J. comp. Physiol.

89, 73--82 (1974) 9 by Springer-Verlag 1974

Detection of Changes in Atmospheric Pressure by the Homing Pigeon, Columba livia

Melvin L. Kreithen and William T. Keeton Division of Biological Sciences, Langmuir Laboratory, Cornell University, Ithaca, New York Received October 23, 1973

Summary. Homing pigeons were tested for their ability to detect air pressure changes in an otherwise constant environment chamber. Ten of 12 birds tested did respond to the pressure changes. The 50% threshold of detection was 10 mm H20 or less, which is approximately equivalent to a change in altitude of 10 in or less. Performance was better in a chamber with artificial background noise than in an abnormally quiet chamber.
Introduction The ability to detect changes in atmospheric pressure would be useful to a bird, both when flying and when on the ground. ~Vhen the bird is flying, a pressure detector could be used as an altimeter. Also, if it were sensitive enough, the rate of climb or descent could be determined from pressure information alone. Moreover, there are patterns of air turbulence which, if detected, could provide directional cues. Such directional information could be of use to nocturnal migrants when they fly in h e a v y cloud cover. I t is becoming increasingly clear t h a t migrating birds are excellent meteorologists. Migration takes place on relatively few nights of each season and these nights are predictable from synoptic weather conditions. I n particular, spring migration tends to be concentrated on evenings of south winds, rising temperature, and falling pressure, whereas fall migratioD is m a x i m u m on days with north winds, falling temperature, and rising pressure (Bagget al., 1950; Bruderer, 1971 ; Nisbet and Drury, 1968; Richardson and ttaight, 1970; Richardson and Gunn, 1971). Muller (1972) found t h a t White-throated Sparrows (Zonotrichia albicollis) kept in outdoor cages showed increased activity on nights when spring migration would normally be heavy. I n the spring, significant correlations were obtained between activity and rising temperature, south winds, and a decrease in atmospheric pressure greater than 17.3 m m H~O. Thus it is apparent t h a t migrating birds go aloft most frequently and in greater numbers on evenings when there are following winds aloft. The metabolic cost of long distance flight is high, and b y

74

M. L. Kreithen and W. T. Keeton

using t h e wind to their a d v a n t a g e , birds m a y be able to e x t e n d the distance f l o ~ on a given a m o u n t of fat reserve. Although most p a r a m e t e r s of w e a t h e r are correlated with one another, the b a r o m e t e r is still a n essential tool for the meteorologist; presumably, barometric i n f o r m a t i o n could be of similar value to a bird i n predicting a n i g h t ' s w e a t h e r conditions. Masher a n d Stolt (1961), who k e p t a b u n t i n g (Emberiza hortulana) in a n e n v i r o n m e n t a l c h a m b e r i n which only air pressure was allowed to v a r y n a t u r a l l y , reported a n e g a t i v e correlation b e t w e e n the level of a c t i v i t y a n d changes i n atmospheric pressure. L e h n e r a n d D e n n i s (1971) have reported t h a t m a l l a r d ducks can be t r a i n e d to peck the appropriate keys of a test a p p a r a t u s w h e n there is a pressure change of :[: 2 psi, 1 psi, a n d ~: 0.4 psi over a n i n t e r v a l of a p p r o x i m a t e l y 2 minutes. These pressures correspond to a l t i t u d e changes of a p p r o x i m a t e l y 1200 meters, 600 meters, a n d 240 meters. The purpose of t h e p r e s e n t s t u d y is to d e t e r m i n e if the h o m i n g pigeon can detect smM1 changes i n atmospheric pressure. I n particular, the experiments concentrate on the kinds of pressure changes t h a t would be experienced b y a bird in free flight.

Methods
The basic materials for the experiments were an airtight chamber, a controlled source of air, and equipment to monitor the heart rate. The sealed pressure chamber (obtained from the U.S. Navy), which was designed for withstanding pressures much greater than any we used, had cast aluminium walls 2.3 cm thick, plus external ribs 1 cm thick. Its internal volume was 40 liters, and the floor dimensions were 44.5 by 30 cm. Air and vacuum were supplied through sound isolation mufflers made of 6-inch lengths of 2-inch diameter galvanized pipe, packed with aquarium floss. For respiration, there was a constant flow of 5 liters/minute of fresh air through the chamber. Changes in chamber pressure were programmed by a system of solenoid-operated needle valves which controlled the rates of air flow into and out of the chamber. Because the compressed air supply and the vacuum source operated at pressures very much greater than the chamber pressure, all changes in chamber pressure were linear with time. Instantaneous heart rate was monitored with a Grass Instrument Co. model 7P4 tachograph. The output of the taehograph is a linear voltage proportional to heart rate, measured on a beat-to-beat basis. A permanent record of chamber pressure, EKG, and heart rate was obtained with a Sanborn model 350 chart recorder. The basic method was simply to change the pressure over a 5 sec interval, hold the new pressure for another 5 see, and then deliver a mild electric shock to the pigeon. After a few such presentations, a conditioned response develops and the heart rate increases when the pressure changes. Fig. 1 shows the cardiac response. Each experiment consisted of 50 trims of pressure change followed by shock. In the chamber, each bird was gently restrained in a leather body harness and placed in a sculptured foam rubber cushion with the body axis horizontal. The head was free to move in any direction. Two EKG surface electrodes were

Detection of Changes in Atmospheric Pressure b y the Homing Pigeons

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Fig. 1. Tracings of actual cardiac rates during an experiment. Upper trace is 10 consecutive frames a t =~ 20 m m H20 pressure change. Hatched area indicates pressure change. Shock follows a t the end of the pressure change. The c h a r t is stopped a t the arrow, and restarted at r a n d o m time intervals. Lower trace is from a control trial using the same bird. I n the upper trace, frame n u m b e r 7 is the only one t h a t does not meet criterion for a cardiac response. I n the control trace, frame n u m b e r 8 has a n acceleration during the stimulus time interval, b u t the magnitude of the acceleration is too small to be counted as a response

attached, one a t the base of the neck, dorsal surface, and the other under the right wing, just posterior to the base of the humerus. Shock electrodes were two silver wires implanted under the skin of the breast, one on each side of the sternum. The shock, when delivered, was 1 ma for 350 msec from a 60 Hz A.C. constant-current source. The control for extraneous cues was to r u n the experiment in the usual way, b u t with a valve opened to the outside of the chamber so t h a t no pressure could accumulate inside. This procedure allowed everything such as air-flow rates, relay noises, valve sounds, etc. to proceed intact, b u t did n o t permit the air pressure to vary. The cardiac acceleration response was measured b y comparing the h e a r t rate before the pressure change with the heart rate during or immediately after the pressure change. For each stimulus presentation, a baseline was established b y determining the peak h e a r t rate in the 5-second interval preceeding the pressure change. For a response to be counted, the h e a r t rate during the 10-second pressurechange interval must have exceeded the baseline rate b y a t least 12 beats per minute. Most cardiac responses easily exceeded this m i n i m u m requirement. Typical baseline h e a r t rates were approximately 140 beats per minute, a n d accelerations of 30 to 60 beats per minute were common (see Fig. 1). The p a t t e r n s and magnitudes of the responses were in complete agreement with the extensive studies b y Cohen and his co-workers of the conditioned cardiac response of the pigeon (Cohen a n d MacDonald, 1971).

76
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M. L. Kreithen and W. T. Keeton

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Fig. 2. Responses to atmospheric pressure changes. Solid circles are percent cardiac responses to 50 trials at the indicated pressure. Solid square is a control experiment (50 trials). Open circles indicate the training sessions o~ 50 trims each; arrows indicate their sequence. Pressures not connected by arrows were presented in mixed order

Results
The results clearly show t h a t homing pigeons can detect small differential changes in air pressure. Twelve pigeons were tested at initial pressures differing from atmospheric b y 100-400 m m H20. Ten of the birds easily met our criteria for regular response. Two birds did not respond satisfactorily after 50 trials and were removed from further experiments (refractory subjects have often been reported in cardiac conditioning experiments; Tuge, Smia and Koga, 1957). Fig. 2 shows the response pattern of one of the birds whose pressure sensitivity was examined in detail. There is a characteristic dip in the number of responses at low pressure differentials. The background level is the value for the control test (0 m m H~O change); this value ranged from 8 to 16% for the various birds tested. Ramp Tests. To determine the pattern of sensitivity to pressure variations between 0 and 20 m m H20, 4 conditioned birds were subjected to a series of linear pressure increases at the rate of 2 m m H20 per second for 10 see. This is similar to the test procedure used b y Dressler (1893), who found the h u m a n threshold for pressure change to be about 40 m m H20. The pressure at which the heart rate began to rise was plotted on a histogram (Fig. 3). The median value of pressure responses ranged from 6.4 to 10.8 m m H~O for positive changes in pressure, and from 7.6 to 8.8 m m H20 for negative changes. Pigeon ~ o . 1103 gave only 2 responses to 50 negative pressure ramps, and was therefor~ not considered to be sensitive to pressure changes between 0 and - - 2 0 m m H20. Threshold Values. There appears to be no sharp threshold of A-pressure sensitivity. As the pressure change approached zero, the percentage of responses decreased proportionately.

Detection of Changes in Atmospheric Pressure by the Homing Pigeons

77

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~ig. 3. Ramp tests. Histogram of responses by four birds to linear pressure changes of ~=20 mm H20 in 10 sec (see text for explanation). Arrows indicate median values. The abcissa shows the pressure-change values a]ong the ramp from 0 to 20 mm H~O. Each data point indicates the pressure at which response began in one trial

There was some evidence of responses to pressure changes down to as little as 1 m m H20. Fig. 4 shows one attempt to find the threshold of sensitivity for bird No. 3560. Experimental trials were presented in mixed sequence, without removing the bird from the chamber, for a marathon session of 16 hours. Responses to a change of + 1 mm H~O were higher than control trials run concurrently. An estimate of the 50 % threshold point, a measure commonly used in psychophysics, is about 6 m m H20. This agrees well with the median value of the ramp test, which was 6.4 mm H~O for this bird. Also on Fig. 4 are data from earlier experiments (closed circles).

The E]/ect o] Acoustic Noise. The performance of the birds was influenced by the ambient noise level in the chamber. The usual effect of reducing the background noise was to decrease the percentage of responses to a given pressure change. Fig. 5 shows the results of nine paired experiments where 50 trials were presented with no noise added to the chamber and 50 trials were presented with continuous noise added through a 4-inch diameter loudspeaker driven by a General Radio random-noise generator. The pressure stimulus was presented in alternating blocks of 10 trials, first with added noise, and then without noise.

78
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M. L. Kreithen and W. T. Keeton

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Fig. 5. Paired experiments showing the effects of ambient noise levels on detection of pressure changes. Test pressures are below each histogram. R indicates a linear pressure ramp of the indicated pressure measured over 10 see

I n 8 of t h e 9 e x p e r i m e n t s , t h e r e was a h i g h e r p e r c e n t a g e of responses w i t h noise a d d e d t o t h e c h a m b e r t h a n w i t h o u t . F i g . 6 shows t h e spectral d i s t r i b u t i o n of sound pressure levels w i t h i n t h e c h a m b e r . I t can be seen t h a t t h e t h i c k walls of t h e c h a m b e r effectively filtered outside sources of noise. I t is u n l i k e l y t h a t t h e b i r d is ever in a n a t u r a l environm e n t as quiet as t h e inside of t h e c h a m b e r w i t h o u t noise a d d e d .

Detection of Changes in Atmospheric Pressure by the Homing Pigeons

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Discussion

The homing pigeon is apparently able to detect atmospheric pressure changes on the order of l0 m m H20 or lower when these are presented over a 5 see interval. The 5-sec interval was an arbitrary, though biologically reasonable, experimental choice; it is probably safe to extend these findings to 30 see or more. Given this sensitivity, it is appropriate to discuss the potential use of this information, and to suggest further experiments. Control o/Altitude. R a d a r studies report the altitudes of migrating birds to be maintained within =j=20 meters, even when clouds obscure the ground, horizon, and sky (Griffin, 1969, 1972). Since a 10 m m H20 A-pressure threshold is equivalent to approximately 10 m of altitude change, it is feasible t h a t a bird could maintain the observed altitude limits using a pressure sense alone. Though it is clear from this study that homing pigeons can detect both positive and negative pressure changes, what is not yet known is whether they can discriminate between increasing and decreasing pressure changes. For a physiological altimeter to function properly, this ability would be useful but not absolutely essential. Locating Thermal Updrafts. Glider pilots use a very sensitive pressure instrument (the variometer) to detect the small rates of altitude change associated with thermal updrafts. Soaring birds with a sufficiently sensitive pressure detector could presumably use pressure information

80

NI. L. Kreithen and W. T. Keeton

in a similar way. The variometer is capable of registering altitude changes as small as 0.005 m/see. This is below the threshold suggested by these experiments. However, the upper end of the variometer scale (5 m/see) falls in the range that might be detectable to a bird. The pilots locate updrafts by a combination of pressure instruments and visual observation of certain cloud patterns that indicate the presence of the updrafts. Roll vortices, gravity waves, and other forms of convective updrafts have characteristic cloud and pressure patterns which, if located, could presumably be useful to a bird in flight. Air Turbulence Detection. There are patterns of air turbulence and other departures from smooth flow which could influence the direction and energy cost of bird flight. For example, the well known fall migration of hawks takes place where wind and topography combine to provide extensive updraft patterns on which the hawks glide (Broun, 1949). Below the mixing layer, gusts with a rapid onset and a gradual decrease in velocity may reveal the direction of the prevailing wind (Nisbet, 1955). Thus both inertial and pressure senses could be used to obtain wind-direction information while flying within the air mass. Pressure-Pattern Flying. Pressure-pattern flying, i.e. flying at a constant pressure altitude and noting, by visual or other means, changes in absolute altitude, is a method of navigation used by aircraft pilots in an emergency when other navigational means are not available. When coupled with simple meteorologicalinformation, pressure-pattern navigation can provide approximations of direction and location, particularly in temperate latitudes, where air masses often follow predictable paths. This would require the ability to hold a reference pressure for several hours. It is not yet known if birds have this capability, but at least the magnitude of the pressure sensitivity is within the appropriate bounds. Detection of Weather Changes. Cold front passage is often marked by a sharp dip in atmospheric pressure (Critchfield, 1966; Hassler, Graber and Bellrose, 1963). In continuous records of natural pressure made during this study, the barometer fell rapidly several times through 10 mm H~O in as little as 30 minutes, marking the passage of cold fronts. For other front passages, the pressure changed 10 mm H20 or more in a few hours or less. If birds could maintain a fixed reference pressure for 30 rain to a few hours, then they might be able to predict weather changes by noting the pressure changes. In particular, they would be able to predict nights when winds aloft were favorable or unfavorable for migratory flight. In general, a falling barometer is an indication of favorable winds for fall migration, and a rising barometer indicates winds suitable for northward migration in the spring. Several workers have indicated that migration or cage activity is correlated with barometric pressure in the

Detection of Changes in Atmospheric Pressure by the Homing Pigeons

81

appropriate way, but it is still not known whether pressure or some other correlated variable is the cause of the increase in activity (Bagg et al., 1950; Masher and Stolt, 1961; Muller, 1972). Notes on M e c h a n i s m s . There is currently no evidence indicating where the pressure receptor might be. However, the interaction between white noise in the chamber and responses to pressure suggests that the ear may play some role. The modification of ambient noise is of course a possible mechanism in i t , l l . The bird normally flies in an environment filled with the sounds of wingbeats, rushing air, and the vocalizations of other birds. A shift in auditory sensitivity associated with changes in air pressure could be used as a means of detecting changes in pressure. Beecher (1951, 1954) has reported the presence in birds of cavernous tissue capable of completely sealing off the external ear when inflated with blood. The tissue can apparently seal off the external ear without pressing on the t y m p a n u m (Beecher, pers. comm.). Such a sealed, and presumably temperatureregulated, air volume could provide the necessary reference cell for detecting absolute pressure. There are, of course, other ways that pressure could be detected by the ears. For example, stretch receptors in the t y m p a n u m could provide the necessary signals. The function of Vitalli's organ is as yet unknown, but it m a y be related to detecting static pressures in the endolymph (Griffin, 1969). The possibility that the ears are the detection sites could be tested by using tubes fitted to the external ear, which would allow the ears and the rest of the body to be tested separately. There are also other potential sources of pressure-detecting mechanisms. Birds have many air-filled spaces any one of which could be a potential pressure sensor. Thus stretch receptors in the walls of an air sac could serve as an isothermal barometer. Alternatively, sensory hairs could be used to detect air flow in and out of hollow bones in a manner analogous to the detection of fluid flow in the semi-circular canals (Lowenstein and Sand, 1940). I n any event, the findings reported here provide a foundation on which future study of the pressure capabilities of birds may be built. We thank Drs. D. R. Griffin, K. Adler, and J. Hatch for reading and criticizing an early draft of this paper. This work was supported by an NSF Graduate Fellowship to M. Kreithen, a grant from the Conlell Office of Sponsored Research, and NSF Research Grants GB 13046X and GB 35199X to W. T. Keeton.

References Bagg, A. ~L, Gunn, W. W. H., Miller, D. S., Nichols, J.T., Smith, W., Wolfarth, F. P. : Barometric pressure patterns and spring bird migration. Wilson Bull. 62, 5-19 (1950)
6 J. comp. Physiol., Vol. 89

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M. L. Kreithen and W. T. Keeton

Beecher, W. J.: A possible navigation sense in the ear of birds. Amer. Midland Naturalist 46, 367-384 (1951) Beecher, W. J. : On coriolis force and bird navigation. Sci. Monthly 79, 27-31 (1954) Broun, M. : Hawks Aloft, 222 p. New York: Dodd-Mead 1949 Bruderer, B.: Radarbeobachtungen fiber den Friihlingszug im Sehweizerischen Mittelland. Ornithol. Beob. 68, 89-158 (1971) Cohen, D. H., MacDonald, R. L.: Some variables affecting orienting and conditioned heart rate responses in the pigeon. J. comp. physiol. Psychol. 74, 122-133 (1971) Critchfield, I-I. J. : General climatology, 2nd ed., 420 p. Englewood Cliffs, N. J. : Prentice Hall 1966 Dressier, F. B.: On the pressure sense of the ear and "facial vision." Amer. J. Psychol. 5, 344-350 (1893) Griffin, D. 1~.: The physiology and geophysics of bird navigation. Quart. l~ev. Biol. 44, 255-276 (1969) Griffin, D. 1~.: Nocturnal bird migration in opaque clouds. In: Galter, S., SehmidtKoenig, K., Jacobs, G., Bellville, 1~., eds., Animal Orientation and Navigation, A Symposium. NASA SP 262. Washington, D. C.: U. S. Govt. Printing Office 1972 Hassler, S. S., Graber, 1~. 1~., Bellrose, F. C. : Fall migration and weather, a radar study. Wilson Bull. 75, 56-77 (1963) Lehner, P. N., Dennis, D. S. : Preliminary research on the ability of ducks to discriminate atmospheric pressure changes. Ann. N. Y. Acad. Sci. 188, 98-109 (1971) Lowenstein, O., Sand, A.: The individual and integrated activity of the semicircular canals of the elasmobranch labyrinth. J. Physiol. (Load.) 99, 89-101 (1940) Masher, J . W . , Stolt, B.: Lufttryckets inverkan pa ortolansparvens (Emberiza hortulana. L.) aktivitet under varflyttningsperioded. Var Fagelvarld 20, 97-111 (1961) Muller, E. E.: Effects of weather on the night time activity of White-throa~d Sparrows. Masters Thesis, Cornell University (1972) Nisbet, I. C. T.: Atmospheric turbulence in bird flight. Brit. Birds 48, 557-599 (1955) Nisbet, I. C. T., Drnry, W. H., Jr. : Short term effects of weather on bird migration: a field study using multivariate statistics. An. Behav. 16, 496-530 (1968) Richardson, W. J., Gunn, W. W. H.: Radar observations of bird movements in east-ceritral Alberta. Can. Wildlife Service Report Series Number 14:35-68 (1971) Richardson, W. J., ttaight, M.E.: Migration departures from starling roosts. Canad. J. Zool. 48, 31-39 (1970) Tuge, H., Shima, I., Koga, K. : Defensive conditioned reflexes in pigeons. Physiol. J. U.S.S.R. (Seehenov) 48, 766-776 (1957) Melvin L. Kreithen and William T. Keeton Division of Biological Sciences Langmuir Laboratory, Cornell University Ithaca, New York 14850, USA