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Short distance phase shifts revisited: tracking clock-shifted homing pigeons (Rock Dove Columba livia)

close to the loft RICHARD HOLLAND’*, FRANSISCO BONADONNA2, LUlGl DALL‘ANTONIA3, SILVANO BENVENUTV, THERESA

BURT DE PERERA’& TIM GUILFORD’ ’Department of Zoology, South Parks Road, Oxford, OX1 3PS, UK

2Dipartimento di Scienze del Comportamento Animale e dell’Uomo University of Pisa, Via Volta 6, 1-56126 Pisa, Italy *lnstituto di Elaborazione della informazione CNR, Via S. Maria 46, 56100, Pisa, Italy

Clock-shifted homing pigeons (Rock Dove Colurnba livia) were tracked from familiar release sites using a direction recorder. At relatively short distances from the home loft (< 3.2km), it was discovered that two different mechanisms for homing were present. One involved the sun compass and the other was independent of this. At a further site (9.95 km) none of the birds used the sun compass for navigation. The possibilities for the non-sun compass-based mechanism are discussed.

Experimental attempts to understand the nature of spatial representation in wide-ranging vertebrates are normally restricted to the laboratory where movement decisions can be tracked with sufficient precision (Cheng 1988, Biegler & Morris 1993, Kamil ,& Jones 1997). When such experiments are performed in the field, for example in a homing task, measurements are typically restricted to just one part of the journey, usu- ally the initial phase, and for homing pigeon studies this has become a classic experimental method known as the vanishing bearing (see Papi 1992 for review). Pigeons use a time-compensated sun compass for orientation (Schmidt-Koenig 1958) and by shifting their internal clock experimentally, predictable deflec- tions from the home direction can be obtained a t vanishing. Most studies reliably report such deviations in vanishing bearings even a t familiar sites (Fuller et al. 1983, Luschi & Dall’Antonia 1993) and as little as 1 km from the loft (Craue 1963). Craue’s experiment was of particular importance as he demonstrated that pigeons showed the full deflecting effect of clock-shift unless they had a direct view of the loft. A follow up by Keeton (1974) showed that a t 3.6 km even a direct view of the loft did not cancel the effect of clock-shift.

*Corresponding author. Present address: School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588- 01 18, USA. Email: rah106@hotmail.com

This has been cited as evidence that pigeons do not use landmarks independently of the sun compass to home in their familiar area (Wiltschko 1996). However, the mean deflection is often less than predicted (Bingman & Ioale 1989, Walraff et al. 1994, Wiltschko et aI. 1994, Chappell 1997), and it is possible that the common statistical tendencies towards clock-shift observed in the distribution of individual vanishing bearings may be obscuring individual flexibility in navigation strategies. At present however, exactly what these individual tendencies are is obscure: have some pigeons learnt another mechanism for homing and corrected their initially false orientation on recognizing a mismatch between the sun compass and the second strategy?

The ideal way to monitor flexibility amongst indi- viduals would be to track each individual bird. This has proved difficult in the past because techniques such as visual tracking from aircraft or helicopters is expensive and satellite systems are currently too large to be fitted to a pigeon (Alerstam 1996). However, the develop- ment of an ‘on board’ route recorder (Bramanti et al. 1988) which records magnetic compass headings in a microchip for downloading, analysis and route recon- struction, has made relatively cheap trackmg of the whole homing route more readily available. By using this method in our experiments we have been able to look at the individual behaviour of clock-shifted birds when released from sites in the familiar area. The

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11 2 R. Holland et al.

particular aims of the experiment were to look at the effect of releases from short distances where Graue (1963) and Keeton (1974) found that the result of clock-shift was most variable, mainly due to the sight of the loft, and from a site further away, beyond the distance where the loft was shown to be a factor. The results indicate that pigeons have two strategies for homing in the familiar area, and at the same site different individuals may choose a different homing mechanism.

METHODS

5 1'47'; longitude l"19') were the experimental subjects. They received extensive pretest training prior to the experiments, having received 20 releases up to 25 km from the loft approximately in the cardinal compass directions. The birds then received four releases from each of the test sites. In order to accustom them to flying with the route recorders, the birds received two training releases with dummy weights before the training releases from the test sites began. These were made of perspex and weighed the same as a route recorder (1 3 g). They were attached in the same way, by Velcro.

Route recorder Release sites

This device carries a needle compass which is equipped with a transducer to convert the angular values into electrical resistance values. The compass consists of a pair of magnetic needles fixed to a greyscale disc. An LED-photoresistor is located under- neath this and as the bird's heading varies, so does the position of the LED with respect to the disc and the variation in the photoresistor is recorded into a digital memory at regular time intervals (multiples of 2 s).

In order to produce a track, a constant speed of 60 km/h has to be assumed, which tests have confirmed to be acceptable (Benvenuti et al. 1996). An ~ S - D O S

based software program 'Elabora' is used to reconstruct the track. As well as the headings, the position of the home and release sites, the wind velocity and direction on the day of release need to be known in order to pro- duce an accurate track. If the angular difference between home and the final point of the track was more than 10" out, then it was rejected. However, the

Four release sites were chosen, in approximately opposing compass directions: Yarnton (1.9 km from the loft, home direction 200"); Portmeadow (2.1 km, home direction 282"); Marley Lodge (2 km, home direction 327"); and Swinford (3.2 km, home direction 63"). At no site was the loft visible to the observer but the landscape varied between sites. At Yarnton, only trees blocked the view a t ground level. At Swinford, Wytham Hill (165 m asl) lay between the release site and loft. At Marley Lodge, Wytham village and the corner of Wytham hill blocked the birds' view to the loft and at Portmeadow the birds were released from behind Wolvercote village.

In addition to the short distance sites, a more distant site near Oddington (9.95 km from the loft, home direction 232") was chosen. This distance was outside the range at which sight of the loft cancels the deflecting effect of clock-shift (>3.6km, Keeton 1974).

reliability of the device is indicated by the fact that the angular difference was usually less than So, a very small fraction of the track (Benvenuti et al. 1996). Obviously as a data logger, the recovery of the device is essential for data retrieval.

The first device developed was 30 g in weight, but a second and third generation of route recorders have now been developed with larger memory capacity (currently 32 kbytes). The third-generation device weighs 13 g. It is normally attached to the bird's back by gluing Velcro to the body of the bird and then

Test releases

In all releases, birds were transported to the release site in a closed-sided van in release boxes which had holes for ventilation. Birds were only released when the sun's disc was visible.

1.9-3 km sites

Five experimental birds were clock-shifted six hours fast for eight days and five control birds were kept in a

attaching the device to the Velcro

Subjects and pretraining

light-tight room under normal day phase for the same period. The control and clock-shifted birds received one release from each of the four release sites. At the release sites, birds were released singly with a 10-min

Ten one- to two-year-old homing pigeons (Rock Dove gap between each release. Three clock-shifted birds Calumba liuia) housed and raised at the lofts at the were released in succession before changing to Oxford University field station, Wytham, UK (latitude control birds. Their arrival a t the loft was noted by a n

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Clock-shifted homing pigeons 1 13

observer. The time at which the bird crossed a pre- assigned boundary approximately 100 m from the loft was recorded. In this way, circling at the loft, during which the bird would not be flying at its constant cruising speed, could be discounted. All clock-shifted birds returned to the loft before the end of their sub- jective day, and were put back in clock-shift immediately.

In addition to the four releases under fast shift, one release with the same birds shifted six hours slow was undertaken from Portmeadow. The clock-shifting procedure was the same for these birds as for the fast clock-shifted birds. The birds were given three days to reacclimatize from the fast-shifted releases. They spent eight days in the clock-shift loft before the experiment began.

9.95 km site

After the short distance releases, the birds released at the 1.9-3.2 km sites were given two days in clock-shift and one more bird was added to the clock-shift group (having been given eight days in clock-shift). At the release site, birds were released singly and carried a route recorder. There was a 10-min gap between each release and three birds of one condition (i.e. experi- mental or control) were released in succession before any birds of the opposite condition were released. An observer at the loft noted the arrival time of each bird.

RESULTS

Short distance releases

Figures 1 4 show the tracks of the control and fast clock-shifted birds at the four short-distance release sites. While many of the clock-shifted birds had direct tracks comparable to the control birds, four birds showed deflected tracks indicative of an effect of clock-shift. Bird 1 (Fig. Zb), bird 2 (Fig. 3b) and birds 3 and 4 (Fig. 4b) all deflected initially in the direction predicted by a fast clock-shift before correcting and returning to the loft. The angular deflection from home when these birds were I .5 km from the loft was 173" in the case of bird 1, 1 1 1 ' in the case of bird 2, 92" in the case of bird 3 and 61 O in the case of bird 4. This distance corresponds approximately to the point at which they would have vanished from sight through 10 x 40 binoculars. Interestingly, these birds travelled a distance roughly corresponding to the distance of the release site from the home loft before they correct. In the case of bird I , the distance before correcting was 3.1 km compared with 2 km from release site to home. In the case of bird 2, the distance before correcting was 3.9 km compared with 3.1 km from release site to home and in the case of birds 3 and 4 the distance before correcting was 1.55 km compared with 2.1 km from release site to home. We hypothesize from this that the birds knew the distance they needed to travel before reaching home, and when this did not happen

b \ \Yarnton

ington . /j/ r lx

R. lsis

Figure 1. The tracks of (a) controls and (b) experimental birds at Yarnton. The map has been redrawn from an Ordnance Survey map to show only key features. Individual clock-shifted and control birds are represented by the same dotted line in each subsequent figure. H represents the home loft and R the release site.

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1 14 R. Holland et al.

Yarnton a

1 km -

Figure 2. The tracks of (a) controls and (b) experimental birds at Marley Lodge. 1 marks the bird that deflected in the expected clock-shifted direction. H represents the home loft and R represents the release site.

C

Eynsharn

Cassington

1 km D I

8 8

hW Reservoir

Figure 3. The tracks of (a) controls and (b) experimental birds at Swinford. 2 marks the bird that deflected in the expected clock- shifted direction. H represents the home loft and R represents the release site.

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Clock-shifted homing pigeons 1 15

a

1 krn - Yarnton k!? b

A Cassington

cote

Yarnton k? Cassington fi

Figure 4. The tracks of (a) controls and (b) experimental birds at Portmeadow. 3 and 4 mark the birds that deflected in the expected clock-shifted direction. H represents the home loft and R represents the release site.

they switched to an alternative strategy. A bird from the release with slow-shifted birds (Fig. 5) was partic- ularly interesting with respect to correcting to reach home. This bird, released on Portmeadow, initially deflected in the direction predicted by a slow clock- shift. I t then passed over Yarnton, from where it had

Figure 5. The track of a slow clock-shifted bird which deflected in the expected clock-shifted direction. Filled circles mark places where the bird had previously been released. H represents the home loft and R represents the release site.

been released previously, and deflected again by approximately 90" with respect to home. It then passed over Cassington, from where it had also been released before, and again deflected with respect to home and then eventually returned to the loft. This suggests a different hypothesis, that the bird was retahng a sun compass bearing every time it passed over a familiar site. This provides another possible way by which clock-shifted birds could eventually return home, as suggested by Walcott (1 996).

Oddington

The tracks of both the experimental and the control birds that were released from Oddington were direct homeward routes (Fig. 6). The experimental birds showed no evidence that they were using their faulty sun compass to orient from this site, although their homing times were significantly greater than the controls (Mann-Whitney U test: P < 0.05), which perhaps indicates that they recognized a conflict between the sun compass and the orientation cues they decided to use.

DISCUSSION

Although these results are only preliminary, they suggest that the pigeons had two distinct strategies for homing. At the 1.9-3 km sites, some clock-shifted birds chose to use the sun compass and thus had deflected

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11 6 R. Holland et al.

a

H

Wytham Wood \ / \< \ I "

b

Figure 6. The tracks of (a) controls and (b) experimental birds released from Oddington. H represents the home loft and R represents the release site.

routes. Interesti-ngly, it was not the same bird that clock-shifted at each site. This shows that the same birds used different homing mechanisms from different sites. It is not entirely clear why a bird should choose tRe sun compass at one site and an alternative mechanism at another, although a recent laboratory experiment by Chappell and Cuilford (1 997) suggests that the type of landmark available (local or distant cues) might be a factor, with local cues being sun- compass independent and distal cues being sun- compass reliant.

The clock-shifted birds with direct routes, both at the 1.9-3 km sites and all the birds at the 9.5 krn site, must have been using some alternative strategy not relying on the sun compass. There are three possibili- ties for this.

1. Beaconing The birds may have 'beaconed' to the loft if it was in view. Beaconing occurs when an animal learns to associate a single landmark with its goal or some feature of the goal itself (Collet 1987). In the case of the experiments reported here, it would be the home loft. This is a plausible explanation for the straight tracks at Portmeadow, Marley Lodge and Yarnton. Previous experiments (Graue 1963, Keeton 1974) have demonstrated that if a clock-shifted bird can see the loft then it usually ignores the sun compass, provided it is less than 3.6 km from the loft. This cannot explain the results of the release at Oddington

however, nor the results at Swinford, where the height of the hill was such that it was unlikely the birds would have seen the loft at the height they flew (around 30 m, Wagner 1972).

Alternatively, the birds may have beaconed to some feature which they could see close to the loft. This is a possible explanation for the clock-shifted birds with straight tracks at Swinford, as Wytham hill blocked the view of the loft. It may also explain the straight tracks of clock-shifted birds at the 9.5 km site. If this hypoth- esis is correct then this would contradict previous results. Graue (1963) found that if the loft was not in view, but some other building nearby was, then the birds still deflected under clock-shift.

2. Pilotage The birds may have piloted. Pilotage has been defined by Papi (1992) as orientation involving a topographical map of learned landmarks, without reference to a compass. This is generally considered to be more complex than 'just -associations between a landmark and the goal, and involves the geometric relationships between landmarks to locate a goal out of visual range (Kamil & Jones 1997). These landmarks may have been learned during previous releases from the sites or during exploratory flights. There is no clear evidence for pilotage by pigeons as yet, and many authors discount it as a mechanism for homing by pigeons from the familiar area (e.g. Fuller et al. 1983, Luschi & Dall'Antonia 1993, Wiltschko 1996). Recent experi-

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Clock-shifted homing pigeons 1 17

ments by Braithwaite and Guilford (1991, 1995) have shown that visual information independent of the home loft is, however, used to home from familiar sites so pilotage remains one possible explanation for the result of these experiments.

3. Switch to alternative compass The birds may have switched to a non-time-compen- sated compass on learning that the sun compass was faulty. Several tests have shown behavioural evidence that pigeons switch to a magnetic compass if the sun compass is unavailable due to cloud (Keeton 1971, although see Moore 1988, Walcott & Green 1974, Ioale 1984) but there is no behavioural evidence for any other compass being used by the pigeon. It has been demonstrated that birds prefer to use the sun compass if it is available, but recent experiments have shown that the magnetic compass may be used to calibrate it (Wiltschko & Wiltschko 1996). However, evidence from' small-scale arena experiments shows

bird was using the same rule as the fast-shifted birds in determining that it had travelled the distance necessary to reach home but had failed to do so. However, this bird had no alternative strategy and so it recalculated the sun compass bearing. Secondly, that the bird flew over a familiar site that it knew was not in the home direction, but having no other strategy with which to home, it based a new sun compass bearing on the new familiar site information. This would spiral it in towards the loft.

I t is not possible to determine which of the strategies discussed here was being used at this stage, but experiments are planned to test these hypotheses, in particular the role of the magnetic compass a t familiar release sites and also the types of visual cues available to the birds on release. Using the route recorder to track clock-shifted birds has given us new insights into the way pigeons represent their familiar area and has opened up new avenues of research.

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1-25.

Received 1 April 1998; revision accepted 21 December 1998

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