Field studies of avian nocturnal migratory orientation II. Experimental manipulation of orientation in white-throated sparrows (Zonotrichia albicollis) released aloft

Anim. Behav., 1982, 30, 768-773

FIELD STUDIES OF AVIAN NOCTURNAL MIGRATORY ORIENTATION II. EXPERIMENTAL MANIPULATION OF ORIENTATION IN WHITE-THROATED SPARROWS (ZONOTRICHIA ALBICOLLIS) RELEASED ALOFT BY KENNETH P. ABLE, VERNER P. BINGMAN, PAUL KERLINGER & WILLIAM GERGITS

Departrnent of Biological Sciences, State University of New York at Albany, Albany, New York, 12222 Abstract; Migrant white-throated sparrows (Zonotrichia albicollis) were released from boxes carried aloft by balloon and tracked with radar. All birds were released on clear nights when winds were light and opposed to the normal migration direction for the season. Birds were treated in one of two ways: Lens birds were fitted with frosted lenses prior to release; No Lens birds were released without lenses. No Lens birds that engaged in straight and level flight generally headed in the predicted migratory direction and as a group were not oriented with respect to wind direction. Lens birds did not head in the predicted migratory direction, but instead oriented downwind. This orientation behaviour is consistent with the relationship of orientation cues inferred from the field observations described in part I of this paper. The data show that flying birds deprived o f all detailed form vision can determine wind direction. In part I of this paper, Able (1982) described the relationships among stars, sun and wind direction as cues in the orientation of nocturnal passerine bird migrants. Based on data from free-flying wild birds obtained with tracking radar and portable ceilometers, it appeared that either the stars or sun near sunset was sufficient to enable the birds to select an appropriate migratory heading. If solid overcast precluded use of both visual cues, the birds resorted to downwind orientation even when this resulted in flight in a seasonally inappropriate direction. These data were drawn from a swarm of migrants that may contain as many as 75 species and individuals of varying age, experience, and migratory goal. Overcast skies and opposed winds are unfavourable conditions for nocturnal migration and the number of birds aloft on such nights is usually markedly reduced. It cannot be assumed that the migrants aloft under such conditions represent a random sample of the potential migrant pool; thus one may question whether the different conditions may be legitimately compared. We have attempted to test some of the predictions of these field observations by releasing and radar tracking individuals of a single species, the white-throated sparrow (Zonotrichia albicollis). Specifically, we have examined the relationships between visual and non-visual cues by releasing control individuals and birds wearing frosted lenses under identical nighttime conditions.

Methods Single white-throated sparrows were released at night from boxes carried aloft by heliumfilled balloons using procedures essentially identical to those described by Demong & Emlen (1978). The birds were captured during migration at the release site (Berne, Albany County, New York) and held in activity cages. Individuals with large amounts of subcutaneous fat and showing intense nocturnal restlessness were preferentially selected for release. Demong & Emlen (1978) have found that the likelihood that a given bird will initiate what appears to be migratory flight upon release is a function of these variables. No later than 1 h before dark the birds were transferred to a light-tight carrying case. They were removed individually and placed in the cardboard release boxes no sooner than 30 min prior to launching. Frosted lenses were made of clear vacuumformable vinyl (5 mil thickness) using a Mattel Vac-u-Form (Mattel, Inc.) with a 7-mm steel ball bearing as the form. To make the lenses translucent, we lightly sanded the entire outer surface with fine emery paper until it became uniformly cloudy in appearance. Through these lenses one is unable to resolve even the most contrasting forms at more than 2 cm. Only the grossest patterns of light and dark are visible at greater distances. The lenses were lightly lubricated with vaseline and gently inserted under the eyelids of the bird. They were 768

ABLE ET AL.: ORIENTATION OF RELEASED BIRD MIGRANTS

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a n d 27 lens-bearing birds (24 in the spring, three in the fall). O f the tracks o f the N o Lens birds, three were too short to be useful ( < 100 m), f o u r h a d evidence t h a t the r a d a r h a d switched to a n o t h e r bird, one was very nonlinear (r o f headings < 0.40), a n d eight descended at rates greater than 5 m/s (b/ised on criteria established by D e m o n g & Emlen 1978). These tracks have been excluded f r o m analysis; descriptive d a t a on the r e m a i n i n g 17 tracks are given in T a b l e I. One t r a c k o f a Lens b i r d was t o o short, two h a d switches, three were n o n linear, a n d 11 descended steeply; d a t a o n the r e m a i n i n g 10 tracks are in T a b l e I2 O f the released birds that engaged in m o r e o r less straight a n d level flight, as defined above, a large p r o p o r t i o n still descended g r a d u a l l y over the relatively s h o r t distances t h a t they were tracked. Just over h a l f (59 ~ ) o f the N o Lens birds a n d 8 0 ~ o o f the Lens birds descended steadily. These figures u n d o u b t e d l y reflect b o t h the m o t i v a t i o n o f b i r d s to initiate m i g r a t i o n u n d e r u n f a v o u r a b l e weather conditions a n d the effects o f the visual i m p a i r m e n t experienced by

held in place by the eyelids a n d did n o t actually rest on the c o r n e a o f the b i r d ' s eye. Tests perf o r m e d on caged birds showed t h a t birds were able to remove t l e plastic lenses after several hours. W e m a d e releases u n d e r n a r r o w l y defined conditions. Skies were essentially clear so that m o s t stars were visible. W i n d s were light a n d o p p o s e d to the n o r m a l direction o f m i g r a t i o n for the season. Birds were released only after all visible traces o f sunset glow h a d d i s a p p e a r e d . T h e individual 5- o r 10-s t r a c k segments were used to c o m p u t e a m e a n t r a c k direction, a n d the length o f this resultant vector (r) gives a n i n d i c a t i o n o f the straightness o f the t r a c k (see Batschelet 1975). W i n d velocities o b t a i n e d f r o m the t r a c k o f the b a l l o o n carrying the b o x were used to c o m p u t e headings a n d air speeds for each o f the respective t r a c k segments b y the triangle o f velocities. Results

W e have released 33 w h i t e - t h r o a t e d s p a r r o w s w i t h o u t lenses (17 in the spring, 16 in the fall)

Table I. Details of Tracks of White-throated Sparrows Released Aloft

Date No Lens

11May1978 25May 1978 29May 1977 31 May 1979 1 June 1978 8 June 1977 9Oct. 1978

21Oct. 1978 1 Nov. 1977

Alt. range (m)

2000 2215 2040 2115 2350 2455 2030 2120 2340 1935 1950 2010 1840 1855 1855 1955 2010

1119-1238 1116--1000 995-1060 1599-1710 1672-1458 1508-1366 1031- 665 1867-1571 1294-1520 865-1089 975-868 875-701 1038-543 673-553 1266-2196 1161-1299 963-1082

135 ~ 240 265 298 110 130 90 75 75 85 86 85-100 50 50 35 35 355

8m/s 10 5 2 8 6 10 9 10 14 18 17-10 10 10 7 7 7

18 236 55 330 66 95 57 78 65 100 99 118 103 69 358 10 60

0.97 0.79 0.59 0.71 0.88 0.88 0.83 0.97 0.99 0.84 0.99 0.90 0.43 0.67 0.82 0.89 0.47

347 208 69 358 17 74 42 88 27 170 150 128 190 123 321 328 96

0.99 0.49 0.63 0.54 0.84 0.79 0.87 0.90 0.92 0.52 0.89 0.63 0.51 0.66 0.69 0.58 0.44

14.2 1.3 16.9 9.2 8.6 13.7 18.4 6.0 5.8 3.6 5.6 10.1 10.6 3.6 10.0 8.9 9.5

2145 2310 2140 2205 2230 2320 2050 2110 2130 2240

450-145 1170-1054 1038-292 1499-1949 1312-958 1495-1148 1018-869 960-837 1516--880 1280-2088

220 200 335 75 30 45 90 90 115 100

6 8 5 10 6 7 10 10 7 6

233 235 302 77 82 89 137 122 85 95

0.99 0.85 0.80 0.98 0.99 0.97 0.88 0.98 0.43 0.78

249 254 275 79 108 123 190 164 39 67

0.99 0.67 0.63 0.89 0.99 0;98 0.99 0.91 0.38 0.75

1.4 10,1 2.7 6.9 10.8 8.8 10.8 7.8 4.1 1.0

Wind velocity

Track direction ~ r

Heading direction r

Mean air speed (m/s)

Time (EST)

Lens

25May1978 29May 1977 8June 1977 1June 1978

ANIMAL

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BEHAVIOUR,

the Lens birds. Unfortunately, we cannot say whether these birds continued to descend and landed or eventually levelled off and continued to fly. Although there was considerable interindividual variability, the air speeds of the N o Lens birds were generally typical of passerine nocturnal migrants and the mean of 9.2 m/s was identical to the average reported by Demong & Emlen (1978) for released birds of the same species. There was a tendency for the Lens birds to have lower air speeds; most notably none had air speeds as high as the higher cases among N o Lens birds. This trend is not surprising, but the difference between the groups (No Lens :~ = 9 . 2 m/s, SO = 4.7 m/s; Lens ~ = 6.4 m/s, SD == 3.9 m/s) was not statistically significant ( M a n n Whitney U-test, one-tailed). For those tracks that were sufficiently long, wingbeat signatures from the error signal of the automatic gain control circuit (AGC) showed that nearly all of the No Lens birds and some of the Lens birds adopted the 'flap-pause' flight pattern typical of passerine nocturnal migrants. We conclude that once steeply descending and climbing birds were eliminated, the two groups exhibited comparable flight behaviour. Figure 1 presents summaries of the flight orientation of the released birds. In the spring releases, the mean track and heading directions of the N o Lens birds were significantly oriented toward the northeast (resultant of mean track directions = 52.9 ~ r = 0.61, P < 0.05, Rayleigh test; resultant o f mean heading directions = 39.5 ~ r = 0.62, P < 0.05, Rayleigh test), the predominant direction of spring migration in eastern New York (Able 1974, and unpublished data). Most of the smaller number of autumn

.

~

,. s SPRING CONTROLS

L_

~Ns FALL CONTROL6

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No Lens birds headed southeast and had track directions toward the east, but two birds heading in nearly the opposite direction rendered the distribution of headings not significantly oriented (resultant of mean track directions-~ 72.3 ~ r = 0.75, P < 0.01, Rayleigh test; resultant of mean heading directions -- 141.5 ~ r --=-0.40, P < 0.10, Rayleigh test). Autumn migration in a southeastward direction is of regular occurrence in this region and it is the predominant orientation direction of white-throated sparrows in orientation cages (Bingman & A b l e 1979, and unpublished data). Thus in both seasons, most birds released without translucent lenses headed in a direction consistent with the known behaviour of free-flying birds and the orientation of this species in circular cages. In contrast, the headings of the No Lens birds that were excluded a priori because of steep descent rates ( > 5 m/s) yielded no significant direction in either spring or fall. This difference supports the idea that the birds that did not descend steeply exhibited real migratory behaviour. The compass headings of Lens birds are also shown in Fig. 1 (all are from spring). Neither the distribution of headings nor that of tracks was significantly oriented by the Rayleigh test and neither mean was in the expected direction for the season (resultant of mean track directions = 111.4 ~ r = 0.43; resultant of mean heading directions = !42.3 ~ r = 0.25). Under comparable conditions, birds with unimpaired vision were usually able to orient in the appropriate seasonal migratory direction, whereas those wearing lenses did not. There was also a clear difference between Lens and No Lens birds when their headings were examined with respect to the wind direction at their flight altitudes (Fig. 2). Lens birds headed significantly downwind (resultant of mean heading directions with respect to downwind (set at DOWNWIND

DOWNWIND

" \ " ~ - ~ " Ns LENS CONTNOLS

Fig. 1. Compass headings (mean of alI segments of the radar tracks) of the released birds. Left circle shows No Lens birds released in spring, middle circle shows No Lens birds released in fall, and right circle shows Lens birds (all spring). Significance levels refers to Rayleigh tests on the distributions.

LENS

Fig. 2. Headings of released birds plotted with respect to wind direction (downwind is at the top of each circle). Open circles refer to fall releases, solid circles to spring releases. Significance levels refer to V-tests with downwind as the predicted direction.

ABLE ET AL.: ORIENTATION OF RELEASED BIRD MIGRANTS 0 ~ = 31.6~ r = 0.55; P < 0.05, Rayleigh test; P < 0.025, V-test with downwind as predicted direction; resultant of mean track directions with respect to downwind -- 17.1~ r = 0.87; P < 0.001, Rayleigh test; P < 0.0005, Vtest with downwind as predicted direction). The headings of No Lens birds were not oriented with respect to wind direction (r = 0.22). Because of the drifting effects of wind, their track directions were significantly oriented downwind (resultant of mean track directions --- 0.2~ r = 0.67; P < 0.001, Rayleigh test; P < 0.0005, Vtest). (For both Lens and No Lens groups, no significant downwind trend in headings was evident among those birds excluded a priori because of steeply descending tracks.) We co~clude that the Lens birds oriented their flight with respect to the downwind direction whereas No Lens birds headed in directions independent of the wind. It was surprising how few birds of both types showed signs of disorientation. The results for only three birds wearing frosted lenses and one No Lens bird had a distribution of headings suggesting randomness (these distributions cannot be tested statistically for orientation because the track segments are not independent). One can, however, compare the straightness of the series of headings comprising each flight using the r values measuring vector length. There is no significant difference between Lens and No Lens birds in this regard (Mann-Whitney U-test, two-tailed). Thus, even birds with severely impaired vision were able to maintain a compass heading selected within a very few seconds after release from the box. Discussion

In assessing the box release technique, Demong & Emlen (1978) developed five criteria that would be indicative of normal migratory behaviour on the part of released birds: (1) a large percentage of the birds should maintain altitude and initiate long-distance flights; (2) the proportion of released birds that initiate migratory flights should correlate with the internal physiological state of the bird (e.g. amount of subcutaneous fat); (3) the proportion of released birds initiating flight should be greatest when weather conditions are favourable for natural migration; (4) released birds should show the 'flap-pause' wingbeat pattern typica ! of passerine nocturnal migrants; and (5) the flight directions of released birds should be oriented in a migratory direction. Our releases of No Lens

771

birds are essentially a successful replication of the control releases performed by Demong & Emlen wifll the same species at Wallops Island, Virginia. With respect to their criteria, our results were quite comparable. Approximately 257o of the No Lens birds appeared to land shortly after release. This figure is essentially the same as that reported by Demong & Emlen for birds released under 'inhibitory' weather conditions (our releases were always made in opposed winds). These birds did not orient in the predicted seasonal direction. Both No Lens and Lens birds showed flap-pause wingbeat patterns, although the Lens birds were less consistent in this regard. Our air speeds were comparable to the average they reported. The orientation of the control birds that maintained altitude was generally in the appropriate seasonal direction and suggests that most of these birds initiated at least short duration migratory flights upon release from the boxes. This criterion cannot be used to infer anything about the behaviour of the Lens birds because their headings were not oriented with respect to true compass directions. In addition, all but two descended steadily throughout the length of their tracks. It is, therefore, less convincing that they were exhibiting migratory behaviour; however, they were oriented with respect to wind direction versus those Lens birds that descended steeply and presumably landed. Assuming for the moment that the behaviour of both groups of birds was a product of migratory motivation, the orientation of the birds was essentially what we would have predicted from the behaviour of wild migrants described in part 1 of this paper (Able 1982). No Lens birds with full access to nighttime visual cues including stars were able to rapidly select an appropriate migratory direction. Lacking visual orientation information, Lens birds behaved much like wild migrants deprived of such information by overcast. They flew more or less straight and level, but oriented downwind rather than in the appropriate seasonal direction selected by No Lens birds released on the same nights. There is, however, an important difference between the Lens birds in these experiments and wild birds flying under solid overcast. Both are deprived of the celestial cues usually presumed to be used in migratory orientation, but the unmanipulated migrants have a full view of the cloud-covered sky, the horizon and the land-

772

ANIMAL

BEHAVIOUR,

scape below. Their downwind orientation could be effected in several ways involving stationary features on the ground (e.g. by maximizing ground speed). These options were not open to the Lens birds, which were essentially flying blind. It is extraordinary that they were able, even crudely, to determine wind direction in flight without aid o f external visual reference cues. It is even more remarkable that they could do so within a few seconds of release from the box. Any knowledgeable pilot will attest to the near impossibility of this task. Yet the Lens birds had significant downwind velocities re the air, i.e. they were actively flying downwind, not being simply drifted with the wind. 9How a bird might determine the wind direction within the air mass in which it is flying has generated considerable speculation in the literature (Nisbet 1955; Bellrose 1967; Griffin 1969, 1973; Emlen 1975; Able 1977, 1980). Any method involving assessment of ground speed or lateral drift displacement seems to be ruled out in this case because of the visual impairment. Fine-scale gust anisotropy remains a theoretical possibility and there is much evidence that such atmospheric structure exists on a scale usable by migrating birds. Its occurrence is, however, highly variable in time and space. Even though the birds do not appear to determine wind direction with great precision (Fig. 2), based on present knowledge it seems unlikely that reliable information on wind direction could be extracted from gust structure in a few tens of seconds by a flying bird (J. C. Kaimal, personal communication). The only other data that are comparable to our Lens birds are the homing pigeons fitted with frosted lenses and released by Schlichte and Schmidt-Koenig (Schmidt-Koenig & Schlichte 1972; Schlichte 1973). In wind speeds greater than Beaufort 3, the pigeons wearing frosted lenses actively flew downwind, ' . . . vanishing faster and sometimes--depending upon wind direction--straight opposite of controls (wearing clear lenses) that were beating into the wind' (Schmidt-Koenig, personal communication). The behaviour of the pigeons can be visually observed upon release and might shed some light on the means by which they determine the wind direction. The obvious similarity between the behaviour of these pigeons and our Lens birds suggests that downwind orientation may constitute a general adaptive response to such visual impairment.

30,

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If the flights of both Lens and No Lens birds were migratory in nature, the results o f these experiments with a single short-distance nocturnal migrant species closely paralleled observations on free-flying birds tracked from among the swarm of wild migrants. We have shown that stars alone seem sufficient for appropriate migratory orientation even if winds are opposed. Depriving the birds of visual input from stars or the ground below resulted in downwind orientation, suggesting that under these conditions of very rapid decision-making birds are unable to determine the correct migratory direction in the absence of visual cues. Birds wearing frosted lenses were able to orient with respect to wind direction very rapidly after release, suggesting that an as yet unknown mechanism enables a flying bird to determine the wind direction in the absence of detailed visual information.

Acknowledgments We wish to thank S. T. Emlen and N. J. Demong for discussing details of the release technique with us, K. Schmidt-Koenig for providing unpublished data on pigeons wearing frosted lenses, and J. C. Kaimal for discussing atmospheric gust structure. H. V. B. Hirsch kindly loaned us his Vac-u-Form device. This research was generously supported by a National Science Foundation grant to K. P. A. Birds used in these studies were obtained and housed under Federal Scientific Collecting permit PRT 2-605 NY, Federal Bird Marking and Salvage Permit 20269, and New York Scientific Collector's License 0668. REFERENCES Able, K. P. 1974. Wind, track, heading and the flight orientation of migrating songbirds. In: Proc. Conf. Biol. Aspects of the Bird/Aircraft Collision Problem

(Ed. by S. A. Gauthreaux), pp. 331-357. Clemson, S.C. Able, K. P. 1977. The flight behaviour of individual passerine nocturnal migrants: a tracking radar study. Anita. Behav., 25, 924-935. Able, K. P. 1980. Mechanisms of orientation, navigation and homing. In: Animal Migration, Orientation and Navigation (Ed. by S. A. Gauthreaux), pp. 283-373. New York: Academic Press. Able, K. P. 1982. Field studies of avian nocturnal migratory orientation. I. Interaction of sun, wind and stars as directional cues. Anita. Behav., 30, 761767. Batschelet, E. 1965. Statistical Methods for the Analysis of Problems in Animal Orientation and Certain Biological Rhythms. Washington, D. C.: A.I.B.S.

monograph. Bcllrose, F. C. 1967. Radar in orientation research. Proe. XIV Int. Ornithol. Congr., 281-310.

ABLE ET AL.: ORIENTATION OF RELEASED BIRD MIGRANTS Bingman, V. P. & Able, K. P. 1979. The sun as a cue in the orientation of the white-throated sparrow, a nocturnal migrant. Anim. Behav., 27, 621-622. Demong, N. J. & Emlen, S. T. 1978. Radar tracking of experimentally released migrant birds. Bird_Banding, 49, 342-359. Emlen, S. T. 1975. Migration: orientation and navigation. In: Avian Biology, Vol. 5 (Ed. by D. S. Farner & J. R. King), pp. 129-219. New York: Academic Press. Griffin, D. R. 1969. The physiology and geophysics of bird migration. Q. Rev. Biol., 44, 255-276. Griffin, D. R. 1973. Oriented bird migration in or between

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opaque cloud layers. Proc. Am. phil. Soc., 117, 117-141. Nisbet, I. C. T. 1955. Atmospheric turbulence and bird flight. Br. Birds., 48, 557-559. Schlichte, H. J. 1973. Untersuchungen i2ber die Bedeutung optischer Parameter fiir das Heimkehrverhaltela der Brieftaube. Z. Tierpsychol., 32, 257-280. Schmidt-Koenig, K. & Schlichte, H. J. 1972. Homing in pigeons with impaired vision. Proc. Nat. Acad. Sci., 69, 2446-2447.

(Received 12 August 1981; revised 14 December 1981; MS. number: A2705)