RESEARCH ARTICLE Atmospheric propagation modeling indicates homing pigeons use loft-specific infrasonic ʻmapʼ cues

Transcription

1 687 The Journal of Experimental Biology 216, Published by The Company of Biologists Ltd doi:1.1242/jeb RESERCH RTICLE tmospheric propagation modeling indicates homing pigeons use loft-specific infrasonic ʻmapʼ cues Jonathan T. Hagstrum US Geological Survey, Menlo Park, C 9425, US jhag@usgs.gov SUMMRY Results from an acoustic ray-tracing program using daily meteorological profiles are presented to explain ʻrelease-site biasesʼ for homing pigeons at three experimental sites in upstate New York where W. T. Keeton and his co-workers at Cornell University conducted extensive releases between 1968 and 1987 in their investigations of the avian navigational ʻmapʼ. The sites are the Jersey Hill and Castor Hill fire towers, and another near Weedsport, where control pigeons from the Cornell loft vanished in random directions, in directions consistently >5 deg clockwise and in directions ~15 deg clockwise from the homeward bearing, respectively. Because Cornell pigeons were disoriented at Jersey Hill whereas birds from other lofts were not, it is inferred that Jersey Hill lies within an acoustic ʻshadowʼ zone relative to infrasonic signals originating from the Cornell loftʼs vicinity. Such signals could arise from ground-to-air coupling of near-continuous microseisms, or from scattering of direct microbaroms off terrain features, both of which are initially generated by wave wave interactions in the deep ocean. HRP runs show that little or no infrasound from the loft area arrived at Jersey Hill on days when Cornell pigeons were disoriented there, and that homeward infrasonic signals could have arrived at all three sites from directions consistent with pigeon departure bearings, especially on days when these bearings were unusual. The general stability of release-site biases might be due to influences of terrain on transmission of the homeward signals under prevailing weather patterns, whereas short-term changes in biases might be caused by rapid shifts in atmospheric conditions. Supplementary material available online at Key words: avian navigation, avian map, Columba livia, release-site bias, infrasound, microbarom, microseism. Received 22 March 212; ccepted 17 October 212 INTRODUCTION fter more than 5 years of intensive study, how homing and migratory birds navigate over great distances remains an open question (Kennedy and Norman, 25). Kramer s (Kramer, 1952) early work on avian orientation with circular cages showed that many birds use the Sun s azimuthal position as a time-compensated compass, and he proposed a simple map-and-compass model to explain their navigational behavior (Kramer, 1953). Support for this model has come from experiments in which homing pigeons have had their internal clocks shifted prior to release: pigeons depart release sites generally in the homeward direction, but those with their biological clocks shifted slow (or fast) with altered light:dark cycles will depart clockwise (or counterclockwise) off the homeward direction in the northern hemisphere (Schmidt-Koenig, 1958; Wiltschko et al., 1994). pparently, the clock-shifted birds have correctly determined their location relative to home ( map step) before incorrectly interpreting the homeward bearing from the Sun s azimuth within a shifted time frame ( compass step). Other avian compasses are known to depend on rotation of the stars (Emlen, 1975), inclination of the geomagnetic field (Wiltschko and Wiltschko, 1995) and patterns of skylight polarization (Muheim et al., 26), but the long-range avian map has yet to be understood. lthough the sensory basis of the avian map has been rigorously investigated, no consensus has been reached on which sense or senses are involved (Semm and Beason, 199; Wiltschko, 1996; Wallraff, 25). The possibility of birds using visual landmarks for crucial long-range map cues has been eliminated because pigeons fitted with frosted lenses can return from unfamiliar sites >1 km away to within a few kilometers of their loft; sight, however, is required for their final approach (Schmidt-Koenig and Schlichte, 1972; Schmidt-Koenig and Walcott, 1978). Natural infrasounds (low-frequency acoustic waves below the range of human hearing; <2 Hz) have also been considered as possible map cues (Griffin, 1969; Yodlowski et al., 1977; Quine, 1982), but no perennial geographic sources were recognized, and no clear evidence of their use by birds was found (Walcott, 1996). Laboratory tests, however, show that homing pigeons can detect sounds down to at least.5 Hz (Kreithen and Quine, 1979), and infrasonic cues remain an attractive option for long-range homing because these signals can travel thousands of kilometers in the atmosphere with little attenuation. Other experimental results have been interpreted in support of the alternate concepts of birds using either olfactory (Papi, 1989; Wallraff, 25) or magnetic cues (Walker et al., 22; Wiltschko and Wiltschko, 29) as sources of map information. It is difficult to envision, however, how birds can accurately navigate over great distances using as yet unidentified odors that would have to form stable gradients within a turbulent atmosphere. Moreover, empirical evidence indicates that such gradients are unlikely to exist (Becker and van Raden, 1986; Waldvogel, 1987; Waldvogel, 1989). It has also been suggested that birds use gradients of the geomagnetic field (Wiltschko and Wiltschko, 29), but the poleward gradient in total intensity (<4 nt km 1 ), for instance, would likely be obscured by

2 688 The Journal of Experimental Biology 216 (4) commonly observed crustal magnetizations (~1 5 nt km 1 ) and/or diurnal field variations (~2 3 nt day 1 ) of equivalent or greater magnitude. One or more additional geophysical gradients with E W orientation, necessary for bicoordinate navigation, are also unknown and likely non-existent on large scales. Because the olfactory and magnetic map hypotheses are unresolved, it is possible that birds are using a different set of map cues. Furthermore, birds might not be using a bicoordinate map at all (Gould, 28), and could be employing some other means of determining their homeward orientation (the term map, however, will be used here throughout for convenience). Both Kramer (Kramer, 1959) and Keeton (Keeton, 1973) believed that release-site biases and sites of long-term disorientation are related to irregularities in the avian navigational map. Release-site biases are regular deviations in the orientations of departing birds off the geographic homeward direction and are found at most sites to varying degrees. Moreover, they tend to be consistent at any one site for pigeons from a given loft (Keeton, 1974; Wallraff, 25). lthough generally stable through time, the biases can also change on an hourly, daily or yearly basis (Wallraff, 25). dditionally, at some release sites pigeons can be completely lost, departing year after year in random directions (Keeton, 1974; Walcott and Brown, 1989). Schmidt-Koenig (in Brown, 1971) pointed out that sites of disorientation are not uncommon, and suggested that at least one such site exists at varying directions and distances to all lofts. In his investigations of avian navigation, Keeton (Keeton, 1973; Keeton, 1974) concentrated pigeon releases at three sites in upstate NY (Fig. 1) that he felt had particular significance to understanding the avian map: the Jersey Hill fire tower, 12 km W of the Cornell loft in Ithaca, where Cornell birds vanished randomly (Keeton, 1974; Walcott and Brown, 1989); the Castor Hill fire tower, 143 km NNE of the Cornell loft, where birds consistently showed large westward or clockwise biases (~5 to 9 deg) from the homeward direction (Keeton, 1973; Keeton, 1974); and a site near Weedsport, 74 km N of the Cornell loft, where the birds regularly vanished ~15 deg clockwise off the homeward direction (Keeton, 1974; Keeton et al., 1974; Larkin and Keeton, 1976). To determine whether release site biases could be due to atmospheric and/or topographic influences on the transmission of infrasonic cues to pigeon release sites, as suggested previously (Hagstrum, 2), atmospheric propagation modeling incorporating daily meteorological profiles was undertaken for those days birds were released at Jersey Hill, Castor Hill and Weedsport using a raytracing program [Hamiltonian coustic Ray-tracing Program for the tmosphere (HRP)] (Jones et al., 1986). Ray-tracing theory, in particular, was selected so that propagation directions of the modeled infrasound could be compared with departure bearings of the experimental birds. fter Bill Keeton s untimely death in 198, an extensive database containing most of his published and unpublished pigeon (Columba livia) release data was made available to all researchers upon request (Brown et al., 1984). MTERILS ND METHODS tmospheric infrasounds Infrasounds can travel great distances through the atmosphere with little attenuation. coustic absorption increases as the square of frequency, so, for example, 9% of the energy of a 1 Hz tone is absorbed by 7 km (at sea level), and the distance for 9% absorption of a 1 Hz tone of equivalent initial energy is 3 km, whereas at.1 Hz this distance exceeds the circumference of Earth (Bedard and Georges, 2). In addition, pressure waves from exceptionally powerful explosions (e.g. the Krakatau eruption in New York State Jersey Hill fire tower Lake Ontario Weedsport Castor Hill fire tower 3 km Cornell loft Fig. 1. Digital elevation model (DEM) of the Finger Lakes region of upstate NY, US (see inset), showing locations of the Cornell loft ( N, W) just E of Ithaca, near the southern tip of Lake Cayuga, and experimental pigeon release sites at the Jersey Hill ( N, W) and Castor Hill ( N, W) fire towers, 12 km W and 143 km NNE of the loft, respectively. The location of the Weedsport release site ( N, W) is also shown, 74 km N of the loft. 1883, the Tunguska meteorite in 198 and nuclear tests during and after 1945) have been recorded after traveling several times around Earth (Evers and Haak, 21). t lower frequencies, wavelengths become longer, and are ~34 m for 1 Hz and ~3.4 km for.1 Hz tones (Bedard and Georges, 2). The static sound speed (C t ) is proportional to the square root of air temperature in K (Fig. 2), and travel directions of infrasonic waves (ray paths) are controlled primarily by temperature and horizontal wind (Norris et al., 21). dding or subtracting the horizontal wind speed to C t in the direction of propagation determines the effective sound speed (C eff ), which is calculated by HRP and accounts for the combined refractive effects of temperature and wind. Refraction of rays from a ground source back towards the surface occurs at heights in the atmosphere where C eff is greater than the surface value and can be caused by increasing wind speed (wind shear), temperature (inversions) or both (Evers and Haak, 21). Horizontal winds also create a moving medium by which sound waves are translated through advection. The normal temperature structures of the troposphere and mesosphere bend infrasonic waves upward, whereas those of the stratosphere and thermosphere refract them back towards the surface (Fig. 2). Sounds refracted upward can cause zones of silence or acoustic shadow zones up range at ground level that end where the waves return to the surface from either stratospheric or thermospheric reflections. tmospheric conditions affecting infrasound propagation can change rapidly (Norris et al., 21), and seasonal and geographic changes in atmospheric structure are also known to complicate the travel paths of infrasounds from distant sources (Bedard and Georges, 2). Historical pigeon releases Between 1968 and 1987, 984 experimentally untreated or control birds from the Cornell loft were individually released on 81 days under sunny skies at the Jersey Hill fire tower (Fig. 1). In almost

3 Homing pigeons use infrasonic ʻmapʼ cues 689 ltitude (km) Speed of sound (m s 1 ) Distance (km) 89 deg deg 69 deg deg Mesosphere 29 deg 39 deg (return) Temperature 19 deg 9 deg 1 Troposphere Zone of silence Thermosphere Stratosphere deg (return) Sound speed 3 K C Temperature Fig. 2. Cross-section of Earthʼs atmosphere showing vertical profiles of temperature and static sound speed (thick lines), which have positive and negative gradients that define the atmosphereʼs main layers. Computed ray paths of sound waves without wind (thin lines) show both stratospheric and thermospheric returns with distance from the source at km altitude and km distance (see Materials and methods, tmospheric infrasounds). Values next to ray paths indicate initial launch angles of rays from horizontal. The classic ʻzone of silenceʼ at ground level is between the source and first ground reflection of a return ray from the stratosphere (after Donn, 1978). all cases, the birds departed randomly or nearly so (Fig. 3) (Walcott and Brown, 1989). Moreover, homing performance was poor: Cornell pigeons released at Jersey Hill had longer flight times and much higher attrition rates than birds released at other sites in NY and P (Keeton, 1974; Walcott and Brown, 1989). irplane tracking of pigeons released from Jersey Hill showed that they flew aimlessly about the area for at least 45 min (Keeton, 1974). Birds returned to and released at Jersey Hill a second and third time had no improvement in homing performance, unlike birds repeatedly released at other sites (Keeton, 1974). Groups of pigeons with small magnets or brass bars attached to them (Keeton, 1971) were also similarly lost at Jersey Hill (supplementary material Fig. S1,B), and aeromagnetic maps and magnetic surveys made at Jersey Hill showed no indication of an anomalous field there (Brown, 1971; Walcott and Brown, 1989). Remarkably, birds from other lofts located at various directions and distances from Jersey Hill (N, 97 km; ENE, 113 km; W, 121 km; SE, 354 km) were able to orient there and return home to these lofts (Walcott and Brown, 1989), even on those days when Cornell birds were disoriented and homed poorly (e.g. Fig. 3B,C). Walcott and Brown (Walcott and Brown, 1989) conducted a series of experiments at Jersey Hill and concluded that it was not the genetic stock of the birds, but the location of their loft, that determined whether or not they could orient at Jersey Hill. Results for one release at Jersey Hill on 13 ugust 1969 stand out: on this day Cornell pigeons were well oriented (Fig. 3D), and their vanishing bearings were tightly clustered to the NE (Keeton, 1974). The next day the birds were returned to Jersey Hill, but they again departed randomly (Brown, 1971). Disorientation of Cornell birds was not restricted to Jersey Hill, but also occurred at other release sites in its vicinity (supplementary material Fig. S2, Table S1). The bulk of the releases made from this region were at Jersey Hill due to the excellent visibility in all directions from its fire tower. lthough departure bearings from a single release at the Castor Hill fire tower (Fig. 1) have relatively little scatter, deviations of mean vanishing bearings under both sunny and overcast skies were mostly large (>5 deg) and clockwise (Keeton, 1973). Pigeons released at Castor Hill and followed by airplane flew 25 to 32 km W before they changed course and headed S toward the Cornell loft (Walcott, 25). Young birds new to Castor Hill showed greater deviations from the homeward bearing (Fig. 4) than older, more experienced birds familiar with the release site (Fig. 4B). There was an unusual group of birds, labeled the no-bias or F birds, that exhibited lower within-release scatter and substantially smaller mean biases at Castor Hill (Fig. 4C). The offspring of these birds behaved similarly, indicating that their enhanced ability was an inherited trait (Walcott, 25). Young birds and F birds released on the same day at Castor Hill departed in significantly different directions, consistent with the mean directions for their two groups (Fig. 4D). Control birds released at other sites near Castor Hill showed similar clockwise deflections of their departure bearings off the homeward one (supplementary material Fig. S3). On one day, 22 July 197, Cornell pigeons released at Castor Hill departed in near random directions (Fig. 4E) and appeared lost (Keeton, 1973). The most releases of Cornell pigeons at any one site (295) were made from a drumlin just N of Weedsport (Fig. 1). Releases of K birds made up the largest share of these (236). K birds, named after the K index of geomagnetic activity, were experienced Cornell pigeons repeatedly released at single sites under sunny conditions to test for any correlation between their initial bearings and the daily K index at the Fredericksburg Geomagnetic Observatory (V, US) (Keeton et al., 1974; Larkin and Keeton, 1976). Groups of K pigeons with magnets or brass bars attached to them were also released at Weedsport, but again the magnets produced no significant effect (supplementary material Fig. S4). lthough the pigeons released at Weedsport were remarkably well grouped and consistent in their departure bearings (Fig. 5B), an extraordinary shift in this bearing occurred on 6 June 1974 (T. Larkin, personal communication). On 5 June 1974 (release 116) the released birds departed with a mean bearing of 175 deg (Fig. 5C), on 6 June (release 111) they departed with a mean bearing of 127 deg (Fig. 5B,D) and on 7 June (release 1113) their mean departure bearing was 179 deg (Fig. 5E). Both the K (Fredericksburg, V, US) and Kp (planetary) indices indicate that the geomagnetic field was relatively quiet during this period of time (J. L. Gannon, written communication; kp_ap.html). Data mining Sources and characteristics of the experimental pigeon release data, meteorological data and ray-tracing program HRP are described below. The Keeton database is currently available from C. Walcott

4 69 The Journal of Experimental Biology 216 (4) B C 23 Oct Oct Cornell loft 143 Gray s loft 143 Cornell loft D 13 ug 1969 E F birds Cornell loft 258 Cornell loft Fig. 3. Vanishing bearings (black circles) for untreated (control) pigeons released individually at the Jersey Hill fire tower (Fig. 1) under sunny skies. Each data point represents the bearing of an individual bird, and geographic north is at the top of the circle. Dashed lines indicate the homeward direction (Cornell loft, 85 deg; Grayʼs loft, 95 deg). The mean vector (arrow) has a bearing (ϕ) and length (r) that is for randomly oriented birds and 1 (radius of circle) for those perfectly grouped. () Cornell birds released on 81 days between 1968 and 1987 [N=984 birds released, r=.7, ϕ=16 deg (after Walcott and Brown, 1989)]. (B) Poorly oriented Cornell birds released on 23 October 1973 (N=11, r=.32, ϕ=31 deg). (C) Well-oriented pigeons from Grayʼs loft, 24 km E of Jersey Hill, also released on 23 October 1973 (N=11, r=.753, ϕ=83 deg). (D) Cornell birds released on 13 ugust 1969, the day they were best oriented with the highest r value (N=7, r=.921, ϕ=33 deg). (E) Poorly oriented Cornell F birds released on 3 days between ugust 1973 and October 1973 (N=36, r=.322, ϕ=284 deg). at Cornell University (Department of Neurobiology and Behavior, Ithaca, NY, US), and a program that sorts and displays the database (Keeton) is available from T. Larkin (bstract Tools, Brooktondale, NY, US). Unfortunately, not all of the Cornell pigeon release data for Jersey Hill are in the Keeton database, and the full data set shown in Fig. 3 is no longer available. The Keeton database contains a total of 2545 releases, and 4 of these were made at Jersey Hill ( N, W). Of these, 3 releases of mostly control birds (N=511), which were made on 26 days, were selected for this study (supplementary material Fig. S1C, Table S1). The selected releases also include untreated no-bias or F birds (Fig. 3E), and others wearing magnets and brass bars (supplementary material Fig. S1,B). The data used here are for clearly disoriented birds (supplementary material Fig. S1C), and, because of the normal geomagnetic field at Jersey Hill, it is inferred that the magnetic (or brass) bar treatments were not the cause of their disorientation. For the Castor Hill fire tower ( N, W), a total of 62 pigeon releases are in the Keeton database, and 49 releases of control birds (N=678) on 39 days are used here (supplementary material Table S2). Of the 134 releases at Weedsport ( N, W) involving untreated K birds, 78% had mean vectors with lengths (r) >.9. From these, releases on 51 days with N 6 and r.95 were selected for this study, although release 116 on 5 June 1974 was also included with a r of.944 (Fig. 5, supplementary material Table S3). Updated meteorological data are available in the lower atmosphere from more than 8 stations worldwide (Parker and Cox, 1995), and C F birds Young birds D B 18 June YRL F Old birds E 22 July Fig. 4. Vanishing bearings (black circles) for Cornell pigeons released individually at the Castor Hill fire tower (Fig. 1) under sunny skies. The diagrams are explained in the Fig. 3 legend; the homeward direction (dashed line) is 2 deg. () Young birds (<1 year old, experienced and first flight, new to site) released on 8 days between October 1971 and September 198 (N=92, r=.713, ϕ=272 deg). (B) Older birds (>1 year old, experienced, familiar with site) released on 12 days between July 1969 and September 198 (N=118, r=.761, ϕ=244 deg). (C) F birds (older, experienced, familiar with site, that show a minimum bias at Castor Hill; see Materials and methods, Historical pigeon releases) released on 1 days between June 1975 and September 1979 (N=149, r=.874, ϕ=222 deg). (D) Yearling (YRL; N=11, r=.96, ϕ=273 deg) and F (N=15, r=.882, ϕ=228 deg) birds released on the same day with significantly different (45 deg) mean departure bearings. (E) Control birds released on the day they were unable to orient and thus departed in near random directions (N=11, r=.68, ϕ=33 deg).

5 Homing pigeons use infrasonic ʻmapʼ cues 691 K birds N B C D E Mean vectors 5 June June June Fig. 5. Vanishing bearings (black circles) for Cornell pigeons released individually at the drumlin just N of Weedsport (Fig. 1) under sunny skies. The diagrams are explained in the Fig. 3 legend; the homeward direction (dashed line) is 173 deg. () K birds (yearling or older, experienced at site; supplementary material Table S3) released on 51 days between May 1972 and June 1975 (N=545, r=.966, ϕ=187 deg). The circular diagram is rotated 9 deg clockwise with north (N) to the right. (B) Mean release vectors for K birds shown in including release 111. (C) K birds released (release 116) on 5 June 1974 (N=7, r=.944, ϕ=175 deg). (D) K birds released (release 111) on 6 June 1974 (N=1, r=.952, ϕ=127 deg) when they were unusually oriented to the SE as shown in B. (E) K birds released (release 1113) on 7 June 1974 (N=6, r=.957, ϕ=179 deg) when they again showed a typical departure bearing at Weedsport. are available online from the NO/ESRL Radiosonde Database ( The rawinsonde profiles (including wind direction and speed) used in this study are from the lbany (WMO #72518; N, W) and Buffalo (WMO #72528; N, W) weather stations in upstate NY. These data were obtained daily at : and 12: GMT from instrument packages carried aloft by weather balloons that measured various atmospheric parameters and generally reached the lower stratosphere (~16 km). The 12: GMT data (8: EDT) were collected closest in time to the Cornell pigeon releases and are used here. The atmospheric HWM- 7 wind (Hedin et al., 1996; Drob et al., 28) and NRLMSIS- temperature (Picone et al., 22) models with global coverage from ground to thermosphere are also used to represent atmospheric conditions above the daily rawinsonde profiles. These two models provide statistical mean estimates for a given date, time and location that are based on data from satellite, radar, ground-based optical observations and rocket probes (Norris et al., 21). HRP is available at raytracing/. The program traces three-dimensional paths of acoustic rays through inhomogeneous atmospheres and accounts for both vertical and horizontal refraction, as well as advection (Jones et al., 1986). Zero amplitude is predicted within shadow zones, however, because the propagation effects of diffraction and scattering are not determined (Norris et al., 21). In this study, the simplest characterization of the atmosphere is made: atmosphere conditions over the entire propagation path are modeled from a single set of profiles, and it should be noted that this representation does not include fine-scale atmospheric structure or define the rangedependent environment. Topographic profiles between the virtual transmitter and receiver (release site), defining the reflecting terrain s height (Jones, 1982), can also be entered into the program. HRP accepts only terrain models having smooth surfaces with continuous slope and curvature, and both weather and topographic profiles were represented in HRP by fitted sequences of linear segments, joined with hyperbolic functions, which effectively smoothed the data sets (Jones et al., 1986). HRP launches rays at any azimuth and elevation (angle from horizontal), and program runs were generally made between ±9 deg of the direct azimuth to a given release site at 5, 1 or 2 deg intervals. Within a run, rays were launched at elevations between and 9 deg at 1,.5 or.1 deg steps. For this investigation, HRP s virtual acoustic source was placed initially at the Cornell loft ( N, W), based on the hypothesis that Jersey Hill sits within an acoustic shadow zone relative to the loft area (Hagstrum, 2). The grounds for selecting this scenario will be discussed more fully in the Discussion. RESULTS Jersey Hill Ray-tracing runs for the selected days birds were released at Jersey Hill were made using the 12: GMT (8: EDT) rawindsonde data from Buffalo, NY, and show two modes. In most cases (17 of 26 runs), rays launched westward from the loft are refracted upward above the troposphere as a result of the atmosphere s daily temperature and wind fields forming an acoustic shadow zone at Jersey Hill (Fig. 6). For the second mode (eight of 26 runs), rays launched above elevation angles of 4 to 16 deg are similarly refracted upward, but below this angle rays were channeled by wind shear and/or temperature inversions within an ephemeral duct at the surface (Fig. 6B). The ducted infrasound would be expected to arrive at Jersey Hill on these days, but reflections from the actual terrain have not been taken into account. The terrain rises from 313 m at the loft to 679 m at Jersey Hill, and is quite irregular across the N S grain of the Finger Lakes (Fig. 1). smoothed topographic profile based on a digital elevation model (DEM) of upstate NY was subsequently included in the HRP runs (Fig. 6C), and ducted rays were mostly reflected off the terrain at large enough angles to pass upward through the duct (reflected launch angles >4 deg; Fig. 6B). Thus, it appears that little or no sound emanating from the loft area would normally have arrived at Jersey Hill on the release days. On 13 ugust 1969, however, Cornell birds were unusually well oriented at Jersey Hill, and the ray-tracing results are

6 692 The Journal of Experimental Biology 216 (4) B Height (km) Jersey Hill 24 September : EDT 12 C Zone of silence Jersey Hill 1 September : EDT Jersey Hill 1 September : EDT deg 265 deg 265 deg Range at sea level (km) Fig. 6. HRP runs for two release days at Jersey Hill when Cornell birds were disoriented. The right edge of diagrams is at the Cornell loft, the left edge is at Jersey Hill, and the diagrams are oriented along the azimuth given in the lower left corner. Launch angles for all diagrams are from to 9. deg at step intervals of 1. deg in and.5 deg in B and C. () 24 September 1968 release (release 124) when Jersey Hill was in an acoustic shadow zone relative to the loft area (inset: N=22, r=.33, ϕ=17 deg). (B) 1 September 1979 release (release 2274) showing nearsurface ephemeral ducting between the loft and Jersey Hill without actual topography (inset: N=2, r=.454, ϕ=128 deg). Note that the vertical scale changes between panel and panels B and C. (C) 1 September 1979 release (release 2274) including topography showing reflection of the rays at the ground surface upward through the duct. The topographic profile is from a 3 m DEM of upstate NY to which the topographic profile used by HPR has been fitted (see Materials and methods, Data mining). distinctly different. Fig. 7 depicts a HRP run for this day with rays launched directly at Jersey Hill along a 265 deg azimuth; the rays are neither refracted upward above the troposphere nor ducted at the surface. Rays launched at azimuths less than 265 deg are refracted upwards beyond a few tens of kilometers (Fig. 7B), but those launched along azimuths between 275 and 315 deg (e.g. Fig. 7C) are refracted back to the surface NNE of Jersey Hill where, according to Huygens principle, the surfacereflected rays would form secondary sources. The location of these secondary sources is generally consistent with a NE departure of birds from Jersey Hill on 13 ugust 1969 (Fig. 3D). By the next day, 14 ugust 1969, HRP runs show that atmospheric conditions had returned to normal, again placing Jersey Hill within an acoustic zone of silence relative to the loft (Fig. 2, Fig. 7D). To determine how unusual the wind and temperature fields were on 13 ugust 1969, HRP runs were made for an additional 122 days, arbitrarily selected between 1 June and 3 September In the results for modeled days (148 total), rays directed at Jersey Hill (265 deg launch azimuth) were refracted upward above the troposphere on 77 days (e.g. Fig. 6), formed near-surface ducts as well on 64 days (e.g. Fig. 6B,C), and were similar to the 13 ugust 1969 result on only 7 days (e.g. Fig. 7 C). Thus, atmospheric conditions like those on 13 ugust 1969 in upstate NY are relatively rare, and based on the modeled data would occur ~5% of the time. Cornell birds were released at Jersey Hill 3 days per year on average, so encountering conditions like those on 13 ugust 1969 would be unlikely, which is consistent with Keeton s group having encountered them only once. Castor Hill Propagation modeling for the Castor Hill release days was performed using the 12: GMT (8: EDT) rawinsonde data from both the Buffalo and lbany weather stations. Overall, results from the two stations are similar, but those based on the Buffalo rawinsonde data are reported here because the Buffalo station, for the most part, is closer to the acoustic transit paths between the loft and the release site. Rays launched directly at Castor Hill (2 deg azimuth) from the Cornell loft show ephemeral ducting along the surface on 26 of 39 total days, and refraction upward through the troposphere on 13 remaining days. Intervening topography, reaching a maximum elevation of ~56 m, also tends to reflect the ducted rays upward (Fig. 8), effectively forming a barrier to ducted infrasound transmission between the Cornell loft (313 m) and Castor Hill (45 m). DEM of upstate NY including Castor Hill and the Cornell loft is shown in Fig. 9, along with the mean departure bearings for young birds; older, more experienced birds and F birds released at Castor Hill (Fig. 4 C). The mean vector for the F birds has been extended by a dashed line to show that it points to a topographic gap in the ppalachian Highlands of southern NY State made by the Lake Cayuga valley (1 in Fig. 9, Fig. 1). Near-surface ducting of rays traveling northward along Lake Cayuga from the loft would form secondary sources for rays traveling directly across the lowlands to Castor Hill once the highlands had been cleared. Propagation runs show that ducted rays along Lake Cayuga (32 deg azimuth) were strongly favored on most of the Castor Hill release days (34 of 39) and on all but two of the 13 days that F birds were released there (Fig. 8B). Near-surface ducting of rays between northern Lake Cayuga across the lowlands to Castor Hill (Fig. 8C) was favored less frequently by the Buffalo and lbany rawinsonde data sets, and, for example, occurred on 22 of the 39 total days control birds

7 Homing pigeons use infrasonic ʻmapʼ cues 693 Height (km) Jersey Hill 13 ugust : EDT 2. C B Jersey Hill 13 ugust : EDT deg 245 deg Jersey Hill 13 ugust : EDT 2. Jersey Hill 14 ugust : EDT deg 265 deg Range at sea level (km) D Fig. 7. HRP runs for 2 days in ugust 1969 when Cornell birds were released at Jersey Hill. The diagrams are explained in the Fig. 6 legend. () 13 ugust 1969 (release 258), the day Cornell pigeons were best oriented at Jersey Hill (inset: N=8, r=.921, ϕ=33 deg); 265 deg launch azimuth from loft showing rays are neither refracted upwards above the troposphere nor ducted at the surface. Launch angles are from 6. to 9. deg, with steps of.1 deg. (B) 13 ugust 1969; 245 deg launch azimuth showing rays refracted upward. Launch angles are from 6. to 9. deg, with steps of.1 deg. The topographic profile is along the 265 deg azimuth. (C) 13 ugust 1969; 295 deg launch azimuth showing rays returning to the surface NNE of Jersey Hill, the direction in which the birds departed (see Materials and methods, Historical pigeon releases). Launch angles are from 4. to 9. deg, with steps of.1 deg. The topographic profile is along the 265 deg azimuth. (D) 14 ugust 1969; 265 deg launch azimuth. Launch angles are from 1. to 9. deg, with steps of 1. deg. Cornell pigeons were returned to Jersey Hill, but again departed in random directions. Release data for this day (circular diagram) are not in the Keeton database, but were mentioned by Keeton (Brown, 1971) during a panel discussion. were released and on 7 of the 13 days F birds were released at Castor Hill. Rays launched to the NW from the Cornell loft also show nearsurface ducting on 36 of the 39 Castor Hill release days (Fig. 8D), stratospheric reflections on those release days occurring during October and November (1 days; Fig. 8E), and thermospheric reflections on 37 of the 39 release days. coustic signals, however, are much more highly attenuated in the thermosphere because of its lower density, so these signal paths will not be considered further. For the stratospheric reflections, return rays intersect the surface at between ~2 and 3 km from the loft area, far enough to also reach, along with the near-surface ducted rays, potentially returnreflecting terrain along the NE-trending northern shore of Lake Ontario. Infrasonic signals originating from secondary sources at land-surface reflections and returning across Lake Ontario to Castor Hill (Fig. 8F) could explain why young birds, in particular, depart Castor Hill to the W (Fig. 4). Signals returning to Castor Hill from these secondary sources along the mean departure bearings for each of the release days could have been ducted near the surface of Lake Ontario on 18 days and reflected from the stratosphere on 22 days. On all but eight of the release days, near-surface and/or stratospheric return paths to Castor Hill existed for these westerly secondary sources (e.g. Fig. 8F). The day Cornell pigeons appeared lost at Castor Hill, 22 July 197 (Fig. 4E), was one of 8 days that HRP runs showed weak to no near-surface ducting or stratospheric reflections of rays to the W of Castor Hill. pparently, near-surface ducting of infrasound from the loft along Lake Cayuga and across to Castor Hill was also problematic on this day: runs using weather data from lbany support ducting along Lake Cayuga (32 deg azimuth) but not across to Castor Hill (4 deg azimuth), and runs with Buffalo weather data indicate near-surface ducting along a 4 deg azimuth, but not a 32 deg azimuth. Thus, it is likely that no infrasonic cues were transmitted to Castor Hill from the Cornell loft area on the one day that released Cornell pigeons appeared lost there. Weedsport HRP runs for the Weedsport release days were also made using the Buffalo 12: GMT (8: EDT) rawinsonde data. The results for 21 May 1974 have been selected as representative of pigeon releases at Weedsport (supplementary material Table S3), and Fig. 1 shows a HRP run for this day along the direct azimuth (353 deg) from the Cornell loft (Fig. 9). s the modeling shows, infrasound was most often transmitted along this azimuth within near-surface ephemeral ducts, with some rays having been reflected upward by prominent topographic features; therefore, a diminished number of rays and weakened homeward signal likely reached the release site. Ducting (e.g. Fig. 6, Fig. 7D, Fig. 1D) was observed along the 353 deg azimuth on 47 of the 51 days selected for this study (supplementary material Table S4). Similar to Castor Hill, modeling results show that near-surface ducting along the 32 deg azimuth, aligned with the southern Lake Cayuga valley (1 in Fig. 9), was also favored (49 of 51) on the Weedsport release days (Fig. 1B). On most days (43 of 51), infrasound was ducted across from Lake Cayuga to Weedsport with little or no attenuation of rays by surface reflections along the 7 deg azimuth (Fig. 9, Fig. 1C). Thus, although some level of infrasound from the loft area was often transmitted directly to Weedsport, more intense levels likely arrived there from a path along Lake Cayuga and across to Weedsport that avoided the direct azimuth s higher intervening topography (Fig. 9).

8 694 The Journal of Experimental Biology 216 (4) Height (km) C Castor Hill 14 ugust : EDT Castor Hill 14 ugust : EDT E 5 2 deg 4 deg Castor Hill 22 October : EDT 12 B D Castor Hill 14 ugust : EDT deg 1226 Castor Hill 18 June : EDT 12 1 F deg Castor Hill 18 June : EDT 12 Fig. 8. HRP runs ( C) for the 14 ugust 1975 release (release 1226) of F birds (inset: N=12, r=.814, ϕ=244 deg), and for several days (D F) when young birds were released at Castor Hill (see Fig. 9). The diagrams are explained in the Fig. 6 legend. ll launch angles are from to 9. deg with 1. deg steps except for B, which has launch angles from 4. to 9. deg. () Rays launched toward Castor Hill (2 deg azimuth) from the Cornell loft. Some rays appear to pass through the ground because the topographic profile used by HRP has been smoothed compared with the DEM profiles shown here. (B) Rays launched from the Cornell loft along Lake Cayuga (32 deg azimuth). Note the change in vertical scale. (C) Rays crossing over from northern Lake Cayuga to Castor Hill along a 4 deg azimuth (opposite F birdsʼ mean departure bearing of 22 deg). (D) 18 June 1976 (inset: N=11, r=.96, ϕ=273 deg); rays launched NW from the Cornell loft (32 deg azimuth) showing near-surface ducting and thermospheric reflections. (E) 22 October 1968 (inset: N=14, r=.933, ϕ=289 deg); rays launched to the NW showing nearsurface ducting and both stratospheric and thermospheric reflections. (F) 18 June 1976 (release 1579); rays launched along the return azimuth (93 deg), opposite the young birdsʼ mean departure bearing from Castor Hill (273 deg), showing some nearsurface ducting as well as stratospheric and thermospheric reflections deg 2 93 deg Range at sea level (km) Generally, near-surface ducting of rays launched from the Cornell loft along the Fall Creek valley (4 deg azimuth) was not favored (Fig. 9, Fig. 1D), and little to no ducting occurred along this azimuth on 29 of the 51 Weedsport release days (supplementary material Table S4). gain, 6 June 1974 appears to have been an exceptional day (see Fig. 5D), here in terms of weather conditions. lthough ducting occurred along the 4 deg azimuth from the Cornell loft on this day (Fig. 1E), it did not occur along the 353, 32 or 7 deg azimuths (Fig. 11). Infrasound ducted NE from the loft would tend to pass through the lower elevation valleys, and could have traveled along the Fall Creek, west branch of the Tioughnioga River and Tully valleys (5, 6 and 7 in Fig. 9) before arriving at Weedsport from near the observed 127 deg mean departure bearing (Fig. 5D). Propagation modeling using Buffalo meteorological data, however, indicates that infrasound transmitted N through the Tioughnioga River and Tully valleys, with azimuths similar to 7 and 353 deg, respectively, would have been refracted upwards on 6 June 1974 (Fig. 9). The propagation of infrasound through these valleys would likely have involved diffraction and/or scattering of the acoustic waves, which, unfortunately, cannot be determined by HRP. In addition, ducted rays traveling across to Weedsport from the northern end of Tully Valley along a 37 deg azimuth were reflected upward by intervening topography (Fig. 1F). Departure bearings of Cornell pigeons released on 6 June 1974 from Weedsport were somewhat spread out, but a significant number of birds selected a more easterly bearing (~12 deg) than the mean (Fig. 5D, Fig. 1E,F), which corresponds to more topographically subdued

9 Homing pigeons use infrasonic ʻmapʼ cues 695 Lake Ontario 7 deg 1 K 32 deg Weedsport deg 4 deg 2 deg 3 4 Young 4 deg Old 37 deg 5 Cornell loft Castor Hill fire tower and non-obstructive terrain (Fig. 9). Thus, even though HPR runs indicate that infrasound from the loft area would not have arrived at Weedsport from the SE on 6 June 1974, this result is probably inaccurate because of an incorrect azimuth (37 deg) and the limitations of HRP. DISCUSSION Infrasonic source That pigeons from other lofts in upstate NY, even those from a loft just 24 km W of Ithaca, could regularly orient at Jersey Hill (e.g. Fig. 3B,C) when Cornell birds could not indicates that a loft s direction and distance from a release site are of crucial importance to the map function (Walcott and Brown, 1989). This is supported by observations that release-site biases tend to be consistent for birds from a given loft (Keeton, 1974; Wallraff, 25). Moreover, the rare occurrence of Cornell birds orienting and homing directly from F km Fig. 9. Digital elevation model (DEM) of upstate NY including locations of the Cornell loft just E of Ithaca, the Castor Hill fire tower, 143 km NNE of the loft, and Weedsport, 74 km N of the loft. The mean departure vectors for young, older and F birds released at Castor Hill, and K birds released at Weedsport, are shown (Figs 4, 5), and the F and K vectors have been extended by a dashed lines to show that they generally point to the northern opening of (F ) and down (K) the Lake Cayuga valley (1), within the ppalachian Highlands of southern NY State. Other locations are indicated by the following numbers: 2, Owasco Lake valley; 3, Skaneateles Lake valley; 4, Otisco Lake valley; 5, Fall Creek; 6, West Branch Tioughnioga River valley; and 7, Tully Valley. Dashed lines indicate direct lines to Castor Hill and Weedsport from the loft (black) and possible paths of acoustic signals detected by released F and K birds (white). Values next to the dashed lines indicate launch azimuths of rays (deg) towards the release sites (Figs 8, 1). Jersey Hill, or departing Weedsport in an extraordinary direction to the SE, both coincident with unusual atmospheric conditions (Fig. 3D, Fig. 7C, Fig. 1E), shows that the atmosphere is likely an integral factor in the avian map. The generally observed hourly to daily changes in release-site biases (Wallraff, 25) also point to processes acting on atmospheric time scales as the probable cause of these changes. map cue that can be absent at some sites while present at others, be available at a single site for birds from one loft but not others, and change rapidly depending on atmospheric conditions is in all likelihood an acoustic one, and, because of the distances involved, must be infrasonic. Thus, disorientation of Cornell birds at Jersey Hill can be readily explained by a shadow zone in the region relative to a single source area associated with the Cornell loft (Fig. 6,C). n avian acoustic map consisting of multiple sources of infrasonic signals at various directions and distances from Jersey Hill can be ruled out because it would be highly unlikely, under variable atmospheric conditions, for multiple shadow zones to consistently overlap there over a 2-year period (Fig. 3). In a previous study (Hagstrum, 2), I suggested that infrasonic signals possibly used by homing pigeons could come from the ubiquitous ground-to-air coupling of microseismic waves in steepsided terrain. Microseisms are composed mostly of surface waves continuously generated in the solid earth by non-linear interactions of oceanic waves with similar frequencies traveling in nearly opposite directions. These seismic waves have frequencies that range from ~.1 to ~.5 Hz with a spectral peak at ~.2 Hz (Rind, 198; rrowsmith et al., 21). Microseisms are recorded globally by seismic stations, even within deep continental interiors, and often define the background noise levels on seismic recordings. The average ground displacement due to microseisms ranges from ~.5 to ~5 μm, and can be related to dominant sources in the North tlantic and Pacific Oceans that follow the seasonal pattern of oceanic storms in the northern and southern hemispheres (Rind, 198; Kedar et al., 28; rrowsmith et al., 21). lthough continuous acoustic radiation coupled with the land surface has not been isolated in records from infrasound arrays, the ground-to-air coupling of higher amplitude earthquake-generated surface waves in mountainous terrain has often been observed at arrays distant to these sources (Young and Greene, 1982; Le Pichon et al., 22; Le Pichon et al., 23; Le Pichon et al., 26; rrowsmith et al., 29). For example, a magnitude (M L ) 4.3 earthquake occurred on 28 pril 27 near Folkestone, UK, in a region of relatively subdued topography. Infrasound from the coupling of surface waves proximal to the epicenter was recorded at a station (FLERS) located ~284 km to the SSW in France. Modeling of a 23 km stretch of 75-m-high coastal cliffs between 1 and 18 km from the epicenter as a series of 35 pistons independently generating acoustic waves produced synthetic microbarograms in close agreement with the FLERS station s recordings (Greene et al., 29). coustic wavelengths are inversely proportional to frequency, and an infrasound tone of.2 Hz has a wavelength in air of 1.7 km at room temperature (e.g. Bedard and Georges, 2). The total ground area needed, vibrating in unison with 1 μm amplitude at.2 Hz, to generate an overall signal that pigeons can hear at a 1 km range at ~12 db SPL (Kreithen and Quine, 1979), would be on the order of 1 km 2 (B. Thigpen, written communication;. J. Bedard, Jr, written communication). Dimensions of the infrasonic source areas can also be inferred from the accuracy of pigeon homing: experiments in which frosted lenses were fitted over pigeons eyes prevented them from seeing landmarks in the loft s vicinity needed for their final

10 696 The Journal of Experimental Biology 216 (4) Height (km) Weedsport 21 May : EDT 2. Weedsport 21 May : EDT 2. B Weedsport 21 May : EDT deg 32 deg C Weedsport 21 May : EDT deg.4 4 deg D Fig. 1. HRP runs ( D) for the 21 May 1974 release (release 191) of K birds (inset: N=7, r=.987, ϕ=188 deg), and (E,F) for the 6 June 1974 release (release 111) of K birds (inset: N=1, r=.952, ϕ=127 deg) at Weedsport. The diagrams are explained in the Fig. 6 legend. ll launch angles are from to 9. deg with.5 deg steps. () Rays launched directly toward Weedsport (353 deg azimuth) from the Cornell loft (see Results, Weedsport). (B) Rays launched from the Cornell loft along Lake Cayuga (32 deg azimuth). (C) Rays crossing over from Lake Cayuga to Weedsport along a 7 deg azimuth (opposite the birdsʼ mean departure bearing of 187 deg). (D,E) Rays launched from the Cornell loft along a 4 deg azimuth up the Fall Creek valley on 21 May and 6 June 1974, respectively. (F) Rays launched across to Weedsport from Tully Valley (see Fig. 9) opposite to the birdsʼ mean departure bearing (127 deg), showing that rays within near-surface ducting were reflected upward by the terrain along this azimuth (see Results, Weedsport) E Weedsport 6 June : EDT 2. F Weedsport 6 June : EDT deg.4 37 deg Range at sea level (km) approach (Schmidt-Koenig and Walcott, 1978). Even so, these birds were able to return within.5 to 5 km of their loft (supplementary material Fig. S5). Regions of subdued terrain might result in larger acoustic source areas surrounding the loft, resulting in less accurate homing at close range in the absence of sight. The switch to sight navigation by pigeons near their loft would presumably occur once the birds had entered the acoustic source area. Thus, birds distant to their home terrain could be identifying its characteristic acoustic radiation from steep-sided facets, normal to their position, continuously excited within a narrow frequency band by microseismic energy. Because sound intensity from a given source follows the inverse-square law, birds at distances increasingly beyond ~1 km from their loft area would probably be listening to acoustic radiation from an expanded area of steep-sided terrain oriented toward their position and generating sound pressure levels that they could hear. However, the acoustic energy from intervening horizontal surfaces would be directed vertically upward and appear acoustically transparent to birds at distant points. Homing pigeons must be trained at varying directions and increasing distances from their loft area in order to develop and hone their navigational abilities. During this process the birds may be learning to recognize their loft area s changing acoustic signature from the different release locations. nother plausible source of characteristic infrasound from the loft area could be the scattering of direct microbaroms off topographic features (M. Haney, written communication); only those features with dimensions similar to or larger than the infrasonic wavelengths would cause significant scattering. Microbaroms are