered with 550 g (0.35 g/cm2) of conspecific excreta. The C and E scratch pads were then put back into the cages in a systematic order to avoid side bias. Feed was delivered automatically onto the scratch pads as a litter substrate. The frequency of visits and the total time spent performing different behaviors on C and E pads were video-recorded [the time of video recording was relative to litter (feed) delivery on the scratch pads] for a total of 10 min/d, 3 times/wk, over a period of 4 weeks. Overall, the allocation of the time budget for different behaviors was found to be—in order of greatest to least amount of time—resting, locomotor behaviors (walking and running), foraging, and dust bathing. Laying hens showed a relative preference for E scratch pads by visiting them more frequently (P = 0.001), and spent more time (P = 0.035) foraging on them, whereas they rested for more time (P < 0.001) on C scratch pads. The relative preference for E scratch pads during foraging signifies the innate importance of foraging substrates in enriched cages for laying hens. Similarly, the longer use of C scratch pads for resting indicates the need for an ideal and clean resting surface in enriched cages. INTRODUCTION Enriched cages have been designed to overcome the limitations of conventional cages to support behaviors that laying hens are highly motivated to perform (Weeks and Nicol, 2006). These cages provide a varying amount of horizontal space for locomotion and other behaviors such as nesting, perching, foraging, and dust bathing (Appleby et al., 2002; Lay et al., 2011). In enriched cages, foraging and dust bathing are typically performed on scratch pads, which are sections of synthetic turf of various designs and other artificial materials. These cages also are equipped with a mechanism that delivers a small amount of litter material, such as feed, onto these scratch pads, upon which hens can scratch, forage, and dust bathe (Scholz et al., 2011). However, not all farmers provide feed as a foraging and dust bathing substrate regularly, or otherwise provide it in small amounts, as feed represents the major cost of production for farmers (Lee et al., 2016). The result is that no litter substrate is delivered onto the scratch pads, and so little motivation is offered for hens to scratch, forage, and dust bathe upon them. Furthermore, defecation onto, and accumulation of, excreta on the scratch pads causes them to become soiled and unhygienic. Poor scratch pad hygiene can become an increasing health threat and is, therefore, a welfare concern. Excreta on the scratch pads may be a vector for fungi, viruses, bacteria, and toxins (Himathongkham and Riemann, 1999; Zarrin et al., 2010; Imran and Ali, 2014), in addition to contributing to poor air quality, with high levels of dust and ammonia (Turnbull and Snoeyenbos, 1973; Weaver and Meijerhof, 1991). Collectively, these downstream consequences of poor hygiene can lead to decreased feather cleanliness, and give rise to health issues such as ulcerative footpad dermatitis (i.e., bumblefoot) (EFSA, 2005). Furthermore, poor hygiene in enriched cages can be a food safety concern, as unclean conditions promote egg dirtiness and bacterial contamination of eggshells, which translate to an economic loss for farmers (Guinebretière et al., 2012). For these reasons, in addition to expensive cleaning techniques, farmers often choose to remove scratch pads from their cages, or are reluctant to use them at all, which could jeopardize the welfare of laying hens housed in enriched cages. While there are considerable disadvantages for hens and farmers when it comes to soiled scratch pads, there may be some hidden benefits associated with excreta contact as well. Despite the evidence that dirty scratch pads in enriched cages are a hygienic challenge, some studies have reported that certain wild bird species benefit nutritionally from foraging on and consuming excreta. McGowan (1995) observed that parent birds of many passerine species consume the excreta of their neonatal offspring shortly after hatching, due to the excreta's high nutritional value. In addition, other bird species also have been found to ingest the excreta of other animals, mainly for its nutritional benefits. Ungulate excreta, for example, contain high levels of intact carotenoids, which are essential for vertebrates and have pigmentary, as well as antioxidant and immunostimulant, functions (Negro et al., 2002). As a result, the Egyptian vulture, Neophron percnopterus, is commonly seen foraging on and consuming cow, goat, and sheep excreta (Negro et al., 2002). Apart from micronutrients, food (i.e., prey) items likely to be found in excreta may be another reason that animals forage on animal dung: hooded crows (Corvus corone) preferentially forage on fresh horse excreta, as it is a reliable source of dung beetles (Horgan and Berrow, 2004). For laying hens, however, the nutritional benefits of foraging on or consuming excreta, if any, are unknown. In nature, wild red junglefowl (Gallus gallus) spend more than 60% of their time foraging in natural litter (Dawkins, 1989). In commercial housing systems, domestic hens continue to demonstrate this high motivation to forage, even when they are provided feed ad libitum, which can be accessed at no cost (Bubier, 1996). In litter-based housing systems, laying hens scratch, peck, and dust bathe in the litter substrate (Merril and Nicol, 2005), which is often unchanged over the entire duration of a laying period, leading to the accumulation of a considerable amount of excreta. In the case of laying hens housed in enriched cages, excreta and litter material (if provided) on the scratch pads may be the only foraging substrates available in the midst of a wire grid floor. It is clear that the excreta-soiled scratch pads in enriched cages are undesirable from a hygienic point of view, and solutions to improve the health and welfare of laying hens kept in these housing systems should be addressed. However, there is a knowledge gap regarding how laying hens respond to excreta in the short and long terms. As a first step to bridging this gap, this study was conducted with the objectives of examining how feed (litter substrate) on clean (C) compared to excreta-soiled (E) pads could influence hens’ choice regarding where to forage, and once on the scratch pads, how hens allocate their time towards performing different behaviors on each type of scratch pad. As hens instantly started to defecate on the C pads, we considered their preferences for C or E pads one h after they were put into the cages, in order to keep the choices distinguishable. MATERIALS AND METHODS Ethical Statement The research protocol was approved by the University of Guelph Animal Care Committee (Animal User Protocol Number 3169) prior to the start of data collection. Animals and Husbandry A total of 288 laying hens of 4 breeds (White Leghorn, Rhode Island Red, Columbian Rock, and Barred Rock) was obtained from the University of Guelph Arkell Research Station at 25 wk of age. Hens were housed in enriched cages manufactured by FDI Cage Systems of Mitchell, Ontario (369 cm × 65 cm; 18 hens/cage, 4 breeds/cage, 16 cages total). Each enriched cage (Figure 1) was partitioned into 2 identical compartments for the purpose of the experiment, and each individual compartment was equipped with a curtained nest area (107 cm2/hen; red curtains), perches running lengthwise (13.7 cm/hen), a scratch pad (details described below), automatic feeders on the outside of the cage (10 cm/hen), and nipple drinkers (1.5 hens/nipple). Feed and water were provided ad libitum. The light period was 14L: 10D. Figure 1. View largeDownload slide Schematic layout of an enriched cage for 18 laying hens featuring 2 identical compartments freely accessible through a pop hole (not to scale). Figure 1. View largeDownload slide Schematic layout of an enriched cage for 18 laying hens featuring 2 identical compartments freely accessible through a pop hole (not to scale). Experimental Design Two identical compartments in each cage were joined by a pop hole to allow hens to move freely between compartments. A white plastic sheet (visual barrier) was added between the width and length of the 2 compartments, aside from the pop hole, to prevent the transfer of visual information between the cages and treatments. Each compartment contained one scratch pad (31 × 51 cm; 88 cm2/hen); together, the 2 scratch pads per cage occupied approximately 28% of the total surface area of the cage floor. The square scratch pads consisted of brown, synthetic Astroturf, which resembled natural grass in both appearance and texture. On a daily basis one h (10:00 h) before starting video recording, half of the scratch pads were removed and cleaned, while the other half were cleaned and then covered with 550 g (0.35 g/cm2) of fresh conspecific excreta, which was determined to be the average amount of excreta produced in a d by 18 laying hens. One C and one E pads were then put back into each cage in such a way that allocation of treatments across sides (right or left) was evenly spread. Feed (approximately 6 g/delivery) was delivered automatically for one min onto both scratch pads by a spiral conveyor pipe (feed auger) every 2 hours. A pilot study identified that hens were most active on the scratch pads at 11:00 h, 6 h after the lights were turned on. The video was recorded (including the time when feed was delivered) and analyzed for 10 min at 11:00 h, as soon as the feed was delivered from the auger onto the C and E pads, 3 times/wk, over a period of 4 wk (resulting in a total of 64 h of analyzed video recordings). As hens started to defecate on the clean scratch pads, all of our 10-minute observation periods took place one h after exposure of hens to the treatments. Also, due to the discrepancy of a few s created by feed delivery from one cage to the other, the time to start behavioral recording for each cage was carefully accounted for while analyzing the videos. Lastly, the laying hens were habituated to the experimental setup (scratch pads and handling) over a period of 10 d before the video recordings began. Behavioral Measures Continuous video recording of laying hen behavior on the scratch pads was conducted at normal speed (25 frames/s) using video cameras (Samsung SNO-5084R, Samsung Techwin Co., Gyeonggido, Korea) placed over each cage. The number of visits to C and E scratch pads (per min, 10 min total), the duration of the visits, and the durations of the behaviors referred to in Table 1 were analyzed using INTERACT® software (Mangold International GmbH, Graf-von-Deym Str. 594,424 Arnstorg, Germany). Table 1. List of mutually exclusive behaviors that occurred on scratch pads. Behaviors  Description  Foraging  Scraping or pecking scratch pads with feet or beak, respectively  Dust bathing  Performing dust bathing elements such as bill raking, wing shaking, scratching, lying on the side, and head rubbing, as described by Kruijit (1964)  Resting  Sitting on the scratch pads, without any other activity  Locomotor  Walking or running on the scratch pads  Behaviors  Description  Foraging  Scraping or pecking scratch pads with feet or beak, respectively  Dust bathing  Performing dust bathing elements such as bill raking, wing shaking, scratching, lying on the side, and head rubbing, as described by Kruijit (1964)  Resting  Sitting on the scratch pads, without any other activity  Locomotor  Walking or running on the scratch pads  View Large Statistical Analysis The model was fitted using PROC GLIMMIX of the SAS System (v9.4, SAS Institute Inc., Cary, NC, 2016). The data analysis was based on the mixed modeling approach for randomized experiments with repeated measures (Piepho et al., 2004). To analyze the number of visits, foraging duration, dust bathing duration, resting duration, and locomotor behavior duration, a generalized linear mixed model was employed with the fixed effect of scratch pad treatment (C and E), breed (White Leghorn, Rhode Island Red, Columbian Rock, and Barred Rock) and treatment × breed interaction. The average bird weight per cage was used as a covariate, and cage was used as a random effect. The number of visits was fitted with a Poisson distribution, whereas all other variables were logarithmically transformed prior to analyses to achieve normality. Due to the repeated measures taken on the same group of birds (cage) at different time points (d), an autoregressive covariance structure of order 1 was fitted to the cage-by-day effect. The degrees of freedom were adjusted using the Kenward–Roger method. All results are presented as least square means ± standard error (SE). Statistical significance was considered at P < 0.05 in all cases. RESULTS The times allocated to various behaviors on both the C and E pads within the 12, 10-minute observation periods are presented as percentages in Table 2. In general, the most common behaviors laying hens performed on both the C and E scratch pads were resting, followed by locomotor behaviors and foraging. Dust bathing occurred to a lesser degree. No eggs were laid on the scratch pads during the experimental period. Hens visited the E pads more (P = 0.001; F1,376 = 18.03) frequently than the C pads (3.6 ± 0.13 vs. 3.2 ± 0.13 visits/min). Hens spent a longer time (P < 0.001; F1,374 = 200.82) resting on C pads compared to the E pads (Figure 2C). No significant differences were observed with respect to dust bathing behavior (Figure 2B) or locomotor behaviors (Figure 2D) between the C and E scratch pads. However, hens were found to forage for a longer time (P = 0.035; F1,155.5 = 4.74) on the E pads compared to the C pads (Figure 2A). Interestingly, while foraging on the E scratch pads, some of the hens were observed consuming excreta. There was no significant effect of breed, breed by treatment interaction, or average body weight on any of the behavioral responses. Figure 2. View largeDownload slide Mean duration of foraging (A), dust bathing (B), resting (C), and locomotor (D) behaviors of laying hens on clean and excreta-soiled scratch pads out of 10-minute observation period. Values represent least square means ± standard error. Different letters (a and b) represent treatments that differed significantly (P < 0.05). Figure 2. View largeDownload slide Mean duration of foraging (A), dust bathing (B), resting (C), and locomotor (D) behaviors of laying hens on clean and excreta-soiled scratch pads out of 10-minute observation period. Values represent least square means ± standard error. Different letters (a and b) represent treatments that differed significantly (P < 0.05). Table 2. Percentage of time spent performing different behaviors by laying hens on clean (C) and excreta-soiled (E) scratch pads during 10-minute recording sessions over a 3-week period.   Treatments  Behaviors  C  E  Foraging  21.5  25.0  Resting  46.7  43.0  Dust bathing  4.4  3.5  Locomotor behaviors  28.3  27.6    Treatments  Behaviors  C  E  Foraging  21.5  25.0  Resting  46.7  43.0  Dust bathing  4.4  3.5  Locomotor behaviors  28.3  27.6  View Large DISCUSSION This study investigated whether laying hens behave differently on, and if they have a relative preference for foraging on, scratch pads with or without excreta. The results presented show that during the observation period (i.e., for 10 min commencing 6 h after the lights were turned on), laying hens spent the greatest amount of time resting, followed by locomotor behaviors, foraging, and then at a much lower proportion, dust bathing. Moreover, some preferences existed with regards to whether a behavior is performed on a scratch pad with or without excreta. It seems likely that these preferences are related to the physical and chemical aspects of the foraging material (feed or a mixture of feed and excreta) provided on the scratch pads, and the behavior that they promote. However, as there was no provision to preclude olfactory and auditory modes of communication, we cannot distinguish whether the hens were responding to visual cues of feed–excreta mixture or whether olfactory (excreta odor) cues and/or acoustic cues (foraging sounds) may have played a role in the decisions of the hens. In terms of the duration of foraging and the number of visits made to forage on the scratch pads, the laying hens preferred the scratch pads with the feed–excreta mixture, although the difference was small. The primary reason for this may be that the feed present on the clean scratch pads was rapidly removed by the eating and scratching activities of the birds. Thus, with feed no longer present, the hens’ initial interest towards the scratch pads may have quickly waned. Fresh excreta allow feed to remain attached to and linger on the surface of the scratch pads, perhaps maintaining hens’ interest for slightly longer periods of time, or making it more difficult for feed to be extracted, or both. This greater interest and challenge posed by the scratch pads soiled with excreta may have resulted in the higher number of visits to and longer durations of time spent foraging on those pads, relative to those that were clean. However, it remains questionable whether the hens were responding to feed, excreta, or a combination of both. Additionally, we cannot ignore the social environment, i.e., the presence of hens on scratch pads prior to the observational period, which could have affected subsequent behavioral measurements. In our study, hens showed a high degree of pecking and scratching behavior on scratch pads with the feed–excreta mixture, despite the presence of ad libitum feed in the feeding trough. Several studies have indicated that animals expend additional energy to “work” for food, even if an identical quality and quantity is more easily available (Osborne, 1977; Inglis et al., 1997; Lindqvist et al., 2006; Harlander-Matauschek and Häusler, 2009). This may explain why hens preferred to forage more on the scratch pads on which excreta was mixed with feed particles, making it more difficult for the hens to obtain feed from the pads. This not only provides hens with an opportunity to perform additional work to obtain food, but consequently, it may also increase physical and mental activity levels in hens, allowing them to actively interact with stimuli to gather information about the environment (Newberry, 1999). The higher level of foraging on the excreta-soiled scratch pads also demonstrates that hens are highly motivated to spend a portion of their time foraging. Some of the hens also were observed to consume excreta from the scratch pads while pecking at them. To the best of our knowledge, there is no information available on the nutritional benefits of coprophagy in laying hens. However, it has been shown in wild birds that important micronutrients can be obtained by feeding on the excreta of other species, or that of their own (McGowan, 1995; Negro et al., 2002). The investigation of the nutritional components of laying hen excreta and their potential benefits to laying hens was not within the scope of this study, but the possibility that poultry excreta contain significant levels of relevant minerals, such as potassium and phosphorous (Nicholson et al., 1996), could be considered in future studies. Laying hens spent a significant amount of time (i.e., over one-third of the total observation period) resting on the scratch pads. The soft surface of the scratch pads is likely more comfortable to rest on than the bare wire floors of the cage (Reed et al., 1966), and their placements in the corners of the cage may have created a secluded area to which hens can retreat. In further consideration of the cage design, hens may have avoided resting on the perches, due to a high chance of being disturbed on them, and chosen to rest on the scratch pads instead. Perches were located directly in front of the pop holes, which were used by the hens to travel between the cage compartments, and to access the feed troughs (Figure 1). This may have resulted in high traffic levels around the perches, encouraging the hens to seek resting areas in a more secluded and distal location. Hens were specifically observed to rest for a longer duration on the clean pads, compared to the scratch pads with excreta, although the difference was small (3.5 vs 3.1 min). A possible explanation for this may be the higher frequency of foraging behaviors on the excreta-soiled scratch pads, which resulted in more social disturbances on those pads. We did not detect a relative preference for dust bathing on the clean scratch pads or the scratch pads soiled with excreta. Birds prefer to dust bathe in dry material (Scholz et al., 2011) and as such, we expected our hens to prefer to dust bathe on the clean scratch pads with feed, as opposed to the pads with excreta, which were moist. However, as mentioned above, constant pecking and scratching may have resulted in the rapid removal of feed from the surface of the clean scratch pads. The resulting absence of feed as a dry, ideal dust bathing substrate on the clean pads, in combination with the presence of excreta as a less attractive substrate on the excreta-soiled pads, may be a reason for the lack of a significant difference in dust bathing behavior. Additionally, dust bathing was observed to a much lesser degree compared to other behaviors. Laying hens generally do not dust bathe on a daily basis, and the scratch pads may have been too small for this behavior to be performed more often (Vestergaard, 1982; Lindberg and Nicol, 1997; Alvino et al., 2013; Louton et al., 2016). Furthermore, although dust bathing behavior may occur at any time of d, hens tend to show peak dust bathing in the afternoon (Vestergaard et al., 1990; Campbell et al., 2016). We conducted our study in the late morning, which also might have influenced the dust bathing results. Although this short-term study cannot predict relevant long-term effects on the behavior of laying hens kept in enriched cages, it generates important findings. First, while farmers add scratch pads to cages with the intention of providing hens with a foraging and dust bathing area, the scratch pads in this study fulfilled a multifunctional purpose, as shown by the percentages of time spent performing different behaviors on the pads. Second, we found that laying hens have a relative, albeit small, preference for foraging for feed on excreta-soiled scratch pads, compared to clean pads. While our intention is not to recommend the addition of scratch pads soiled with excreta to enriched cages based on this relative preference, it does underline the strong motivation of hens to forage in response to the environment in which they live, even if that environment features a substrate (e.g., excreta) that humans find inappropriate, or that some herbivorous animals would avoid (Cooper et al., 2000). This raises another important and unanswered question: What are the short- and long-term consequences of foraging upon or ingesting excreta on the behavior of laying hens, especially in consideration of the shift from conventional cages to alternative housing systems? Although indications of discomfort due to contact with excreta in alternative housing systems may not be very severe or obvious, the duration of exposure to excreta and its consequences on avian behavior and physiology is relevant to animal welfare, and should be investigated in the future. ACKNOWLEDGEMENTS This study was funded by the AgriInnovation program under the Growing Forward 2 policy framework, Canada. We thank the staff of the Arkell Research Station for their help. REFERENCES Alvino G. M., Tucker C. B., Archer G. S., Mench J. A.. 2013. Astroturf as a dustbathing substrate for laying hens. Appl. Anim. Behav. Sci.  146: 88– 95. Google Scholar CrossRef Search ADS   Appleby M. C., Walker A. W., Nicol C. J., Lindberg A. C., Freire R., Hughes B. O., Elson H. A.. 2002. Development of furnished cages for laying hens. Br. Poult. Sci.  43: 489– 500. Google Scholar CrossRef Search ADS PubMed  Bubier N. E. 1996. The behavioral priorities of laying hens: The effect of cost/no cost multi-choice tests on time budgets. Behav. Processes.  37: 225– 238. Google Scholar CrossRef Search ADS PubMed  Campbell D. L. M., Makagon M. M., Swanson J. C., Siegford J. M.. 2016. Litter use by laying hens in a commercial aviary: dust bathing and piling. Poult. Sci.  95: 164– 175. Google Scholar CrossRef Search ADS PubMed  Cooper J., Gordon I. J., Pike A. W.. 2000. Strategies for the avoidance of faeces by grazing sheep. Appl. Anim. Behav. Sci.  69: 15– 33. Google Scholar CrossRef Search ADS PubMed  Dawkins M. S. 1989. Time budgets in Red Junglefowl as a baseline for the assessment of welfare in domestic fowl. Appl. Anim. Behav. Sci.  24: 77– 80. Google Scholar CrossRef Search ADS   EFSA. 2005. Opinion of the Scientific Panel on Animal Health and Welfare (AHAW) on a request from the Commission related to the welfare aspects of various systems of keeping laying hens. EFSA J . 197: 1– 23. Guinebretière M., Huneau-Salaün A., Huonnic D., Michel V.. 2012. Cage hygiene, laying location, and egg quality: The effects of linings and litter provision in furnished cages for laying hens. Poult. Sci.  91: 808– 816. Google Scholar CrossRef Search ADS PubMed  Harlander-Matauschek A., Hausler K.. 2009. Understanding feather eating behavior in laying hens. Appl. Anim. Behav. Sci.  117: 35– 41. Google Scholar CrossRef Search ADS   Himathongkham S., Riemann H.. 1999. Destruction of Salmonella typhimurium, Escherichia coli O157:H7 and Listeria monocytogenes in chicken manure by drying and/or gassing with ammonia. FEMS Microbiol. Lett.  171: 179– 182. Google Scholar CrossRef Search ADS PubMed  Horgan F. G., Berrow S. D.. 2004. Hooded crow foraging from dung pats: Implications for the structure of dung beetle assemblages. Biol. Environ.  104: 119– 124. Inglis I. R., Forkman B., Lazarus J.. 1997. Free food or earned food? A review and fuzzy model of contrafreeloading. Anim. Behav.  53: 1171– 1191. Google Scholar CrossRef Search ADS PubMed  Imran Z. K., Ali R. I.. 2014. The risk of several fungi associated with bird waste. Int. J. Med. Sci. and Clinic. Invent.  1: 558– 562. Kruijit J. P. 1964. Ontogeny of social behavior in Burmese red jungle fowl (Gallus gallus spadiceus) Bonaterre. Behav. Supp.  12: 1– 201. Lay D. C. Jr, Fulton R. M., Hester P. Y., Karcher D. M., Kjaer J. B., Mench J. A., Mullens B. A., Newberry R. C., Nicol C. J., O’sullivan N. P, Porter R. E.. 2011. Hen welfare in different housing systems. Poult. Sci.  90: 278– 294. Google Scholar CrossRef Search ADS PubMed  Lee H. W., Louton H., Schwarzer A., Rauch E., Probst A., Shao S., Schmidt P., Erhard M. H., Bergmann S.. 2016. Effects of multiple daily litter applications on the dust bathing behavior of laying hens kept in an enriched cage system. Appl. Anim. Behav. Sci.  178: 51– 59. Google Scholar CrossRef Search ADS   Lindberg A. C., Nicol C. J.. 1997. Dustbathing in modified battery cages: Is sham dustbathing an adequate substitute? Appl. Anim. Behav. Sci.  55: 113– 128. Google Scholar CrossRef Search ADS   Lindqvist C., Zimmerman P., Jensen P.. 2006. Effects of age, sex and social isolation on contrafreeloading in red junglefowl (Gallus gallus) and White Leghorn fowl. Appl. Anim. Behav. Sci.  114: 419– 428. Google Scholar CrossRef Search ADS   Louton H., Bergmann S., Reese S., Erhard M. H., Rauch E.. 2016. Dust-bathing behavior of laying hens in enriched colony housing systems and an aviary system. Poult. Sci.  95: 1482– 1491. Google Scholar CrossRef Search ADS PubMed  Merril R. J. N., Nicol C. J.. 2005. The effects of novel floorings on dustbathing, pecking and scratching behaviour of caged hens. Anim. Welf.  14: 179– 186. McGowan K. J. 1995. A test of whether economy or nutrition determines fecal sac ingestion in nesting corvids. Condor. 97: 50– 56. Negro J. J., Grande J. M., Tella J. L., Garrido J., Hornero D., Donazar J. A., Sanchez-Zapata J. A., BenItez J. R., Barcell M.. 2002. An unusual source of essential carotenoids. Nature . 416: 807– 808. Google Scholar CrossRef Search ADS PubMed  Newberry R. C. 1999. Exploratory behavior of young domestic fowl. Appl. Anim. Behav. Sci.  63: 311– 321. Google Scholar CrossRef Search ADS   Nicholson F. A., Chambers B. J., Smith K. A.. 1996. Nutrient composition of poultry manures in England and Wales. Biores. Technol.  58: 279– 284. Google Scholar CrossRef Search ADS   Osborne S. R. 1977. The free food (contrafreeloading) phenomenon: A review and analysis. Anim. Leam. Behav.  5: 221– 235. Google Scholar CrossRef Search ADS   Piepho H. P., Büchse A., Richter C.. 2004. A mixed modelling approach for randomized experiments with repeated measures. J. Agron. Crop. Sci.  190: 230– 247. Google Scholar CrossRef Search ADS   Reed M. J., White H. D., Huston T. M., May K. N.. 1966. The use of different types of cage bottoms to reduce breast blisters in battery reared broilers. Poult. Sci.  45: 1418– 1419. Google Scholar CrossRef Search ADS   Scholz B., Kjaer J. B., Urselmans S., Schrader L.. 2011. Lipid litter content affects dustbathing behaviour in laying hens. Poult. Sci.  90: 2433– 2439. Google Scholar CrossRef Search ADS PubMed  Turnbull P. C., Snoeyenbos G. H.. 1973. The roles of ammonia, water activity, and pH in the salmonellacidal effect of long-used poultry litter. Avian Dis.  17: 72– 86. Google Scholar CrossRef Search ADS PubMed  Vestergaard K. 1982. The significance of dust bathing for the wellbeing of the domestic hen. Tierhaltung . 13: 109– 118. Vestergaard K., Hogan J. A., Kruijt J. P.. 1990. The development of a behavior system: Dustbathing in the Burmese Red Junglefowl I. The influence of the rearing environment on the organization of dustbathing. Behav . 112: 99– 116. Google Scholar CrossRef Search ADS   Weeks C. A., Nicol C. J.. 2006. Behavioral needs, priorities and preferences of laying hens. World's Poult. Sci. J.  62: 296– 307. Google Scholar CrossRef Search ADS   Weaver W. D. Jr., Meijerhof R.. 1991. The effect of different levels of relative humidity and air movement on litter conditions, ammonia levels, growth and carcass quality for broiler chickens. Poult. Sci.  70: 746– 755. Google Scholar CrossRef Search ADS PubMed  Zarrin M., Jorfi M., Amirrajab N., Rostami M.. 2010. Isolation of Cryptococcus neoformans from pigeon droppings in Ahwaz, Iran. Turk. J. Med. Sci.  40: 313– 316. © 2017 Poultry Science Association Inc. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Poultry Science Oxford University Press

How does the presence of excreta affect the behavior of laying hens on scratch pads?

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Abstract

Abstract Enriched cages for laying hens provide scratch pads for foraging on the wire mesh floors. Apart from foraging on scratch pads, hens also defecate on these pads, causing them to become soiled with excreta. This study was conducted to determine the relative preference of laying hens for foraging on clean (C) scratch pads or scratch pads soiled with excreta (E), and to study the behaviors performed by hens on such pads. A total of 288 laying hens was housed in 16 enriched cages (18 hens/cage), each divided into 2 compartments. On a daily basis, half of the scratch pads (one in each compartment) were removed and cleaned, while the other half were cleaned and then covered with 550 g (0.35 g/cm2) of conspecific excreta. The C and E scratch pads were then put back into the cages in a systematic order to avoid side bias. Feed was delivered automatically onto the scratch pads as a litter substrate. The frequency of visits and the total time spent performing different behaviors on C and E pads were video-recorded [the time of video recording was relative to litter (feed) delivery on the scratch pads] for a total of 10 min/d, 3 times/wk, over a period of 4 weeks. Overall, the allocation of the time budget for different behaviors was found to be—in order of greatest to least amount of time—resting, locomotor behaviors (walking and running), foraging, and dust bathing. Laying hens showed a relative preference for E scratch pads by visiting them more frequently (P = 0.001), and spent more time (P = 0.035) foraging on them, whereas they rested for more time (P < 0.001) on C scratch pads. The relative preference for E scratch pads during foraging signifies the innate importance of foraging substrates in enriched cages for laying hens. Similarly, the longer use of C scratch pads for resting indicates the need for an ideal and clean resting surface in enriched cages. INTRODUCTION Enriched cages have been designed to overcome the limitations of conventional cages to support behaviors that laying hens are highly motivated to perform (Weeks and Nicol, 2006). These cages provide a varying amount of horizontal space for locomotion and other behaviors such as nesting, perching, foraging, and dust bathing (Appleby et al., 2002; Lay et al., 2011). In enriched cages, foraging and dust bathing are typically performed on scratch pads, which are sections of synthetic turf of various designs and other artificial materials. These cages also are equipped with a mechanism that delivers a small amount of litter material, such as feed, onto these scratch pads, upon which hens can scratch, forage, and dust bathe (Scholz et al., 2011). However, not all farmers provide feed as a foraging and dust bathing substrate regularly, or otherwise provide it in small amounts, as feed represents the major cost of production for farmers (Lee et al., 2016). The result is that no litter substrate is delivered onto the scratch pads, and so little motivation is offered for hens to scratch, forage, and dust bathe upon them. Furthermore, defecation onto, and accumulation of, excreta on the scratch pads causes them to become soiled and unhygienic. Poor scratch pad hygiene can become an increasing health threat and is, therefore, a welfare concern. Excreta on the scratch pads may be a vector for fungi, viruses, bacteria, and toxins (Himathongkham and Riemann, 1999; Zarrin et al., 2010; Imran and Ali, 2014), in addition to contributing to poor air quality, with high levels of dust and ammonia (Turnbull and Snoeyenbos, 1973; Weaver and Meijerhof, 1991). Collectively, these downstream consequences of poor hygiene can lead to decreased feather cleanliness, and give rise to health issues such as ulcerative footpad dermatitis (i.e., bumblefoot) (EFSA, 2005). Furthermore, poor hygiene in enriched cages can be a food safety concern, as unclean conditions promote egg dirtiness and bacterial contamination of eggshells, which translate to an economic loss for farmers (Guinebretière et al., 2012). For these reasons, in addition to expensive cleaning techniques, farmers often choose to remove scratch pads from their cages, or are reluctant to use them at all, which could jeopardize the welfare of laying hens housed in enriched cages. While there are considerable disadvantages for hens and farmers when it comes to soiled scratch pads, there may be some hidden benefits associated with excreta contact as well. Despite the evidence that dirty scratch pads in enriched cages are a hygienic challenge, some studies have reported that certain wild bird species benefit nutritionally from foraging on and consuming excreta. McGowan (1995) observed that parent birds of many passerine species consume the excreta of their neonatal offspring shortly after hatching, due to the excreta's high nutritional value. In addition, other bird species also have been found to ingest the excreta of other animals, mainly for its nutritional benefits. Ungulate excreta, for example, contain high levels of intact carotenoids, which are essential for vertebrates and have pigmentary, as well as antioxidant and immunostimulant, functions (Negro et al., 2002). As a result, the Egyptian vulture, Neophron percnopterus, is commonly seen foraging on and consuming cow, goat, and sheep excreta (Negro et al., 2002). Apart from micronutrients, food (i.e., prey) items likely to be found in excreta may be another reason that animals forage on animal dung: hooded crows (Corvus corone) preferentially forage on fresh horse excreta, as it is a reliable source of dung beetles (Horgan and Berrow, 2004). For laying hens, however, the nutritional benefits of foraging on or consuming excreta, if any, are unknown. In nature, wild red junglefowl (Gallus gallus) spend more than 60% of their time foraging in natural litter (Dawkins, 1989). In commercial housing systems, domestic hens continue to demonstrate this high motivation to forage, even when they are provided feed ad libitum, which can be accessed at no cost (Bubier, 1996). In litter-based housing systems, laying hens scratch, peck, and dust bathe in the litter substrate (Merril and Nicol, 2005), which is often unchanged over the entire duration of a laying period, leading to the accumulation of a considerable amount of excreta. In the case of laying hens housed in enriched cages, excreta and litter material (if provided) on the scratch pads may be the only foraging substrates available in the midst of a wire grid floor. It is clear that the excreta-soiled scratch pads in enriched cages are undesirable from a hygienic point of view, and solutions to improve the health and welfare of laying hens kept in these housing systems should be addressed. However, there is a knowledge gap regarding how laying hens respond to excreta in the short and long terms. As a first step to bridging this gap, this study was conducted with the objectives of examining how feed (litter substrate) on clean (C) compared to excreta-soiled (E) pads could influence hens’ choice regarding where to forage, and once on the scratch pads, how hens allocate their time towards performing different behaviors on each type of scratch pad. As hens instantly started to defecate on the C pads, we considered their preferences for C or E pads one h after they were put into the cages, in order to keep the choices distinguishable. MATERIALS AND METHODS Ethical Statement The research protocol was approved by the University of Guelph Animal Care Committee (Animal User Protocol Number 3169) prior to the start of data collection. Animals and Husbandry A total of 288 laying hens of 4 breeds (White Leghorn, Rhode Island Red, Columbian Rock, and Barred Rock) was obtained from the University of Guelph Arkell Research Station at 25 wk of age. Hens were housed in enriched cages manufactured by FDI Cage Systems of Mitchell, Ontario (369 cm × 65 cm; 18 hens/cage, 4 breeds/cage, 16 cages total). Each enriched cage (Figure 1) was partitioned into 2 identical compartments for the purpose of the experiment, and each individual compartment was equipped with a curtained nest area (107 cm2/hen; red curtains), perches running lengthwise (13.7 cm/hen), a scratch pad (details described below), automatic feeders on the outside of the cage (10 cm/hen), and nipple drinkers (1.5 hens/nipple). Feed and water were provided ad libitum. The light period was 14L: 10D. Figure 1. View largeDownload slide Schematic layout of an enriched cage for 18 laying hens featuring 2 identical compartments freely accessible through a pop hole (not to scale). Figure 1. View largeDownload slide Schematic layout of an enriched cage for 18 laying hens featuring 2 identical compartments freely accessible through a pop hole (not to scale). Experimental Design Two identical compartments in each cage were joined by a pop hole to allow hens to move freely between compartments. A white plastic sheet (visual barrier) was added between the width and length of the 2 compartments, aside from the pop hole, to prevent the transfer of visual information between the cages and treatments. Each compartment contained one scratch pad (31 × 51 cm; 88 cm2/hen); together, the 2 scratch pads per cage occupied approximately 28% of the total surface area of the cage floor. The square scratch pads consisted of brown, synthetic Astroturf, which resembled natural grass in both appearance and texture. On a daily basis one h (10:00 h) before starting video recording, half of the scratch pads were removed and cleaned, while the other half were cleaned and then covered with 550 g (0.35 g/cm2) of fresh conspecific excreta, which was determined to be the average amount of excreta produced in a d by 18 laying hens. One C and one E pads were then put back into each cage in such a way that allocation of treatments across sides (right or left) was evenly spread. Feed (approximately 6 g/delivery) was delivered automatically for one min onto both scratch pads by a spiral conveyor pipe (feed auger) every 2 hours. A pilot study identified that hens were most active on the scratch pads at 11:00 h, 6 h after the lights were turned on. The video was recorded (including the time when feed was delivered) and analyzed for 10 min at 11:00 h, as soon as the feed was delivered from the auger onto the C and E pads, 3 times/wk, over a period of 4 wk (resulting in a total of 64 h of analyzed video recordings). As hens started to defecate on the clean scratch pads, all of our 10-minute observation periods took place one h after exposure of hens to the treatments. Also, due to the discrepancy of a few s created by feed delivery from one cage to the other, the time to start behavioral recording for each cage was carefully accounted for while analyzing the videos. Lastly, the laying hens were habituated to the experimental setup (scratch pads and handling) over a period of 10 d before the video recordings began. Behavioral Measures Continuous video recording of laying hen behavior on the scratch pads was conducted at normal speed (25 frames/s) using video cameras (Samsung SNO-5084R, Samsung Techwin Co., Gyeonggido, Korea) placed over each cage. The number of visits to C and E scratch pads (per min, 10 min total), the duration of the visits, and the durations of the behaviors referred to in Table 1 were analyzed using INTERACT® software (Mangold International GmbH, Graf-von-Deym Str. 594,424 Arnstorg, Germany). Table 1. List of mutually exclusive behaviors that occurred on scratch pads. Behaviors  Description  Foraging  Scraping or pecking scratch pads with feet or beak, respectively  Dust bathing  Performing dust bathing elements such as bill raking, wing shaking, scratching, lying on the side, and head rubbing, as described by Kruijit (1964)  Resting  Sitting on the scratch pads, without any other activity  Locomotor  Walking or running on the scratch pads  Behaviors  Description  Foraging  Scraping or pecking scratch pads with feet or beak, respectively  Dust bathing  Performing dust bathing elements such as bill raking, wing shaking, scratching, lying on the side, and head rubbing, as described by Kruijit (1964)  Resting  Sitting on the scratch pads, without any other activity  Locomotor  Walking or running on the scratch pads  View Large Statistical Analysis The model was fitted using PROC GLIMMIX of the SAS System (v9.4, SAS Institute Inc., Cary, NC, 2016). The data analysis was based on the mixed modeling approach for randomized experiments with repeated measures (Piepho et al., 2004). To analyze the number of visits, foraging duration, dust bathing duration, resting duration, and locomotor behavior duration, a generalized linear mixed model was employed with the fixed effect of scratch pad treatment (C and E), breed (White Leghorn, Rhode Island Red, Columbian Rock, and Barred Rock) and treatment × breed interaction. The average bird weight per cage was used as a covariate, and cage was used as a random effect. The number of visits was fitted with a Poisson distribution, whereas all other variables were logarithmically transformed prior to analyses to achieve normality. Due to the repeated measures taken on the same group of birds (cage) at different time points (d), an autoregressive covariance structure of order 1 was fitted to the cage-by-day effect. The degrees of freedom were adjusted using the Kenward–Roger method. All results are presented as least square means ± standard error (SE). Statistical significance was considered at P < 0.05 in all cases. RESULTS The times allocated to various behaviors on both the C and E pads within the 12, 10-minute observation periods are presented as percentages in Table 2. In general, the most common behaviors laying hens performed on both the C and E scratch pads were resting, followed by locomotor behaviors and foraging. Dust bathing occurred to a lesser degree. No eggs were laid on the scratch pads during the experimental period. Hens visited the E pads more (P = 0.001; F1,376 = 18.03) frequently than the C pads (3.6 ± 0.13 vs. 3.2 ± 0.13 visits/min). Hens spent a longer time (P < 0.001; F1,374 = 200.82) resting on C pads compared to the E pads (Figure 2C). No significant differences were observed with respect to dust bathing behavior (Figure 2B) or locomotor behaviors (Figure 2D) between the C and E scratch pads. However, hens were found to forage for a longer time (P = 0.035; F1,155.5 = 4.74) on the E pads compared to the C pads (Figure 2A). Interestingly, while foraging on the E scratch pads, some of the hens were observed consuming excreta. There was no significant effect of breed, breed by treatment interaction, or average body weight on any of the behavioral responses. Figure 2. View largeDownload slide Mean duration of foraging (A), dust bathing (B), resting (C), and locomotor (D) behaviors of laying hens on clean and excreta-soiled scratch pads out of 10-minute observation period. Values represent least square means ± standard error. Different letters (a and b) represent treatments that differed significantly (P < 0.05). Figure 2. View largeDownload slide Mean duration of foraging (A), dust bathing (B), resting (C), and locomotor (D) behaviors of laying hens on clean and excreta-soiled scratch pads out of 10-minute observation period. Values represent least square means ± standard error. Different letters (a and b) represent treatments that differed significantly (P < 0.05). Table 2. Percentage of time spent performing different behaviors by laying hens on clean (C) and excreta-soiled (E) scratch pads during 10-minute recording sessions over a 3-week period.   Treatments  Behaviors  C  E  Foraging  21.5  25.0  Resting  46.7  43.0  Dust bathing  4.4  3.5  Locomotor behaviors  28.3  27.6    Treatments  Behaviors  C  E  Foraging  21.5  25.0  Resting  46.7  43.0  Dust bathing  4.4  3.5  Locomotor behaviors  28.3  27.6  View Large DISCUSSION This study investigated whether laying hens behave differently on, and if they have a relative preference for foraging on, scratch pads with or without excreta. The results presented show that during the observation period (i.e., for 10 min commencing 6 h after the lights were turned on), laying hens spent the greatest amount of time resting, followed by locomotor behaviors, foraging, and then at a much lower proportion, dust bathing. Moreover, some preferences existed with regards to whether a behavior is performed on a scratch pad with or without excreta. It seems likely that these preferences are related to the physical and chemical aspects of the foraging material (feed or a mixture of feed and excreta) provided on the scratch pads, and the behavior that they promote. However, as there was no provision to preclude olfactory and auditory modes of communication, we cannot distinguish whether the hens were responding to visual cues of feed–excreta mixture or whether olfactory (excreta odor) cues and/or acoustic cues (foraging sounds) may have played a role in the decisions of the hens. In terms of the duration of foraging and the number of visits made to forage on the scratch pads, the laying hens preferred the scratch pads with the feed–excreta mixture, although the difference was small. The primary reason for this may be that the feed present on the clean scratch pads was rapidly removed by the eating and scratching activities of the birds. Thus, with feed no longer present, the hens’ initial interest towards the scratch pads may have quickly waned. Fresh excreta allow feed to remain attached to and linger on the surface of the scratch pads, perhaps maintaining hens’ interest for slightly longer periods of time, or making it more difficult for feed to be extracted, or both. This greater interest and challenge posed by the scratch pads soiled with excreta may have resulted in the higher number of visits to and longer durations of time spent foraging on those pads, relative to those that were clean. However, it remains questionable whether the hens were responding to feed, excreta, or a combination of both. Additionally, we cannot ignore the social environment, i.e., the presence of hens on scratch pads prior to the observational period, which could have affected subsequent behavioral measurements. In our study, hens showed a high degree of pecking and scratching behavior on scratch pads with the feed–excreta mixture, despite the presence of ad libitum feed in the feeding trough. Several studies have indicated that animals expend additional energy to “work” for food, even if an identical quality and quantity is more easily available (Osborne, 1977; Inglis et al., 1997; Lindqvist et al., 2006; Harlander-Matauschek and Häusler, 2009). This may explain why hens preferred to forage more on the scratch pads on which excreta was mixed with feed particles, making it more difficult for the hens to obtain feed from the pads. This not only provides hens with an opportunity to perform additional work to obtain food, but consequently, it may also increase physical and mental activity levels in hens, allowing them to actively interact with stimuli to gather information about the environment (Newberry, 1999). The higher level of foraging on the excreta-soiled scratch pads also demonstrates that hens are highly motivated to spend a portion of their time foraging. Some of the hens also were observed to consume excreta from the scratch pads while pecking at them. To the best of our knowledge, there is no information available on the nutritional benefits of coprophagy in laying hens. However, it has been shown in wild birds that important micronutrients can be obtained by feeding on the excreta of other species, or that of their own (McGowan, 1995; Negro et al., 2002). The investigation of the nutritional components of laying hen excreta and their potential benefits to laying hens was not within the scope of this study, but the possibility that poultry excreta contain significant levels of relevant minerals, such as potassium and phosphorous (Nicholson et al., 1996), could be considered in future studies. Laying hens spent a significant amount of time (i.e., over one-third of the total observation period) resting on the scratch pads. The soft surface of the scratch pads is likely more comfortable to rest on than the bare wire floors of the cage (Reed et al., 1966), and their placements in the corners of the cage may have created a secluded area to which hens can retreat. In further consideration of the cage design, hens may have avoided resting on the perches, due to a high chance of being disturbed on them, and chosen to rest on the scratch pads instead. Perches were located directly in front of the pop holes, which were used by the hens to travel between the cage compartments, and to access the feed troughs (Figure 1). This may have resulted in high traffic levels around the perches, encouraging the hens to seek resting areas in a more secluded and distal location. Hens were specifically observed to rest for a longer duration on the clean pads, compared to the scratch pads with excreta, although the difference was small (3.5 vs 3.1 min). A possible explanation for this may be the higher frequency of foraging behaviors on the excreta-soiled scratch pads, which resulted in more social disturbances on those pads. We did not detect a relative preference for dust bathing on the clean scratch pads or the scratch pads soiled with excreta. Birds prefer to dust bathe in dry material (Scholz et al., 2011) and as such, we expected our hens to prefer to dust bathe on the clean scratch pads with feed, as opposed to the pads with excreta, which were moist. However, as mentioned above, constant pecking and scratching may have resulted in the rapid removal of feed from the surface of the clean scratch pads. The resulting absence of feed as a dry, ideal dust bathing substrate on the clean pads, in combination with the presence of excreta as a less attractive substrate on the excreta-soiled pads, may be a reason for the lack of a significant difference in dust bathing behavior. Additionally, dust bathing was observed to a much lesser degree compared to other behaviors. Laying hens generally do not dust bathe on a daily basis, and the scratch pads may have been too small for this behavior to be performed more often (Vestergaard, 1982; Lindberg and Nicol, 1997; Alvino et al., 2013; Louton et al., 2016). Furthermore, although dust bathing behavior may occur at any time of d, hens tend to show peak dust bathing in the afternoon (Vestergaard et al., 1990; Campbell et al., 2016). We conducted our study in the late morning, which also might have influenced the dust bathing results. Although this short-term study cannot predict relevant long-term effects on the behavior of laying hens kept in enriched cages, it generates important findings. First, while farmers add scratch pads to cages with the intention of providing hens with a foraging and dust bathing area, the scratch pads in this study fulfilled a multifunctional purpose, as shown by the percentages of time spent performing different behaviors on the pads. Second, we found that laying hens have a relative, albeit small, preference for foraging for feed on excreta-soiled scratch pads, compared to clean pads. While our intention is not to recommend the addition of scratch pads soiled with excreta to enriched cages based on this relative preference, it does underline the strong motivation of hens to forage in response to the environment in which they live, even if that environment features a substrate (e.g., excreta) that humans find inappropriate, or that some herbivorous animals would avoid (Cooper et al., 2000). This raises another important and unanswered question: What are the short- and long-term consequences of foraging upon or ingesting excreta on the behavior of laying hens, especially in consideration of the shift from conventional cages to alternative housing systems? Although indications of discomfort due to contact with excreta in alternative housing systems may not be very severe or obvious, the duration of exposure to excreta and its consequences on avian behavior and physiology is relevant to animal welfare, and should be investigated in the future. ACKNOWLEDGEMENTS This study was funded by the AgriInnovation program under the Growing Forward 2 policy framework, Canada. We thank the staff of the Arkell Research Station for their help. REFERENCES Alvino G. M., Tucker C. B., Archer G. S., Mench J. A.. 2013. Astroturf as a dustbathing substrate for laying hens. Appl. Anim. Behav. Sci.  146: 88– 95. Google Scholar CrossRef Search ADS   Appleby M. C., Walker A. W., Nicol C. J., Lindberg A. C., Freire R., Hughes B. O., Elson H. A.. 2002. Development of furnished cages for laying hens. Br. Poult. Sci.  43: 489– 500. Google Scholar CrossRef Search ADS PubMed  Bubier N. E. 1996. The behavioral priorities of laying hens: The effect of cost/no cost multi-choice tests on time budgets. Behav. Processes.  37: 225– 238. Google Scholar CrossRef Search ADS PubMed  Campbell D. L. M., Makagon M. M., Swanson J. C., Siegford J. M.. 2016. Litter use by laying hens in a commercial aviary: dust bathing and piling. Poult. Sci.  95: 164– 175. Google Scholar CrossRef Search ADS PubMed  Cooper J., Gordon I. J., Pike A. W.. 2000. Strategies for the avoidance of faeces by grazing sheep. Appl. Anim. Behav. Sci.  69: 15– 33. Google Scholar CrossRef Search ADS PubMed  Dawkins M. S. 1989. Time budgets in Red Junglefowl as a baseline for the assessment of welfare in domestic fowl. Appl. Anim. Behav. Sci.  24: 77– 80. Google Scholar CrossRef Search ADS   EFSA. 2005. Opinion of the Scientific Panel on Animal Health and Welfare (AHAW) on a request from the Commission related to the welfare aspects of various systems of keeping laying hens. EFSA J . 197: 1– 23. Guinebretière M., Huneau-Salaün A., Huonnic D., Michel V.. 2012. Cage hygiene, laying location, and egg quality: The effects of linings and litter provision in furnished cages for laying hens. Poult. Sci.  91: 808– 816. Google Scholar CrossRef Search ADS PubMed  Harlander-Matauschek A., Hausler K.. 2009. Understanding feather eating behavior in laying hens. Appl. Anim. Behav. Sci.  117: 35– 41. Google Scholar CrossRef Search ADS   Himathongkham S., Riemann H.. 1999. Destruction of Salmonella typhimurium, Escherichia coli O157:H7 and Listeria monocytogenes in chicken manure by drying and/or gassing with ammonia. FEMS Microbiol. Lett.  171: 179– 182. Google Scholar CrossRef Search ADS PubMed  Horgan F. G., Berrow S. D.. 2004. Hooded crow foraging from dung pats: Implications for the structure of dung beetle assemblages. Biol. Environ.  104: 119– 124. Inglis I. R., Forkman B., Lazarus J.. 1997. Free food or earned food? A review and fuzzy model of contrafreeloading. Anim. Behav.  53: 1171– 1191. Google Scholar CrossRef Search ADS PubMed  Imran Z. K., Ali R. I.. 2014. The risk of several fungi associated with bird waste. Int. J. Med. Sci. and Clinic. Invent.  1: 558– 562. Kruijit J. P. 1964. Ontogeny of social behavior in Burmese red jungle fowl (Gallus gallus spadiceus) Bonaterre. Behav. Supp.  12: 1– 201. Lay D. C. Jr, Fulton R. M., Hester P. Y., Karcher D. M., Kjaer J. B., Mench J. A., Mullens B. A., Newberry R. C., Nicol C. J., O’sullivan N. P, Porter R. E.. 2011. Hen welfare in different housing systems. Poult. Sci.  90: 278– 294. Google Scholar CrossRef Search ADS PubMed  Lee H. W., Louton H., Schwarzer A., Rauch E., Probst A., Shao S., Schmidt P., Erhard M. H., Bergmann S.. 2016. Effects of multiple daily litter applications on the dust bathing behavior of laying hens kept in an enriched cage system. Appl. Anim. Behav. Sci.  178: 51– 59. Google Scholar CrossRef Search ADS   Lindberg A. C., Nicol C. J.. 1997. Dustbathing in modified battery cages: Is sham dustbathing an adequate substitute? Appl. Anim. Behav. Sci.  55: 113– 128. Google Scholar CrossRef Search ADS   Lindqvist C., Zimmerman P., Jensen P.. 2006. Effects of age, sex and social isolation on contrafreeloading in red junglefowl (Gallus gallus) and White Leghorn fowl. Appl. Anim. Behav. Sci.  114: 419– 428. Google Scholar CrossRef Search ADS   Louton H., Bergmann S., Reese S., Erhard M. H., Rauch E.. 2016. Dust-bathing behavior of laying hens in enriched colony housing systems and an aviary system. Poult. Sci.  95: 1482– 1491. Google Scholar CrossRef Search ADS PubMed  Merril R. J. N., Nicol C. J.. 2005. The effects of novel floorings on dustbathing, pecking and scratching behaviour of caged hens. Anim. Welf.  14: 179– 186. McGowan K. J. 1995. A test of whether economy or nutrition determines fecal sac ingestion in nesting corvids. Condor. 97: 50– 56. Negro J. J., Grande J. M., Tella J. L., Garrido J., Hornero D., Donazar J. A., Sanchez-Zapata J. A., BenItez J. R., Barcell M.. 2002. An unusual source of essential carotenoids. Nature . 416: 807– 808. Google Scholar CrossRef Search ADS PubMed  Newberry R. C. 1999. Exploratory behavior of young domestic fowl. Appl. Anim. Behav. Sci.  63: 311– 321. Google Scholar CrossRef Search ADS   Nicholson F. A., Chambers B. J., Smith K. A.. 1996. Nutrient composition of poultry manures in England and Wales. Biores. Technol.  58: 279– 284. Google Scholar CrossRef Search ADS   Osborne S. R. 1977. The free food (contrafreeloading) phenomenon: A review and analysis. Anim. Leam. Behav.  5: 221– 235. Google Scholar CrossRef Search ADS   Piepho H. P., Büchse A., Richter C.. 2004. A mixed modelling approach for randomized experiments with repeated measures. J. Agron. Crop. Sci.  190: 230– 247. Google Scholar CrossRef Search ADS   Reed M. J., White H. D., Huston T. M., May K. N.. 1966. The use of different types of cage bottoms to reduce breast blisters in battery reared broilers. Poult. Sci.  45: 1418– 1419. Google Scholar CrossRef Search ADS   Scholz B., Kjaer J. B., Urselmans S., Schrader L.. 2011. Lipid litter content affects dustbathing behaviour in laying hens. Poult. Sci.  90: 2433– 2439. Google Scholar CrossRef Search ADS PubMed  Turnbull P. C., Snoeyenbos G. H.. 1973. The roles of ammonia, water activity, and pH in the salmonellacidal effect of long-used poultry litter. Avian Dis.  17: 72– 86. Google Scholar CrossRef Search ADS PubMed  Vestergaard K. 1982. The significance of dust bathing for the wellbeing of the domestic hen. Tierhaltung . 13: 109– 118. Vestergaard K., Hogan J. A., Kruijt J. P.. 1990. The development of a behavior system: Dustbathing in the Burmese Red Junglefowl I. The influence of the rearing environment on the organization of dustbathing. Behav . 112: 99– 116. Google Scholar CrossRef Search ADS   Weeks C. A., Nicol C. J.. 2006. Behavioral needs, priorities and preferences of laying hens. World's Poult. Sci. J.  62: 296– 307. Google Scholar CrossRef Search ADS   Weaver W. D. Jr., Meijerhof R.. 1991. The effect of different levels of relative humidity and air movement on litter conditions, ammonia levels, growth and carcass quality for broiler chickens. Poult. Sci.  70: 746– 755. Google Scholar CrossRef Search ADS PubMed  Zarrin M., Jorfi M., Amirrajab N., Rostami M.. 2010. Isolation of Cryptococcus neoformans from pigeon droppings in Ahwaz, Iran. Turk. J. Med. Sci.  40: 313– 316. © 2017 Poultry Science Association Inc.

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Poultry ScienceOxford University Press

Published: Mar 1, 2018

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