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Applying chemical stimuli on feathers to reduce feather pecking in laying hens
Applied Animal Behaviour Science 132 (2011) 146–151
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Applying chemical stimuli on feathers to reduce feather pecking in laying hens Alexandra Harlander-Matauschek a,∗ , T. Bas Rodenburg b a b
Department of Small Animal Breeding and Poultry Science, University of Hohenheim, 470c, 70599 Stuttgart, Germany Animal Breeding and Genomics Centre, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands
a r t i c l e
i n f o
Article history: Accepted 3 April 2011 Available online 30 April 2011 Keywords: Feather eating Feather pecking Laying hens Learning Aversion
a b s t r a c t Recent studies have shown that spraying a distasteful substance (quinine) on a bird’s feather cover reduced short-term feather pecking. The present experiment evaluated if other substances offer similar or better protection against feather pecking. One hundred and twenty birds were divided into 12 groups of 10 birds each. Over a period of 10 days the birds’ response to 10 feathers coated with one of the 11 distasteful substances was observed and recorded. Feathers were soaked in a 1% garlic solution, 1% almond oil, 1% clove oil, 1% clove solution, quinine sulphate solution in four concentrations (0.1%, 1%, 2%, 4%), 0.6 mol magnesium chloride solution, anti-peck spray or an angostura solution. The control group received uncoated feathers. The number of feathers plucked, rejected or eaten was counted 60 min after presenting the feathers. All substances reduced feather plucking (p < 0.0001) and consumption (p < 0.0001) significantly, compared to uncoated feathers. Quinine concentrations of 2% and 4% were most effective. This study was the first to investigate the aversive potential of different substances to deter feather peckers from the feathers of other birds. The findings may be useful in the development of spraying devices to prevent feather pecking when other management tools fail. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Feather pecking is a very prominent unsolved problem in poultry worldwide. It can occur in many species including domestic hens (Blokhuis et al., 2007), turkeys (Busayi et al., 2006), ducks (Gustafson et al., 2007), pheasants (Kjaer, 2004) and quails (Bilcik and Bessei, 1993). It is particularly a problem in loose housing systems, where active feather-pecking birds have access to a large number of victims (Keeling, 1995). Pecked laying hens with bad plumage condition loose more heat and consume more feed than unpecked hens (Herremans et al., 1989), and potential customers may be deterred from buying eggs due to the unappetizing appearance of pecked birds. Aside
∗ Corresponding author at: Animal Welfare and Ethology, University of Giessen, Germany. Tel.: +49 6419938747; fax: +49 6419938759. E-mail addresses: [email protected], [email protected] (A. Harlander-Matauschek). 0168-1591/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2011.04.004
from the economical aspects, feather pecking is a welfare concern. Feather removal is painful for the victim (Gentle and Hunter, 1991). Wounds resulting from feather removal may bleed and eventually lead to cannibalism, which can result in mortality rates of 20% and higher in laying hens (Blokhuis et al., 2007). It is generally assumed that feather pecking is redirected behaviour with an underlying unfulfilled motivation either to forage (Blokhuis, 1986) or to dust-bath (Vestergaard and Lisborg, 1993), however, evidence for the latter is more controversial. Additionally, feather pecking in laying hens may indicate that the bird is performing this behaviour due to an unfulfilled behavioural need (Weeks and Nicol, 2006). Although a variety of risk factors affecting the development of feather pecking have been identified (e.g. Lambton et al., 2010), remedies for this behaviour are still needed. In practice, birds like laying hens, turkeys, Muscovy ducks and pheasants are often routinely beak-trimmed to prevent feather pecking and cannibalism. Beak trimming is criticized due to acute and
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chronic pain and due to the removal of sensory receptors and free nerve endings in the bill tip (Gentle et al., 1997), but is used as the lesser of two evils. In spite of the unsolved feather pecking problem, beak trimming will be banned in laying hens in many European countries in the near future (Van Horne and Achterbosch, 2008). Along with vision, audition and touch, chemosensory cues are involved in the foraging decisions of birds (Werner and Clark, 2003). It is widely accepted that gustatory sensation (Skelhorn and Rowe, 2006), olfaction (Roper and Marples, 1997) and irritation (Gentle and Hill, 1987) compose the chemical senses of birds. Many insects and plants secrete chemosensory cues when they are attacked by predators (Eisner and Meinwald, 1966). Many toxins commonly used in defence mechanisms by invertebrates and plants taste bitter to deter predators. Pecking at bittertasting objects evokes disgust responses from the bird and it will avoid pecking at similar objects (e.g. Hogan, 1973). Odour perception in birds is mediated by olfaction and nasal trigeminal chemoreception (Mason and Silver, 1983). The former is described as the sense of smell, the latter is part of the common chemical senses, a system designed to protect birds from the harmful effects of irritants. Stimulation of trigeminal chemoreceptors may serve as a cue for avoidance (Jakubas and Mason, 1991). Additionally, olfactory cues may serve as conditional stimuli to which learned food aversions can be formed when paired in the presence of toxicants or irritants (Clark and Mason, 1987). Previous studies have shown that feather pecking is positively associated with feather ingestion (McKeegan and Savory, 1999, 2001), meaning that feathers are part of the diet in severely feather-pecking birds (HarlanderMatauschek and Häusler, 2009). In different species quinine is widely used as an aversive substance in learning experiments (e.g. Alcock, 1970). Harlander-Matauschek et al. (2008) showed that laying hens learned to avoid eating loose feathers when they had been soaked in a bitter-tasting quinine solution. Additionally, when the feather cover of adult laying hens was sprayed with the bitter-tasting quinine, the birds learned that feathers from conspecifics were not attractive to peck at for a period of time (Harlander-Matauschek et al., 2009). The present experiment was conducted to identify nonharmful substances suitable for humans and birds which can be used to keep feather peckers away from the plumage of other birds. We investigated the consumption of feathers coated with solutions of natural products (garlic, almond, clove) different concentrations of quinine, magnesium chloride, commercial anti-peck spray and “Angostura Bitter”. Coating treatments were not combined. For ethical and scientific reasons we used a piece of plastic with feathers attached as a model. We used laying hens at the end of their laying period to test which substances most effectively deterred hens from eating feathers. 2. Methods 2.1. Animals and housing One hundred and twenty birds from a high featherpecking selection line were used. The beaks of the hens
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were not trimmed. The birds in the present study originated from a selection experiment (Kjaer et al., 2001) in which birds were divergently selected on high and low feather pecking activity for six generations. The birds of the present experiment were the fourth generation after selection from Kjaer et al. (2001). Birds were reared and kept in a deep litter system prior to the experiment. At 62 weeks of age birds were transferred to individual cages measuring 43 cm × 43 cm × 45 cm (length × width × height). The feed trough was placed at the front and a nipple drinker at the back of the cage. Each cage was supplemented with a perch of 20 cm length. The cages were separated by nontransparent boards so that the birds had no physical or visual contact with their neighbours. The hens were kept in a ventilated windowless room at a constant temperature (20 ◦ C). Lights were on from 0400 until 1800 h. The Hohenheim University mash layer ration (17.2% CP, 11.1 MJ/kg) and water were provided ad libitum. The test phase started after 1 week of adaptation to the experimental situation. 2.2. Preparation of coated feathers Feathers were plucked from dead birds of the high feather-pecking selection line (Kjaer et al., 2001), put in 60 l plastic bags and stored in a refrigerator for hygienic reasons. To reduce the palatability of the feathers, 100 g of feathers was soaked in 1000 ml 1% garlic solution (granulated, Kotanyi GmbH, Austria), 1% almond oil (Sigma–Aldrich Chemie, Germany), 1% clove oil (Sigma–Aldrich Chemie, Germany), 1% clove solution (grounded, Kotanyi GmbH, Austria), 0.1%, 1%, 2%, 4% quinine sulphate solution (Acros Organics BVBA, Geel, Belgium), 0.6 mol magnesium chloride (Sigma–Aldrich Chemie, Germany) solution in 1000 ml pure anti-peck spray (FED-PICK, FP 48 Sprühlösung, Dr. Hesse Tierpharma GmbH & CoKG, Germany) or in pure “Angostura Bitter” (Hemmeter, Germany) for 12 h. We then allowed feathers to dry for 12 h. Because almond and clove oil do not readily mix with water, they were first diluted in ethanol (1:2) to prepare a solution. To produce a quinine solution, quinine sulphate dihydrate was weighed and diluted with aqua bidestillata. Some drops of sulphuric acid were pipetted to dissolve all the quinine by swirling thoroughly. Aliquots of the stock solutions were used to achieve the experimental concentrations. Because quinine solutions are used successfully as aversive substances in learning experiments in birds and other species (e.g. Alcock, 1970; Skelhorn and Rowe, 2006), we assumed that quinine solutions would be more effective (produce rapid and stable avoidance) than other solutions. However, quinine agents have side effects (Langford et al., 2003), so we wanted to find the lowest effective concentration with the highest avoidance reaction. In humans, quinine is commonly added to soft drinks and used in the treatment of e.g. nocturnal leg cramps. The effects of an oral overdose may impair vision and can cause death by cardiotoxicity (Langford et al., 2003). The smallest reported dose is 1.5 g per oral in an adult and 900 mg in a child (Winek et al., 1974). To our knowledge, dermal and inhalation data in humans and birds are not available.
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Quinine solutions are described by humans as bitter (Glendinning, 1994) and are odourless and colourless. Magnesium chloride, likewise odourless and colourless, is described by humans primarily as bitter-tasting with additional sensations in decreasing order of salty, metallic, astringent, sour and sweet (Lawless et al., 2003). The characteristic almond odour of almond oil acts as a discriminative stimulus for flavour-avoidance learning in domestic chicks (Roper and Marples, 1997). Garlic and clove oils, with their major active compounds allicin and eugenol, both act as irritants (Clark and Shivik, 2002; Salazar et al., 2008). The anti-peck spray can, though subjectively, be described as similar in odour, colour and taste to black tar. “Angostura Bitter” is a food and beverage flavouring. It is composed of natural herbs and spices including roots of gentian, bitter orange, cloves, cardamom, cinnamon and chinchona bark. The exact recipe is a trade secret. White feathers soaked in anti-peck spray turned dark, whereas feathers soaked in angostura turned light brown. Concentrations as referenced in the literature to produce aversion in birds (Engelmann, 1934; Gittleman et al., 1980; Mason and Linz, 1997; Roper and Marples, 1997) were chosen. In the case of quinine, concentrations lower than 2% and 4% were tested for effectiveness. 2.3. Behavioural tests One hundred and twenty laying hens were divided into 12 groups of 10 birds each. Each group received a different kind of feather treatment. Birds were daily presented with 10 feathers soaked in one of the following treatments for 10 consecutive days. The feathers were coated with one of the following substances: 1% garlic, 1% almond oil, 1% clove oil, 1% clove, 0.1%, 1%, 2%, 4% quinine sulphate, 0.6 mol magnesium chloride solution, anti-peck spray, angostura. The control group received uncoated feathers. Feathers were inserted into a transparent piece of stiff plastic (10 cm × 8 cm), which was fixed next to the food every morning (10:00 h). The number of feathers found on the cage floors, in the feed troughs and in the drop pans (=rejected feathers) was counted 60 min after presenting the feathers. The number of feathers eaten was calculated by subtracting the sum of the feathers found (rejected feathers) by the number of feathers presented. The drop pans were cleaned before presenting the feathers. 2.4. Ethical note The use of all animals and methods in this study was approved by the University of Hohenheim Animal Care Committee. 2.5. Statistical analysis An ANOVA model was fitted using PROC GLIMMIX of the SAS System (Version 9.1.3, SAS Institute Inc., Cary, NC, USA) to analyze the number of feathers pulled out, rejected and eaten as a repeated measurement (Piepho et al., 2004). The models included the following fixed factors: ‘flavoured feathers’ (1% garlic, 1% almond oil, 1% clove oil, 1% clove, 0.1%, 1%, 2%, 4% quinine sulphate, 0.6 mol magnesium chlo-
ride, anti-peck, angostura, unflavoured) and ‘day’ (10 days). A random effect was modelled by combining the repeated factor ‘day’ with the random effect ‘animal’. The covariance was modelled by the compound symmetry structure (type = CS). The data were analyzed by a logit link and the binomial variance function. The degrees of freedom were adjusted using the Kenward–Roger method (Kenward and Roger, 1997). Differences for least square means were tested using t-tests. Data are presented as mean ± standard error. 3. Results The average number (±SE) of feathers plucked, rejected and eaten (overall) was 3.49 ± 0.47, 1.17 ± 0.18 and 2.33 ± 0.30, respectively. There was a significant difference in the number of feathers plucked between the different treatments (F11,1179 = 24.35, p < 0.0001, Fig. 1). A rank ordering (from most to least) using the number of feathers plucked gives a sequence of uncoated, clove, clove oil, garlic, angostura, anti-peck, 1% quinine, 0.1% quinine, almond, magnesium chloride, 2% quinine and 4% quinine. Differences of least square means showed that a significantly higher number of uncoated feathers was plucked than feathers coated with clove (t1134 = 3.88, p < 0.0001), clove oil (t1069 = 5.79, p < 0.0001), garlic (t1147 = −6.32, p < 0.0001), angostura (t1158 = 7.14, p < 0.0001), anti-peck (t1126 = 7.72, p < 0.0001), 1% quinine (t1167 = −8.25, p < 0.0001), 0.1% quinine (t1179 = −8.53, p < 0.0001), almond (t1179 = −8.88, p < 0.0001), magnesium chloride (t1179 = −8.87, p < 0.0001), 2% quinine (t1179 = −12.08, p < 0.0001) and 4% quinine (t1179 = −12.23, p < 0.0001). The number of plucked feathers coated with 2% quinine and 4% quinine did not differ from each other. Differences of least square means showed a higher number of magnesium chloride coated feathers plucked than 2% quinine (t1179 = −4.05, p < 0.0001) and 4% quinine (t1179 = 5.00, p < 0.0001). The number of magnesium chloride coated feathers did not differ from the number of almond, 0.1% quinine, 1% quinine and anti-peck coated feathers plucked. There was a significant difference in the number of coated feathers rejected (F11,1179 = 22.13, p < 0.0001, Fig. 1). A rank ordering (from most to least) using the number of rejected feathers gives a sequence of clove oil, anti-peck, clove, unflavoured, angostura, garlic, almond, 1% quinine, 0.1% quinine, magnesium chloride, 2% quinine and 4% quinine. Differences of least square means showed that the number of uncoated feathers rejected was not significantly different from the number of rejected feathers coated with clove oil, anti-peck or clove solution. However, differences of least square means showed that significantly more uncoated feathers were rejected than feathers soaked in angostura (t880 = 2.63, p < 0.0089), garlic (t968 = −3.83, p < 0.0001), almond (t1179 = −2.73, p < 0.0065), 1% quinine (t1183 = −5.53, p < 0.0001), 0.1% quinine (t1179 = −6.42, p < 0.0001), magnesium chloride (t1179 = −7.19, p < 0.0001), 2% quinine (t1179 = −7.32, p < 0.0001), and 4% quinine (t1179 = −7.31, p < 0.0001). There was no significant difference in the number of magnesium chloride, 2% quinine and 4% quinine coated feathers rejected.
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8 7 6 5 4 3 2 1 0
uncoated E R P clove E R P clove oil E R P garlic E R P angostura E R P anti-peck E R P quinine 1% R P quinine 0.1% R P almond oil E R P MgCl2 E R P quinine 2% R P quinine 4% R P
mean number of eaten/rejected/plucked feathers
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Fig. 1. Mean number + SE of coated and uncoated feathers eaten (E), rejected (R) and plucked (P) in a rank order from most to least plucked over a period of 10 days.
There was a significant difference in the number of coated feathers eaten (F11,1179 = 19.02, p < 0.0001, Fig. 1). A rank ordering (from most to least) using the number of feathers eaten gives a sequence of uncoated, clove, garlic, clove oil, 1% quinine, magnesium chloride, 0.1% quinine, angostura, almond, anti-peck, 2% quinine, 4% quinine. Differences of least square means showed that significantly more uncoated feathers were eaten than clove (t841 = 3.78, p < 0.0002), garlic (t893 = −4.59, p < 0.0001), clove oil (t881 = 6.31, p < 0.0001), 1% quinine (t940 = −6.16, p < 0.0001), magnesium chloride (t996 = −6.29, p < 0.0001), 0.1% quinine (t1005 = −6.29, p < 0.0001), angostura (t1179 = −2.65, p < 0.008), almond (t1015 = −7.17, p < 0.0001), anti-peck (t1100 = 9.12, p < 0.0001), 2% quinine (t1179 = −10.38, p < 0.0001) and 4% quinine (t1179 = −10.38, p < 0.0001). The numbers of 2% quinine and 4% quinine coated feathers eaten did not differ from each other. However, differences of least square means showed a higher number of feathers sprayed with anti-peck eaten than with 2% quinine (t1179 = −2.23, p < 0.0261) and 4% quinine (t1179 = −3.21, p < 0.0014) treated. A lower number of anti-peck than almond coated feathers were eaten (t1179 = −2.09, p < 0.0366). The number of coated feathers plucked, rejected or eaten was not affected by ‘day’. 4. Discussion Our experiment showed that laying hens discriminated between uncoated and coated feathers. All treatments decreased palatability of feathers due to a lower number of feathers plucked and eaten. However, we found clear differences in the effectiveness of treatments. Quinine concentrations of 2% and 4% were most effective in lowering the number of feathers plucked and eaten compared to other quinine concentrations and treatments. All substances and concentrations used in the present study reduced plucking and consumption of coated feath-
ers relative to uncoated feathers. This result refers to the ability of the bird to recognize sensory signals and to discriminate between palatable and unpalatable feathers. Our results are consistent with experiments where 1% garlic oil coated food (Mason and Linz, 1997), 0.6 mol magnesium chloride solution (Engelmann, 1934), bitter almond oil odour (Roper and Marples, 1997), 2% (Skelhorn and Rowe, 2005) and 4% quinine coated food (Skelhorn and Rowe, 2006) deterred species from consumption. This finding is remarkable. It may mean that the water-impermeable feather did retain chemicals we used in the present experiment on its surface, but, probably in a lower intensity as when added to drinking water. Except in 2% and 4% quinine treatment, feather plucking and consumption was not completely eliminated. Quinine is a natural alkaloid with potential toxic properties which produces nausea in birds (Alcock, 1970). Although it is not possible to determine how laying hens perceive quinine, birds found it aversive at concentrations of 2% and 4%. The mechanism behind this aversion may be via taste buds in the oral cavity which detect and avoid natural bitter alkaloids or by negative gastrointestinal or emetic consequences. The second consideration leads to stronger and longer lasting aversive conditioning (Garcia and Hankins, 1975). The other chemicals used in the present experiment did not promote an avoidance reaction as strong or durable as that achieved with 2% and 4% quinine. Chemicals acting externally or peripherally are less effective because peripheral discomfort does not form strong aversions (Werner and Clark, 2003). It could be considered that the other chemicals of the present study acted via visual cues, odour, irritation (irritating compounds cause sensory pain), taste or their interactions, which did not produce a strong or lasting avoidance. This consideration may explain the continued cycle of feather eating in feathers coated with chemicals other than 2% and 4% quinine. Feathers coated with 2% and 4% quinine were avoided most. Both quinine concentrations were similarly effec-
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tive. Lower concentrations (0.1%, 1%) of quinine were not as effective. It could be suggested that concentrations of 2% and 4% quinine ingested acted as positive punishment. Birds suffered from its noxious effects and formed a stronger association between the quinine and the bitter taste at these concentrations and used the taste to avoid pulling out the feathers of the plastic model. However, it is possible that 2% and 4% quinine was extremely distasteful (bitter) and therefore prevented ingestion of feathers. The number of feathers coated with 0.6 mol magnesium chloride, 1% almond oil, 0.1% quinine, 1% quinine, anti-peck and angostura which were plucked did not differ from each other. One percent garlic, 1% clove and 1% clove oil coated feathers were less effective than the chemicals mentioned before. In nature, many prey species combine chemical defence mechanisms with other cues (bad taste, bad smell, bright colour). This presumably evolved because this offers better protection than single modes of defence (Avery, 1985). Chemical agents such as garlic, clove and almond have different active ingredients which probably activate smell, irritation or taste and which are not mutually exclusive. The addition of visual cues such as the darker colours in the anti-peck and “Angostura Bitter” treatments, exhibited an additional visual cue. However, they were not as effective as 2% and 4% quinine coated feathers. When feathers were plucked, a higher number of feathers were eaten than rejected, irrespective of the chemical treatment. This was not the case in anti-peck coated feathers. Birds plucked the anti-peck coated feathers, but reduced their consumption, indicating that they do not want to experience the effect, whichever that may be, after ingesting such feathers. For a potential victim it does not matter if the feather is rejected or eaten, the feather is pulled out of the skin. This may indicate that the antipeck spray was not an effective agent to inhibit feather manipulation (picking, grasping, pulling, plucking) in the experimental setting. However, the high number of feathers eaten in the other treatments suggests that gustatory factors play a role in the consumption of feathers in the present experiment. It could, however, be argued that laying hens were kept individually and were bored. When white synthetic string devices were offered to individually caged hens, these devices were pecked at and manipulated, but remained in place and were not eaten (unpublished data). Our study showed that all chemical agents significantly decreased the number of feathers plucked and eaten. The 2% and 4% quinine treatment eliminated feather plucking and consumption completely, whereas the other treatments had a lesser effect. In the current study we used high feather-pecking birds selected on high feather-pecking activity over 10 generations. It would be interesting to test if the chemical agents used in this experiment would be more successful in deterring hens from feather plucking, when commercial breeds with a lower motivation to peck at feathers would be tested. Importantly, spraying feathers with an aversive agent is a management tool which may raise concerns. The practice ignores the underlying motivation of the birds and does not address the decrease in the feather peckers welfare if severe feather pecking has beneficial consequences for the
pecker (e.g. gastro-intestinal benefits due to increasing gut motility via ingested feathers). However, a recent epidemiological study in the UK showed that 68.5% of laying hen flocks at 25 weeks of age and 85.6% of laying hen flocks at 40 weeks of age showed severe feather pecking and plumage damage (Lambton et al., 2010). The authors recommend greatest weight should be given to improve environmental rearing and laying conditions (e.g. beneficial and appropriate foraging material) to decrease the problem of feather pecking. However, when management attempts fail, spraying with an aversive agent could be a solution during laying (Harlander-Matauschek et al., 2010). So, aversive chemicals are best considered a part of integrated strategies to reduce severe feather pecking in problem flocks. In practice, efforts to develop an aversive spraying solution might focus on natural products or food additives which are less toxic and environmentally safer, as the development of such tools will be monitored by health, food, veterinary and environmental agencies. However, long-term and strong avoidance will come only from such chemicals that produce adverse physiological effects (chemicals acting internally may have the best chance). Therefore efforts should be undertaken to develop spraying devices, where the addition of cues could permit reduction in the rate of harmful substances without losses in effectiveness. Acknowledgements We are grateful to Carmen Ostertag for her invaluable help preparing the chemical solutions, to Joergen Kjaer, who selected the ancestors of the birds used for the present experiment and to Chris Baes for her invaluable help to improve the English text. References Alcock, J., 1970. Punishment levels and the response of black-capped chickadees (Parus atricapillus) to three kinds of artificial seeds. Anim. Behav. 18, 592–599. Avery, M.L., 1985. Repellents: integrating sensory modalities. In: Mason, J.R. (Ed.), Proceedings of the Second DWRC Special Symposium. Denver, CO, August 8–10, pp. 2–17. Bilcik, B., Bessei, W., 1993. Feather pecking in Japanese Quail—comparison of six different lines. In: Nichelmann, M., Wierenga, H.K., Braun, S. (Eds.), Proc. Intern. Congress Appl. Ethol., 3. Joint Meeting. Berlin, Germany, pp. 291–293. Blokhuis, H.J., 1986. Feather pecking in poultry: its relation with groundpecking. Appl. Anim. Behav. Sci. 16, 63–67. Blokhuis, H.J., Fiks-Van Niekerk, T., Bessei, W., Elson, A., Guemene, D., Kjaer, J., Maria Levrino, G.A., Nicol, C.J., Tauson, R., Weeks, C.A., Van de Weerd, H.A., 2007. The LayWel project: welfare implications of changes in production systems for laying hens. World Poult. Sci. J. 63, 101–114. Busayi, R.M., Channing, C.E., Hocking, P.M., 2006. Comparisons of damaging feather pecking and time budgets in male and female turkeys of a traditional breed and a genetically selected male line. Appl. Anim. Behav. Sci. 96, 281–292. Eisner, T., Meinwald, J., 1966. Defensive secretion of arthropods. Science 153, 1341–1350. Clark, L., Mason, J.R., 1987. Olfactory discrimination of plant volatiles by the European starling. Anim. Behav. 35, 227–235. Clark, L., Shivik, J., 2002. Aerosolized essential oils and individual natural product compounds as brown treesnake repellents. Pest Manag. Sci. 58, 775–783. Engelmann, C., 1934. Versuche über den Geschmackssinn von Taube, Ente und Huhn. Z. Vergl. Physiol. 20, 626–645.
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Applying chemical stimuli on feathers to reduce feather pecking in laying hens Alexandra Harlander-Matauschek a,∗ , T. Bas Rodenburg b a b
Department of Small Animal Breeding and Poultry Science, University of Hohenheim, 470c, 70599 Stuttgart, Germany Animal Breeding and Genomics Centre, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands
a r t i c l e
i n f o
Article history: Accepted 3 April 2011 Available online 30 April 2011 Keywords: Feather eating Feather pecking Laying hens Learning Aversion
a b s t r a c t Recent studies have shown that spraying a distasteful substance (quinine) on a bird’s feather cover reduced short-term feather pecking. The present experiment evaluated if other substances offer similar or better protection against feather pecking. One hundred and twenty birds were divided into 12 groups of 10 birds each. Over a period of 10 days the birds’ response to 10 feathers coated with one of the 11 distasteful substances was observed and recorded. Feathers were soaked in a 1% garlic solution, 1% almond oil, 1% clove oil, 1% clove solution, quinine sulphate solution in four concentrations (0.1%, 1%, 2%, 4%), 0.6 mol magnesium chloride solution, anti-peck spray or an angostura solution. The control group received uncoated feathers. The number of feathers plucked, rejected or eaten was counted 60 min after presenting the feathers. All substances reduced feather plucking (p < 0.0001) and consumption (p < 0.0001) significantly, compared to uncoated feathers. Quinine concentrations of 2% and 4% were most effective. This study was the first to investigate the aversive potential of different substances to deter feather peckers from the feathers of other birds. The findings may be useful in the development of spraying devices to prevent feather pecking when other management tools fail. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Feather pecking is a very prominent unsolved problem in poultry worldwide. It can occur in many species including domestic hens (Blokhuis et al., 2007), turkeys (Busayi et al., 2006), ducks (Gustafson et al., 2007), pheasants (Kjaer, 2004) and quails (Bilcik and Bessei, 1993). It is particularly a problem in loose housing systems, where active feather-pecking birds have access to a large number of victims (Keeling, 1995). Pecked laying hens with bad plumage condition loose more heat and consume more feed than unpecked hens (Herremans et al., 1989), and potential customers may be deterred from buying eggs due to the unappetizing appearance of pecked birds. Aside
∗ Corresponding author at: Animal Welfare and Ethology, University of Giessen, Germany. Tel.: +49 6419938747; fax: +49 6419938759. E-mail addresses: [email protected], [email protected] (A. Harlander-Matauschek). 0168-1591/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2011.04.004
from the economical aspects, feather pecking is a welfare concern. Feather removal is painful for the victim (Gentle and Hunter, 1991). Wounds resulting from feather removal may bleed and eventually lead to cannibalism, which can result in mortality rates of 20% and higher in laying hens (Blokhuis et al., 2007). It is generally assumed that feather pecking is redirected behaviour with an underlying unfulfilled motivation either to forage (Blokhuis, 1986) or to dust-bath (Vestergaard and Lisborg, 1993), however, evidence for the latter is more controversial. Additionally, feather pecking in laying hens may indicate that the bird is performing this behaviour due to an unfulfilled behavioural need (Weeks and Nicol, 2006). Although a variety of risk factors affecting the development of feather pecking have been identified (e.g. Lambton et al., 2010), remedies for this behaviour are still needed. In practice, birds like laying hens, turkeys, Muscovy ducks and pheasants are often routinely beak-trimmed to prevent feather pecking and cannibalism. Beak trimming is criticized due to acute and
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chronic pain and due to the removal of sensory receptors and free nerve endings in the bill tip (Gentle et al., 1997), but is used as the lesser of two evils. In spite of the unsolved feather pecking problem, beak trimming will be banned in laying hens in many European countries in the near future (Van Horne and Achterbosch, 2008). Along with vision, audition and touch, chemosensory cues are involved in the foraging decisions of birds (Werner and Clark, 2003). It is widely accepted that gustatory sensation (Skelhorn and Rowe, 2006), olfaction (Roper and Marples, 1997) and irritation (Gentle and Hill, 1987) compose the chemical senses of birds. Many insects and plants secrete chemosensory cues when they are attacked by predators (Eisner and Meinwald, 1966). Many toxins commonly used in defence mechanisms by invertebrates and plants taste bitter to deter predators. Pecking at bittertasting objects evokes disgust responses from the bird and it will avoid pecking at similar objects (e.g. Hogan, 1973). Odour perception in birds is mediated by olfaction and nasal trigeminal chemoreception (Mason and Silver, 1983). The former is described as the sense of smell, the latter is part of the common chemical senses, a system designed to protect birds from the harmful effects of irritants. Stimulation of trigeminal chemoreceptors may serve as a cue for avoidance (Jakubas and Mason, 1991). Additionally, olfactory cues may serve as conditional stimuli to which learned food aversions can be formed when paired in the presence of toxicants or irritants (Clark and Mason, 1987). Previous studies have shown that feather pecking is positively associated with feather ingestion (McKeegan and Savory, 1999, 2001), meaning that feathers are part of the diet in severely feather-pecking birds (HarlanderMatauschek and Häusler, 2009). In different species quinine is widely used as an aversive substance in learning experiments (e.g. Alcock, 1970). Harlander-Matauschek et al. (2008) showed that laying hens learned to avoid eating loose feathers when they had been soaked in a bitter-tasting quinine solution. Additionally, when the feather cover of adult laying hens was sprayed with the bitter-tasting quinine, the birds learned that feathers from conspecifics were not attractive to peck at for a period of time (Harlander-Matauschek et al., 2009). The present experiment was conducted to identify nonharmful substances suitable for humans and birds which can be used to keep feather peckers away from the plumage of other birds. We investigated the consumption of feathers coated with solutions of natural products (garlic, almond, clove) different concentrations of quinine, magnesium chloride, commercial anti-peck spray and “Angostura Bitter”. Coating treatments were not combined. For ethical and scientific reasons we used a piece of plastic with feathers attached as a model. We used laying hens at the end of their laying period to test which substances most effectively deterred hens from eating feathers. 2. Methods 2.1. Animals and housing One hundred and twenty birds from a high featherpecking selection line were used. The beaks of the hens
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were not trimmed. The birds in the present study originated from a selection experiment (Kjaer et al., 2001) in which birds were divergently selected on high and low feather pecking activity for six generations. The birds of the present experiment were the fourth generation after selection from Kjaer et al. (2001). Birds were reared and kept in a deep litter system prior to the experiment. At 62 weeks of age birds were transferred to individual cages measuring 43 cm × 43 cm × 45 cm (length × width × height). The feed trough was placed at the front and a nipple drinker at the back of the cage. Each cage was supplemented with a perch of 20 cm length. The cages were separated by nontransparent boards so that the birds had no physical or visual contact with their neighbours. The hens were kept in a ventilated windowless room at a constant temperature (20 ◦ C). Lights were on from 0400 until 1800 h. The Hohenheim University mash layer ration (17.2% CP, 11.1 MJ/kg) and water were provided ad libitum. The test phase started after 1 week of adaptation to the experimental situation. 2.2. Preparation of coated feathers Feathers were plucked from dead birds of the high feather-pecking selection line (Kjaer et al., 2001), put in 60 l plastic bags and stored in a refrigerator for hygienic reasons. To reduce the palatability of the feathers, 100 g of feathers was soaked in 1000 ml 1% garlic solution (granulated, Kotanyi GmbH, Austria), 1% almond oil (Sigma–Aldrich Chemie, Germany), 1% clove oil (Sigma–Aldrich Chemie, Germany), 1% clove solution (grounded, Kotanyi GmbH, Austria), 0.1%, 1%, 2%, 4% quinine sulphate solution (Acros Organics BVBA, Geel, Belgium), 0.6 mol magnesium chloride (Sigma–Aldrich Chemie, Germany) solution in 1000 ml pure anti-peck spray (FED-PICK, FP 48 Sprühlösung, Dr. Hesse Tierpharma GmbH & CoKG, Germany) or in pure “Angostura Bitter” (Hemmeter, Germany) for 12 h. We then allowed feathers to dry for 12 h. Because almond and clove oil do not readily mix with water, they were first diluted in ethanol (1:2) to prepare a solution. To produce a quinine solution, quinine sulphate dihydrate was weighed and diluted with aqua bidestillata. Some drops of sulphuric acid were pipetted to dissolve all the quinine by swirling thoroughly. Aliquots of the stock solutions were used to achieve the experimental concentrations. Because quinine solutions are used successfully as aversive substances in learning experiments in birds and other species (e.g. Alcock, 1970; Skelhorn and Rowe, 2006), we assumed that quinine solutions would be more effective (produce rapid and stable avoidance) than other solutions. However, quinine agents have side effects (Langford et al., 2003), so we wanted to find the lowest effective concentration with the highest avoidance reaction. In humans, quinine is commonly added to soft drinks and used in the treatment of e.g. nocturnal leg cramps. The effects of an oral overdose may impair vision and can cause death by cardiotoxicity (Langford et al., 2003). The smallest reported dose is 1.5 g per oral in an adult and 900 mg in a child (Winek et al., 1974). To our knowledge, dermal and inhalation data in humans and birds are not available.
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Quinine solutions are described by humans as bitter (Glendinning, 1994) and are odourless and colourless. Magnesium chloride, likewise odourless and colourless, is described by humans primarily as bitter-tasting with additional sensations in decreasing order of salty, metallic, astringent, sour and sweet (Lawless et al., 2003). The characteristic almond odour of almond oil acts as a discriminative stimulus for flavour-avoidance learning in domestic chicks (Roper and Marples, 1997). Garlic and clove oils, with their major active compounds allicin and eugenol, both act as irritants (Clark and Shivik, 2002; Salazar et al., 2008). The anti-peck spray can, though subjectively, be described as similar in odour, colour and taste to black tar. “Angostura Bitter” is a food and beverage flavouring. It is composed of natural herbs and spices including roots of gentian, bitter orange, cloves, cardamom, cinnamon and chinchona bark. The exact recipe is a trade secret. White feathers soaked in anti-peck spray turned dark, whereas feathers soaked in angostura turned light brown. Concentrations as referenced in the literature to produce aversion in birds (Engelmann, 1934; Gittleman et al., 1980; Mason and Linz, 1997; Roper and Marples, 1997) were chosen. In the case of quinine, concentrations lower than 2% and 4% were tested for effectiveness. 2.3. Behavioural tests One hundred and twenty laying hens were divided into 12 groups of 10 birds each. Each group received a different kind of feather treatment. Birds were daily presented with 10 feathers soaked in one of the following treatments for 10 consecutive days. The feathers were coated with one of the following substances: 1% garlic, 1% almond oil, 1% clove oil, 1% clove, 0.1%, 1%, 2%, 4% quinine sulphate, 0.6 mol magnesium chloride solution, anti-peck spray, angostura. The control group received uncoated feathers. Feathers were inserted into a transparent piece of stiff plastic (10 cm × 8 cm), which was fixed next to the food every morning (10:00 h). The number of feathers found on the cage floors, in the feed troughs and in the drop pans (=rejected feathers) was counted 60 min after presenting the feathers. The number of feathers eaten was calculated by subtracting the sum of the feathers found (rejected feathers) by the number of feathers presented. The drop pans were cleaned before presenting the feathers. 2.4. Ethical note The use of all animals and methods in this study was approved by the University of Hohenheim Animal Care Committee. 2.5. Statistical analysis An ANOVA model was fitted using PROC GLIMMIX of the SAS System (Version 9.1.3, SAS Institute Inc., Cary, NC, USA) to analyze the number of feathers pulled out, rejected and eaten as a repeated measurement (Piepho et al., 2004). The models included the following fixed factors: ‘flavoured feathers’ (1% garlic, 1% almond oil, 1% clove oil, 1% clove, 0.1%, 1%, 2%, 4% quinine sulphate, 0.6 mol magnesium chlo-
ride, anti-peck, angostura, unflavoured) and ‘day’ (10 days). A random effect was modelled by combining the repeated factor ‘day’ with the random effect ‘animal’. The covariance was modelled by the compound symmetry structure (type = CS). The data were analyzed by a logit link and the binomial variance function. The degrees of freedom were adjusted using the Kenward–Roger method (Kenward and Roger, 1997). Differences for least square means were tested using t-tests. Data are presented as mean ± standard error. 3. Results The average number (±SE) of feathers plucked, rejected and eaten (overall) was 3.49 ± 0.47, 1.17 ± 0.18 and 2.33 ± 0.30, respectively. There was a significant difference in the number of feathers plucked between the different treatments (F11,1179 = 24.35, p < 0.0001, Fig. 1). A rank ordering (from most to least) using the number of feathers plucked gives a sequence of uncoated, clove, clove oil, garlic, angostura, anti-peck, 1% quinine, 0.1% quinine, almond, magnesium chloride, 2% quinine and 4% quinine. Differences of least square means showed that a significantly higher number of uncoated feathers was plucked than feathers coated with clove (t1134 = 3.88, p < 0.0001), clove oil (t1069 = 5.79, p < 0.0001), garlic (t1147 = −6.32, p < 0.0001), angostura (t1158 = 7.14, p < 0.0001), anti-peck (t1126 = 7.72, p < 0.0001), 1% quinine (t1167 = −8.25, p < 0.0001), 0.1% quinine (t1179 = −8.53, p < 0.0001), almond (t1179 = −8.88, p < 0.0001), magnesium chloride (t1179 = −8.87, p < 0.0001), 2% quinine (t1179 = −12.08, p < 0.0001) and 4% quinine (t1179 = −12.23, p < 0.0001). The number of plucked feathers coated with 2% quinine and 4% quinine did not differ from each other. Differences of least square means showed a higher number of magnesium chloride coated feathers plucked than 2% quinine (t1179 = −4.05, p < 0.0001) and 4% quinine (t1179 = 5.00, p < 0.0001). The number of magnesium chloride coated feathers did not differ from the number of almond, 0.1% quinine, 1% quinine and anti-peck coated feathers plucked. There was a significant difference in the number of coated feathers rejected (F11,1179 = 22.13, p < 0.0001, Fig. 1). A rank ordering (from most to least) using the number of rejected feathers gives a sequence of clove oil, anti-peck, clove, unflavoured, angostura, garlic, almond, 1% quinine, 0.1% quinine, magnesium chloride, 2% quinine and 4% quinine. Differences of least square means showed that the number of uncoated feathers rejected was not significantly different from the number of rejected feathers coated with clove oil, anti-peck or clove solution. However, differences of least square means showed that significantly more uncoated feathers were rejected than feathers soaked in angostura (t880 = 2.63, p < 0.0089), garlic (t968 = −3.83, p < 0.0001), almond (t1179 = −2.73, p < 0.0065), 1% quinine (t1183 = −5.53, p < 0.0001), 0.1% quinine (t1179 = −6.42, p < 0.0001), magnesium chloride (t1179 = −7.19, p < 0.0001), 2% quinine (t1179 = −7.32, p < 0.0001), and 4% quinine (t1179 = −7.31, p < 0.0001). There was no significant difference in the number of magnesium chloride, 2% quinine and 4% quinine coated feathers rejected.
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8 7 6 5 4 3 2 1 0
uncoated E R P clove E R P clove oil E R P garlic E R P angostura E R P anti-peck E R P quinine 1% R P quinine 0.1% R P almond oil E R P MgCl2 E R P quinine 2% R P quinine 4% R P
mean number of eaten/rejected/plucked feathers
9
Fig. 1. Mean number + SE of coated and uncoated feathers eaten (E), rejected (R) and plucked (P) in a rank order from most to least plucked over a period of 10 days.
There was a significant difference in the number of coated feathers eaten (F11,1179 = 19.02, p < 0.0001, Fig. 1). A rank ordering (from most to least) using the number of feathers eaten gives a sequence of uncoated, clove, garlic, clove oil, 1% quinine, magnesium chloride, 0.1% quinine, angostura, almond, anti-peck, 2% quinine, 4% quinine. Differences of least square means showed that significantly more uncoated feathers were eaten than clove (t841 = 3.78, p < 0.0002), garlic (t893 = −4.59, p < 0.0001), clove oil (t881 = 6.31, p < 0.0001), 1% quinine (t940 = −6.16, p < 0.0001), magnesium chloride (t996 = −6.29, p < 0.0001), 0.1% quinine (t1005 = −6.29, p < 0.0001), angostura (t1179 = −2.65, p < 0.008), almond (t1015 = −7.17, p < 0.0001), anti-peck (t1100 = 9.12, p < 0.0001), 2% quinine (t1179 = −10.38, p < 0.0001) and 4% quinine (t1179 = −10.38, p < 0.0001). The numbers of 2% quinine and 4% quinine coated feathers eaten did not differ from each other. However, differences of least square means showed a higher number of feathers sprayed with anti-peck eaten than with 2% quinine (t1179 = −2.23, p < 0.0261) and 4% quinine (t1179 = −3.21, p < 0.0014) treated. A lower number of anti-peck than almond coated feathers were eaten (t1179 = −2.09, p < 0.0366). The number of coated feathers plucked, rejected or eaten was not affected by ‘day’. 4. Discussion Our experiment showed that laying hens discriminated between uncoated and coated feathers. All treatments decreased palatability of feathers due to a lower number of feathers plucked and eaten. However, we found clear differences in the effectiveness of treatments. Quinine concentrations of 2% and 4% were most effective in lowering the number of feathers plucked and eaten compared to other quinine concentrations and treatments. All substances and concentrations used in the present study reduced plucking and consumption of coated feath-
ers relative to uncoated feathers. This result refers to the ability of the bird to recognize sensory signals and to discriminate between palatable and unpalatable feathers. Our results are consistent with experiments where 1% garlic oil coated food (Mason and Linz, 1997), 0.6 mol magnesium chloride solution (Engelmann, 1934), bitter almond oil odour (Roper and Marples, 1997), 2% (Skelhorn and Rowe, 2005) and 4% quinine coated food (Skelhorn and Rowe, 2006) deterred species from consumption. This finding is remarkable. It may mean that the water-impermeable feather did retain chemicals we used in the present experiment on its surface, but, probably in a lower intensity as when added to drinking water. Except in 2% and 4% quinine treatment, feather plucking and consumption was not completely eliminated. Quinine is a natural alkaloid with potential toxic properties which produces nausea in birds (Alcock, 1970). Although it is not possible to determine how laying hens perceive quinine, birds found it aversive at concentrations of 2% and 4%. The mechanism behind this aversion may be via taste buds in the oral cavity which detect and avoid natural bitter alkaloids or by negative gastrointestinal or emetic consequences. The second consideration leads to stronger and longer lasting aversive conditioning (Garcia and Hankins, 1975). The other chemicals used in the present experiment did not promote an avoidance reaction as strong or durable as that achieved with 2% and 4% quinine. Chemicals acting externally or peripherally are less effective because peripheral discomfort does not form strong aversions (Werner and Clark, 2003). It could be considered that the other chemicals of the present study acted via visual cues, odour, irritation (irritating compounds cause sensory pain), taste or their interactions, which did not produce a strong or lasting avoidance. This consideration may explain the continued cycle of feather eating in feathers coated with chemicals other than 2% and 4% quinine. Feathers coated with 2% and 4% quinine were avoided most. Both quinine concentrations were similarly effec-
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tive. Lower concentrations (0.1%, 1%) of quinine were not as effective. It could be suggested that concentrations of 2% and 4% quinine ingested acted as positive punishment. Birds suffered from its noxious effects and formed a stronger association between the quinine and the bitter taste at these concentrations and used the taste to avoid pulling out the feathers of the plastic model. However, it is possible that 2% and 4% quinine was extremely distasteful (bitter) and therefore prevented ingestion of feathers. The number of feathers coated with 0.6 mol magnesium chloride, 1% almond oil, 0.1% quinine, 1% quinine, anti-peck and angostura which were plucked did not differ from each other. One percent garlic, 1% clove and 1% clove oil coated feathers were less effective than the chemicals mentioned before. In nature, many prey species combine chemical defence mechanisms with other cues (bad taste, bad smell, bright colour). This presumably evolved because this offers better protection than single modes of defence (Avery, 1985). Chemical agents such as garlic, clove and almond have different active ingredients which probably activate smell, irritation or taste and which are not mutually exclusive. The addition of visual cues such as the darker colours in the anti-peck and “Angostura Bitter” treatments, exhibited an additional visual cue. However, they were not as effective as 2% and 4% quinine coated feathers. When feathers were plucked, a higher number of feathers were eaten than rejected, irrespective of the chemical treatment. This was not the case in anti-peck coated feathers. Birds plucked the anti-peck coated feathers, but reduced their consumption, indicating that they do not want to experience the effect, whichever that may be, after ingesting such feathers. For a potential victim it does not matter if the feather is rejected or eaten, the feather is pulled out of the skin. This may indicate that the antipeck spray was not an effective agent to inhibit feather manipulation (picking, grasping, pulling, plucking) in the experimental setting. However, the high number of feathers eaten in the other treatments suggests that gustatory factors play a role in the consumption of feathers in the present experiment. It could, however, be argued that laying hens were kept individually and were bored. When white synthetic string devices were offered to individually caged hens, these devices were pecked at and manipulated, but remained in place and were not eaten (unpublished data). Our study showed that all chemical agents significantly decreased the number of feathers plucked and eaten. The 2% and 4% quinine treatment eliminated feather plucking and consumption completely, whereas the other treatments had a lesser effect. In the current study we used high feather-pecking birds selected on high feather-pecking activity over 10 generations. It would be interesting to test if the chemical agents used in this experiment would be more successful in deterring hens from feather plucking, when commercial breeds with a lower motivation to peck at feathers would be tested. Importantly, spraying feathers with an aversive agent is a management tool which may raise concerns. The practice ignores the underlying motivation of the birds and does not address the decrease in the feather peckers welfare if severe feather pecking has beneficial consequences for the
pecker (e.g. gastro-intestinal benefits due to increasing gut motility via ingested feathers). However, a recent epidemiological study in the UK showed that 68.5% of laying hen flocks at 25 weeks of age and 85.6% of laying hen flocks at 40 weeks of age showed severe feather pecking and plumage damage (Lambton et al., 2010). The authors recommend greatest weight should be given to improve environmental rearing and laying conditions (e.g. beneficial and appropriate foraging material) to decrease the problem of feather pecking. However, when management attempts fail, spraying with an aversive agent could be a solution during laying (Harlander-Matauschek et al., 2010). So, aversive chemicals are best considered a part of integrated strategies to reduce severe feather pecking in problem flocks. In practice, efforts to develop an aversive spraying solution might focus on natural products or food additives which are less toxic and environmentally safer, as the development of such tools will be monitored by health, food, veterinary and environmental agencies. However, long-term and strong avoidance will come only from such chemicals that produce adverse physiological effects (chemicals acting internally may have the best chance). Therefore efforts should be undertaken to develop spraying devices, where the addition of cues could permit reduction in the rate of harmful substances without losses in effectiveness. Acknowledgements We are grateful to Carmen Ostertag for her invaluable help preparing the chemical solutions, to Joergen Kjaer, who selected the ancestors of the birds used for the present experiment and to Chris Baes for her invaluable help to improve the English text. References Alcock, J., 1970. Punishment levels and the response of black-capped chickadees (Parus atricapillus) to three kinds of artificial seeds. Anim. Behav. 18, 592–599. Avery, M.L., 1985. Repellents: integrating sensory modalities. In: Mason, J.R. (Ed.), Proceedings of the Second DWRC Special Symposium. Denver, CO, August 8–10, pp. 2–17. Bilcik, B., Bessei, W., 1993. Feather pecking in Japanese Quail—comparison of six different lines. In: Nichelmann, M., Wierenga, H.K., Braun, S. (Eds.), Proc. Intern. Congress Appl. Ethol., 3. Joint Meeting. Berlin, Germany, pp. 291–293. Blokhuis, H.J., 1986. Feather pecking in poultry: its relation with groundpecking. Appl. Anim. Behav. Sci. 16, 63–67. Blokhuis, H.J., Fiks-Van Niekerk, T., Bessei, W., Elson, A., Guemene, D., Kjaer, J., Maria Levrino, G.A., Nicol, C.J., Tauson, R., Weeks, C.A., Van de Weerd, H.A., 2007. The LayWel project: welfare implications of changes in production systems for laying hens. World Poult. Sci. J. 63, 101–114. Busayi, R.M., Channing, C.E., Hocking, P.M., 2006. Comparisons of damaging feather pecking and time budgets in male and female turkeys of a traditional breed and a genetically selected male line. Appl. Anim. Behav. Sci. 96, 281–292. Eisner, T., Meinwald, J., 1966. Defensive secretion of arthropods. Science 153, 1341–1350. Clark, L., Mason, J.R., 1987. Olfactory discrimination of plant volatiles by the European starling. Anim. Behav. 35, 227–235. Clark, L., Shivik, J., 2002. Aerosolized essential oils and individual natural product compounds as brown treesnake repellents. Pest Manag. Sci. 58, 775–783. Engelmann, C., 1934. Versuche über den Geschmackssinn von Taube, Ente und Huhn. Z. Vergl. Physiol. 20, 626–645.
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