Navigation by homing pigeons: updated perspective

Ethology Ecology & Evolution 13: 1-48, 2001

Navigation by homing pigeons: updated perspective HANS G. WALLRAFF Max-Planck-Institut für Verhaltensphysiologie, D-82319 Seewiesen, Germany (E-mail: [email protected]) Received 5 April 2000, accepted 18 September 2000

During the last decade, some progress has been made in recognizing and separating the principal components determining the homing behaviour of pigeons. This study, an updated continuation of a previous review (WALLRAFF 1990), focuses on new results and improved insight into three constituents that basically characterize pigeon homing. (1) It has been confirmed by continued experimental research that olfactory access to environmental air appears to be a necessary precondition for homefinding from unfamiliar areas everywhere on earth. Empirical research in this context has now also entered the atmosphere. Starting from a theoretical navigation system based on gradients of ratios among three or more atmospheric trace substances, volatile airborne compounds were investigated by means of gas chromatography in a circular area with a diameter of 400 km in Germany. Ratio gradients in a number of hydrocarbons were found which imply spatial information suitable for navigational performances on a level observed in pigeon homing. Angular relationships between variations of compound ratios in space and in dependence on wind direction indicate possibly useful atmospheric preconditions for the development of an “olfactory map”. These interrelations need further investigation and the chemical compounds actually used by pigeons are yet to be identified. (2) Various experiments using olfactory and/or visual deprivation, partly combined with a shifted sun compass, strongly suggest that inside a familiar area pigeons make use of the visual landscape to find the way home. Thus, in a familiar area the home-finding system appears to be redundant in that it can utilize both olfactory and visual environmental signals. Visual orientation by means of topographical features seems to rely on an aerial panoramic view over an extended area rather than on the distinction of small-scale landmarks observed only in a narrow range along previous homing routes. In the past, its possible influence on experimental results has probably often been underestimated. (3) Almost as important as the identification of factors used for homefinding is the recognition of other factors that influence the pigeons’ departure directions from the release site. Three such components have been identified which may modify or mask the directional output of the home-navigation system. Initial bearings of pigeons are often (a) polarized towards a loft-specific preferred compass direction (PCD), (b) deflected by attracting or repelling topographical features, and (c) influenced by the compass directions flown in previous homing flights. Under certain circumstances, initial orientation can be disturbed by treatments inducing stress or preventing the opioid-controlled compensation of stress. Such treatments, as for instance transport in darkness or in an oscillating magnetic field, can temporarily abolish the pigeons’ motivation to orient homeward, but do not affect their ability ultimately to find the way home.

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H.G. Wallraff There is no indication that any other kind of information, neither olfactory nor visual, might be used by displaced pigeons to determine their position relative to home. Seemingly conflicting and controversial issues assembled in the literature are discussed in the Appendix. KEY WORDS:

navigation, orientation, homing, pigeon, landscape, olfaction, atmosphere, volatile organic compounds.

Introduction . . . . . . . . . . . . 1. Distracting factors interfering with homeward orientation 1.1. Home-independent directional tendencies . . 1.1.1. Preferred compass direction (PCD) . . . 1.1.2. Deflecting landscape features . . . . 1.1.3. After-effects of previous homing flights . . 1.2. Stress-associated effects on motivation . . . 1.3. Consequences for methods and interpretations . 2. Home-finding by means of the familiar visual landscape 2.1. Non-olfactory homing . . . . . . . 2.2. Effects of visual deprivation . . . . . . 2.3. Relationships between landscape and sun compass 2.4. Brain asymmetry and visual orientation . . . 2.5. Conclusion and perspective . . . . . . 3. Home-finding by means of atmospheric odours . . 3.1. Homing experiments . . . . . . . 3.1.1. Recent results . . . . . . . . 3.1.2. Older results revisited . . . . . . 3.2. Gradients in atmospheric trace gases . . . 3.2.1. Theoretical considerations . . . . . 3.2.2. Empirical findings . . . . . . . 3.2.3. Suitability for navigation . . . . . 3.3. Unsolved problems . . . . . . . . 4. Home-finding by other means? . . . . . . Appendix: Critical survey of the literature . . . . Acknowledgements . . . . . . . . . . References . . . . . . . . . . . .

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INTRODUCTION

The hypothesis that displaced pigeons find their way home by means of olfactory and visual environmental signals has been consolidated during the decade following the publication of my last review on pigeon homing (WALLRAFF 1990). Other potential signals, either known or still undetected, appear to play a very subordinate role at best. The present updated continuation of the review aims to substantiate this hypothesis and tries to explain the pigeons’ navigation system on the basis of current research findings. Also, I shall continue to discuss several debated issues which make the matter still appear confusing in the literature. In my view, the current state of knowledge is not as contradictory as its public appearance. This study focuses on three major topics which are not entirely new but which have been more clearly recognized and separated and more deeply investigated during the last years: (1) For logical and methodological reasons, it is necessary to separate the factors actually involved in the process of home-finding from concomitant factors that

Navigation by homing pigeons

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also determine the birds’ orientation behaviour but are not directly included in that process. Neglect of such distinctions can easily lead to erroneous interpretations. (2) It seems to me that the role of familiar features of the visual landscape in pigeon homing has long been underestimated. I shall try to assess the position of learned landscape patterns in the pigeons’ homing system. Improved knowledge in this respect also facilitates analyses and appropriate interpretations as applied to the more fascinating problems of non-visual navigation. (3) The importance of airborne odours in pigeon homing has gained broadened experimental support. In addition, empirical research has recently started to advance into the atmosphere with respect to its suitability as a source of largerange positional information. Spatial distributions of ratios among volatile trace substances were found that could potentially be used to find the way home from unfamiliar areas at a level of performance similar to that achieved by pigeons. In a concluding section, I shall point out why I consider it unlikely that any further sources of positional information, neither olfactory nor visual, are actually used by pigeons for purposes of home-finding. Finally, in an appendix, I shall critically inspect the literature. I shall try to resolve the confusions which made the field of avian navigation so difficult to survey over many years. Discussions of debated aspects will largely be postponed to this Appendix, so that the main text outlines the field as I currently see it. Not included are the neuroethological aspects of pigeon homing which have recently been reviewed by BINGMAN et al. (1998b). Dealing with a complex network in a linear sequence makes many crossreferences necessary. They are mostly set in square brackets and refer to other sections, to figures in other sections or to “Part 1”, i.e., to WALLRAFF (1990) which now acts as the first part of a review whose second part is the present study.

1. DISTRACTING FACTORS INTERFERING WITH HOMEWARD ORIENTATION

Vanishing bearings of a group of pigeons released individually and observed with binoculars at a given release site are mostly clustered around a direction that does not point directly towards home but deviates more or less to the left or right, albeit rarely by more than 90°. Initially, during the early stages of research, the mean vanishing direction was naively identified with the pigeons’ subjectively assessed direction towards home. Site-specific deviations from the true homeward direction (“release-site biases”: WALLRAFF 1959b, KEETON 1973) were interpreted as navigational errors resulting from a non-fit between the birds’ navigational “map” and the real physical conditions to which this map refers. There is little doubt that such non-fits do actually occur, but today we know that they are not the only causes of release-site biases. Other causes, which have nothing to do with position determination, are interacting as well. 1.1. Home-independent directional tendencies 1.1.1. Preferred compass direction (PCD) A very common and widespread phenomenon is the polarisation of initial bearings towards a loft-specific preferred compass direction (PCD) (SCHMIDTKOENIG 1963, 1970; WALLRAFF 1967, 1970, 1978, 1986, 1991; WINDSOR 1975; IOALE`

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1995). It becomes most clearly visible if initial bearings from a number of sites symmetrically distributed around home are combined (Fig. 1). Independence of this directional preference from the process of homeward orientation is particularly evident by its persistence, and even more pronounced expression, in anosmic pigeons in which the homing process does not successfully take place [3.1; fig. 7 in Part 1]. If the release-site biases only reflected errors in determining the direction towards home (e.g. KEETON 1973, 1974; WILTSCHKO 1993; WILTSCHKO & WILTSCHKO 1998, 1999a, 1999b; WALKER 1998, 1999), they should disappear with the disappearance of homeward orientation. An error alone cannot survive if the performance, of which it is an error, does not exist. The PCD is differently expressed around different loft sites and in differently experienced pigeons; it is further dependent on uncontrolled circumstances varying in time (e.g. WALLRAFF 1978, 1986; KIEPENHEUER et al. 1993). In inexperienced pigeons, the PCD is sometimes stronger than the homeward tendency, whereas in well-homeward-oriented experienced pigeons nothing of it may be visible at all (Fig. 1, OLF). If homeward orientation is eliminated, however, even the experienced birds reveal a hidden PCD (Fig. 1, ANO). A biologically meaningful function of the PCD is still unknown. A social role to facilitating flock cohesion in the case of a sudden event inducing an escape response (MATTHEWS 1962, THAKE 1981, WALLRAFF 1986, PAPI 1995) is a reasonable

Fig. 1. — Initial orientation of untreated pigeons (top) and of anosmic pigeons with sectioned olfactory nerves (bottom). Each peripheral symbol indicates the mean vanishing bearing of one experiment including a sample of 6-20 birds; arrows indicate second-order mean vectors derived from these mean bearings (radius = 1 = no scatter). Left four diagrams are from 60 releases of inexperienced (first flight) pigeons at 28 sites positioned in central symmetry around the home loft near Würzburg, Germany, at distances of 7-300 km. Right four diagrams are from 8 symmetrical releases of pigeons of the same loft with considerable previous homing experience [see fig. 2 in Part 1]. Each release mean is plotted in two diagrams, one showing its deviation from the direction towards home and the other one its compass direction. (Data from WALLRAFF 1982 and WALLRAFF et al. 1986, 1989).


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but speculative hypothesis without experimental support. At any rate, it seems unlikely that the PCD has a navigational function in the context of home-finding (as assumed earlier: WALLRAFF 1967, 1974a). A pigeon is not more successful in homing if it deviates from a direct course towards home in accordance with the PCD than if it deviates by a similar amount but in another direction which is not generally preferred (WALLRAFF & KIEPENHEUER 1994). Similar angular relationships between homeward direction and PCD, but also real map errors [Fig. 16], may cause clusters of similar release-site biases at neighbouring sites (GANZHORN 1990, 1992). PCDs have frequently been observed in wild birds apart from any recognizable linkage with homing (“nonsense” orientation of MATTHEWS, e.g. 1961, 1984; see also SANDBERG et al. 1991, ÅKESSON 1993, BALDACCINI et al. 1999, MUHEIM et al. 1999, etc.). It is also unclear which factors control the development of a particular PCD that is specific for pigeons of a particular loft. PCDs can be altered by manipulating wind conditions in the home aviary (WALLRAFF 1978, IOALE` & BENVENUTI 1983), but more recent findings by IOALE` (1996) raise doubts whether these experimentally created PCDs are equivalent to those spontaneously developed by the birds. A screen at only one side of the aviary induced initial bearings that tended towards a compass direction pointing away from the screened side (Fig. 2, AN-DN). However, the induced directions appeared not completely independent of the spontaneous PCD as developed by the unscreened control birds (Fig. 2, EN) which was either strengthened (CN) or weakened (DN) or deflected to the left (AN) or to the right (BN). If the four mean vectors resulting from the four symmetrical screenings are combined, the original PCD is still present in just the same way as in the controls (compare large arrows in FN and EN). Clearly different, however, is the degree of homeward directedness of the initial bearings (FH versus EH). This outcome suggests that the screens did not alter the “true” PCD but caused the creation of a deficient olfactory map. With a northwesterly screen, for instance, the pigeons could smell air masses arriving from northwest, but were unable to associate their odour composition with northwesterly winds as would have been appropriate. The PCD is not generally directed against the most frequent wind (WALLRAFF 1978). Pigeons living in neighbouring lofts with roughly identical wind patterns can show very differently oriented PCDs (SCHMIDT-KOENIG 1963, WALLRAFF 1970). The whole complex of interrelations between wind, atmospheric odours, homeward orientation and PCD is not yet sufficiently clear. Clarification can only be expected from experiments in which long-term anosmic pigeons, together with untreated controls, are exposed to natural and manipulated wind conditions (screenings, deflections), so that effects depending on olfaction can be separated from other components. Such experiments are so far lacking. Available indications suggest that a PCD develops independently of olfactory inputs (WALLRAFF 1978 and unpublished; PAPI et al. 1989). Shielding of winds all around, however, seems to inhibit its expression (WALLRAFF 1978, IOALE` et al. 1978; see also fig. 13 in Part 1).

1.1.2. Deflecting landscape features It is immediately obvious that prominent structures of the landscape, such as coastlines, lakes, mountains or valleys, influence the pigeons’ homing routes (WAG` et al. 1994). But also at release sites in a fairly flat and nonNER 1968, 1972; IOALE spectacular surrounding, the observer often gets the impression that the pigeons

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are attracted by a village or even by a single farm house. One or more initially preferred directions at a given site often point towards a nearby village (KIEPENHEUER 1993). At a single site, such coincidences might occur by chance. In a statistical analysis using data from 28 release sites, however, it has been confirmed that pigeons from a certain loft were generally attracted by human settlements, while they tended to avoid flying over wooded country (Fig. 3). The bearing distributions were more influenced by the topographical features the birds had overflown before they vanished from sight rather than by features they could see 1-2 km further ahead in their current direction of flight. Although it is mostly impossible to verify topographical influences at a particular site with certainty, there is no doubt that, in general, such influences contribute to the appearance of release-site biases. Responsiveness to landscape features appears to depend on the kind of environment surrounding the home loft.

Fig. 2. — Initial orientation of pigeons raised and kept in square aviaries with a wind screen on one side. The shielded side is indicated in AN-DN by a bar in the respective direction. Mean vectors per release from 6 roughly symmetrical sites are shown, 4 at distances 15-24 km and 2 (triangles) at 4055 km. The directions towards home are shown in AN-EN by corresponding symbols on the periphery. Large arrows symbolize second-order mean vectors derived from the 6 individual vectors. The same release vectors are arranged according to their compass alignment (AN-FN) and according to their deviation from the homeward direction (AH-FH). EN and EH refer to pigeons from an unscreened control aviary. The F diagrams summarize the results of A-D, giving their mean vectors with filled arrowheads and a third-order vector combining the results of the four partially screened aviaries. (Modified from IOALE` 1996: figs 4-5).


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Fig. 3 refers to a loft that was installed in a house within an isolated cluster of a few buildings in a rural setting. Pigeons from another loft, which was more remote from human settlements, were much less attracted by villages near the release site (WALLRAFF 1994b). It has not yet been tested in what way pigeons from a loft in the midst of a larger village or town respond to villages neighbouring a release site. It seems conceivable, for instance, that the release-site biases of pigeons settled in the city of Frankfurt (e.g. GRÜTER et al. 1982, WILTSCHKO & WILTSCHKO 1985a) are to a higher degree determined by nearby human settlements rather than by a PCD, whereas those of the rural pigeons of the Würzburg loft (e.g. WALLRAFF 1982, 1986) reflect more conspicuously the influence of a PCD.

1.1.3. After-effects of previous homing flights Pigeons in only their second or third release often initially show some preference for the direction in which they were successfully flown during their previous homing flight (WALLRAFF 1959a, 1967, 1974b, 1988b). The expression of this “secondary PCD” is very variable. Sometimes the mean direction of initial bearings follows exactly the previous homing course, even if it deviates by 90° or 180° from the actual homeward direction. More often, the direction chosen on the basis of the

Fig. 3. — Influence of human settlements (filled symbols) and wooded areas (open symbols) on vanishing bearings of pigeons released at 28 sites around their loft near Würzburg. The ordinate gives the mean proportional difference between the frequency of respective landmarks at a given distance and the frequency of pigeons vanishing in the direction of these landmarks (plus means more and minus fewer pigeons than would be expected if the birds would fly uninfluenced by topographical features). The dotted area marks the approximate distance range within which the pigeons vanished from sight. Shapes of symbols indicate level of significance for difference from zero: diamonds P < 0.01, squares P < 0.05, circles P > 0.05. (Modified from WALLRAFF 1994b).

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actual current condition is only more or less modified. Naturally, such influences can only be detected in a single release when birds with different pre-experience are simultaneously included. As this is mostly not the case, these effects contribute undetected, and to an unknown degree, to the great variability of biases among individual experiments. In more experienced pigeons, having performed many homing flights from fairly symmetrical directions, an after-effect, especially of the very last preceding release, can usually not be separated (SCHMIDT-KOENIG 1976). An asymmetric release pattern, however, has a directional training effect also in quite experienced birds (GRAUE 1965). Extremely intense compass training by more than 60 consecutive releases from the same site was obviously so effective that pigeons with a shifted sun compass did not hesitate to overfly the very familiar landscape on a wrong course deviating from that flown some 60 times before (FÜLLER et al. 1983).

1.2. Stress-associated effects on motivation Various experiments have been described in which pigeons exposed to artificial magnetic fields before release showed disturbed initial orientation upon release (e.g. WILTSCHKO et al. 1978, BENVENUTI et al. 1982, PAPI et al. 1983, IOALE` & TEYSSE`DRE 1989). Naturally, these results were discussed with respect to a possible involvement of the geomagnetic field in home-finding. Recent experiments conducted by the PAPI group, however, strongly suggest that the observed effects should be categorized into a section not dealing with navigational signals but with distracting factors which merely interfere with the pigeons’ physical and motivational state rather than with their homing mechanism. The elucidating investigations proceeded from an extended literature dealing with influences of oscillating or otherwise varying weak magnetic fields on the responses of animals, mainly rodents and molluscs, to aversive and stressful stimuli (e.g. KAVALIERS & OSSENKOPP 1986, 1991; PRATO et al. 1997). The affected molecular processes include the opioid system which mediates analgesic responses and attenuates sensitivity to potentially stressinducing conditions. It has been shown that, also in pigeons, an oscillating magnetic field inhibits analgesia (DEL SEPPIA et al. 1995). On the other hand, injection of the opiate antagonist naloxone disturbed initial homeward orientation of pigeons in a manner similar to pre-release exposure to an oscillating magnetic field (PAPI & LUSCHI 1990, PAPI et al. 1992). Also, such a field reduced the concentration of related opioid receptors in the brain, indicating that susceptibility to sedative endogenous opioids decreased. In several experiments, not only artificial magnetic fields but also potentially stress-inducing treatments before release, such as transportation in darkness or immobilization, weakened or abolished initial homeward orientation (WILTSCHKO & WILTSCHKO 1981, 1985b; DEL SEPPIA et al. 1996). When the pigeons were secured against stress by a tranquillizer, however, neither magnetic oscillations nor transport in darkness exerted any influence (LUSCHI et al. 1996). Thus, the effects of these treatments, when they occurred, did not concern the still operating navigational mechanism but merely the motivational state of the birds (see also LUSCHI et al. 1999, WALLRAFF 2000b). Apparently, when stress exceeded a certain threshold, the pigeons did not immediately orient their flight homewards but escaped either in an arbitrary direction, in a direction induced by topographical features, or in accordance with their PCD. In all controlled cases the pigeons returned home at


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normal speeds. Thus, their home-finding mechanism cannot have been significantly affected. The initial disturbances did not occur in all related experiments, but only in those with Italian pigeons (BENVENUTI & IOALE` 1988) and in Germany with pigeons that were less than 3 months old (WILTSCHKO & WILTSCHKO 1985b). Apparently, sensitivity to potentially stressful conditions is a variable depending on genetic strain and age. Probably it depends also on individual experiences. The dominance of the PCD over homeward orientation observed in fairly young inexperienced pigeons, and the reversed dominance in old experienced birds [Fig. 1], may have something to do with different sensitivity to stress induced by the handling procedures associated with displacement experiments. Most of the first-flight pigeons met with these procedures for the first time, while the old birds had been accustomed to them during many previous displacements. I would not even exclude the possibility that correlations of initial orientation with magnetic storms and disturbed behaviour observed at magnetic anomalies (Part 1; WALCOTT 1991, 1996; WILTSCHKO & WILTSCHKO 1995) might belong to this stress complex. Magnetic storms include irregular magnetic oscillations and a bird flying over the irregularly varying contours of an anomaly is exposed to temporal variations as well. Thus, conditions are, in principle, similar to those in experiments with oscillating artificial fields, albeit the amplitudes of natural oscillations may usually be smaller (for correlations of physiological phenomena with geomagnetic storms see OSSENKOPP et al. 1983, GHIONE et al. 1998). Although, at first glance, the categorizing of magnetic anomalies in this section appears to be out of place, it may be worth testing pigeons protected against stress by a tranquillizer at an anomaly at which non-treated birds show disturbed orientation (in analogy to the experiments by LUSCHI et al. 1996). If delicate differences in sensitivity thresholds depending on strain, age, loft conditions etc. were decisive for potential responses, some inconsistencies in related experiments (e.g. WALCOTT 1992) might become understandable.

1.3. Consequences for methods and interpretations It is important to identify not only the factors that are necessary for homefinding but also those that are not necessary but, nevertheless, co-determine the pigeons’ initial orientation behaviour. Lack of separation of these two categories can easily lead (and has led) to confusions and misinterpretations. Unfortunately, however, a clear separation is often or mostly impossible within a single release experiment. In a set of appropriately designed experiments as a whole, however, true homeward orientation can usually be distinguished from other directional tendencies and distracting influences, provided that the following three requirements are met: (1) If an experimental treatment disturbs solely initial orientation while homing speeds and return rates remain unaffected, it does not immediately indicate interference with the home-finding mechanism but may merely result from transitory alterations of the pigeons’ motivational state. Additional indicators are necessary to decide whether short-term conditions might have exerted a short-term navigational effect. (2) A number of release sites should be used that are, at least pairwise, distributed in central symmetry around the home site. This is a precondition to separate PCD orientation from homeward orientation [Part 1: fig. 2; here: Fig. 1].

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(3) In order to recognize a possible effect of an experimental treatment on the mechanism of home-finding, it is insufficient to take solely the initial bearings of untreated control birds as a reference. The direction towards home needs to be considered in addition. Both groups, experimentals and controls, usually have home-independent directional tendencies in common which may comprise tendencies towards a PCD, towards or away from certain topographical features and/or towards a previous homeward direction [1.1]. Fig. 4 shows an example in which the general similarity of bearings observed in pigeons with and without olfactory access to natural air is quite obvious (curve c), but in which, nevertheless, control and experimental birds differed significantly in homeward orientation (curves a and b). In this particular example, home-independent directional tendencies manifested in both groups (and most likely involving all three above mentioned kinds of influence) are even stronger than homeward tendencies in the untreated birds. In other cases, homeward orientation predominates [Part 1: fig. 7, A versus F]. Distracting directional preferences certainly vary in amount at different release sites or under other different circumstances. In a single release, they may hide homerelated tendencies to a large degree or even completely. Differences between experimental and control birds may then be quite small and insignificant. If in a series of symmetrical releases control pigeons deviate from experimentals most frequently towards home, however, even small differences may sum up to a significant overall result. The most appropriate indicators of true homeward orientation are the

Fig. 4. — Absolute angular deviations of mean vanishing bearings of pigeons with and without access to natural air from the direction towards home (a, b) and from each other (c). Frequency distributions of release means per 15° sector (n = 102 releases including both types of pigeons; 4 release sites in the cardinal directions 30 km from the home loft at Würzburg). Frequencies of a and c are different from a uniform distribution (line “mean”) with P < 0.0001; b is not significantly different from it; a differs from b with P < 0.001 (χ2 tests using 45° classes). Numbers “% < 90°” give percentages of release means differing from the reference direction by less than 90°. (Data included in KIEPENHEUER et al. 1993, fig. 1, supplemented by unpublished results).


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homeward components of initial bearings at symmetrical sites and the differences between homeward components of differently treated birds. (The homeward component is the rectangular projection of a vector, consisting of direction and length, on the axis running through release site and home site).

2. HOME-FINDING BY MEANS OF THE FAMILIAR VISUAL LANDSCAPE

Homing pigeons usually live in a well-structured landscape. It would be surprising if they did not make use of its visual appearance for purposes of homefinding. Clearly, if orientation by means of familiar landmarks comprised the whole story of pigeon homing, it would lose its particular fascination. But in order to recognize and understand the more enigmatic and fascinating facets beyond the range of “trivial” landmark orientation, it is necessary to determine which orientational performances the pigeons can achieve within this range. In this context, “range” has a double meaning: spatial extension around home as well as limitations of mechanisms using different environmental clues. Visual landscape features can only be helpful within an area that has been explored during previous flights, whereas olfactory signals obviously provide positional information also in unfamiliar more distant areas. 2.1. Non-olfactory homing It has long been known that in a second or third release of the same pigeons at the same site usually no dramatic change of orientation behaviour occurs. Release-site biases remain fairly stable and homing performances are merely slightly improved (WALLRAFF 1959a, KEETON 1973). Thus, possible familiarity with the landscape does not have an immediately obvious effect. Since other factors determining the birds’ behaviour are still at work, they might still predominate and mask the birds’ recognition of the visual environment. However, even the removal of one of these factors, olfactory access to ambient air, has little effect in such areas whose visual features are potentially familiar to the birds from earlier homing flights, whereas it prevents homeward orientation outside of the pigeons’ familiar range where visual features cannot contain positional information (PAPI et al. 1980a, PAPI 1986, BENVENUTI et al. 1992a; see also below Fig. 8). Even sites at which the pigeons had not yet been previously released, but which are inside a previously visited area including release sites down to a distance of 10 km from the current release site, are “familiar” in this sense (WALLRAFF & NEUMANN 1989, WALLRAFF et al. 1993; fig. 4 in Part 1; see also below Fig. 9). The lack of influence of olfactory deprivation inside such an area, but not outside of it, can most parsimoniously (i.e., without proposing enigmatic unknown factors) be interpreted by the hypothesis that homeward orientation without olfactory signals is achieved by referring to visual topographical features in an area somewhat exceeding the range of a pigeon’s previous immediate presence. Fig. 5 gives additional hints supporting this hypothesis. The homeward components of vanishing bearings (black columns), obtained after some two, three or more minutes of flight, were quite similar in pigeons unfamiliar with the area but allowed to smell natural air before release (F–O+) and in pigeons familiar with the area but prevented from smelling natural air (F+O–). Yet there was a considerable

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difference within the first 40 sec of flight. The F+O– birds, which were unable to collect olfactory information prior to release, did not yet show any homeward orientation, whereas the F–O+ birds, depending solely on previously received odours, were fairly well homeward oriented from the beginning. This difference is most plausible on the assumption that the F+O– pigeons required some time to gain height and survey over the landscape before they could draw conclusions about their position, whereas the F–O+ pigeons had already drawn this conclusion prior to release and could not profit from looking around in an unfamiliar area. (The intermediate behaviour of the F+O+ birds suggests that even with olfactory information the pigeons pay attention to the familiar visual landscape and try to bring it into coincidence with this information before they decide on a course to fly. The F–O– birds, receiving neither visual nor olfactory signals indicating position, remained disoriented with respect to home over the whole period of observation).

2.2. Effects of visual deprivation Other approaches aimed to exclude visual contact with the landscape by means of frosted contact lenses attached to the pigeons’ eyes. Pooled initial bearings of birds wearing such lenses were similar to those of controls with unimpaired vision even if the pigeons used were very experienced and released only 15 km

Fig. 5. — Mean homeward components of initial bearings 20 and 40 sec after release and at vanishing from sight. Pigeons of four groups differing in familiarity with the area (“F”) and olfactory condition before release (“O”) were released in alternating sequence: F+O+ = familiar with the area and before release exposed to natural air; F–O+ = unfamiliar with the area and before release exposed to natural air; F+O– = familiar with the area and before release kept in filtered air; F–O– = unfamiliar with the area and before release kept in filtered air. F+ means previously released in the surrounding area, but not at a site closer than 10 km to the actual release site. A few minutes before release, all birds received nasal anaesthesia; 4 releases at 2 sites; n ≈ 30 bearings per group. (Data from the experiments described by WALLRAFF et al. 1993).


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from the loft, where the landscape should have been quite familiar (SCHLICHTE & SCHMIDT-KOENIG 1971, SCHMIDT-KOENIG & SCHLICHTE 1972). Unfortunately, however, only initial-orientation data corresponding to curve c in Fig. 4 were communicated, so that nothing can be deduced about possibly different deviations from the direction towards home. The only published data including home as a reference and allowing one to compare visually impaired and unimpaired birds under otherwise equal conditions are those shown in Fig. 6. The pigeons wearing frosted lenses generally shortened their distance to the loft, but their routes were much less directly homeward oriented than those of the controls. It remains undecided whether the weaker performances were due to reduced availability of positional information or to general behavioural disturbance. At any rate, the results do not suggest that pigeons ignore visual clues. It appears possible that the tracks of the experimental birds reflect the level of performance achievable by pure olfactory navigation over the short distances used. The use of familiar non-olfactory signals is, or can be, redundant as long as the birds are allowed to smell natural air [Fig. 5]. Thus, to test for the possible importance of visual inputs it is necessary to exclude olfactory signals in addition. Clearly no indication for the involvement of a third factor has been found in exper-

Fig. 6. — Flight routes of pigeons released under sunny conditions 15 km north of their loft in Göttingen, Germany, and tracked by radiotelemetry. Solid lines refer to birds wearing frosted lenses, broken lines to birds wearing clear lenses. Circles indicate determined positions of birds in flight, asterisks indicate locations where birds remained sitting. (Modified from SCHMIDT-KOENIG & WALCOTT 1978).

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iments combining transitory visual impairment with transitory anosmia (STRENG & WALLRAFF 1992). Initial orientation as well as homing performance were found at decreasing levels in the following order: nothing impaired, only olfaction impaired, only vision impaired, both senses impaired. The twofold impaired pigeons did not show any trace of initial homeward orientation and their homing speeds were by far the lowest (arrival at the loft with meanwhile unimpaired vision and olfaction). Thus, the findings support the hypothesis that non-olfactory homing from familiar sites is visual homing. Nevertheless, I consider the results indicative but not definitely compelling. Even the birds deprived only of image vision were not significantly homeward oriented at vanishing (but homed significantly faster than the double-treated birds). Unlike anosmia, image blindness disturbs almost all kinds of elementary behavioural activities, including walking and flying, so that specific deficits in orientation can hardly be separated from more general behavioural deficits. Even though additional anosmia degraded performances further, thus indicating that with olfaction they were not yet at the deepest possible point, it cannot be excluded that nasal anaesthesia merely enhanced the stressful conditions acting on the pigeons in a non-specific way. BRAITHWAITE & GUILFORD (1991), BRAITHWAITE (1993), BRAITHWAITE & NEWMAN (1994) and BURT et al. (1997) restricted visual deprivation to the time before flying. For a period of 5 min prior to release, each pigeon was placed in a box with clear or opaque sides, respectively, allowing or preventing a view of the surrounding landscape. Birds that were allowed to preview the landscape returned significantly faster from sites in a range of 1-5 km from home, provided that they had previously been released at that particular site. Thus, these pigeons obviously did pay attention to the visual landscape. However, the experiments were conducted in the close vicinity of the loft, where landmark orientation has been conceded even by the opponents of its application in homing flights over longer distances (e.g. SCHMIDTKOENIG 1979, WILTSCHKO & WILTSCHKO 1998).

2.3. Relationships between landscape and sun compass Since it proved problematic to obstruct the pigeons’ view of the landscape during flight, it appeared advisable to look for more indirect indications about the possible role of visual clues in home-finding over familiar terrain. Deflections of initial bearings of clock-shifted pigeons, regularly observed at quite familiar as well as at unfamiliar sites, were often considered to indicate that visual landmarks are not used for orientation, because the birds readily fly away from the visible structures that would have guided them home (KEETON 1974; SCHMIDT-KOENIG 1979; SCHMIDT-KOENIG & GANZHORN 1991; WILTSCHKO 1991, 1996; WILTSCHKO & WILTSCHKO 1998). However, if inspected more closely, just these experiments strongly suggest that pigeons do make use of familiar topographical features for home-finding. It has long been known that deflections of initial bearings caused by clockshift, although consistently occurring with the predicted sign, are often smaller in amount than predicted on a pure sun-compass basis. In SCHMIDT-KOENIG’s summaries (e.g. 1979; SCHMIDT-KOENIG et al. 1991), the mean deflection of pigeons with their clocks shifted 6 hr forward is only 70°, while the mean difference between expected and actual sun azimuth was in the range of approximately 110-120° (see WALLRAFF 1974a, WILTSCHKO et al. 1994). Moreover, mean angular dispersion per release was greater in birds with shifted than in those with unshifted clocks, indi-


15

cating that the clock-shifted birds felt exposed to less clear-cut conditions than the controls. Such effects can be expected if the birds were influenced by both the pattern of familiar landmarks indicating one direction as appropriate and the seemingly shifted sun indicating another direction. The conflicting condition to which a sample of individually flying birds is exposed may then result in a mean bearing somewhere between full and no deflection and in an increased angular dispersion between the birds. Such a conflict cannot occur in unfamiliar areas where the landscape does not contain positional information. It is very likely that in many of the experiments conducted by SCHMIDT-KOENIG (1958, 1961) and WILTSCHKO et al. (1994) the old experienced pigeons they used were more or less familiar with the area in which they were released. Moreover, from previous releases under clockshift many birds may have learned to distrust the shifted sun compass and instead to follow, wherever possible, the familiar landscape directly. These are retrospective assumptions being in general agreement with the experimental conditions described by the authors. In other experiments, the relevant conditions were a priori controlled according to the following rationales. In an unfamiliar environment, pigeons are thought to determine their position by means of airborne odours. Once they have concluded where they are with respect to home, they ask their sun compass to determine that direction. If the sun compass is shifted by clock-shift, they follow the angular shift without hesitation not realizing that something is wrong (Fig. 7A) (see also NEUSS & WALLRAFF 1988; fig. 1 in Part 1). A familiar landscape, however, providing not only information on the birds’ own position but presenting a spatial pattern of a large area around, would by itself guide the right way. During familiarization, the pigeons could observe the sun together with the landscape and thus could associate a certain compass course with the alignment of a certain landscape. For a bird afterwards released with its circadian clock shifted by 6 hr, the sun is in a wrong position with respect to the landscape. Which of the two sources of information should the bird trust? Its confusion should be particularly strong if the determination of position is based exclusively on visual landmarks, i.e., if olfactory signals are excluded. In fact, under this condition the effect of a 6 hr clock-shift is quite variable and inconsistent; deflections from control birds as well as from home are, on average, considerably reduced (Fig. 7C). With both olfactory and visual signals available, somewhat reduced deflections and not so widely scattered bearings have been observed (Fig. 7B). Variable effects of clock-shifts similar to those seen in olfactorily deprived birds in familiar areas were observed in normal pigeons released at very short distances from the loft ranging between 1 and 3 km (GRAUE 1963, KEETON 1974, SCHMIDT-KOENIG 1979, HOLLAND et al. 2000). These birds were in a comparable situation. Odours could not be used in the close proximity of the loft and the sun did not fit in the expected way with the landscape. Splits between following the sun and following the landscape were sometimes observed among bearings of individual pigeons at the same site and sometimes among the majority of birds at one site and another. Such splits need not indicate the application of basically different mechanisms as suggested by HOLLAND et al. (2000). They merely reflect the dichotomous condition when sun and landscape, usually used in accordance with each other, are at variance (see WALLRAFF 1991: fig. 6D-F). The birds have no choice but to neglect one kind of signal or to make a compromise. Variable effects of clock-shifts on homing routes were also observed from more distant release sites in familiar areas (PAPI et al. 1991, BONADONNA et al. 2000). They suggest that the landscape tends to dominate over the sun particularly at sites or in areas where conspicuous features such

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as coastlines or mountain ridges act as guidelines and/or barriers. It is very likely that varying local topographical features also contributed to the great variability of the vectors shown in Fig. 7C. For more detailed considerations about clock-shifts and landscape see WALLRAFF (1991) and WALLRAFF et al. (1994, 1999). 2.4. Brain asymmetry and visual orientation An inventive approach indicating involvement of visual signals in pigeon homing has recently been published by ULRICH et al. (1999). Pigeons were trained to home from one or two sites 24-32 km distant from home. To test for a possible influence of brain hemispheric differences in visuospatial cognition, they were then released with a cap occluding either the left or the right eye. Against binocular viewing, pigeons with the left eye open homed significantly slower, but not pigeons

Fig. 7. — Angular deviations of mean single-release vectors of initial bearings of pigeons whose circadian clock was shifted 6 hr forward, from corresponding vectors of non-shifted controls. The deviation (abscissa) is given as a percentage of the varying angle between actually observed sun azimuth and expected sun azimuth according to the phase-shifted time scale of the experimental birds (depending on date and site of release, this angle ∆Az varied between 88 and 144°). A is from normal pigeons in a largely unfamiliar area (F–), B from normal pigeons in a familiar area (F+) and C from pigeons deprived of olfactory access to natural air (O–) released in a familiar area (F+). Symbols refer to different series of experiments whose conditions in detail were not standardized (● in A and B+C from different series). (From WALLRAFF et al. 1999; see there for references to data sources).


17

monocularly seeing with the right eye. In view of previous evidence of a superiority of the right eye / left hemisphere in discrimination learning, the authors conclude that these “results show that visuospatial orientation in birds can be lateralised in favour of the left brain hemisphere and lend further support to the view that vision is important for pigeons homing on a familiar route”.

2.5. Conclusion and perspective It is so apparent that many arthropods, vertebrates and other animals make use of visual landmarks for their orientation in space, including homing, that particular citations are not necessary. Therefore, it is reasonable to set the “null hypothesis” that the homing pigeon is not an exception. There is no reason why its landmark orientation should be restricted to a limited spatial range, aside from the fact that this kind of orientation is always restricted to landmarks with which the individual has become familiarized by experience. Thus, it would be necessary to disprove the above null hypothesis in order to reject it rather than to prove its validity. So far, I do not see any experiment that actually disproves the most likely and most trivial hypothesis that non-olfactory signals utilized for home-finding from familiar sites are visual features of the landscape. It is hardly possible to achieve direct positive evidence for the use of such features, but the circumstantial evidence described above strongly supports the landscape hypothesis. Also, the role of the hippocampal formation in pigeon homing appears quite equivalent to its known role in mammalian landmark orientation (BINGMAN et al. 1998b). Olfactory signals are, of course, still available once an area has become familiar to the birds. Also distracting factors [1.1] are not, or need not be, removed by familiarization. In many cases, landscape orientation may be redundant; in some cases, when olfactory signals are weak or ambiguous, it may be helpful; and in cases when such signals are not available at all, homing may still be possible by means of landmarks alone. Conflicting situations, and hence unclear results, may occur in experiments implying clock-shifts, deflector aviaries or olfactory site simulations, if they are conducted in a familiar area. The finding that familiarization can act over distances of 10 km and possibly more [2.1] makes definition of a not yet used release site as “unfamiliar” uncertain, if it lies within a grid of experienced release sites around. But also “familiar” is not a clear definition. A site can be more or less familiar for a given bird, depending on spatial and temporal distances of earlier experiences and on their frequency. Also, the conspicuousness of topographical features (mountains, lakes, towns etc. versus flat “empty” country) in the release area as well as at the home site may play some role. It appears possible, for instance, that pigeons from a loft in a large city with tall buildings are in a particularly favourable situation for landmark-based homing. In the course of their homing flights, they may become familiarized with the conspicuous skyline of their home town which is visible over considerable distances. At least at release sites not too far away, pigeons from such a loft (e.g. WILTSCHKO et al. 1994, SANDBERG et al. 1999) might respond in a “familiar-area manner” while less extensively trained than other pigeons whose loft is in a rural environment lacking a conspicuous large landmark labelling the goal. Retrospectively, I have the impression that the role of the visual landscape in pigeon homing has been underestimated over many years (cf. WALLRAFF et al. 1994). Many results described in the literature should now be seen with some

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reservation because, at least potentially, they might include influences of the familiar landscape. Such influences are likely to occur when veteran pigeons experienced in homing from many sites are tested at fairly short distances from home [e.g. fig. 3 in Part 1]. It is often difficult or impossible to estimate whether, or to what degree, a given result might have been affected by such interfering conditions. In future experiments, this aspect should be considered more carefully. The observation that pigeons become familiarized with an area over some distance suggests that visually oriented birds do not follow a chain of individually learned small-scale landmarks such as houses, villages, forests, rivers, roads, etc., connecting the release site with the home site. It seems more likely that the pigeons make use of a large-scale aerial panoramic view over a wide area which may be represented in the birds’ brain as a “topographical map” (possibly a “cognitive map”), which allows evaluation of a landscape from viewpoints with varying parallax, including points at which the birds had not yet been before (as previously suggested by BAKER 1984). This assumed “visual topographical map” of an area does not seem to provide more accurate positional information than the assumed “olfactory gradient map” [3.2], so that familiarity with a site or an area does not result in remarkably improved homeward orientation. A bird’s view differs considerably from a human’s view of the world (WALDVOGEL 1990). The bi-monocular visual field of a pigeon covers a little less than 360° in the horizontal plane (DONOVAN 1978). This wide field may not only be useful to detect a suddenly emerging predator but also to survey an extended aerial panorama of the landscape underneath. Referring to previously experienced large-scale characters of an area rather than to individual landmarks would facilitate vision-based homing from sites which themselves have not yet been visited before. However, this kind of non-detailed topographical mapping might provide merely a rough idea of the direction towards home. Unfortunately, we know very little about the pigeons’ visual world. We should not too narrowly extrapolate from our own sensory capabilities and restraints. (It would be worthwhile to test in the laboratory whether pigeons are able to pay attention to two or more distant objects in an extended angular range of some 90° simultaneously, i.e., without focussing them in succession).

3. HOME-FINDING BY MEANS OF ATMOSPHERIC ODOURS

During the last decade, olfactory navigation has continued to be a controversial topic discussed by proponents (PAPI 1991; WALLRAFF 1991, 1996; BENVENUTI et al. 1992b), by opponents (SCHMIDT-KOENIG 1991, SCHMIDT-KOENIG & GANZHORN 1991, WILTSCHKO 1996) and by neutral observers (ABLE 1996, ROPER 1999). No basically new ideas have grown up, but the empirical basis has been broadened by further experiments with pigeons and extended by analytical approaches into the chemical atmospheric environment. 3.1. Homing experiments 3.1.1. Recent results The fundamental results leading to the conclusion that home-finding even from unfamiliar areas is based on volatile airborne substances received by olfaction


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have been reviewed in Part 1. During the decade since 1990, no results at variance with this conclusion have been published, but several additional results support it. Anosmia induced by zinc sulphate. Using a new method of olfactory deprivation, tests were extended to additional geographical regions. Intranasal irrigation with a solution of zinc sulphate (ZnSO4) causes dysfunction of the olfactory mucosa lasting several days. It has been shown by laboratory tests that, using appropriate concentrations of ZnSO4, the pigeons’ sense of smell is strongly impaired, probably eliminated (SCHLUND 1992). Effects of treatment with ZnSO4 on homing were analogous to the effects of olfactory nerve section as reported in Part 1. The examples shown in Fig. 8, obtained with pigeons of SCHMIDT-KOENIG’s loft near Tübingen, Germany, suggest a similar dependence on the degree of (non-)familiarity with the release area and on the distance of displacement [fig. 3 in Part 1]: homing success was most strongly reduced over the longer distances from fairly unfamiliar areas and least reduced over the shorter distances from fairly familiar sites. In these experiments, initial bearings were quite weakly homeward oriented even in the control pigeons, so that impressive effects of ZnSO4 treatment on initial orientation could not occur. In experiments in Italy, where the controls were better homeward oriented, a highly significant complete breakdown of initial homeward orientation in ZnSO4-treated birds was evident at unfamiliar release sites but not at a familiar site (BENVENUTI et al. 1992a). Similar experiments were conducted in two regions of North America and in England (BINGMAN & BENVENUTI 1996, BINGMAN et al. 1998a, GUILFORD et al. 1998; see also BENVENUTI et al. 1998). The accuracy of the initial homeward orientation of control birds was variable depending on the region, whereas ZnSO4-treated pigeons failed to orient homewards at unfamilar sites everywhere. BENVENUTI & GAGLIARDO (1996) combined unilateral nose-plugging with unilateral ZnSO4 irrigation in quite the same way as PAPI et al. (1980b) did with nerve section [Part 1]. The differences between ipsilaterally and contralaterally treated birds in initial orientation as well as in homing performance were also very similar to those obtained in the earlier experiments. Thus, also the effect of ZnSO4 on pigeon homing can hardly be explained solely by non-olfactory side-effects. Micro-environmental conditions. Navigational information contained in the atmosphere does not only vary with geographical position but also depends on the kind of environment from which the inhaled air originates. Pigeons enabled to smell air from the free airspace in an open landscape were significantly better in initial homeward orientation than pigeons ventilated with air coming from a level close to the ground in a forest or in a maize field (WALLRAFF et al. 1992). Spatial range. Two fairly recent publications made clear that the spatial range of olfactory navigation is not a fixed radius around the home but depends on the particular geographical relationship between home site and release site. Pigeons displaced over 300 km across the Alps from a loft in southern Germany to northern Italy were not only disoriented, but flew, apparently well-oriented, over considerable distances further southwards away from home. Pigeons from another loft, however, located even 500 km north, flew from the same release site predominantly northwards. Simultaneous releases of anosmic birds showed that the two diverging directional preferences were based on olfactory signals (WALLRAFF 1993). A possible explanation of these results, considering the orographical situation, is in line with the gradient hypothesis discussed below, which is also compatible with the results

NS

Fig. 8. — Mean homeward components of initial bearings (left) and return rates (right) of pigeons made anosmic by ZnSO4 and of control pigeons. Columns refer to results from individual releases at various sites within the indicated distance ranges, surrounding frames refer to overall means. Birds “unfamiliar” with the release site had not yet been released at the particular sites used here, but had been repeatedly released from other sites at distances up to 60 km. Birds “familiar” with the release site, generally experienced over distances of up to at least 40 km, had made one flock release at the current site a few days before. Thus, “unfamiliar” and “familiar” indicate gradual rather than absolute differences in the birds’ previous homing experience; especially the sites 9-24 km from home were probably in a generally fairly familiar area, whereas the more distant “familiar” sites were in only weakly familiarized surroundings. P values refer to the results of the Wilcoxon matched-pairs test applied to corresponding values (columns) of Control vs ZnSO4. (Data from SCHLUND 1992 and SCHMID & SCHLUND 1993).


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of BENVENUTI et al. (1994) indicating analogous spatial limitations in the smallerscale mountainous structures of the Italian Apennines. Here, limits for homeward orientation obtainable without olfactory outward-journey information were found between 60 and 120 km, whereas within topographically smoother regions of Germany such limits had not yet been reached at distances of 180 km (WALLRAFF 1980a, 1980b). Other results. KIEPENHEUER et al. (1993) accumulated more data showing that filtration of ambient air before release combined with nasal anaesthesia upon release [Part 1] prevents initial homeward orientation and reduces homing speed. They analysed in more detail the relationships between home-related and homeindependent components of the pigeons’ homing behaviour [1.1]. WALLRAFF’s (1994a) statistical analyses suggest that the olfactory clues utilized by the pigeons in unfamiliar areas are considerably noisy and provide a merely probabilistic basis for home orientation. DALL’ANTONIA et al. (1999), using recorders tracking the birds’ complete homing routes, found these routes differing from each other in predictable dependence on the two different sites at which the pigeons could smell natural air before they were transported, without access to natural air, to a third site for release. A few other recent investigations will be mentioned in the Appendix.

3.1.2. Older results revisited Nasal anaesthesia. Fig. 9 illustrates three aspects of temporary olfactory deprivation induced by application of an anaesthetic into the pigeons’ nostrils prior to release. (1) Prolonged homing times are not merely an effect of trauma or else nonspecific disturbance. If this were the case, decreasing effects with increasing dis-

Fig. 9. — A: Homing times (minutes per km bee-line distance) of pigeons released under nasal anaesthesia (open symbols) and of untreated control pigeons (filled symbols). Symbols indicate medians of single releases obtained at different symmetrically distributed sites. B: Differences between the medians for experimental and control birds per release, also including means and 95% confidence intervals of the two distance classes. The P value results from a comparison of the distance classses using the Mann-Whitney U test. The dashed line at 15 km indicates the upper limit of preceding training flights. (Data from WILTSCHKO et al. 1987).

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tances of release would be expected, because over longer distances the time of drug action covers a smaller portion of the homing time. However, just the contrary happened: homing speeds were significantly lowered only over the longer distances. (2) This dependence on distance can most plausibly be interpreted as a support of the above-mentioned hypothesis that the visual landscape can be utilized for homefinding over a range somewhat exceeding the range of previous physical presence [2.1, 2.5]. Before the experiments started, the pigeons had been trained up to a distance of 15 km, then were released between 17 and 23 km and thereafter between 30 and 34 km. Apparently, their previous knowledge of the area enabled the birds to home at largely normal speeds without using olfactory signals even when released at sites several kilometres away from earlier visited sites. This was no longer possible, however, when the distances were further increased over a larger gap into increasing two-dimensional extension. (3) These findings, obtained by WILTSCHKO et al. (1987) around Ithaca, New York, confirm once more that pigeons appear to utilize olfactory clues for homing wherever they are investigated. Olfactory site simulation. In fig. 8 of Part 1, effects of exposure to ambient air at a site different from the release site on initial orientation has been illustrated by two examples out of a series of experiments. Since the conclusiveness of these experiments has been doubted (WILTSCHKO 1996; see Appendix), they are summarized in Fig. 10 as a whole. It is evident that the experimental birds oriented towards the simulated home direction as equally well as the control birds towards true home (Fig. 10, E versus A, overall homeward components = c H = 0.32 versus 0.28). The smaller negative value of = c H = – 0.20 in C is explicable by the fact that the two directions of a pair of releases (“true home” and “false home”) were not always exactly opposite to each other. The third group of pigeons used in these experiments, participating in the detour to the “false site”, but at no time allowed to smell unfiltered air, ranged between the two other groups. Correspondingly to other experiments [e.g. Fig. 1; Part 1: fig. 7], these birds completely deprived from smelling natural air showed a general compass tendency towards WSW most clearly, but in principle, all three groups had this PCD in common (Fig. 10F-H). In assessing the greatly scattered bearings in these experiments, the reader should bear in mind that the “open” birds were released several hours after they had been enabled to smell natural air. (For corresponding differences between the three groups in homing speed, see fig. 9 in Part 1). 3.2. Gradients in atmospheric trace gases Considering all the experimental data now available, it is very difficult to escape the conclusion that pigeon homing from unfamiliar areas is substantially based on olfactory perception and appropriate evaluation of trace substances diluted in the atmosphere. Intuitive resistance against this conclusion is natural [Appendix], as it is all but obvious in what way airborne trace gases could enable goaloriented navigation over hundreds of kilometres. It seems inconceivable that the unstable atmosphere might provide sufficiently stable spatial gradients of whatever kind without which a navigation system covering large unfamiliar areas is hardly possible [Part 1]. However, given the amount and diversity of related homing data, we have no choice but to search for such gradients despite understandable scepticism about their existence. In the following section, I shall explain a working hypothesis on possible gradient structures (see also Part 1 and WALLRAFF 1989b,


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Fig. 10. — Vanishing bearings observed in 10 releases, pairwise consecutively conducted at roughly opposing sites at distances of 25-55 km, with three differently treated groups of pigeons. “False open” pigeons were first transported, while breathing charcoal-filtered air, to a “false site” roughly opposite to the later release site, were enabled to smell there natural air for a period of 3 hr, and were then transported, again with filtered air, to the actual release site. “False filter” pigeons made the same trip, but were never allowed to smell unfiltered air. “True open” pigeons were transported, with filter, directly to the release site, were allowed to smell the natural air at this site for the same period of 3 hr, and waited there, again with filter, for the arrival of the other birds and subsequent individual releases alternating between members of the three groups. All birds started under nasal anaesthesia. Diagrams show the pooled individual bearings on the periphery, mean vectors per release as arrows (radius = vector length 1) and second-order mean vectors derived from them as a centre of a 95% confidence ellipse. The same bearings are shown as deviations from three reference directions: the actual true homeward direction (left), the direction pointing towards home from the site where the “False open” birds had been exposed to natural air (middle) and north (right). P values inside the diagrams result from using the V test referring to the “upward” direction (A-E) or from using the Rayleigh test (F-H) (BATSCHELET 1981). P values between diagrams refer to twosample comparisons of “upward” components of individual bearings using the Mann-Whitney U test. In this condition, A versus C is significant, with P < 0.0001; a second-order test applied to the 10 pairs of mean vectors in A and C gave P < 0.01. (Modified from BENVENUTI & WALLRAFF 1985).

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1991), then I shall describe actual observations of such structures in nature, and finally I shall show that the empirical atmospheric data can in fact be used to compose a model navigation system whose outputs are similar to the performances observed in pigeons.

3.2.1. Theoretical considerations The conventional idea of bi-coordinate navigation proposes two gradients intersecting at a sufficiently large angle, optimally at 90°. Straightforwardly applied to the atmosphere, the concentrations of two trace compounds should have fairly stable gradients in two different directions. Moreover, birds should be able to measure absolute concentrations of two odours separately. Both demands appear fantastic rather than realistic. Physically, it is hardly conceivable that the concentration of any airborne substance at a given site can remain roughly constant under varying weather conditions, such as temperature and wind direction, and, in addition, that this concentration gradually increases and decreases from that site in roughly constant opposing directions. Physiologically, determination of absolute intensities is problematic; even less feasible appears separate determination of two absolute intensities within the same modality. Potentially closer to reality might be the expectation that birds are able to determine the ratios among quantities of two or more odorous compounds independently of their absolute concentrations. Based on such ratios, we distinguish between fragrances of flowers, fruits or perfumes whose specific smell results from the proportional mixture of a number of chemical compounds. We perceive a stable odour quality of each mixture within a wide range of absolute concentrations and a change of quality when ratios among components change. Focusing on ratios among substances rather than on absolute concentrations may also be more promising with respect to the expectable stability of spatiotemporal patterns in the atmosphere. If birds would use gradients of ratios among compounds to determine position, two compounds would not be sufficient, because a ratio between two quantities could provide only one coordinate. With a minimum of three compounds, however, any position would have a unique ratio pattern, provided that the ratio gradients are perfectly monotonic and sufficiently divergent. The schematic examples in Fig. 11 illustrate that position determination would not be affected by temporally varying absolute concentrations which might, for instance, fluctuate with temperature. It would not be a problem if pigeons were released on one day at one site in condition A and on another day at another site in condition B. Even a patchy pattern showing varying trace gas densities in different regions would remain suitable as long as the location-dependent proportions remain stable (compare CW-E and DW-E in Fig. 11). Referring to ratios rather than to absolute quantities does not automatically solve the problems connected with varying wind directions. Winds might not change all proportions completely, however, but might displace a given gradient pattern as a whole, leaving its internal structure fairly stable. With a northeasterly wind, for instance, the pattern shown in Fig. 11, A2D or B2D, might be displaced so that the relatively large number of black dots from the northeasterly quadrant are shifted to the location of a pigeon loft in the centre. As a navigationally positive consequence, the pigeons might learn, at home, that winds from northeast are correlated with a relative increase of compound “black”, winds from southwest with a


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Fig. 11. — A2D and B2D: Fictitious two-dimensional field, 400 × 400 km, within which the portions of three different compounds, distinguished by symbols, vary along differently oriented gradients (upward slopes indicated by small arrows). Absolute concentrations are different in the two graphs, but site-specific ratios among the compounds are identical. AW-E-DW-E: Quantities along the westeast axis running through the centre. AW-E and BW-E, showing absolute concentrations, correspond to A2D and B2D. When the ratio of each compound is calculated as a percentage of the sum of all three compounds, the resulting diagram DW-E is identical for A and B. The regularly increasing and decreasing percentages DW-E result also from the much less regularly varying concentrations shown in CW-E (corresponding two-dimensional pattern not shown).

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relative decrease. When later released at a site with an unusually large portion of “black”, the birds may remember this correlation and conclude that they are northeast of their home site. A mechanism of this kind would be in good agreement with the aviary experiments described in Part 1. However, it would be connected with the serious negative consequence that the spatial position of the whole twodimensional pattern of ratios would be unstable. No invariable set of ratios would characterize the home site or any other location. Thus, additional preconditions must be introduced to make the mechanism operational. The simplest solution would be that wind-induced shifts of proportions, although recognizable to the birds, are small against differences depending on position. The problem of ambiguity (does relative increase of “black” indicate wind from or displacement to NE?) would then arise only at short distances where olfactory navigation has a lower limit. It seems not very likely that ratio gradients in trace gases, if existing at all, are so little modified by varying winds, but as a possibility it should not be discarded a priori. Alternatively, the birds could take the current wind conditions into account and regard a flexible, wind-dependent ratio spectrum as a home reference. If they do so, however, they apparently do it not by means of direct measurements of wind direction using their sun compass upon release. In this case, the sun compass would be involved in the process of position determination. Clock-shifts would cause false conclusions about wind direction, hence about the home spectrum to be taken as a reference and hence about the birds’ position in relation to home. Recalculation of initial bearings only on the basis of differences in sun azimuth would not lead to a level of home orientation as high as that of control birds (Part 1; NEUSS & WALLRAFF 1988, WALLRAFF et al. 1999). Thus, the birds might use indirect signals which possibly involve more reliable information on prevailing wind conditions in a larger spatial and temporal scale than measurement of the momentary local wind. It has been shown that, theoretically, such information could be deduced from atmospheric trace substances whose proportional contribution to a set of utilized compounds varies with wind direction but varies very little in dependence on position (WALLRAFF 1989b). All these considerations concern conceivable basic structures (for application in a navigation model, see WALLRAFF 1989b). Even if they would fit reality in principle, it cannot be expected that real structures are so schematically clean. Also, it need not be proposed that they are. Homeward orientation of pigeons is quite inaccurate and intermingled with substantial stochastic noise. There are reasons to assume that noise is more inherent in the environmental signals used rather than in the animals’ actions of processing these signals (WALLRAFF 1994a). To reach the levels of performance obtained by pigeons, spatial signals need not be very reliable and unambiguous. A larger number of considerably noisy gradients may lead to similar levels as a smaller number of more regular gradients (WALLRAFF 1989a). Thus, it would be advantageous if birds would use more than the minimum of three airborne compounds.

3.2.2. Empirical findings The above considerations served as a basis for an investigation of atmospheric trace gases within a radius of 200 km around Würzburg, Germany, which was previously the home-site centre for many homing experiments with pigeons [e.g. fig. 5 in Part 1]. Using small tubes filled with adsorbent carbon material, airborne volatile


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organic compounds (VOCs) were collected at the centre as well as at 96 sites regularly distributed around it. The collected samples were analysed by gas chromatography and statistically evaluated (WALLRAFF & ANDREAE 2000). Usually 200-350 compounds were recorded per chromatogram, but statistical evaluations were focused on 16 compounds that were clearly identified in each of the 224 analysed samples obtained in the course of 16 crosswise symmetrically arranged trips during three summers under variable weather conditions. Amounts of VOCs contained in the different samples varied considerably, but the shapes of the chromatographic peak patterns were quite similar throughout (Fig. 12). Data of interest were the proportional variations of peak sizes within these patterns and their spatial relationship to the geographical positions at which the samples had been collected. The basic unit for calculations was the amount of one compound as a percentage of the sum of two or more compounds within the same chromatogram (see boxes in Fig. 12). If the 16 omnipresent VOCs were combined pairwise, 120 combinations were available. For each compound within a pair, the mean percentage resulting from 192 chromatograms (2 per peripheral site) was determined. From the standardized differences from this mean, together with the spatial distribution of the sampling sites, a “parameter of eccentricity” was computed which indicates the degree of spatially oriented separation of above-mean and below-mean ratios

Fig. 12. — Parts of two typical gas-chromatograms showing the peaks of 16 more thoroughly analysed chemical compounds. Numbers give C (carbon) indices used for identification (6 compounds included in Fig. 14 with prefix C). Ordinates are in relative but corresponding units; note the different ranges. The boxes contain example calculations using areas (relative units) and resulting ratios for one pair of compounds. (From WALLRAFF & ANDREAE 2000).

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(for details of computations see WALLRAFF & ANDREAE 2000). In the case of a spatially uniform distribution of the differences, eccentricity would be zero. Most of the actually observed values are considerably larger (filled columns in Fig. 13). However, with a limited number of measurements and sites, even random distributions would usually deviate from zero to some degree. Possible random deviations can be determined by linking the chromatograms not to their actual sites of origin but to randomly selected other sampling sites. Average deviations from zero resulting from 105 independent replications of such mixing procedures are shown by the cross-hatched histogram in Fig. 13. The highest actual values have not been reached in any one of the 105 random permutations; the 99.9% range of their medians does not include the actual median. The circular insert in Fig. 13 shows the individual sampling sites with the corresponding standardized ratios between the two compounds providing the highest eccentricity value. Each of the 16 substances, being always one partner among 15 pairs, is differently localized in the black histogram of Fig. 13. If the six highest ranking com-

Fig. 13. — Statistical expression of gradient character in spatial distributions of ratios among pairs of compounds, measured in terms of “eccentricity”. Filled columns give the frequency distribution of eccentricities of 120 ratios among 16 pairwise combined substances resulting from the actual geographical distribution of air samples. Cross-hatched columns show the mean distribution of the same ratios resulting from 105 permutations in which the air samples were distributed to the sampling sites at random. The filled circle at 16.5 km indicates the median of the actually observed distribution, the dot at 7.7 km the second-order random median with the 99.9% range of medians per replication. The circular insert (radius 200 km, north on top) shows the ratios among two compounds, C4.0 and C5.3, at the 96 sampling sites. Sites where the portion of compound C4.0 was above mean are marked with filled circles, those where it was below mean with open circles (their sizes indicating differences from the mean). Ellipses give 95% confidence areas of mean locations of “black” and “white” sites, respectively. (Modified from WALLRAFF & ANDREAE 2000).


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pounds (which are farthest outside of the range reachable by chance and were determined identically using an independent second computational algorithm) are separated and their ratios calculated not pairwise but as a percentage of the sum of all six, their relative amounts form “mountainous landscapes” with differently oriented overall slopes (Fig. 14). The distributions are quite noisy, but in principle they fit the expectations illustrated in Fig. 11. Each site in the inspected region of Germany is characterized by a particular ratio spectrum of the six substances.

Fig. 14. — Relief maps showing standardized ratios of six compounds among each other as measured in the region around Würzburg. Areas where the relative abundance of the respective compound was above its overall mean are bright, those with values below average dark. Small diagrams show means in classes of distance along the computed gradient slope whose upwards direction is indicated (ordinate = difference from overall mean in units of standard deviation). (From WALLRAFF & ANDREAE 2000).

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Most likely, none of these six compounds is actually used by pigeons to find the way home. Except for isoprene, they are all anthropogenic hydrocarbons. However, inhomogeneous distribution of sources and sinks, chemical conversions, variable lifetimes and atmospheric transport patterns are quite equivalent in anthropogenic and in naturally emitted biogenic VOCs. If ratio gradients exist among some airborne compounds, they can be expected to exist among other, also natural VOCs in a similar fashion as well. The chemical tracers analysed in detail were predominantly those that were present in the air at fairly high concentrations and hence were most accessible to the applied method. It was evident, however, that several other, not always detected and not chemically identified VOCs have similar gradient patterns in the ratios among each other. The gradients so far recognized using fairly crude techniques are probably not the clearest ones actually existing in the atmosphere. Less remarkable than the revealed spatial order is the observation that ratios among VOCs vary temporally in relation to wind direction. Such influences could have been expected. It is remarkable, however, that at least some spatial gradients hold their alignments fairly stable even under conditions of opposing winds or of air masses arriving from different directions. It is further remarkable that a correlation exists between the upwards direction of the spatial ratio gradient of a given compound and the wind direction under which the ratio increases (Fig. 15). In the

Fig. 15. — Angular relationships between wind-dependent and site-dependent directions of eccentricity of ratios among 525 pairs out of 72 compounds (selected according to frequency of presence in the chromatograms and to amounts of eccentricity). Example for reading: in 25% of the compound pairs, the maximum relative increase of one of the partners occurred with winds deviating 45 ± 15° clockwise from the direction of its maximum spatial increase (e.g., ratio of compound A relative to B, which was spatially largest in regions northwest of the centre, was temporally largest with winds from north). (Modified from WALLRAFF & ANDREAE 2000).


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analysed data, the two directions diverge by a mean angle of approximately 45°. It is not yet clear whether this angle is generally representative or is more or less biased by chance-based predominance of anticyclonic weather conditions during data sampling. At any rate, a systematic relationship seems to exist between VOC ratio variations as correlated with wind on the one hand and location on the other hand. Thus, also this hypothetical prediction [3.2.1] has been met, albeit not in a most simple and ideal way which would have produced a near-zero angle of divergence. The presently available data set is too small to enable definitive conclusions on long-term geometrical relationships between winds and spatial distributions of trace gases. 3.2.3. Suitability for navigation In a next step we ask whether the six distributions shown in Fig. 14 can be used as a “map” basis for home-finding. On condition that computer-born model pigeons are thought to have gained, before displacement, some approximate knowledge of the compass alignment of the six gradients, it is possible to deduce, for any site within the investigated area, from the six local ratios a direction that aims to approach the centre (Fig. 16; details of computations in WALLRAFF 2000a). Some of

Fig. 16. — Using the VOC ratio distributions and gradient directions shown in Fig. 14, estimates of homeward directions were computed for an array of 196 sites within a radius of 200 km around “home” near Würzburg (north at the top). The sector between direction towards the centre and the computed direction is filled black. Areas of circles are proportional to the lengths of computed homing vectors (relative units). The overall mean vector resulting from the 196 directions deviates from home by – 2° and has a length of 0.78. (From WALLRAFF 2000a).

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the computed directions are completely wrong, but at 94% of the sites the deviation from home (= centre) is less than 90° and the overall homeward component is, with a value of 0.77, better than that usually found in experiments with pigeons. In Fig. 17, computer results based on observed atmospheric data are compared with observations obtained with real pigeons. Fig. 17A does not only summarize (with its heavy curve) the directions exhibited in Fig. 16, but shows in addition that even VOC data obtained while winds came from opposing directions (thin curves) provide results in the range of the performances of living birds. In order to make simulated homing routes or distributions of recovery sites appear realistic, it is necessary to introduce considerable stochastic noise. Then the individual model pigeons fly differently and the overall outcome is quite comparable to results obtained in the field (Fig. 18). Results still in the range of the performances of living pigeons cannot only be reached by using the six paradigmatic VOCs used to produce Figs 16-18, but also by using several other combinations of three or more compounds, although, of course, not every arbitrary combination is suitable. In the above simulations, the directions of the VOC gradients were taken from Fig. 14 and considered as known. Experiments with pigeons confined in aviaries in which winds were manipulated in various ways [Part 1] suggest that the birds achieve this knowledge by associating varying VOC ratios with contemporaneous wind directions. Fig. 15 has shown that the two parameters are in fact correlated. It is not yet clear whether the birds can ignore the current weather conditions (especially wind directions) during the time of their homing flight (as may be suggested by Fig. 17) or whether they have to take these conditions into account, possibly by using additional information derived from VOCs as suggested in an earlier model (WALLRAFF 1989b). 3.3. Unsolved problems Investigation of VOC ratio distributions in the atmosphere with respect to their suitability for navigation has just begun. More data obtained simultaneously using an extended grid of locations for VOC sampling would be necessary to achieve a satisfactory understanding of the dependence of VOC ratios on both the geographical location and the variations of weather and wind. By using improved techniques, more biogenic VOCs should be included which theoretically are suitable candidates for being exploited by navigating birds. The final search for concrete airborne substances that are actually used for home-finding may follow thereafter, but this has not the highest priority. The way by which winds are integrated in the system requires further clarification not only with respect to associated atmospheric VOC ratio changes and spatial gradients but also with respect to the pigeons’ responses to winds in connection with olfactory conditions as well as with possibly interfering PCD effects [1.1.1; Part 1: p. 108]. On the physiological side, questions such as olfactory sensitivity thresholds, non-adaptability and signal processing in the context of navigation are completely unsolved. Just because olfaction is a classical sensory modality whose functional mechanism is investigated and understood in many respects, it seems incredible that birds can smell where they are within an unknown area covering tens or hundreds of thousands of square kilometres. Concentrations of biogenic VOCs in the atmosphere are usually very low, often considerably below the olfactory thresholds so far measured in birds (WALDVOGEL 1989, ROPER 1999). This fact appears to con-


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Fig. 17. — Homeward orientation of model pigeons using the VOC ratios of Fig. 14 (A) and of real pigeons (B). A: The heavy solid curve shows the frequency distribution of absolute angular deviations from the centre as calculated in Fig. 16. Thin curves show corresponding results obtained with winds (≥ 5 km/hr) coming from only one hemicircle as indicated (e.g., from north ± 89°). The broken curve refers to wind speeds ≥ 5 km/hr irrespective of wind direction. Column “n” gives the number of air samples on which the computations are based, column “% < 90°” the percentage of sites at which the computed direction deviates by less than 90° from the direction towards the centre. B: Corresponding frequency distributions of mean vanishing bearings of real pigeons in 9 series of experiments conducted at fairly symmetrical release sites around home. Open symbols refer to inexperienced pigeons displaced for the first time. For details of sources see original. (From WALLRAFF 2000a).

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tain another serious argument against olfactory navigation. As in the case of atmospheric gradients, however, we are challenged to search for solutions not only within the limits of our “simplicity filters” (GRIFFIN 1978) and conventional thinking. Recent experiments have shown that, in humans, inhaled airborne substances at very low concentrations (down to 10-8 M and possibly lower) can activate specific regions in the brain (SOBEL et al. 1999), regulate physiological functions (STERN & MCCLINTOCK 1998) and modulate psychological state (JACOB & MCCLINTOCK 2000), although the chemical signals cannot consciously be detected as odours. Thus, we need not expect that it should be possible to determine relevant olfactory thresholds by means of conventional training techniques such as operant or cardiac conditioning. Although olfaction is a classical sensory modality, its use in navigation may be similar, under aspects of sensory and neural physiology, to the use of the geomagnetic field providing compass information. In either case, birds are permanently exposed to the relevant stimuli which do not change rapidly as they usually do in training experiments (cf. WILTSCHKO & WILTSCHKO 1996). In the case of atmospheric odours, rapid changes cannot even be provoked by the animals themselves (as they can by means of body turns in the magnetic field). Permanent exposure to the airborne trace gases must not result in reduced sensitivity by adaptation. We should not be too much surprised if the method by which birds evaluate atmospheric odours for purposes of navigation will turn out to differ from the rules known within the scope of conventional olfaction. The common use of terms such as odour and olfaction in the context of navigation should merely express that relevant stimuli are received by the olfactory system. There are still considerable gaps in our knowledge with respect to either part of the system, the atmospheric environment as well as the birds. Within both parts, however, there is also a considerable amount of empirical data available which are all compatible with the ratio-gradient hypothesis outlined above. On this basis, future research can be addressed to progressively more narrowly defined problems.

Fig. 18. — Homing routes of model pigeons using the VOC ratios of Fig. 14; determination of positions distorted by some stochastic noise. Eight release sites 150 km distant from home near Würzburg, at each site 10 pigeons starting. A: complete paths. B: simulation of recovery sites: end points of shorter routes; ranges of random errors greater than in A. (From WALLRAFF 2000a).


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4. HOME-FINDING BY OTHER MEANS?

Passively displaced pigeons determine their position relative to their home site by means of airborne olfactory signals and, only within a familiar area, by means of the visual landscape. There is no indication that they might utilize any other kind of site-based or route-based information. I am aware that the writer of such statements is easily labelled biased and narrow-minded. However, it is not the aim of scientific research to remain, unimpressed by its own findings, open-minded for everything for ever, but to reduce initially visible or later emerging possibilities to ultimately remaining actualities. As regards the types of navigational signals used by pigeons for homing, I believe that this process has been accomplished. Presently I do not see any necessity to propose other or additional sources of positional information besides the two mentioned above. They include a lot of unsolved problems on which future research should be focused [2.5, 3.3]. Investigating structures and ways of involvement of basically identified environmental clues promises much stronger heuristic impact than continued dealing with empirically largely excluded clues or with fictitious spatial gradients whose physical nature remains undefined. Since the sun-navigation hypothesis (MATTHEWS 1953, PENNYCUICK 1960) has been falsified (e.g. KRAMER 1961, KEETON 1974, WALLRAFF 1974a, SCHMIDT-KOENIG 1979), the most frequently discussed competitor of an olfactory map is a magnetic map. However, all attempts to disrupt the pigeons’ navigation mechanism by disturbing magnetic inputs failed to prevent the birds from finding the way back to their home loft (references and further discussions in Part 1 and WALLRAFF 1983, 1999; WALCOTT 1991). Nevertheless, there has been much speculation about magnetic maps. Such speculations are still going on (GOULD 1998; WALKER 1998, 1999), although they lack any empirical support. Even authors who tend(ed) to favour the idea of a magnetic map, either came to the conclusion that “it is hard to believe that pigeons use a magnetic map” (WALCOTT 1991) or, at least, conceded “that magnetic cues are not essential” for homing (WILTSCHKO & WILTSCHKO 1995). It should be added that available evidence even argues against the assumption that the geomagnetic field might serve as a (usually redundant) backup source of positional information. If olfactory signals are eliminated, pigeons are obviously unable to replace them by magnetic signals [Part 1]. The case of magnetic navigation appears similar to that of sun navigation. Either of these navigation systems is theoretically possible in principle, most clearly with respect to positions along the north-south axis. However, physically and physiologically problematic details (e.g. gradients involving merely minute quantitative differences within the distance range of pigeon homing, spatial and temporal magnetic noise exceeding the range of necessary precision, chronometry in the case of sun navigation), together with the even more problematic second coordinate, may not have allowed the evolution of suitable position-fixing mechanisms based on such global grids (for difficulties with geomagnetism see LEDNOR 1982, WALCOTT 1991, ÅKESSON & ALERSTAM 1998, WALLRAFF 1999). As directional references for compass orientation, however, requiring much lower precision than map functions, both the sun and the geomagnetic field are quite successfully used by birds (e.g. SCHMIDT-KOENIG et al. 1991, WILTSCHKO & WILTSCHKO 1995). A number of experiments in which exposure to artificial magnetic fields deteriorated initial orientation but not homing performance gave rise to some confusion over many years, even more so, as the effects were restricted to certain genetic strains or to very young pigeons. Eventually it turned out that all or most of these

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experiments concerned distracting factors transitionally affecting motivation at the time of release but not the process of determining the direction towards home. Therefore they are now discussed in the appropriate section [1.2]. Since also path integration (sometimes called route-based navigation or route reversal) can be excluded in all the experiments using passive displacement (see Part 1 and WALLRAFF 2000b), there is no other explicit mechanism or environmental clue in sight that might alternatively or in addition to atmospheric trace gases and the visual landscape be used by pigeons to find the way home. Also, there is no indication that additionally an enigmatic “factor X” might be at work and no reason to propose unidentified additional resources. I do not exclude unexpected discoveries in the future, but according to current knowledge I see no result or argument that stands against the hypothesis that atmospheric trace gases perceived by olfaction are a necessary as well as a sufficient source of information that is used by pigeons, together with a sun compass (or a magnetic compass), to find the way home from unfamiliar distant areas where visual landmarks cannot be used.

APPENDIX: CRITICAL SURVEY OF THE LITERATURE In Part 1 and in the above sections I described the present state of our knowledge about pigeon homing as I see it resulting from empirical research and associated theoretical considerations. In the related literature as a whole, however, the state currently reached appears confusingly unclear and controversial (see WALCOTT 1996). Surveys of the matter published by SCHMIDT-KOENIG (1987, 1991), SCHMIDT-KOENIG & GANZHORN (1991) or WILTSCHKO & WILTSCHKO (1998, 1999a, 1999b) have little in common with those by PAPI (1986, 1991, 1995) or WALLRAFF (1990, 1991, 1996). It is necessary, therefore, to discuss also the divergent views and to explain why I reject the various conclusions, interpretations and objections that are not in agreement with the presentations given in Part 1 and above. I cannot discuss each publication and each aspect, but I try to include all that may appear relevant. Articles published before 1990 have already been considered in Part 1. Although there is disagreement about all three main topics of this “Part 2”, the most important controversial topic is olfactory navigation. Therefore, I take the opponent article by R. WILTSCHKO (1996) as a first guideline along which the diverging views will be discussed. A few further issues will follow thereafter. Multiplicity of navigational clues and regional differences. It has often been easy to deal with apparently inconsistent or contradictory results by assuming that pigeons make use of multiple, more or less redundant environmental clues to determine their position and that they preferentially use different clues in different regions or depending on varying local circumstances (e.g. KEETON 1974, WILTSCHKO et al. 1987, SCHMIDT-KOENIG & GANZHORN 1991, GANZHORN 1992, WALCOTT 1996). Thereby, and if the assumed clues are not all specified, it is possible to interpret almost every result but also to avoid a real explanation. Moreover, results obtained under methodologically clear-cut conditions are usually not ambiguous and do not indicate involvement of multiple or alternative clues in position determination. Unimpeachable evidence of reliably non-olfactory homeward orientation from reliably unfamiliar areas has so far not been obtained anywhere on earth. What has been different in different experiments was the level of homeward directedness and homing performance in untreated control birds (i.e., the efficiency of olfactory navigation, which makes differences against anosmic birds variable), the possible availability of familiar visual landmarks [Figs 8-9], the effectiveness of olfactory deprivation before or upon release [Part 1: p. 104] and/or the portion of home-independent directional preferences [1.1] that were common to both control and experimental birds.


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Availability of suitable signals in the atmosphere. The understandable immediate disbelief in the existence of suitable spatial structures in the atmosphere has been corroborated by three publications which may seem to provide evidence that olfactory navigation is in fact unfeasible. BECKER & VAN RADEN (1986), discussing undoubtedly existing meteorological problems, end up with a distinction between long-lived and short-lived substances whose gradients are thought to be unusable for navigation on opposing grounds: they are considered too large-ranged and flat or too small-ranged and irregular, respectively. This distinction provokes the logical conclusion (already drawn by PAPI 1986) that medium-lived substances might be suitable. Moreover, the authors do not consider the case of ratios between substances. Two compounds, for instance, may have small-range sources and sinks in common while the ratio between them systematically shifts over a longer distance [Fig. 11, CW-E and DW-E]. By pure reflection on a complex system, not yet specifically investigated under the given aspect, it is hardly possible to exhaustively predict which particular effects and interrelations may or cannot occur. WALDVOGEL (1987) describes trajectories and plume distributions of artificial tracer aerosols released into the atmosphere. This point-source investigation measuring absolute concentrations of limited quanta over space and time, as well as the connected discussion (see also WALDVOGEL 1989), is unsuited to testing for large-scale proportional relationships as outlined above. Similarly unsuitable for this purpose are the concentrations of a few most frequent pollutants (NO, NOx, SO2 etc.) in and above several Bavarian towns as reported by GANZHORN & PAFFRATH (1995). All three studies were based on the premise that the birds should be able to deduce positional information from separately measured concentrations of individual compounds. It is a priori unlikely that this premise is appropriate [3.2.1]. Nevertheless, these publications have been quoted as if they provide evidence that olfactory navigation cannot be possible (SCHMIDT-KOENIG 1987, 1991; WALDVOGEL 1989; SCHMIDT-KOENIG & GANZHORN 1991; WILTSCHKO 1996). In reality, such negative results and conclusions merely show that not every kind of data extractable from the atmosphere can be exploited for navigational purposes, but they cannot provide evidence that there is nothing in the air that might be exploitable. The analytical way described above [3.2.2] may also not be optimal. At least, however, it shows that navigationally exploitable structures can be found in the atmosphere. Pooled data and individual releases. WILTSCHKO (1996) emphasizes that usually only pooled initial orientation data of anosmic pigeons, summarizing many releases at different sites, reveal “disorientation”, whereas in the individual releases either scatter is increased or the birds are well-oriented but deviate in their mean direction from the controls. This is quite true, but it implies no argument against olfactory navigation. I have discussed many times that such varying results are caused by differently expressed directional preferences that have nothing to do with the position relative to home and hence are not affected by anosmia [1.1]. Just because of these interferences of home-independent directional preferences, it is often impossible to draw firm conclusions from individual releases. Only the pooling of data from many symmetrical releases shows the definite existence or lack of homeward orientation [1.3]. “Possibility of non-olfactory effects” (quotation marks indicate headings in WILTSCHKO 1996). It is unclear whether the effect of nasal anaesthesia on initial orientation after preceding unimpeded smelling observed by WILTSCHKO et al. (1989) reflects impairment of olfactory orientation or a stress-induced response. At any rate, these findings do not degrade the conclusiveness of the many releases in which both experimentals and controls were equally anaesthetized [Fig. 10; Part 1: fig. 7]. The brief abstract by DORNFELDT (1979) does not contain any experimental details making the results assessable. The clock-shift experiments by BINGMAN & IOALE` (1989) and WALLRAFF et al. (1994) in familiar areas underline the specific effect of olfactory deprivation rather than question it (they are here included in Fig. 7C). WILTSCHKO’s (1996) fig. 1 (now published in more detail by SANDBERG et al. 1999), showing a strange unexplained result, is no basis for raising doubts about quite different experiments conducted by others.

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“Behaviour at familiar sites”. The three items enumerated by WILTSCHKO (1996) do not contain valid arguments against the usage of visual landscape features. (1) BENVENUTI & FIASCHI (1983) combined the attachment of frosted lenses with olfactory impairment by means of contralateral section of one olfactory nerve and plugging of one nostril (not causing complete anosmia: WALLRAFF 1988a). They used an experimental procedure very different from typical homing experiments. A group of pigeons was trained, with gradually increasing sensory impairment, to home from either one of two sites only 3 and 7 km away from the loft. In the final tests, the birds with twofold sensory impairment still vanished in different directions appropriate to the release site used, but none of the 16 birds reached the vicinity of the loft, whereas 7 of 20 birds impaired only in vision and all birds impaired only in olfaction arrived there. The initial orientation data from these dual-choice training experiments in the close neighbourhood of the loft do not prove that pigeons pay no attention to familiar visual landmarks if they are available and that, in homing over longer distances from unpredictable sites, a third factor providing positional information is involved which is neither olfactory nor visual (for a more detailed discussion see p. 216 in STRENG & WALLRAFF 1992) [2.2]. (2) I do not see any reason why a pigeon’s range of view, within which it takes notice of landscape features, should be restricted to a narrow strip of land underneath its flight path [2.1, 2.5]. (3) The clockshift experiments by FÜLLER et al. (1983) were conducted after intense compass training which apparently dominated over influences of the landscape (see WALLRAFF et al. 1994, 1999) [1.1.3]. I agree that “it is difficult to see why odours ... should suddenly cease to play an important role after one homing flight” from a given site (WILTSCHKO 1996). Why should they, indeed? Odours do not cease to play a role, but other useful signals are now available in addition. I wonder who might have “repeatedly hypothesized that birds might change their navigational strategy and rely solely on familiar landmarks” when released at familiar sites (WILTSCHKO & WILTSCHKO 1998: 184, without a citation). Only if experimentally forced by olfactory deprivation, must the birds rely solely on familiar visual landmarks. The recognition of the possible involvement of visual signals in homing is so difficult because in a familiar area the system is bi-factorial. “A paradoxical pattern of responses”. The experiments with pigeons raised and housed in different loft conditions (WILTSCHKO 1996, fig. 2) have been extensively discussed in Part 1 (pp. 104-106). While ignoring this discussion, WILTSCHKO (1996) does not reject my arguments. Thus, they stand uncontradicted. Although the arguments imply criticism of the applied method (incomplete anosmia before release), WILTSCHKO & WILTSCHKO did, over 10 years, not refute this objection by demonstrating homeward orientation in pigeons reliably prevented from smelling environmental odours. If an experiment creates a “paradox”, it is very likely that some unconsidered circumstances were involved (in the present case, incomplete anosmia combined with phenomena discussed in sections 1.1 and 1.3). Deflector lofts. It is true that, in quantitative terms, the experiments conducted so far with deflector lofts are not fully satisfactory. As pointed out in Part 1 (p. 108), this is probably due to sub-optimal experimental arrangements. WILTSCHKO’s (1996) fig. 3, showing differences between findings at sites considered familiar or unfamiliar, even underlines my suspicion that in these short-distance releases landscape features often co-determined the results, possibly even at so-called unfamiliar sites. Incomplete deflections may be similarly explicable as the incomplete deflections caused by clock-shift [2.3]. Given the sparse information provided by WALDVOGEL & PHILLIPS (1991) on procedural details of their more recent deflector experiments (not considered by WILTSCHKO 1996), it appears possible that their birds’ homeward orientation was exclusively based on familiar landscape features. The modified deflector aviaries did not induce any deflections of the pigeons’ bearings at all. Most likely, the added “anti-cheating slats” caused so much turbulence in the cages that the birds could not recognize regular wind patterns and hence could not develop an olfactory map. The authors “believe” that the pattern of airflow was not disrupted but fail to provide evidence supporting their belief. Their own interpretations based on involvement of polarized skylight are utterly speculative and lack any plausibility. For a discussion of the earlier deflector loft experiments, see Part 1 (pp. 108-110).


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Olfactory site simulation. Not even I understand WILTSCHKO’s (1996) description of our site simulation experiments [3.1.2 and Part 1]. I am not certain whether at least the intended description is correct (at any rate incorrectly used is the term “anosmic”: no bird was anosmic before release, all birds were anosmic upon release). It is untrue that, “when pooled, none of the groups was homeward oriented” [Fig. 10] (BENVENUTI & WALLRAFF 1985). WILTSCHKO’s table 1 is aimed to demonstrate that the pigeons making the detour with or without access to natural air at the “false site” [“False open” and “False Filter” in Fig. 10] oriented towards similar directions. In fact, the two groups show similarities [Fig. 10, G and H], but these similarities do not concern homeward orientation which alone is affected by olfactory inputs. Such similarities are the rule rather than an exception [Fig. 1 above and fig. 7 in Part 1] and make it obligatory to include the direction towards home as a reference, when the role of olfactory clues is the topic of interest, instead of comparing differently treated groups only among each other [1-3, Fig. 4]. In WILTSCHKO’s table 1 (which compares only birds with other birds as a reference), a third line could be added referring to “Anosmic pigeons released at A”. The results would be similar to those in line 2, although the comparisons were made between pigeons that shared neither the route of transportation nor the release site. Even if not really understanding WILTSCHKO’s text and table, a non-expert reader understands the message that the data presented by BENVENUTI & WALLRAFF (1985) are inconclusive. As this false message seems to include a particularly strong objection against crucial experiments, it is particularly misleading. “Open questions about the role of olfactory input”. Under this heading, WILTSCHKO (1996) assembles a number of arguments from which doubts are deduced about the navigational role of olfactory inputs. I cannot consider anyone of these arguments really powerful against the bulk of discounted positive evidence. Weights become obvious by the apparent necessity to refer to very weak and most inconclusive sources, such as DORNFELDT (1979) or GANZHORN & PAFFRATH (1995), in order to gather arguments. As usual in opponent articles (e.g. SCHMIDTKOENIG & GANZHORN 1991, WALKER 1999), assumed or known non-olfactory side-effects of olfactory deprivation (e.g. DORNFELDT & BILO 1990) are emphasized, while experiments in which their possible action was neutralized [Part 1: fig. 7 and pp. 102-103] remain unconsidered. Some of the arguments are simply unintelligible. As extensively outlined by WALLRAFF et al. (1994, 1999), clock-shift experiments with olfactorily deprived pigeons do not suggest interference with the sun compass but with the expected fit between sun position and familiar landscape [2.3, Fig. 7]. Effectiveness of olfactory deprivation only at unfamiliar sites has always been seen as an indication that non-olfactory signals usable as an alternative are available only at familiar sites [2]. I cannot understand how this point can be reversed as an argument against olfactory navigation. If olfactory inputs would “play another role” in the sense that they are in some way a precondition for the functioning of a non-olfactory navigation mechanism, without carrying themselves navigational information, it is difficult to explain the filter experiments and the site simulation experiments [Part 1: figs 7-9; here: Figs 5 and 10] in which both control and experimental birds could smell before release and both were released under nasal anaesthesia. Preferred compass direction (PCD). Less understandable than their opponent position against olfactory navigation is WILTSCHKO & WILTSCHKO’s (e.g. 1985a, 1999a, 1999b; WILTSCHKO 1993) denial of a PCD as a frequently interfering factor despite the fact that an empirical observation cannot really be denied. The matter has so often been discussed (e.g. WALLRAFF 1986, 1991) that it is useless to do it once more [1.1.1; Figs 1 and 10; Part 1: fig. 7]. The observation that little of a PCD can be detected in most of the WILTSCHKO data around Frankfurt (but see SCHMIDT-KOENIG 1970 and Part 1: fig. 13) does not imply evidence that it nowhere exists and that release-site biases exclusively reflect distortions of gradient-map factors. Such distortions are expected to exist in addition [Fig. 16], but together with other deflecting factors whose possible influence in the Frankfurt area has so far not been communicated [1.1.2]. From the fact that origin and function of the PCD are not yet understood, it cannot be deduced that the PCD does not exist and does not co-determine release-site biases.

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(We need not understand the “nature” of gravity in order to observe and calculate its effects and to accept its existence). Path integration, “route reversal”, “route-based navigation”. It is apparent that adult pigeons, while passively transported to a release site, do not profit from any kind of path integration operating independently of external site-specific clues [Part 1]. A “change in navigational strategy” from path integration, used only during a few weeks in the pigeons’ early lifetime, to later map-based navigation, as proposed by WILTSCHKO & WILTSCHKO (e.g. 1985b, 1998, 1999a, 1999b), is not experimentally proved and is logically unconvincing (WALLRAFF 2000b). In response to my criticism, WILTSCHKO & WILTSCHKO (2000) deal with the matter as they have done many times before and again they ignore the most crucial issues. (1) Disturbed initial orientation alone does not prove the lack of information on the direction towards home [1.2, 1.3]. The few reported data including homing performance (WILTSCHKO & WILTSCHKO 1985b) do not suggest an influence of transport conditions on homing ability. (2) It is disproportionate to construct, on such an unsettled experimental basis, an extra strategy “for beginners” which the pigeons clearly do not need for the formation of a navigational map. Pigeons permanently confined in an aviary (e.g. KRAMER 1959; WALLRAFF 1967, 1970, 1979), and hence prevented from making any exercise flights during which they might profit from path integration, are well home-oriented when displaced over 100 km and more. WALKER (1999) and WILTSCHKO & WILTSCHKO (2000), doubting that such pigeons can develop a proper map system, assume that their homing ability relies on route-based information. They fail to explain, however, in what way a wall of wood or glass around the home aviary, which precludes homeward orientation not only at departure but for ever, might affect the recording and integration of motions during transport. There is not the slightest indication that aviary pigeons use a navigational strategy basically different from that used by birds allowed to fly near their home. Aviary experiments actually provide instructive hints as to the nature of the navigational map [Part 1]. For a more detailed discussion see WALLRAFF (2000b). Infrasound. HAGSTRUM (2000) has recently refreshed the hypothesis that long-range infrasonic waves might form a map used by pigeons to determine positions (see also QUINE 1982). His contribution is highly speculative and does not contain any empirical evidence in support of this idea. (Disruptions of four pigeon races occurring concurrently with intersecting infrasonic shock waves from Concorde supersonic aircraft can hardly be recognized as evidence. How many supersonic flights did not affect simultaneous pigeon races? How many races were disrupted with no Concorde flying in that region? Disrupted pigeon races were occasionally observed long before Concordes acoustically polluted the atmosphere). In pigeons whose sensitivity to infrasound was impaired by perforation of their tympanic membranes, SCHÖPS (1991) and SCHÖPS & WILTSCHKO (1994) observed at some sites deteriorated and at others improved initial orientation. As the two abstracts do not contain experimental details, the range of possible interpretations (including points made in section 1.3) cannot be assessed. Bilateral removal of the related receptor organ, cochlea and lagena, did not impair homing capabilities over distances of 150 km and more (WALLRAFF 1972). I do not see any distinct indication, and hardly a realistic chance, that infrasound signals might be involved in pigeon navigation. Unexplained effects. It would be possible to write a long chapter about conspicuous effects observed in experiments on pigeon homing that could initially not be explained or were first interpreted incorrectly. Some of these effects led later to a better understanding of pigeon navigation, others turned out to be caused by unrecognized behavioural peculiarities, by overlooked concomitant conditions or by deficiencies of the applied methods. Some such effects are still pending without a satisfactory explanation. Among them are the airbag / detour results (“experiment 2”) by GANZHORN & BURKHARDT (1991), the magnetic anomaly / loft location experiments by WALCOTT (1992) and the plastic container / clock-shift experiments by SANDBERG et al. (1999). I do not consider it likely that anyone of these and other so far unexplained effects belongs to the category of findings that finally might lead to an improved or basically altered perception of pigeon homing.


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Mosaic versus gradient hypothesis of olfactory navigation. When PAPI et al. (1972) detected the importance of olfaction for pigeon homing, they suggested a hypothesis proposing the evaluation of qualitatively different odours carried by winds from different directions. This “mosaic hypothesis” (WALLRAFF 1980b) appeared reasonable for very short distances (winds coming from north over a nearby lake carry an odour that is different from an odour coming with easterly winds over a wood, etc.), but it has also been applied to greater distances. BENVENUTI et al. (1994) deduce an argument in favour of the mosaic hypothesis from their finding that, in Italy, limiting distances are not very great. Pigeons appeared unable to obtain olfactory positional information at sites more than 100 km away from home. However, apart from the fact that in Germany the distance limit has been found to be beyond 180 km [3.1.1], it is unclear in what way a mosaic system might function even within a radius of some 50 km. It has never been explained what “an odour” as an element of a mosaic map means. If it means a single compound, it would be necessary to explain in detail how such a system might operate with any arbitrary location acting as a potential home site and how many compounds it would need (for difficulties see WALLRAFF 1991). If it means a bouquet composed of several compounds, however, the quality of the resulting odour depends on the ratios among them, i.e., on their proportional quantitative relationships. In that case we are considering a ratio gradient system associating an odour with a “more northerly character” with winds from north, etc. [3.2.1]. Areas embracing sufficiently monotonic gradients are certainly differently extended in different regions and may be particularly small in a mountainous narrow strip of land with the sea on either side, such as Italy. To end the discussion with compromising words, we may speak of a mosaic of gradient fields, whose geographically varying sizes determine the operational range of olfactory navigation in a given region.

ACKNOWLEDGEMENTS I thank Floriano Papi and an anonymous referee for their helpful comments on the manuscript.

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