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Human-induced tachycardia in wild and tame mallard (Anas platyrhynchos)
Camp. Biochem. fhysid.
Vol. 92A,
0300-9629/89 $3.00 + 0.00 0 1989 Pergamon Press plc
No. I, pp. 125-128, 1989
Printed in Great Britain
HUMAN-INDUCED TACHYCARDIA IN WILD AND TAME MALLARD (ANAS PLATYRHYNCHOS) M. HEISE Institut fur Meereskunde, Abteilung Meereszoologie, Dtisternbrooker
Weg 20, D-2300 Kiel, FRG
(Received 20 June 1988)
Abstract-l. The effect of regular handling on fear reactions was investigated in mallard (Anus pluryrhynchos) by exposing six hand-reared and four wild ducks to an approaching human being and recording heart rates with an external ECG device. 2. All ducks reacted to the approach with tachycardia, but the response was significantly less in tame birds. 3. Hand-reared females showed less response than males. No sex-linked differences were apparent in the wild ducks. 4. Decreasing responses throughout the experiments were only found in tame birds. 5. Fear or stress reactions can apparently be diminished through habituation induced by regular handling.
INTRODUCTION
Stress is the non-specific response of the body to any demand and may be engendered by a great variety of exogenous and endogenous agents, e.g. fear (Selye, 1976). The appearance or approach of predators, or exposure to novel objects or environments can evoke fear (Russell, 1979). Thus, many conditions suitable for conducting physiological experiments constitute stressful situations for the study animal (Kanwisher et al., 1981). In particular, the presence of the experimenter during the test is likely to induce stress effects that affect the data being collected. Fear responses can, however, be diminished by regular handling of the test animal (Jones and Faure, 1981). Heart beat frequency is a good indicator of an animal’s “emotional state”, changing as a function of fear (Ball and Amlaner, 1980). In tufted ducks (Aythya fuligulu), for example, a strong bradycardia occurs during periods of forced submersion whereas voluntarily diving birds increased heart beat frequency (Woakes and Butler, 1983). Since human beings constitute a powerful stimulus for evoking fear in birds (Jones et al., 1981), heart rates of hand-reared and wild mallards (Anus plutyrhynchos) approached by an experimenter were measured. ECG signals were obtained using a selfbuilt external electrocardiograph. Both tame and wild ducks were subdivided into males and females to investigate the occurrence of sex-linked differences in their stress reactions. MATERIALS AND
METHODS
Experiments were conducted with four groups of mallard (Anus platyrhynchos): tame females, tame males, wild females and wild males. Each tame group comprised three animals obtained at the age of 3 days from a commercial breeder. The birds were fed on commercial dry pellets ad libirum and housed in a 48 m2 outdoor cage containing a shallow water basin. They were handled 10min daily for 2 months and every second day for another 10 months.
The experiments started when the birds were about 1 year old. The two wild groups each contained two individuals caught by net in eastern Schleswig-Holstein 2 days before experiments started. ECG signals were amplified by an electrocardiograph built from commercial electronical components (Fig. l), and a Linseis LS 23 chart strip recorder registered the traces. The electrocardiograph was connected to the sensory electrodes via co-axial cable and microclips. One day before the experiment a gilded safety pin electrode was placed beneath the duck’s right wing, and another into the bird’s cervical skin. In preliminary tests the animals got used to the electrodes within a few hours. No dermal irritations were observed even after more than two weeks. Five consecutive experiments were carried out with each duck in a 2 x 10 m indoor corridor. The recording equipment stood in an adjacent room. Forty minutes before the session the animal was connected to the electrocardiograph and set into a perspex box (28 x 37 x 29 cm). A single trial consisted of twenty-three 12-set periods: during the first two periods the heart rate of the “undisturbed” animal was recorded. In the third period the experimenter came into sight of the bird at a distance of 8.5 m. At the beginning of each following 12-set period a I m step was made towards the box until the bird-observer distance was 0.5 m. The observer then turned and walked back to the 8.5 m mark in the same way before finally going out of sight. The final three periods were used to obtain post-experimental resting data. Trials were repeated at IO-min intervals. To standardize the approach as much as possible, all trials were carried out by one experimenter always wearing the same clothes. RESULTS
Heart rates varied from 80 beats per min (resting tame female) to 515 bpm (wild female at 0.5 m distance). The mean resting value was 122 bpm (SD = 15) for tame females, 140 bpm (SD = 15) for tame males, 137 bpm (SD = 12) for wild females, and 138 bpm (SD = 12) for wild males. These are not significantly different from each other (P > 0.1). All ducks increased heart beat frequency as soon as the observer stepped into view (Fig. 2; peak 1). Subsequently, there was a significant tachycardia 125
M. HEISE
126
IN 1
IN2
T l..T2 O? 1..OP4 OP5 Dl..D2
= = = =
BC549c TLD64 TL061 lN4148
Fig. 1. Circuit diagram of the electrocardiograph. IN 1 and IN 2 denote the electrodes, OUT leads to a chart strip recorder
5oD _
TAME FEMALES
TAME MALES
400 300 -
PEAK 2
1
‘i+Lt(r~r*b*
-g
$4
’
i
i-b+&,
100 12s *
12s I*~sII“*L...l..‘
85
4.5
0.5 0.5
.“,t~,,l‘,.lr,,,r,,,r,.
4.5
I START
a.5
8.5
I
I
STOP
DISTANCE
4.5
0.5
4.5
8.5
I
START
TO DUCK /
a5
STOP
METRES
Fig. 2. Heart rates of mallard ducks approached by the experimenter. For each group, data were pooled from three tame or two wild ducks, respectivefy; each bird was tested four times. Values are given as means _+weighted SD (Sachs, 1974). Open circles denote pre- and post-experimental resting values.
Fear tachycardia in mallard
related to the distance between animal and experimenter up to a maximum heart rate at a birdobserver distance of 0.5 m (Fig. 2; peak 2); heart rates did not change significantly between the active and the stationary phase within each 12~see period (P > 0.05). During the approach the hand-reared mallards were attentive, but not physically active. The wild ducks, in addition to showing a sharper increase in heart rate, at a distance of 0.5 m occasionally hissed at the observer, rose with erect feathers or even tried to escape. In the calculation of means the first trial of every session was discarded because only steady-state responses were of interest. Differences in peak 1 were significant between wild and tame females (Mann Whitney U test, Lioj8.,z = 15, P c O.Ol), wild and tame males (U,,,, ,2 = 21, P < 0.02) and between tame males and tame females ( Uoj12,,2= 32, P < 0.02) but not between wild males and wild females (P > 0.1). Differences in peak 2 were highly significant (P < 0.005, P < 0.001) between all groups, except between wild males and wild females (P > 0.1). All tame birds gradually became habituated to the experiment, both heart rate peaks decreasing from the first to the fifth trial, whereas in the wild malfards this effect could not be detected (Fig. 3). Decreases for both peaks were significant in the tame ducks (F = 50.9, P c 0.005 for peak 1; F = 60.2, P = 0.005 for peak 2). In the wild ducks values of both peaks showed no significant slope (F = 0.9, P > 0.5 for peak 1; F = 0, P > 0.5 for peak 2). DISCUSSION
The results indicate that in mallard regular handling leads to reduced fear of the experimenter through habituation. A similar effect has been noted in reguiarly handled domestic chicks (Jones and Faure, 1981). The shape of the heart rate curves in general is comparable to the findings of Ball and Amlaner (1980) for herring gulls (Lana argentatus) except that
5 400 ~ ‘.&_“___a
______0 D
D_*
r 2 - 0.00
z 5
I
I
1
I
1
t
1
2
3
4
5
127
the gulls showed no equivalent to the ducks’ “peak 1” (Fig. 2). In the gull experiments, however, the approach began at a distance of 50 m where heart rates increased gradually at first and then sharply from about 10m onwards. In my experiments, the starting distance of 8.5 m seems to be well within the ducks’ range of attentiveness, the sudden appearance of the experimenter causing a temporary tachycardia. As these increases were always of short duration and moderate intensity, they were interpreted as “attention peaks” or primary defense reaction (sensu Edmunds, 1974), which starts with an “orienting response” (Pavlov, 1927) and prepares the animal for secondary reactions, i.e. aggressive or fear behaviour. The second rise of heart rates appeared to be essentially correlated with the distance between anima1 and experimenter. Motion itself, being reduced to a minimum, seemed to be of secondary importance, a step causing no significnat increases compared to the stationary phase within the same period. However, direction of movement appeared to be important. Heart rates in the first half of a trial (when the experimenter walked towards the duck) were always higher than the corresponding values of the second half (when the experimenter walked away). This indicates that the birds differentiated between the stimulus being likely to increase or to decrease. Since the wild ducks’ reactions on close approach fit former definitions of stress or fear behaviour as “behaviour concerned with removing or protecting the animal from a source of noxious stimulation” (Archer, 1979) or “the psychophysiological response to perceived danger” (Jones and Faure, 1981), the second heart rate peak can be classified as “stress peak”, initializing or already belonging to a flight response, a form of secondary defence (sensu Edmunds, 1974). Observed sex-linked differences in heart rate are similar to the findings of Desforges and Wood-Gush (1975), who investigate stress reactions in Aylesbury ducks and wild mallard. They report that tame females were markedly more placid than tame males whereas in the wild ducks no significant differences could be detected. In wild birds the fear-evoking stimulus was apparently too strong causing full avoidance behaviour in both sexes. It might be assumed from the broader shape of the stress peak in the wild males that they feit disturbed earlier than the wild females, which would denote that females in general are less sensitive to disturbance than males. This would have to be supported by more experimental evidence. The study indicates that the presence and approach of a human induces physiological changes in mallard ducks and that the extent of the change may be sex-linked. Stress effects caused by the experimenter can apparently be reduced by habituation. Cognizance of this is important in physiological experiments since broadly similar findings are to be expected in other animals.
I TRIAL
NO.
Fig. 3. Mean heart rates of wild (open symbols) and tame mallard ducks (closed symbols) in the course of the experiments. Circles show values of peak I; squares denote values of peak 2.
Acknowledgemenrs-This study forms part of my diploma thesis supervised by D.VAdelung. I am grateful to F. Winkelmann for his heln in desianina the electrocardiograph, and to R. Wilson for comm&ts& the manuscript. The study was supported by a grant of the Deutsche Forschungsgemein~haft, DFG Ad 241I 1- 1.
128
M. REFERENCES
Archer J. (1979) Behavioural aspects of fear. In Fear in Animals and Man (Edited by Sluckin W.), pp. 56-85. Van Nostrand Reinhold, New York. Ball N. J. and Amlaner C. J. (1980) Changing heart rates of herring gulls when approached by humans. In A Handbook on Biotelemetr>Wand Radio Tracking (Edited by Amlaner C. J. and Macdonald D. W.). DD. . . 589-594. Pergamon Press, Oxford. Desforges M. F. and Wood-Gush D. G. M. (1975) A behavioural comparison of domestic and mallard ducks: habituation and flight reactions. Anim. Behav. 23, 692-697.
M. (1974) Defense in Animals: A Survey of Antipredator Defertees. Longman, New York.
Edmunds
Jones R. B. and Faure J. M. (1981) The effects of regular handling on fear responses in the domestic chick. Behav. Proc. 6, 135-143.
HEISE
Jones R. B., Duncan I. J. H. and Hughes B. 0. (1981) The assessment of fear in domestic hens exposed to a looming human stimulus. Behav. Proc. 6, 121-133.
Kanwisher J. W., Gabrielsen G. W. and Kanwisher N. (1981) Free and forced diving in birds. Science 211, 717-719. Russell P. A. (1979) Fear-evoking stimuli. In Fear in Animals and Man (Edited by Sluckin W.), pp. 86-124. Van Nostrand Reinhold, New York. Pavlov J. P. (1927) Conditioned Reflexes. Oxford University Press, London. Sachs L. (1974) Angewundte Statistik. Springer, Berlin. Selye H. (1976) Stress in Health and Disease. Buttenvorths, London. Woakes A. J. and Butler P. J. (1983) Swimming and diving in tufted ducks, Aythya filigula, with particular reference to heart rate and gas exchange. J. exp. Biol. 107, 31 l-329.
Vol. 92A,
0300-9629/89 $3.00 + 0.00 0 1989 Pergamon Press plc
No. I, pp. 125-128, 1989
Printed in Great Britain
HUMAN-INDUCED TACHYCARDIA IN WILD AND TAME MALLARD (ANAS PLATYRHYNCHOS) M. HEISE Institut fur Meereskunde, Abteilung Meereszoologie, Dtisternbrooker
Weg 20, D-2300 Kiel, FRG
(Received 20 June 1988)
Abstract-l. The effect of regular handling on fear reactions was investigated in mallard (Anus pluryrhynchos) by exposing six hand-reared and four wild ducks to an approaching human being and recording heart rates with an external ECG device. 2. All ducks reacted to the approach with tachycardia, but the response was significantly less in tame birds. 3. Hand-reared females showed less response than males. No sex-linked differences were apparent in the wild ducks. 4. Decreasing responses throughout the experiments were only found in tame birds. 5. Fear or stress reactions can apparently be diminished through habituation induced by regular handling.
INTRODUCTION
Stress is the non-specific response of the body to any demand and may be engendered by a great variety of exogenous and endogenous agents, e.g. fear (Selye, 1976). The appearance or approach of predators, or exposure to novel objects or environments can evoke fear (Russell, 1979). Thus, many conditions suitable for conducting physiological experiments constitute stressful situations for the study animal (Kanwisher et al., 1981). In particular, the presence of the experimenter during the test is likely to induce stress effects that affect the data being collected. Fear responses can, however, be diminished by regular handling of the test animal (Jones and Faure, 1981). Heart beat frequency is a good indicator of an animal’s “emotional state”, changing as a function of fear (Ball and Amlaner, 1980). In tufted ducks (Aythya fuligulu), for example, a strong bradycardia occurs during periods of forced submersion whereas voluntarily diving birds increased heart beat frequency (Woakes and Butler, 1983). Since human beings constitute a powerful stimulus for evoking fear in birds (Jones et al., 1981), heart rates of hand-reared and wild mallards (Anus plutyrhynchos) approached by an experimenter were measured. ECG signals were obtained using a selfbuilt external electrocardiograph. Both tame and wild ducks were subdivided into males and females to investigate the occurrence of sex-linked differences in their stress reactions. MATERIALS AND
METHODS
Experiments were conducted with four groups of mallard (Anus platyrhynchos): tame females, tame males, wild females and wild males. Each tame group comprised three animals obtained at the age of 3 days from a commercial breeder. The birds were fed on commercial dry pellets ad libirum and housed in a 48 m2 outdoor cage containing a shallow water basin. They were handled 10min daily for 2 months and every second day for another 10 months.
The experiments started when the birds were about 1 year old. The two wild groups each contained two individuals caught by net in eastern Schleswig-Holstein 2 days before experiments started. ECG signals were amplified by an electrocardiograph built from commercial electronical components (Fig. l), and a Linseis LS 23 chart strip recorder registered the traces. The electrocardiograph was connected to the sensory electrodes via co-axial cable and microclips. One day before the experiment a gilded safety pin electrode was placed beneath the duck’s right wing, and another into the bird’s cervical skin. In preliminary tests the animals got used to the electrodes within a few hours. No dermal irritations were observed even after more than two weeks. Five consecutive experiments were carried out with each duck in a 2 x 10 m indoor corridor. The recording equipment stood in an adjacent room. Forty minutes before the session the animal was connected to the electrocardiograph and set into a perspex box (28 x 37 x 29 cm). A single trial consisted of twenty-three 12-set periods: during the first two periods the heart rate of the “undisturbed” animal was recorded. In the third period the experimenter came into sight of the bird at a distance of 8.5 m. At the beginning of each following 12-set period a I m step was made towards the box until the bird-observer distance was 0.5 m. The observer then turned and walked back to the 8.5 m mark in the same way before finally going out of sight. The final three periods were used to obtain post-experimental resting data. Trials were repeated at IO-min intervals. To standardize the approach as much as possible, all trials were carried out by one experimenter always wearing the same clothes. RESULTS
Heart rates varied from 80 beats per min (resting tame female) to 515 bpm (wild female at 0.5 m distance). The mean resting value was 122 bpm (SD = 15) for tame females, 140 bpm (SD = 15) for tame males, 137 bpm (SD = 12) for wild females, and 138 bpm (SD = 12) for wild males. These are not significantly different from each other (P > 0.1). All ducks increased heart beat frequency as soon as the observer stepped into view (Fig. 2; peak 1). Subsequently, there was a significant tachycardia 125
M. HEISE
126
IN 1
IN2
T l..T2 O? 1..OP4 OP5 Dl..D2
= = = =
BC549c TLD64 TL061 lN4148
Fig. 1. Circuit diagram of the electrocardiograph. IN 1 and IN 2 denote the electrodes, OUT leads to a chart strip recorder
5oD _
TAME FEMALES
TAME MALES
400 300 -
PEAK 2
1
‘i+Lt(r~r*b*
-g
$4
’
i
i-b+&,
100 12s *
12s I*~sII“*L...l..‘
85
4.5
0.5 0.5
.“,t~,,l‘,.lr,,,r,,,r,.
4.5
I START
a.5
8.5
I
I
STOP
DISTANCE
4.5
0.5
4.5
8.5
I
START
TO DUCK /
a5
STOP
METRES
Fig. 2. Heart rates of mallard ducks approached by the experimenter. For each group, data were pooled from three tame or two wild ducks, respectivefy; each bird was tested four times. Values are given as means _+weighted SD (Sachs, 1974). Open circles denote pre- and post-experimental resting values.
Fear tachycardia in mallard
related to the distance between animal and experimenter up to a maximum heart rate at a birdobserver distance of 0.5 m (Fig. 2; peak 2); heart rates did not change significantly between the active and the stationary phase within each 12~see period (P > 0.05). During the approach the hand-reared mallards were attentive, but not physically active. The wild ducks, in addition to showing a sharper increase in heart rate, at a distance of 0.5 m occasionally hissed at the observer, rose with erect feathers or even tried to escape. In the calculation of means the first trial of every session was discarded because only steady-state responses were of interest. Differences in peak 1 were significant between wild and tame females (Mann Whitney U test, Lioj8.,z = 15, P c O.Ol), wild and tame males (U,,,, ,2 = 21, P < 0.02) and between tame males and tame females ( Uoj12,,2= 32, P < 0.02) but not between wild males and wild females (P > 0.1). Differences in peak 2 were highly significant (P < 0.005, P < 0.001) between all groups, except between wild males and wild females (P > 0.1). All tame birds gradually became habituated to the experiment, both heart rate peaks decreasing from the first to the fifth trial, whereas in the wild malfards this effect could not be detected (Fig. 3). Decreases for both peaks were significant in the tame ducks (F = 50.9, P c 0.005 for peak 1; F = 60.2, P = 0.005 for peak 2). In the wild ducks values of both peaks showed no significant slope (F = 0.9, P > 0.5 for peak 1; F = 0, P > 0.5 for peak 2). DISCUSSION
The results indicate that in mallard regular handling leads to reduced fear of the experimenter through habituation. A similar effect has been noted in reguiarly handled domestic chicks (Jones and Faure, 1981). The shape of the heart rate curves in general is comparable to the findings of Ball and Amlaner (1980) for herring gulls (Lana argentatus) except that
5 400 ~ ‘.&_“___a
______0 D
D_*
r 2 - 0.00
z 5
I
I
1
I
1
t
1
2
3
4
5
127
the gulls showed no equivalent to the ducks’ “peak 1” (Fig. 2). In the gull experiments, however, the approach began at a distance of 50 m where heart rates increased gradually at first and then sharply from about 10m onwards. In my experiments, the starting distance of 8.5 m seems to be well within the ducks’ range of attentiveness, the sudden appearance of the experimenter causing a temporary tachycardia. As these increases were always of short duration and moderate intensity, they were interpreted as “attention peaks” or primary defense reaction (sensu Edmunds, 1974), which starts with an “orienting response” (Pavlov, 1927) and prepares the animal for secondary reactions, i.e. aggressive or fear behaviour. The second rise of heart rates appeared to be essentially correlated with the distance between anima1 and experimenter. Motion itself, being reduced to a minimum, seemed to be of secondary importance, a step causing no significnat increases compared to the stationary phase within the same period. However, direction of movement appeared to be important. Heart rates in the first half of a trial (when the experimenter walked towards the duck) were always higher than the corresponding values of the second half (when the experimenter walked away). This indicates that the birds differentiated between the stimulus being likely to increase or to decrease. Since the wild ducks’ reactions on close approach fit former definitions of stress or fear behaviour as “behaviour concerned with removing or protecting the animal from a source of noxious stimulation” (Archer, 1979) or “the psychophysiological response to perceived danger” (Jones and Faure, 1981), the second heart rate peak can be classified as “stress peak”, initializing or already belonging to a flight response, a form of secondary defence (sensu Edmunds, 1974). Observed sex-linked differences in heart rate are similar to the findings of Desforges and Wood-Gush (1975), who investigate stress reactions in Aylesbury ducks and wild mallard. They report that tame females were markedly more placid than tame males whereas in the wild ducks no significant differences could be detected. In wild birds the fear-evoking stimulus was apparently too strong causing full avoidance behaviour in both sexes. It might be assumed from the broader shape of the stress peak in the wild males that they feit disturbed earlier than the wild females, which would denote that females in general are less sensitive to disturbance than males. This would have to be supported by more experimental evidence. The study indicates that the presence and approach of a human induces physiological changes in mallard ducks and that the extent of the change may be sex-linked. Stress effects caused by the experimenter can apparently be reduced by habituation. Cognizance of this is important in physiological experiments since broadly similar findings are to be expected in other animals.
I TRIAL
NO.
Fig. 3. Mean heart rates of wild (open symbols) and tame mallard ducks (closed symbols) in the course of the experiments. Circles show values of peak I; squares denote values of peak 2.
Acknowledgemenrs-This study forms part of my diploma thesis supervised by D.VAdelung. I am grateful to F. Winkelmann for his heln in desianina the electrocardiograph, and to R. Wilson for comm&ts& the manuscript. The study was supported by a grant of the Deutsche Forschungsgemein~haft, DFG Ad 241I 1- 1.
128
M. REFERENCES
Archer J. (1979) Behavioural aspects of fear. In Fear in Animals and Man (Edited by Sluckin W.), pp. 56-85. Van Nostrand Reinhold, New York. Ball N. J. and Amlaner C. J. (1980) Changing heart rates of herring gulls when approached by humans. In A Handbook on Biotelemetr>Wand Radio Tracking (Edited by Amlaner C. J. and Macdonald D. W.). DD. . . 589-594. Pergamon Press, Oxford. Desforges M. F. and Wood-Gush D. G. M. (1975) A behavioural comparison of domestic and mallard ducks: habituation and flight reactions. Anim. Behav. 23, 692-697.
M. (1974) Defense in Animals: A Survey of Antipredator Defertees. Longman, New York.
Edmunds
Jones R. B. and Faure J. M. (1981) The effects of regular handling on fear responses in the domestic chick. Behav. Proc. 6, 135-143.
HEISE
Jones R. B., Duncan I. J. H. and Hughes B. 0. (1981) The assessment of fear in domestic hens exposed to a looming human stimulus. Behav. Proc. 6, 121-133.
Kanwisher J. W., Gabrielsen G. W. and Kanwisher N. (1981) Free and forced diving in birds. Science 211, 717-719. Russell P. A. (1979) Fear-evoking stimuli. In Fear in Animals and Man (Edited by Sluckin W.), pp. 86-124. Van Nostrand Reinhold, New York. Pavlov J. P. (1927) Conditioned Reflexes. Oxford University Press, London. Sachs L. (1974) Angewundte Statistik. Springer, Berlin. Selye H. (1976) Stress in Health and Disease. Buttenvorths, London. Woakes A. J. and Butler P. J. (1983) Swimming and diving in tufted ducks, Aythya filigula, with particular reference to heart rate and gas exchange. J. exp. Biol. 107, 31 l-329.