Stereotyped pecking after feeding by restricted-fed fowls is influenced by meal size

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1 Ž. Applied Animal Behaviour Science Stereotyped pecking after feeding by restricted-fed fowls is influenced by meal size C.J. Savory ), J.S. Mann 1 Roslin Institute ( Edinburgh ), Roslin, Midlothian EH25 9PS, UK Accepted 15 October 1998 Abstract Growing broiler breeder chickens, fed routinely according to a programme of chronic food restriction, typically show increased pacing before feeding time and increased drinking and pecking at non-food objects afterwards. Expression of this behaviour is often stereotyped in form. In two experiments at 8 and 14 weeks of age, they were caged individually, provided with two meals per day at 0900 and 1600 h, and tested with 0900 h meals that differed in either size Ž10, 25, 40 g. but not food form Ž pellets., or food form Ž pellets, mash, influencing meal duration. but not size Ž 15 g.. Measurements of behaviour were made from video recordings between 0915 Ž when all feeding had ceased. and 1600 h. As meal size increased, so did the proportion of time spent in stereotyped object pecking after feeding, while time spent standing Ž only. decreased; there were no other significant effects of either meal size or food form on post-feeding behaviour. The observed effect of meal size on object pecking may be a consequence of the weight of food eaten per se, rather than the time taken to eat it; this conclusion is tentative because results of the food form comparison are not unambiguous. Paradoxically, whereas expression of abnormal behaviour in restricted-fed animals is known to be correlated negatively with total daily food intake, it appears to be correlated positively with meal size within a given level of restriction. q 1999 Elsevier Science B.V. All rights reserved. Keywords: Chicken-stereotyped behavior; Object pecking; Meal size; Food form; Feeding and nutrition 1. Introduction In commercial conditions, all parent stock Ž breeders. of meat-type chickens Ž broilers. are fed on quantitatively restricted rations during the growing period in order to limit ) Corresponding author. National Centre for Poultry Studies, SAC, Auchincruive, Ayr KA6 5HW, UK. Tel.: q ; fax: q ; J.Savory@au.sac.ac.uk 1 Present address. Animal Biology Division, SAC, Bush Estate, Penicuik, Midlothian EH26 0PH, UK r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved. Ž. PII: S

2 210 C.J. SaÕory, J.S. MannrApplied Animal BehaÕiour Science body weight at sexual maturity, and thereby improve health and reproductive performance Ž Hocking et al., Birds fed on the recommended rations, which are usually provided once a day and eaten in -10 min, eat only a third as much as they would with free access to food, and are highly motivated to feed at all times Ž Savory et al., They are much more active than ad libitum-fed control birds, and Ž unlike the latter. show increased pacing before feeding time and increased drinking and pecking at non-food objects afterwards. Their expression of these activities varies between individuals, is often stereotyped in form Žinvariable, repetitive, no apparent function, as defined by Odberg Ž , and is correlated positively with the level of food restriction imposed Ž Kostal et al., 1992; Savory and Maros, Similar behavioural responses to chronic food restriction have been reported in pigs ŽRushen, 1985; Appleby and Lawrence, 1987; Jensen, 1988; Terlouw et al., 1991., cattle Ž Redbo, 1990., rats ŽMoskowitz, 1959; Treichler and Hall, and pigeons Ž Palya and Zacny, 1980; Goodman et al., In restricted-fed animals given one or two meals per day, there is evidence that established oral stereotypies are elicited specifically by food consumption. Thus, expression of such activities tends to be minimal before the first meal of the day and maximal immediately after meals, regardless of either time of day or number of meals ŽPalya and Zacny, 1980; Rushen, 1985; Jensen, 1988; Redbo, 1990; Kostal et al., 1992; Terlouw et al., 1993; Savory and Kostal, Exposure of restricted-fed pigs to a loud novel sound had no such effect Ž Terlouw et al., It has been proposed that these stereotypies represent persistence of Ž unfulfilled. foraging behaviour after all food is eaten Ž Lawrence and Terlouw, Feeding activity is presumably stimulated by ingestion of food, and may continue in apparently inappropriate form in the absence of cues normally associated with satiety. This idea is based on a model proposed by Hughes and Duncan Ž 1988., in which an animal s behaviour gets into a closed loop when it does not have appropriate functional consequences, or does not have them soon enough, and when the behaviour itself is a source of positive feedback. In the study of Terlouw et al. Ž with pigs, ingestion of a smaller or larger meal than usual had little effect on levels of post-feeding stereotypies. By contrast, recent work with broiler breeders has indicated that meal size may indeed influence behaviour. In an experiment, restricted-fed birds on a daily ration of 40 g were provided with two meals of unequal size at 0900 and 1200 h, and conditioned to receiving either the large one Ž 32 g. first, the small one Ž 8 g. first, or the meal sizes in random order. The main finding was that stereotyped pecking at the empty feeder declined from the first to the third hour after the small meal, only when it came first, and did not do so after the large meal Ž Savory et al., This suggested that the rate at which pecking declines after eating Ž Kostal et al., 1992; Savory and Maros, 1993; Savory and Kostal, may depend on the amount that is eaten, and that the 3-h observation period that followed each meal was not long enough to detect a decline after the large meal. There appeared to be no effect on stereotyped behaviour that could be attributed specifically to either anticipation of meal size or unexpected change in Ž anticipated. meal size Žcf. Crespi, Two more experiments investigating the influence of meal size on broiler breeder behaviour are reported in this paper. In one, all birds were tested with small, medium and large meals at 0900 h, on different days, and their behaviour recorded over 7 h until

3 C.J. SaÕory, J.S. MannrApplied Animal BehaÕiour Science a second Ž balancer. meal at 1600 h. This confirmed the effect of meal size on stereotyped pecking described above, so in the other experiment a comparison was made between pelleted and mash food, with the same meal size, to see whether the effect could be due to the duration of feeding Žrate of consumption is greater with pellets than mash; Jensen et al., 1962; Savory, 1980., rather than the amount eaten. 2. Materials and methods: general The same 12 immature female broiler breeder chickens ŽRoss 308, Ross Breeders, Midlothian, UK. were used in both experiments. They were kept in a brooder and fed ad libitum on a starter mash diet until 2 weeks of age, and then moved to a pen and fed once a day on Ž 3 mm. starter pellets according to a restricted feeding programme in the Ross 308 Parent Stock Management Manual. At 6 weeks, they were housed individually in a battery consisting of three tiers of four cages, in a light-proof room where lights were on from 0700 to 1900 h and ambient temperature was maintained at 218C. Each cage measured 30=45=41 cm 3 Ž w=d=h. and had solid sides, back and ceiling, and a front with vertical bars through which the bird could feed from a metal feeder and drink Ž ad libitum. from a 1-l plastic container situated adjacently in a large common trough running along the outside of each tier. Birds could see neighbours on the same tier when their heads were out of the cage fronts, but not birds on other tiers. They continued to be given a single daily restricted ration of Ž 3 mm. grower pellets Ž150 grkg crude protein and 11.0 MJrkg metabolisable energy. at 0900 h, when their drinkers were refilled with water. 3. Experiment Methods At 7 weeks of age, after a week in the cages, the birds daily feeding regime was Ž changed from one meal of 50 g ca. 25% of ad libitum daily intake at the same age; Table 1 Mean Ž ns12. proportions Ž %. of time spent in different activities in the 7 h after a meal of either 10, 25 or 40 g at 0900 h, and significance of effects of meal size, time since feeding, and their interaction Žby split plot ANOVA a. Ž. Meal size g Significance of effects Meal size Time Meal size=time Sitting NS NS NS Standing )) ))) NS Preening NS ) NS Object pecking ) ))) NS Drinking NS ))) NS a ANOVAs were done on angular transformed data, and the mean values shown are Ž untransformed. in the observed scale. ))) P ; )) P -0.01; ) P -0.05; NS not significant Ž P )0.05..

4 212 C.J. SaÕory, J.S. MannrApplied Animal BehaÕiour Science Savory et al., to two meals of 25 g, at 0900 and 1600 h. They were tested at 8 weeks, when their daily ration consisted of either a small Ž 10 g., medium Ž 25 g. or large Ž 40 g. meal at 0900 h, and a balancer Ž 40, 25 or 10 g. meal at 1600 h. Their mean body weight then was 0.82"SE 0.01 kg. Every bird was tested with all three meal sizes on consecutive days, according to a balanced design where at least two meal sizes were always represented in each tier. On each of the three test days, all birds ate all their 0900 h meal in -10 min, and their behaviour was recorded on videotape for every alternate 15 min, commencing at 0915 and ending just before the balancer meal at 1600 h. The recording was done remotely with equipment in another room, and involved no disturbance to the birds. From the video recordings, measurements were made in each 15-min period by noting each bird s behaviour every minute from a single on the dot observation ŽSlater, 1978., according to one of five mutually exclusive categories. These were: sitting Ž only.; standing Ž only, with head either inside or outside the cage, including minimal pacing.; preening Ž nearly always while standing.; object pecking Žwhile standing, mainly at the empty feeder but also at parts of the cage.; drinking Žwhile standing, interspersed with, and indistinguishable from, pecking at the water or drinker without drinking; all birds Fig. 1. Mean Ž ns12. proportions of time spent object pecking and drinking in each hour between two meals at 0900 and 1600 h, when the 0900 h meal differed in either size Ž 10, 25, 40 g. but not food form Ž pellets. Ž Experiment 1., or food form Ž pellets, mash. but not size Ž 15 g. Ž Experiment 2..

5 C.J. SaÕory, J.S. MannrApplied Animal BehaÕiour Science produced wet faecal droppings indicating polydipsia Ž Lintern-Moore, The last two activities Ž but not preening. conformed with the usual definition of stereotypy Ž Odberg, Computer software used for this analysis was written by L. Kostal in Turbo Pascal Ž Borland International, USA.. The behaviour data were converted to proportions of time spent in each activity Ž. 5 by each bird Ž 12. in each hour Ž. 7 on each day Ž. 3. They were transformed by angular Ž arcsine root. transform Ž Bartlett, 1947., to give approximately equal variances. For each activity, they were then analysed by split plot ANOVAs, with birds as plots, using orthogonal polynomials to examine effects Ž including linear or quadratic trends. due to treatment Ž meal size., time Ž h. and their interaction Results Following the 0900 h meal, 8-week old restricted-fed chickens spent most time standing, and more time object pecking than drinking, preening or sitting Ž Table 1.. The only significant Ž P effects of meal size were with standing and object pecking, the former decreasing and the latter increasing as meal size increased. All activities except sitting were affected by the time since feeding. Linear declines in object pecking and drinking Ž Fig. 1. were reflected by a linear increase in standing, and time spent preening Ž quadratic trend. was lowest in the first two and last hours of the 7-h test. There was no significant interaction between meal size and time. 4. Experiment Methods After Experiment 1, the birds returned to receiving one meal at 0900 h according to the same restricted feeding programme as before. Then at 14 weeks, when they weighed 1.36"0.02 kg, they were again provided with two meals per day, at 0900 Ž 15 g. and 1600 h Ž 45 g.. The 0900 h meal alternated between being pellets and mash on six consecutive days, half the birds receiving pellets and half receiving mash on each day according to a balanced design, and the 1600 h meal was in pellet form on all days. Both pellets and mash consisted of the same grower diet as before, pellet diameter was the same as before, and mash particle size was the same as with the original starter mash. On the first four Ž conditioning. days, note was taken of how long it took birds to eat all of their Ž pellets or mash. meal at 0900 h. On the final two Ž test. days, the behaviour of all birds was video-recorded every alternate 15 min from 0915 to 1600 h. The video recordings were analysed, and behaviour data were converted to proportions of time, angular transformed, and analysed by split plot ANOVAs, all as in Experiment 1 except there were now two treatments Ž food form. instead of three Results Ž. At 14 weeks of age, the chickens ate their 0900 h 15 g meal in 2 4 min when it was in pellet form and in 9 13 min when it was mash. After the meal, they again spent

6 214 C.J. SaÕory, J.S. MannrApplied Animal BehaÕiour Science Table 2 Mean Ž ns12. proportions Ž %. of time spent in different activities in the 7 h after a 15-g meal of either pellets or mash at 0900 h, and significance of effects of food forms, time since feeding, and their interaction Žby split plot ANOVA. Food form Significance of effects Pellets Mash Food form Time Food form=time Sitting 0 0 Standing NS ))) NS Preening NS ))) NS Object pecking NS ))) NS Drinking NS )) NS Details as in Table 1. most time standing, more time object pecking than drinking or preening, and did not sit at all Ž Table 2.. There was no significant effect of food form on behaviour, or interaction between food form and time since feeding. Linear declines with time in object pecking and drinking Ž Fig. 1., and linear increases in standing and preening, were all significant. 5. Discussion In a previous study, where restricted-fed broiler breeder chickens were given meals of unequal size at 0900 and 1200 h, it was found that stereotyped Ž object. pecking at the empty feeder declined between meals when the first meal was small Ž 8 g. but not when it was large Ž 32 g. Ž Savory et al., In the same study, time spent drinking declined more after the large meal than after the small one when meal size order was randomised, possibly because food-related thirst was greater after the large meal. In the present study, there was a significant Ž Ps effect of meal size Ž 10, 25, 40 g. on time spent object pecking, but not on drinker directed activity, in the 7 h after a 0900 h meal, and there was no significant interaction between effects of meal size and time since feeding Ž Table 1.. Thus, in both studies, the main effect of meal size on post-feeding stereotyped behaviour was on object pecking. Nevertheless, object pecking and drinking were similar in that expression of both was highest in the hour after feeding, and declined consistently thereafter Ž Fig. 1.. This pattern of behaviour has been reported previously, and there is various evidence indicating that drinking Žwhich is often excessive and not related to food intake., pecking at any non-food object Ž including floor litter. and preening can all substitute with each other as dominant post-feeding activities in restricted-fed broiler breeders ŽKostal et al., 1992; Savory et al., 1992; Savory and Maros, 1993; Savory and Kostal, Possibly object pecking was more sensitive to an effect of meal size here because it took up more time than drinking or preening Ž Tables 1 and 2; also Savory et al., It was suggested previously that the rate at which stereotyped pecking declines after eating may depend on the amount that is eaten Ž Savory et al., Although the

7 C.J. SaÕory, J.S. MannrApplied Animal BehaÕiour Science present data appear to support this proposal Ž Fig. 1., the interaction between meal size and time since feeding was not significant for either a linear Ž P s or a quadratic Ž P s trend in pecking. The results do, however, demonstrate a more general effect of meal size on the amount of object pecking observed after feeding. Paradoxically, therefore, whereas expression of abnormal behaviour in restricted-fed animals is known to be correlated negatively with total daily food intake ŽSavory and Maros, 1993; see also Breland and Breland, 1961; Treichler and Hall, 1962; Falk, 1971; Appleby and Lawrence, 1987., it appears to be correlated positively with meal size within a given level of restriction. No such effect of meal size was found with restricted-fed pigs when either 0.5 or 1.25 kg food was provided at 0900 h instead of the usual 2.5 kg, but a larger Ž 5 kg. meal caused some suppression of chain manipulation and drinking Ž Terlouw et al., In another trial, pigs fed 2.5 kg pellets per day chewed and searched for food in a sand-filled test arena more after eating 1 kg pellets than after eating only 3 pellets Ž ca. 15 g. or nothing at all Ž Haskell et al., Despite the fact that the chickens took roughly four times as long to eat the 0900 h Ž 15 g. meal in mash form as in pellet form in Experiment 2, there was no effect of food form on their post-feeding behaviour Ž Table 2.. This suggests that the observed influence of meal size on object pecking in Experiment 1 Ž Table 1. was a consequence of the weight of food eaten per se, rather than the time taken to eat it. We cannot be certain, however, because the pellet and mash comparison in Experiment 2 would presumably have affected oropharyngeal feedback as well as meal duration, and the possibility that these two effects may have opposed each other cannot be ruled out. Nevertheless, it seems reasonable to conclude that sustained expression of unfulfilled appetitive behaviour Ž Lawrence and Terlouw, depends on persistence of some formž. s of positive feedback resulting from food already eaten. There is evidence in chickens and pigeons that central dopaminergic mechanisms may play a crucial role in control of food restriction-induced stereotypies ŽGoodman et al., 1983; Kostal and Savory, Microdialysis studies with hungry rats have shown a long-lasting increase in extracellular dopamine release in the prefrontal cortex in response to consumption of a single food pellet Ž Feenstra and Botterblom, 1996., and a greater increase in dopamine release in the nucleus accumbens when food was more palatable Ž Martel and Fantino, Possibly such variation in patterns of dopamine activity in the brain, as well as variation in duration of digestive processes, might provide physiological explanations for a positive influence of meal size on post-feeding stereotyped behaviour in restricted-fed chickens. They might also account for a similar reported effect of diet Ž and hence, presumably, palatability and digestibility. on crib-biting behaviour in horses, when meal size was constant Ž Gillham et al., Acknowledgements This work was part of a commission from the UK Ministry of Agriculture, Fisheries and Food. We wish to thank David Waddington for assistance with statistical analyses, and an anonymous referee for helpful comments.

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