Applied Animal Behaviour Science, 22 (1989) 371-375 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
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Short Communication
Experimenter Visibility, Spectacles and Tonic Immobility in the Domestic Fowl R. BRYAN JONES AFRC Institute of Animal Physiology and Genetics Research, Edinburgh Research Station, Roslin, Midlothian EH25 9PS (Gt. Britain)
(Accepted for publication 3 October 1988) ABSTRACT Jones, R.B., 1989. Experimenter visibility, spectacles and tonic immobility in the domestic fowl. Appl. Anim. Behav. Sci., 22: 371-375. Tonic immobility (TI) is widelyused to assess fear in chickens. Because eyes, eye-shapesand the presence of the experimenter often elicit fear, concern was felt lest features such as experimenter visibility/invisibility and the wearing or not of spectacles provided sources of inter-laboratory variability which might confound the general interpretation of TI tests. However,the TI reactions of adult hens were unaffected in the present study by whether or not the experimenter wore spectacles or sunglasses, or by whether they remained visible or retreated out of the bird's sight after inducing TI. The results are discussed in terms of the hens' perception of the experimenter.
INTRODUCTION Although the motivational and defensive aspects of fear are com m onl y recognized (Salzen, 1979; McFarland, 1981; Jones, 1987a), it may have deleterious effects on a chicken's welfare and performance. For example, fear responses which are inappropriate in an intensive environment, e.g., panic or escape, may waste energy and cause injury (Craig et al., 1983; Jones, 1985a). Negative correlations have also been reported between a chicken's underlying fearfulness and its growth and reproductive p erform ance (Bessei, 1984; Jones, 1985a; Jones and Hughes, 1986). T h e ability to measure fear is, therefore, imp o r t a n t and the tonic immobility ( T I ) reaction is widely regarded as a particularly useful test (Gallup, 1979; Jones, 1986). T hi s fear-potentiated, anti-predator reaction is induced by physical restraint and is characterized by temporary suppression of the righting response and reduced responsiveness to external stimulation (Gallup, 1977; Jones, 1986, 1987a). Eyes and eye-shapes often elicit fear and avoidance in chickens (Jones, 1980) and T I was prolonged if a pair of artificial eyes was suspended nearby, if the eyes of a stuffed hawk were visible or if the observer stared at the bird through-
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out the test period (Gallup, 1977). Human beings often elicit fear in chickens (Murphy, 1976; Jones et al., 1981; Jones, 1987b) and the mere visual presence of the experimenter was considered sufficient to prolong immobility in chicks (Gallup et al., 1972). In view of these findings, concern was felt lest features such as whether or not the experimenter was visible or wore spectacles provided sources of inter-laboratory variability which might confound general interpretation. For example, spectacles might either accentuate the eye gestalt and exert an additive effect on TI or, conversely, disrupt eye recognition. Such potentially confounding features could be particularly important if some aspect of stockmanship was being examined. Certain aspects of contact with the experimenter which were hitherto regarded as influential in studies in TI and other fear-related behaviour were, therefore, briefly reviewed and re-examined. The study focused primarily on the potential importance of the eye gestalt and measured the TI reactions of adult hens in the presence or absence of an experimenter who wore either no spectacles, untinted spectacles or sunglasses. MATERIALS AND METHODS
Animals used Isa Brown laying hens (a medium hybrid line derived from a Rhode Island Red X Rhode Island White cross) were used. They had been reared socially on wire floors until their transfer, at 16 weeks of age, to individual cages (450 X 450 X 300 mm) in a three-tier battery system. Since birds housed in toptier cages generally show elevated fearfulness (Jones, 1985b), only those caged in the lower tiers were used in the present study.
Test procedures The TI reactions of 92 hens were measured at 45 weeks of age. Each hen was carried to a separate room and testing always took place between 14.00 and 17.00 h, when all birds had laid. TI was induced by restraining the hen on its back in a wooden cradle (Jones and Faure, 1981 ). Using previously described criteria (Jones and Faure, 1981 ), the number of inductions required to attain TI, the latency from induction until the first alert head movement and the duration of TI (latency to righting) were measured. Each hen was tested individually and once only in one of the four test situations described below. Firstly, following TI induction, the experimenter sat 1 m away and made no unnecessary movements (Experimenter Visible). Secondly, the experimenter wore spectacles consisting of clear, untinted lenses (50X50 mm) in a grey-on-white striped frame during capture, response induction and subsequent observation (Experimenter+Untinted Snectacles}.
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Thirdly, the experimenter wore dark sunglasses (non-reflector) of similar dimensions to the untinted spectacles, but with black frames (Experimenter + Sunglasses). The experimenter remained in the bird's sight throughout the above observations, she faced the bird, but did not stare continuously at it. Fourthly, following TI induction, the experimenter retreated to a shaded area behind a muslin screen and was thus effectively hidden from view (Experimenter Not Visible). Tests were performed in random order and 23 birds were tested in each of the four situations. R E S U L T S AND D I S C U S S I O N
Analysis by the Kruskal-Wallis one-way analysis of variance and the M a n n Whitney U test revealed, respectively, that there were no significant differences across or between treatment groups (Table 1 ). Thus, the hens' TI reactions were unaffected by whether or not the experimenter wore spectacles or sunglasses, or by whether she remained visible or retreated out of sight after inducing TI. The former finding suggests either that exposure to the experimenter's eyes is not an influential variable or, perhaps more likely, that neither untinted spectacles nor sunglasses disrupted the eye gestalt sufficiently to interfere with eye recognition. Indeed, perception of eye-like schemata is considered remarkably flexible in chicks (Scaife, 1976; Jones, 1980) and may remain so in adulthood. It has been argued that a bird induced into TI might regularly monitor the environment for predatory cues, and that righting and escape attempts would be delayed were a visible experimenter perceived as a potential predator (Gallup et al., 1972; Ginsburg, 1975 ). However, the later suggestion that the visual presence of an experimenter during the TI response was crucial for prolonging immobility (Nash, 1977) was not supported by the present findings, which are consistent with the view that TI duration is governed primarily by the antecedent fear state (Gallup, 1977; Jones, 1986). Indeed, the rapid appearance of TABLE1 Tonic immobility responses of laying hens in the presence or absence of an experimenter wearing either no spectacles, untinted spectacles or sunglasses (means ± S E M )
Inductions (no.) Latency to first head movement (s) Duration of tonic immobility (s}
Experimenter visible
Experimenter not visible
1.1+__ 0.1
1.2___ 0.1
1.1± 0.1
1.2± 0.1
73.7 _ 12.3
79.4 ± 11.0
84.2 ___14.3
85.3 _ 15.8
250.5_+34.2
223.0+_48.7
213.7+__33.5
(no.) = n u m b e r (s) =seconds.
Experimenter + Experimenter + untinted spectacles sunglasses
228.8+__38.7
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a high-amplitude, slow-wave EEG pattern after TI induction (Ookawa, 1972; Gentle et al., in preparation) was suggestive of some form of "cut-offf' or dearousal. Speculative explanations for the present impotence of experimenter visibility can be offered if it is assumed that capture and TI induction elicited roughly similar fear states across groups. These include: (1) the birds may have been unaware of the subsequent presence or absence of the experimenter; (2) waning of fear was unaffected by the human component when the overall stimulation within treatments remained constant and unobtrusive; (3) a silent, immobile observer possessed no salient predatory cues; (4) dorsally restrained birds may have received an inverted image of the experimenter which might have interfered with their recognition; and/or (5) since the potentiating effects of experimenter visibility on TI were all observed using chicks (Gallup et al., 1972; Ginsburg, 1975; Nash, 1977), regular exposure to attendants performing their normal, everyday duties may have reduced the perceived aversiveness of the experimenter via habituation in the adult hens used here. Findings regarding the influence of the experimenter in other tests of fear have also been equivocal. For example, it was reported that chickens took longer to vocalize and ambulate in an open field or novel environment if the experimenter remained visible during the test (Gallup and Suarez, 1980; Suarez and Gallup, 1982). Conversely, a recent study found that the open-field responses of chicks of flighty and docile lines were unaffected by either the visual presence or absence of the experimenter during testing or by variations in his orientation (Jones, 1987c). Other variables which may modulate the experimenter's influence on TI, e.g. proximity, eye contact, pre-test habituation, strain and age, are under examination. However, the present findings suggest that elaborate measures to reduce or standardize the post-induction human component during TI testing may not always be necessary. ACKNOWLEDGEMENTS
This work was commissioned and supported by the Ministry of Agriculture, Fisheries and Food. I am also grateful to M.W. Thomson for her technical assistance.
REFERENCES Bessei, W., 1984. Genetische Beziehungen zwischen Leistung, Befiederung und Scheu bei Legehennen. Arch. Geflugelkd., 48: 231-239. Craig, J.V., Craig, T.P. and Dayton, A.D., 1983. Fearful behavior by caged hens of two genetic stocks. Appl. Anita. Ethol., 10: 263-273. Gallup, G.G., Jr., 1977. Tonic immobility: the role of fear and predation. Psychol. Rec., 27: 41-61.
375 Gallup, G.G., Jr., 1979. Tonic immobility as a measure of fear in domestic fowl. Anim. Behav., 27: 316-317. Gallup, G.G., Jr., Cummings, W.H. and Nash, R.F., 1972. The experimenter as an independent variable in studies of animal hypnosis in chickens (GaUus gallus). Anim. Behav., 20: 166-169. Gallup, G.G., Jr. and Suarez, S.D., 1980. An ethological analysis of open-field behaviour in chickens. Anim. Behav., 28: 368-378. Ginsburg, H.J., 1975. Defensive distance and immobility in young precocial birds (GaUus gaUus ). Dev. Psychobiol., 8: 281-285. Jones, R.B., 1980. Reactions of male domestic chicks to two-dimensional eye-like shapes. Anim. Behav., 28: 212-218. Jones, R.B., 1985a. Fearfulness and adaptability in the domestic fowl. IRCS Med. Sci., 13: 797800. Jones, R.B., 1985b. Fear responses of individually caged laying hens as a function of cage level and aisle. Appl. Anim. Behav. Sci., 14: 63-74. Jones, R.B., 1986. The tonic immobility reaction of the domestic fowl: a review. World's Poult. Sci. J., 42: 82-96. Jones, R.B., 1987a. The assessment of fear in the domestic fowl. In: R. Zayan and I.J.H. Duncan (Editors), Cognitive aspects of Social Behaviour in the Domestic Fowl. Elsevier, Amsterdam, pp. 40-81. Jones, R.B., 1987b. Social and environmental aspects of fear in the domestic fowl. In: R. Zayan and I.J.H. Duncan (Editors), Cognitive Aspects of Social Behaviour in the Domestic Fowl. Elsevier, Amsterdam, pp. 82-149. Jones, R.B., 1987c. Open-field behaviour in domestic chicks (Gallus domesticus): the influence of the experimenter. Biol. Behav., 12:100-115. Jones, R.B. and Faure, J.M., 1981. Sex and strain comparisons of tonic immobility ("righting time") in the domestic fowl and the effects of various methods of induction. Behav. Processes, 6: 47-55. Jones, R.B. and Hughes, B.O., 1986. Fearfulness and abnormalities in the chicken's eggshell - is there a link? Proceedings of an International Symposium on Applied Ethology of Farm Animals, Hungarian Society of Agricultural Science, pp. 171-175. Jones, R.B., Duncan, I.J.H. and Hughes, B.O., 1981. The assessment of fear in domestic hens exposed to a looming human stimulus. Behav. Processes, 6: 121-133. McFarland, D., 1981. The Oxford Companion to Animal Behaviour. 1st edn. Oxford University Press, Oxford, 657 pp. Murphy, L.B., 1976. A Study of the Behavioural Expression of Fear and Exploration in Two Stocks of Domestic Fowl. Ph.D. Thesis, University of Edinburgh, 343 pp. Nash, R.F., 1977. Effect of the visual presence of an experimenter on the maintenance of tonic immobility in domestic chickens (Gallus gaUus). Psychol. Rec., 27: 779-782. Ookawa, T., 1972. Polygraphic recordings during adult hen hypnosis. Poult. Sci., 51: 853-858. Salzen, E.A., 1979. The ontogeny of fear in animals. In: W. Sluckin (Editor), Fear in Animals and Man. Van Nostrand Reinhold, New York, pp. 125-163. Scaife, M., 1976. The response to eye-like shapes by birds. II. The importance of staring, paired~ ness and shape. Anim. Behav., 24: 200-206. Suarez, S.D. and Gallup, G.G., Jr., 1982. Open-field behaviour in chickens: the experimenter is a predator. J. Comp. Physiol. Psychol., 96: 432-439.