Olfaction and the homing ability of pigeons in the Southeastern United States

THE JOURNAL OF EXPERIMENTAL ZOOLOGY 276:186-192 (1996)

Olfaction and the Homing Ability of Pigeons in the Southeastern United States

VERNER P. BINGMAN AKD SILVANO BENVENUTI Department of Psychology, Bowlitzg Green State University, Bowling Green, Ohio 43403

ABSTRACT The importance of atmospheric odors for homing pigeon navigation was tested using birds from a loft located in Savannah, GA, in the southeastern United States. When released from a familiar training site, control pigeons and pigeons given intranasal injections of zinc sulfate to produce mosmia both displayed good homeward orientation and homed quickly. When released from three unfamiliar release sites, in contrast, control birds tended to orient southeast, while zinc sulfate-treated birds were more likely to fly northwest. More importantly, while the majority of control pigeons returned to the home loft, few of the zinc sulfate-treated birds returned. The good performance of both groups from the familiar site indicates that zinc sulfate treatment does not impair the general motor ability or motivation of homing pigeons. Therefore, the observed impairment in homing success of the zinc sulfate-treated pigeons from the unfamiliar locations presuriably reflects an impaired ability to use atmospheric odors to navigate home. As such, the data support the hypothesis that successful homing pigeon navigation is based on the perception of atmospheric odors and that olfactory navigation is the primary mechanism used by pigeons over a broad range of geographic areas to approximate their relative position with respect to home from unfamiliar locations. o 1996 Wiley-Liss, Inc.

The ability of homing pigeons to return home from distant, unfamiliar release sites is thought to be based on a two-step navigational process con- sisting of independent map and compass mechanisms (Kramer, '52; Wa.llraff, '90). Although the sensory basis of the compass mechanisms has been we11 described, both the sun and the earth's magnetic field are used (Kramer, '53; Wiltschko and Wiltschko, 'SO), and understanding the sensory basis of the navigational map has been more difficult (Gould, '82; Wallraff, '90; Able, '96).

A large number of experiments have been car- ried out in Italy, Germany, and the United States, the results of which offer compelling evidence that airborne, olfactory cues play a critical role in the operation of the homing pigeon navigational map (for review see Papi, '90; Wallraff, '90). Despite this vast body of supporting evidence, the olfactory hypothesis as an explanation for the operation of the homing pigeon navigational map has been the source of ccmsiderable controversy (Schmidt-Koenig, '87; Able, '96). The most seri- ous argument directed against the olfactory hypothesis is that atmospheric odors may not be similarly important as a navigational cue for all pigeons. For example, it, has been argued that olfaction is less important in some regions of Ger- many and the United States than perhaps in Italy 0 1996 WILEY-LISS, INC.

(Wiltschko et al., '87a) or that the use of olfaction is dependent on the type of experience a pigeon has while young (Wiltschko et al., '87b). However, studies by other workers have contradicted these findings (Benvenuti and Brown, '89; Benvenuti et al., '90; Bingman and Mackie, '92). In summary, although most researchers agree that olfaction plays an important role in homing pigeon navigation (Able, '96), there remains some question with respect to how ubiquitous atmospheric odors are as a navigational cue.

To address this issue, one obvious research strategy is to examine the importance of olfaction for pigeon navigational behavior in a number of different geographical regions. In the present study, we report the results of an experiment de- signed to examine the importance of atmospheric odors for the navigational performance of homing pigeons from Savannah, GA, which lies near the Atlantic coast of the southeastern United States. Savannah is interesting in two respects. First, it is in the United States where olfaction has been previously reported to be perhaps less important as a navigational cue (Wiltschko et al., '87a; but

Received February 29, 1996; revision accepted May 24, 1996. Address reprint requests to Verner P. Bingman, Department of Psy-

chology, Bowling Green State University, Bowling Green, OH 43403.

PIGEON OLFACTORY NAVIGATION IN GEORGIA 187

see Benvenuti and Brown, '89; Bingman and Mackie, '92). Second, Savannah lies in a coastal, hot, and humid environment that might be envi- ronmentally well suited for learning the spatial distribution of atmospheric odors and conse- quently an olfactory navigational map (Waldvogel, '87). This latter consideration would lead one to expect a map strongly influenced by atmospheric odors in this region. Indeed, the results are consistent with the hypotheses of an important role for olfaction in homing pigeon navigation in the southeastern United States.

MATERIALS AND METHODS Experimental animals

A pool of 53 homing pigeons, reared at a loft in Savannah, GA, was used. It is worth noting that the location of the loft was in the backyard of a house located in a heavily wooded residential neighborhood. The local environment around the loft was very reminiscent of the garden loft location of the Wiltschko laboratory in Frankfurt, Ger- many, where pigeons are reported to acquire a navigational map relatively uninfluenced by atmospheric odors (Wiltschko et al., '87b). The birds were all born in the spring of 1995. They were housed in a loft that had an opening facing the north (trap and standing area) but was otherwise closed. Beginning at about 2 months of age, the birds underwent a modest training regimen which consisted of continual free flights around the loft, followed by four group releases from different directions not more than 10 km from home. Follow- ing this preliminary training, all pigeons were then given five training releases from a location (familiar site, see below) 34 km west of the home loft. The first three training releases from this location were group releases. For the last two training releases, birds were released in groups of three. Following training, the experimental releases began.

Experimental releases On September 29, 1995, 24 pigeons were ar-

bitrarily chosen and subjected t o a n intranasal injection of zinc sulfate heptahydrate dissolved in distilled water. Zinc sulfate alters or destroys the olfactory mucosa, effectively rendering pigeons anosmic until regeneration takes place (Benvenuti e t al., '92; Schlund, '92). Zinc sulfate administration is generally considered an anosmic procedure with few if any side effects (Benvenuti and Gagliardo, in preparation). Two

milliliters of a 4% solution was injected into each choana and the solution was allowed to flow out of the nostril (Henvenuti et al., '92). Twenty-four control pigeons were subjected to the same treatment except they were injected with avian Ringer solution.

On September 30, 1995, 12 zinc sulfate and 12 control pigeons were released from the familiar training site west of home (release site A). Later on the same day, the remaining pigeons plus those that had returned from the familiar training site experimental release were taken to a location ap- proximately 10 km east of the loft and group released. This was done in an attempt to eliminate a possible acquired tendency on the part of the pigeons to fly east as a result of the five training releases from the familiar site. On October 1, 1995, 10 zinc sulfate birds and 10 control birds, which were not released from the familiar site, were released from an unfamiliar release site 51 km southwest of home (release site B). On Octo- ber 2, 1995, a third release took place from an unfamiliar site 54 km northwest of the home loft (release site C). Of the 13 control birds released, 11 participated in the familiar training site release (A) and 2 were involved in an experimental release for the first time. Of the 12 zinc sulfate- treated animals, 10 participated in the familiar training site release (A) and 2 were involved in an experimental release for the first time. After the first three releases, the remaining zinc sulfate-treated birds (N = 4) were each given an ad- ditional 1 ml of zinc sulfate solution in each choana. Further, 3 previous control birds and 5 experimentally native birds were given 2 ml of the zinc sulfate solution in each choana. There- fore, for the last experimental release on October 6, 1995, from a location 34 km north of home (release site D, actually in South Carolina), 12 zinc sulfate-treated birds were released. Twelve control birds that had returned from releases B and C also participated.

Except for release C, which took place under sunny conditions, all releases took place under partly cloudy, humid conditions with winds less than 20 km/h. However, the disk of the sun was always visible when a bird was released. For all experimental releases, pigeons were released sin- gly, alternating between treatment groups, and followed with binoculars (1 0 x 40) until disappear- ing from view. Vanishing bearings and vanishing times were recorded with compass and stopwatch, respectively. Arrival times were recorded by an observer stationed at the loft.

188 V.P. BINGMAN AND S. BENVENUTI

Statistics Statistical analysis of the vanishing bearings

was performed with a Ftayleigh test (Batschelet, ,811. Between group calmparisons of vanishing bearings were performed with a Watson U2-test (Batschelet, '811, homing times [only from the familiar training site release (A) because zinc sulfate-treated birds generally did not return from the unfamiliar sites] with a Mann-Whitney U-test, and homing success with a chi-square test.

RESULTS Vanishing bearings

Except for a narrow styetch of salt marshes that border the Atlantic Ocean, coastal Georgia and South Carolina are characterized by extensive pine/oak forests. As a result, we were unsuccess- ful in finding any location where birds could be followed until vanishing in all directions. The four release sites used generally allowed us to follow the pigeons for a reasonable distance (at least 1 km), but it was difficult to keep birds until vanishing because they would regularly disappear behind distant trees. Most of the vanishing bearings recorded were based on birds lost behind trees. However, because we were able to follow all birds for at least 1 min, the recorded bearings probably provide a reasonable, albeit not totally satisfac- tory, indication of the pigeons' directional prefer- ences (Wallraff, '67).

From the familiar site (A) both groups oriented homeward and no differences in vanishing bearings were recorded (Fig. 1, Table 1). From the three unfamiliar release sites (B-D) the results were quite different. The control birds consistently oriented to the southeast regardless of release site (Fig. 1, Table 1). In contrast, the zinc sulfate- treated birds oriented northwest from two release sites (B, C), where their orientation differed from controls at the P c 0.10 level. From release site D, however, they oriented southeast in a manner indistinguishable from controls.

In summary, the control birds oriented in a manner suggesting a strong tendency to fly southeast [preferred compass direction (PCD); Wallraff, '781 immediately upon release. Zinc sulfate produced anosmia, causing a change in that preference to the northwest, but not under all conditions.

Homing time and homing success From familiar release site A, the median hom-

ing time of the control pigeons was 42 min and the zinc sulfate birds 55 min (Fig. 2). This differ-

ence in homing time approached significance (U = 41.5, P c 0.10 two-tailed). No difference in homing success was recorded (Table 2).

From the unfamiliar release sites the pattern was again very different. Homing times were poor (Fig. 21, and because few zinc sulfate birds returned, no between group statistical comparisons were made. However, there was a striking between group difference in homing success (Table 2, the number of birds returning, excluding those that returned with bird(s) from the other group, compared to the number of birds that did not return). Basically, the majority of control birds returned from all three unfamiliar locations, while few zinc sulfate-treated birds returned. A difference in homing success was found for all three releases (at least P c 0.05). Indeed, for all three releases, 22 of a possible 33 control birds returned, while only 5 of a possible 30 zinc sulfate-treated birds returned.

Taken together, the homing success data stand in strong support of the hypothesis that atmospheric odors are a critical source of navigational information that permits homing pigeons to navigate home from unfamiliar locations in the southeastern United States.

DISCUSSION The general failure of the zinc sulfate-treated

birds to return home from the unfamiliar release sites provides one more piece of evidence to the growing body of research findings supporting the critical role of atmospheric odors in homing pigeon navigation (Papi, '90; Wallrd, '90; Able, '96). However, one must be cautious with any kind of anosmic procedure that may potentially cause side effects unrelated to navigation that would impair homing performance. The performance of the zinc sulfate-treated birds from the familiar release site, however, clearly indicates that the experimental treatment did not lead to any impairment that would preclude flying home. This finding is consistent with other studies (Benvenuti et al., '92; Benvenuti and Gagliardo, in preparation) demon- strating no effect of zinc sulfate treatment on homing ability from familiar sites where presumably non-olfactory information acquired during previous training flights can direct the pigeons home.

Nonetheless, the zinc sulfate-treated birds from the familiar site were slightly slower than the controls. The small absolute difference in homing time (Fig. 2) could be used to argue that the zinc sulfate treatment may have had a modest, non- specific effect on homing. However, a similar dif-


N N 4 7 O

54 km

N

34 km

Fig. 1. Vanishing bearings of control (open dots) and zinc sulfate-treated (closed dots) pigeons from the familiar training location (A) and three unfamiliar release sites (€3-D). Each dot represents the vanishing bearing of one bird. Arrows in each circle represent the mean vectors for each group (open heads, controls; filled heads, zinc sulfate-treated). The length

of an arrow corresponds to the mean vector length, which can be read with the scale in A (solid lines, P < 0.05; dashed lines, P > 0.05; see Table 1). Arrows outside each diagram and associated numbers identify the distance and direction home. North (N) is at the top of each diagram.

ference was not observed in another experiment where pigeons with similar experience were given intranasal administration of zinc sulfate (Benvenuti et al., '92). Therefore, because the difference was so small, a more likely explanation for the difference is that even from familiar sites, in the southeastern United States atmospheric odors may make a navigational contribution, and the mar- ginally slower homing times of the zinc sulfate- treated birds were a consequence of not being able to use that information.

Although the purpose of this experiment was to examine the importance of atmospheric odors

for navigation in the southeastern United States, from a discussion perspective, the normative homing data from the controls are also of interest. It has often been noted that the homing performance of pigeons in Italy is unusually good compared to other locations, and it has been suggested that the coastal environment characteristic of Italy in some way makes for easier "olfactory" navigation (Waldvogel, '87). Therefore, it was expected that the birds in coastal Georgia would show similarly impressive navigation. They did not. Indeed, ex- amining Figure 2 and Table 2 one is struck by the poor homing times and homing success of the


TABLE f. Analysis of vanishing bearings for the four experimental releases'

N a r Group difference

Familiar site A (H = go", D = 34 km) Control 11 (12) ggo***.. 0.85 ZnSO4 11 (12) 1050x*x* 0.81 P > O . l O

Unfamiliar Site B (H = 47", 13 = 5 1 km) Control 7 (10) 128"" 0.56

P<O.lO ZnS04 9 (10) 322""** 0.79

Control 11 (13) 11goh-s 0.40 ZnSOd 11 (12) 326""* 0.60

Control 12 (12) 1130*V"* 0.83 ZnSOd 10 (12) 1270**** 0.78

Unfamiliar Site C (H = 138", D = 54 km)

P < O . l O Unfamiliar Site D (H = 180°, D = 34 km)

P>O.10

'N t number of vanishing bearings recorded (number in parentheses = number of birds released); a = means vector angle (north = 360"); NS = non-significant; *P<O.10; **P.:O.O5; **"P<0.01; ****PcO.OOl as measured by the Rayleigh test); r = mean vectbr length. Between group comparisons were performed with a Watson-Williams U2-test.

control birds. In this context, it is worth noting tha t the environment in Georgia differs from Tuscany, Italy, in two respects. As mentioned ear- lier, the loft of the pigeons was located in a wooded residential area with little exposure to unob- structed winds and was similar to the typical rear- ing conditions of the Wiltschko laboratory in Frankfurt, Germany. In Pisa (Tuscany), the lofts are located in an open field with full exposure to passing winds. Wind exposure plays a critical role in olfactory navigational map learning (e.g., Baldaccini e t al., '74) and limited exposure t o winds may impair development of an olfactory

map (Wiltschko et al., '87b), contributing perhaps to the relatively poor performance of the control birds. Additionally, coastal Georgia is characterized by what appeared to be continuous pine/oak forests for at least 100 km in all directions away from the coast. This homogeneous environment, in contrast to the area around Pisa with its many mountains and varying habitats, may provide in- sufficient "spatial atmospheric heterogeneity" to enable birds to learn a precise olfactory map that would permit efficient navigation home.

Another notable feature of the behavior of the control birds was the consistent southeasterly ori-

FAMILIAR S ITE e,

A r 0 LA 1 2 3 4 I 5 I HR LATER

UNFAMILIAR SITES

-@QmL LOST

0 .wy

Fig. 2. Homing times of control (open dots) and zinc sulfate-treated (filled dots) pigeons from the familiar training location (A) and three unfamiliar release sites (B-I>). Each dot represents the homing time for one bird. Note: Pigeons

that returned with a bird(s) from the other treatment group were excluded. Pigeons that returned with a bird(s) from the same treatment group were treated as independent data points.


TABLE 2. Summary of homing success

Returned' Lost Group difference

Familiar site A Control 11 1 ZnS04 10 2

Control 7 1 ZnS04 1 5

Control 7 6 ZnS04 1 11

Control 8 4 ZnSOl 3 9

P>O.10 Unfamiliar site B

P<O.O2 Unfamiliar site C

P<O.O2 Unfamiliar site D

P<0.05

'Birds that returned together with a bird(s) from the other treatment group were excluded from the analysis. Birds that returned together with a bird from the same treatment group were treated as independent data points. Between group comparions were performed with a chi-square test.

entation. This southeasterly PCD (Wallraff, '78) is interesting because it is perpendicular to and therefore the shortest route to the coast, which is oriented northeast-southwest. In other words, given the location of the loft just a few kilometers from the coast, a navigational strategy of first ori- enting in the direction of the coast and then mov- ing parallel to the coast either northeast or southwest is a reasonable, albeit not the most efficient, navigational strategy. Although the tendency to move in a specific compass direction is not as strong in Pisa, a tendency to move in an approximate southwesterly direction there has been well described (Ioal6, '95). An approximate southwesterly PCD in Pisa is also perpendicular to the approximate northwest-southeast oriented coastline there, suggesting that pigeons living near coasts may generally display initial orientation biased in the direction of the coast.

Of further interest is that the southeasterly orientation of the Georgia birds appeared dependent on the perception of atmospheric odors. The anosmic, zinc sulfate-treated birds orientated northwest- erly from two unfamiliar release sites. However, they did orient southeasterly from release site D. Although highly speculative, we wish to suggest that, in coastal Georgia, southeasterly orientation is triggered by some atmospheric quality associated with the Georgia coast. In the absence of such information, the initial orientation of the birds is biased to the northwest. But why did the zinc sulfate-treated birds orient southeast from release site D? Although we have no explanation for this, it is worth noting that spontaneous 180" reversals in PCD directions have been reported (WallrafY, '91).

CONCLUSIONS The data presented in this paper indicate that

for pigeons in coastal Georgia atmospheric odors represent a critical source of environmental information that enables pigeons to determine their relative location with respect to home. Ad- ditionally, the data suggest that the pigeons in this region show a strong tendency to vanish in a southeasterly direction and that this southeasterly PCD is useful in getting birds to the coast and likely influenced by the perception of atmospheric odors. Taken together, the data support a large body of evidence identifying atmospheric odors as a critical element in homing pigeon navigation.

ACKNOWLEDGMENTS We sincerely thank Burt Oostlander, Wendy

Oostlander, and Dick Schultz whose hospitality and homing pigeon knowledge made the experiment both a success and pleasure to carry out. This work was supported by grants from NIH (1R03 MH52315) to V.P.B., NATO (CRG 950084) to V.P.B. and F. Papi, and the Italian National Research Council to F. Papi.

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Olfaction and the homing ability of pigeons in the Southeastern United States