B HAVIOURAL 6 ROCESSES Behavioural
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Field observations of time-place behaviour in scavenging birds Donald M. Wilkie *, Jason A.R. Carr, Amy Siegenthaler, Matthew Kwok Department
of Psychology,
The Uniaersity ofBritish Accepted
Birgit Lenger, Michael Liu,
Columbia, Vancouver, BC, V6T 124, Canada
I I March
1996
Abstract Encoding the spatial location and the time at which significant biological events occur is thought to be a fundamental way in which one form of memory is organized in animals (Gallistel, 1990, The Organization of Learning. MIT Press, Cambridge, MA). If this is true, one would expect to find evidence of this process in a wide variety of animals and in a wide number of situations. We report field observations of scavenging birds at two outdoor locations at which people tend to congregate and eat food, primarily around midday. Scavenging birds appeared to anticipate this peak in food availability and arrived at these locations before the number of people was at a maximum; time of day, not the absolute number of people, was the best predictor of the number of birds at both sites. At a third location where food is not consumed this relationship was not observed. Taken together these observations support the notion that animals represent the spatial and temporal characteristics of biologically important events and use this knowledge to forage efficiently. Kewords:
Time-place behaviour; Anticipation; Anticipatory flocking; Scavenging birds
1. Introduction Gallistel (1990) hypothesized that time-place learning might be a fundamental way in which one form of memory is organized in the brains of animals. His basic notion is that whenever a biologically significant event occurs, animals encode both the time and the spatial location at which it occurred. Such time-place memory codes can be used by animals to guide their behaviour. For example, if a forager regularly finds food at place 1 at time 1 and at place 2 at time 2, its foraging behavior could be optimized by visiting the appropriate place at the appropriate time. This hypothesis assumes that animals are orientated in time and form spatial cognitive maps, processes clearly demonstrated by vast literatures (e.g., Aschoff, 1989; Gallistel, 1990; Gibbon, 1991).
* Corresponding
author.
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0376-6357/96/$15.00 Copyright PII SO376m6357(96)00026-S
(I-604)
822-4650;
Fax: (I-604)
822-6923;
0 1996 Elsevier Science B.V. All rights reserved
e-mail:
[email protected]
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Time-place learning in avian species has been demonstrated in the laboratory. Biebach et al. (1989) published the first laboratory experiment. In their experiment, garden warblers (Sylvia borin) were tested in a Skinner box consisting of a central living area connected to four compartments or ‘rooms’, each containing a grain dispenser. Each day the birds were tested for 12 h. Each feeder was unlocked (making grain available) for a 3-h period each day. For example, the sequence of food availability for a particular bird might be as follows: Room 1, 0600-0900; Room 2, 0900- 1200; Room 3, 1200- 1500; and Room 4, 1500- 1800 h. The birds had to spend 280 s in the living area during each trial before the doors to the four rooms were opened. At each door opening a record was kept of which room was entered. The birds quickly learned to enter the correct room at the correct time in the 12-h session, suggesting that the birds had learned a time-place association. This was demonstrated convincingly in test sessions in which all four feeders were unlocked for the full 12-h period, making food available for visits to any room at any time. Under these conditions the birds continued to visit the correct room at the appropriate time. This demonstrates that cues from an armed feeder were not responsible for guiding the birds to the correct room. Because the birds were rewarded no matter which room choice they made, the time-of-day signal clearly over rode any tendency to repeat a reinforced choice. The effects of a variety of manipulations of the 1ight:dark cycle under which the subjects lived suggested that their time-place behaviour was controlled by the phase angle of a light-entrained circadian oscillator (Biebach et al., 1991). Our laboratory has also demonstrated time-place learning, using pigeons (Columba Zivia). In one of our first experiments (Wilkie and Willson, 1992) pigeons were tested in a transparent square Plexiglas chamber that sat on a table top in a well-lit test room. Several distal visual cues were available to the pigeons (concrete pillar, door, window, etc.). Each wall of the chamber contained a pecking key (transilluminated by red light during test sessions) and a grain dispenser. Sessions lasted 60 min and were divided into four 1%min periods during which pecking a particular key produced grain rewards on a variable-interval schedule. As in the study with garden warblers, the pigeons learned to visit and peck the correct key at the correct time. Later work (Wilkie et al., 1994) suggested that, in the pigeon, time-place behaviour over a 1 h period is subserved by an interval timer that has stopwatch-like properties. In another experiment (Saksida and Wilkie, 1995) pigeons received two brief (17 min) sessions each day, one in the morning between 0900 and 1000 and a second in the afternoon between 1530 and 1630. In both sessions pigeons were tested in a clear Plexiglas box, again located on a tabletop in a well lit room that provided several distal spatial cues. In both sessions all four keys were illuminated but only one (e.g., Key 2) provided food in the morning session and another (e.g., Key 4) provided food in the afternoon. To gauge the pigeons’ expectations of where food would be available all sessions began with a brief period during which the location of pecks were recorded but no food was delivered. The subjects again provided evidence of time-place learning, as they initially pecked the key that would provide food later in the session and rarely pecked the two keys that never produced food. Control procedures (e.g., using only morning or afternoon sessions) ruled out the possibility that subjects had learned an alternation strategy rather than a time-place association. Other tests suggested that the pigeons, like the garden warblers, were basing their time-place behaviour on the phase of an endogenous circadian oscillator. It thus appears that pigeons use two different timing systems in these types of tasks; an interval timer for short periods and a phase timer for longer periods (cf., Wilkie, 1995). Three field studies have confirmed that birds appear to be able to adjust their behaviour to match
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temporal and spatial patterns of food availability thereby confirming the ecological validity of these laboratory studies. Kamil (1978) studied a nectar-feeding bird, the amakihi ( LLUO~Ssirens). He found that once these birds deplete a flower cluster of its nectar they tend to wait for about an hour before revisiting; thus, the primary pattern of visitation was temporal one. Avoidance of depleted clusters was not due to physical differences between visited and unvisited flowers or any obvious spatial pattern of revisitation. Kamil (1978) also remarked on the promise of field studies. He suggested that field studies may reveal the role of learned behaviours in an animal’s biological success. This may be especially evident in the study of foraging behaviour as an animal may be able to greatly improve its foraging efficiency by learning about the spatial and temporal distributions of its food and modifying its behaviour accordingly (see Aschoff, 1989 and Daan and Aschoff, 1982 for similar discussions). In a second field study Rijnsdorp et al. (1981) studied the daily activity patterns of kestrels (Fulco tinnunculus) and their main prey, the common vole (Microtus arualis). Voles live in underground burrows and during daylight they tend to forage on the surface approximately every 2 h. Rijnsdorp et al. (1981) found that kestrel flight-hunting coincided with these peaks in vole surface activity. It appears that the kestrels restricted their flight-hunting to the times-of-day in which a high yield would be expected. Additionally, many kestrels exhibited idiosyncratic daily patterns of activity (e.g., hunt in one location in the morning and in another in the afternoon). However, these habits were modified by daily experience; observations and field experiments revealed that if a bird was successful hunting in an area it tended to return to the same area 24 h later. The authors estimated that by restricting her flight-hunting to times of high potential yield, one kestrel saved lo-22% in her total flight-hunting time. A third study (Daan and Koene, 198 l), suggests that wading oystercatchers ( Huemutopus ostrulegus) anticipate mollusc availability on tidal mudflats. Mollusc close their valves shortly after water run off to prevent desiccation and predation. This makes the timing of foraging bouts by oystercatchers critical. Daan and Koene studied a flock of oystercatchers which formed roosting gatherings in the inland fields of an island. These inland fields were separated from the water by a high dike which provided a visual barrier. Every 5 min during daylight hours field observers recorded the number of birds in the roost and on the mudflats. Daan and Koene found that at approximately the time that the musselbeds became exposed by the retreating tide the birds flew from the island, over the dikes and to the musselbed. When the tide was early, the birds were late and vice versa. It therefore appears that the birds based their departures on an endogenous timing mechanism and not on stimuli directly associated with the state of the mudflats. In the present report additional field evidence of time-place behaviour in birds is presented. Amakihis, kestrels and oystercatchers are specialized foragers as they eat a restricted range of food whose availability clearly varies on a temporal basis. In the present paper we present data on generalist foragers: scavengers, such as pigeons, gulls (Lurus sp.), starlings fSturnu.s rdguris~ and crows (Corcus caurinus) at three busy outdoor locations. Evidence of time-place behavior in generalist foragers would be important as it would suggest that this ability is not an adaptive specialization that has evolved only in specialist foragers with a restricted diet but rather is a capability demonstrated by a wide range of animals. There are two possible mechanisms which could account for a regular pattern of arrivals and departures of scavenging birds at the locations studied. One possibility is that birds’ behaviour is based on the status of an endogenous timing mechanism. In the present context, scavenging birds may visit each location on the basis of the phase angle of an endogenous oscillator or once some interval
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timer attained some value. A second possibility is that birds’ behaviour is controlled by external, periodic, environmental events. As the presence of people is directly related to food availability at the test sites, the birds may visit these sites when large numbers of people are present. This latter form of temporal regulation of behaviour does not require any form of endogenous timing system. We attempted to distinguish between these two alternatives with a regression analysis in which the number of people present and the time-of-day were used to predict the number of birds at the field locations. We hypothesized that if the birds had learned a time-place relationship (1) they would arrive at a site around the same time every day in anticipation of the people and food; and (2) that time would be a better predictor of the numbers of birds at the sites than would be the exact numbers of people on any given day.
2. Materials and methods 2.1. Site I One part of the study was carried out at Granville Island in Vancouver (British Columbia, Canada). Granville Island is located on False Creek between the Burrard and Granville Street bridges. It was once a marshy tidal flat, but it is now a successful waterfront redevelopment project occupying about 35 acres of land. Granville Island attracts about 8 million visitors annually with its many theatres, shops and restaurants. One of the most popular venues is the Public Market which houses 47 merchants including bakeries, butchers, fresh produce shops, confectioneries and fast-food outlets. Thus, the Public Market is a place where many people go to purchase and consume food. Just outside of the Market is an outdoor seating area, a photograph of which is shown in Fig. 1. This area can seat about 150 people at tables and benches. This was the area in which observations were made. The total observation area measured about 345 m*.
Fig. I. Photograph market.
of the Granville Island Site. The depicted
area is a waterside
deck immediately
adjacent to a public
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A variety of birds are found in this area. The most abundant species are pigeons, seagulls, starlings and crows. Some of these birds appear to nest under the two bridges mentioned above. In the daytime, many of them are found either roosting on the nearby rooftops and awnings or foraging on the ground for food. Many of the visitors to the market bring seeds specifically to feed the birds but the birds have also been observed to consume a variety of foods dropped by people eating there. Food left or brought by people seems to be the main food source for these birds. A record was made of the number of birds and people in the square from October 4, 1994 to March 24, 1995, using hand tally counters. A total of 43 trips were made to the Market during this time period, producing a total of 240 counts. An effort was made to cover the majority of the daylight hours. During this period of time, sunrise varied from 6:17 a.m. in October to 6:06 a.m. in March and sunset varied from 5:45 p.m. in October to 6:32 p.m. in March (all times given are Standard Time). Counts were taken at 20-min intervals; at each time, the total number of birds, the total number of people and an estimate of the number of feedings were noted. Both birds on the ground and the rooftops and awnings were counted. As well, both people sitting in the area and walking through the area were counted. Observations were always made from exactly the same location. 2.2. Site 2 Nearly identical procedures were used at the second site, a 245 square meter concrete plaza adjacent to UBC’s Student Union Building (S.U.B.). This building contains a video arcade, computer facilities and several commercial operations such as travel agencies. It also contains many restaurants, with combined seating for over 1000 people. The plaza (see Fig. 2) was near one of the two main entrances to the building and contains many benches that students use as a meeting area. The main difference in procedure from that employed at Site 1 was that only birds on the ground were counted (this turned out to be an important variation). Species of birds frequenting this area were similar to
Fig. 2. Photograph of the Student Union Building Site. The depicted area is a plaza immediately entrances to this building that houses many establishments providing food and drink.
adjacent to one of the main
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Fig. 3. Photograph of the control, Parkade site. The depicted area are grassy fields, graveled parking areas, roadways and sidewalks adjacent to a large car parking structure.
those at Site 1, with the addition of sparrows (Melospiza occasions, between October 4, 1984 and March 24, 1995. 2.3. Control
melodia).
Data were collected
at 476
site
Control data were also taken from an area of the UBC campus in which people do not regularly go to consume food. Data were taken on a total of 16 different days between March 7, 1995 and February 8, 1995. Observations were made from a window on the third floor of the UBC Psychology building which overlooks a campus road, and is situated across the street from a six storey parkade and open parking lot (Fig. 3). The total area within view measured about 55 000 ml. As with the other sites, the number of birds, number of people and number of feedings were counted at 20-min intervals and an attempt was made to cover the majority of daylight hours. 2.4. Obsercers Two observers recorded data at all three sites. Some observations were made simultaneously by the observers to permit an estimation of inter-observer reliability. At the Parkade site the Pearson I^ was 0.89 for number of people and 0.95 for the number of birds. The corresponding values at the other two sites were: S.U.B 0.998, 0.992, Granville Island 0.942, 0.998. 2.5. Data analysis Observed numbers of people and birds were aggregated over observers and days to get a single average number of birds and people at each of the temporal intervals. These averaged counts were used, along with the temporal data, in correlation and regression analyses. Because the average counts of birds and people were not linear with respect to time at the two experimental sites, data were
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Granvlile kiana 250 I(4
Tme
of Day
S U.B
3o/(b) I
__
brds
----kvb 3
3o(c) 20 -
4 10 -
Fig. 4. Numbers of birds and people at various times over the course of days at (a> Granville Island, (b) Student Union Building and Cc) the control Parkade site. A box is drawn around the peak in the number of birds and people in (a) and (b) to illustrate the main finding that birds seem to anticipate the peak in human food dispersal activities.
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analyzed separately for mornings (when the counts of birds and people increased) (when the counts of birds and people decreased).
and afternoons
3. Results 3.1. Incidences of eating behaviour At all three sites a record was kept of the number of birds that were observed to eat food. At the Parkade site no instances of eating were observed. Eating was frequently observed at Granville Island: averaged across all of the observation periods, 17.3 birds were seen to eat at each time period. The corresponding number for the S.U.B. site was 0.24 (i.e., one instance in every four observations at each time-of-day). The different criteria for counting birds at the latter two sites probably explains the difference in the number of observed incidents of eating. At the Granville Island site all birds were counted while at the S.U.B. site only birds on the ground were counted. A bird that found food and flew off to eat it elsewhere was not counted at the S.U.B. but was counted at Granville Island. In any case, these data establish that birds eat scavenged food at the test sites but not at the control site. 3.2. Temporal distribution
of birds and people
The distributions of the average number of birds and people over the course of a day at the three sites are shown in Fig. 4. At the control (Parkade) site most birds were seen in the earliest part of the day. The number of people peaked somewhat later and did not change in any systematic manner over the course of the remaining part of the day. The pattern of bird and people counts was much different at the two test sites. At the S.U.B. and at Granville Island the number of people increased throughout
Table I Pearson correlation
coefficients
CT)
Granville Island morning people time
birds 0.674 0.886
people 0.908
Student Union Building morning people time
birds 0.676 0.907
people
birds 0.022 - 0.620
people
0.817
Parkade all day people time
-0.130
afternoon birds 0.76 I - 0.907
afternoon birds 0.307 - 0.843
people - 0.780
people -0.617
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the morning, peaked at around midday, and declined in the afternoon. There are some differences in the shapes of these distributions; most notably the distribution obtained at the S.U.B has fuller tails and a sharper peak than the same distribution for Granville Island. At both test sites the number of birds, like the number of people, increased during the morning, peaked around midday, and declined during the afternoon. However, the peaks of the bird distributions lie earlier in the day than the people distributions; the number of birds at both the S.U.B. and Granville Island was nearly at a maximum one to two hours before the number of people tended to peak. While the number of birds at the S.U.B. tended to peak at midday, there was a decrease in the number of birds at the S.U.B. just as the number
Granville Island pm
Granvllle Island am
Stw 1
SUB
step 1
Time
am
Step 2 - TIM
T,me
Step 2 - Tlnw d bxde
SU.B pm
8 Peas
Fig. 5. Results of the stepwise multiple regression in which birds was the dependent variable, and time of day and numbers of people were predictors. The data were analyzed separately for mornings and afternoons. In all cases time-of-day was included in the regression in the first step and was associated with rather large values of r-squared. In two of the four cases, the mean number of people contributed additional, independent, predictive power and therefore was included in the second step of the stepwise regression.
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of people reached a maximum. Because only birds on the ground were counted at this site, this decrease may reflect competition between people and birds for space on the ground. 3.3. Statistical analyses Because the distributions of birds and people over a day at the two test sites was non-linear, data for morning and afternoon were analyzed separately. Table 1 shows the Pearson correlation coefficients between the number of birds, number of people and time of day. For the Parkade site there was a modest but significant ( P < 0.05) negative correlation between birds and time, reflecting the fact that the number of birds observed at this site decreased over the day. The correlations amongst the other variables were close to zero and did not approach statistical significance. At the two test sites there was a significant ( P < 0.0 1) and moderately strong positive relationship between the number of birds and number of people. There was a significant (P < 0.01) and even stronger correlation between the number of birds and time of day. Stepwise multiple regression was also performed on the three variables for both test sites, with the data again being divided into morning and afternoon observations. The number of birds was the dependent variable and the mean number of people present and the time-of-day served as predictor variables. The results of this analysis are shown in Fig. 5, which shows the value of the r2 (times 100%) for each step of the regression. The absence of a bar indicates that no factor was added in the second step. The time-of-day was included first in the regression equation in all cases, with quite large associated r’ values. This indicates that in all cases time-of-day was a better predictor of the number of birds than was the mean number of people at the field sites. In two of the four cases, the mean number of people was added in the second step. This indicates that the mean number of people at the test sites provides an additional, independent, improvement in predicting number of the regression equation. The additional predictive gain in including people was quite modest.
4. Discussion Clear evidence of time-place behaviour was found. At both sites birds appeared to anticipate reoccurring peaks in human activity, part of which was deliberate or accidental food distribution. The apparent anticipation of peaks of human activity at both test sites is an important observation suggesting that the scavenging birds were using time of day as a stimulus rather than using the number of people as an environmental stimulus predictive of food. This finding extends the findings of Daan and Koene (1981) in their study of foraging oystercatchers. They found that these birds’ foraging flights from their inland roost to the musselbeds were controlled by the expected time of low tide and not simply by the visual sighting of the mussels; the birds appeared before the musselbeds were usable on days when the ebb tide was late and sat in their roosts until the appropriate time on days when the tide was early. The overall pattern of bird activity at both sites was similar despite differences in how birds were counted at the two sites and despite considerable differences in the environment at the two sites - a waterside public market and a meeting location in the centre of a large university campus. Although we did not systematically record the species of birds at either site, casual observation revealed that
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pigeons, gulls, crows, starlings and sparrows were the most common. The observation of time-place behaviour in these scavenging birds is important in demonstrating the generality of this behaviour across a range of species. Although time-place behaviour has been observed in laboratory pigeons (e.g., Saksida and Wilkie, 19951 the present observations constitute the first field confirmation of this behaviour in non-specialist foragers. This finding is important in that it gives additional credence to Gallistel’s (1990) thesis that time-place memory coding is a fundamental mechanism in the organization of one type of animal memory. Although we have no direct evidence that the time-place behaviour observed in the scavenging birds was in fact learned, the fact the human food-activity has occurred at the two test sites for only approximately 20 years argues against the notion that time-place behaviours are inherited behaviour patterns that have evolved in environments in which resources vary with temporal and spatial regularities. Also the fact that laboratory animals learn arbitrary, artificial time-place associations suggests that time-place learning might be a very general and flexible process - one capable of optimizing behaviour in the face of changing patterns of temporal and spatial regularities in the environment. There is other work, however, which suggests that an animal’s proficiency at time-place learning may be predictively related to its foraging ecology. Falk et al. (1992) examined insectivorous ( Ploceus bicolor) and granivorous (Euplectes hordeaceus) weaver species using the same experimental chambers and procedure as Biebach et al. (1989) that we described earlier. These authors reasoned that as the granivorous species eats mainly seeds. which have no regular daily pattern of availability, they might have a lower tendency to acquire time-place behaviour when compared to insectivorous weavers. The granivorous birds acquired the task faster than the insectivorous birds but both species learnt to visit each location at the correct point in a daily session. Both types of birds appeared to use an endogenous timing mechanism to track the location of food as their pattern of room visits was maintained by both species when all compartments provided food for an entire test day. However, a photoperiod phase advance produced an immediate and dramatic deterioration of the granivorous birds’ time-place behaviour (they appeared to enter rooms at random) whereas the insectivorous birds maintained the order and duration of their room visits but they entered each room approximately 2 h early on the test day. Falk et al. concluded that this, and other related differences between the behaviour of these species in this task, reflect a predisposition towards this form of learning in the insectivorous species. Our data are not inconsistent with their conclusions as both the insectivorous and granivorous species displayed time-place learning. Instead, it appears that a great variety of organisms are capable of time-place learning, but there may be quantitative differences in the robustness of this form of learning in animals which may be predictively related to their foraging ecology. The laboratory work reviewed above suggests that birds use phase timers when required to anticipate environmental regularities in food availability with a period of several hours. It therefore seems unlikely that the birds observed in the present study used a stopwatch-like internal clock to control their arrivals and departures from our field sites (see Wilkie, 1995). The most likely candidate is phase timing subserved by one, or many endogenous circadian oscillators (Gallistel, 19901. A wide variety of physiological and behavioural circadian rhythms are driven by photoperiod (in mammals, see Mistleberger and Rusak (19941; in birds, see Binkley (199011, or meal-entrained endogenous oscillators (in mammals, see Mistleberger (1994); in birds, see Phillips et al. (1993)). Thus the birds may have learned to visit the food patches when some endogenous oscillator, or group of oscillators,
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attain a certain phase angle. whether each individual bird some others might simply behavioural strategies while (e.g., Giraldeau and Lefebvre,
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One question left unanswered by the present results is the question of made use of a timer. Perhaps some birds time the arrival at a site but ‘join the crowd’. Evidence that individual birds may use different foraging has been reported in the literature on observational learning 1987).
Acknowledgements This research was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). J.A.R.C. was supported by a Sir Dudley Spurling Scholarship.
References Aschoff, J., 1989. Temporal orientation: Circadian clocks in animals and humans. Anim. Behav., 37: 881-896. Biebach, H., Gordijn, M. and Krebs, J., 1989. Time-place learning by garden warblers, Sv/t)ia h-in. Anim. Behav., 37: 353-360. Biebach, H., Falk, H. and Krebs, J., 1991. The effect of constant light and phase shifts on a learned time-place association in garden warblers (Sylvia borin): Hourglass or circadian clock? J. Biol. Rhythms, 6: 353-365. Binkley, S., 1990. The Clockwork Sparrow: Time, Clocks, and Calendars in Biological Organisms. Prentice-Hall, Englewood Cliffs, NJ. Daan, S. and Aschoff, J., 1982. Circadian contributions to survival. In: J. Aschoff, S. Daan and G.A. Groos (Editors), Vertebrate Circadian Systems: Structure and Physiology. Springer-Verlag, New York, NY. Daan, S. and Koene, P., 1981. On the timing of foraging flights by oystercatchers, Huematopus ostrultyys, on tidal mudflats. Neth. J. Sea Res., 15: l-22. Falk, H., Biebach, H. and Krebs, J.R., 1992. Learning a time-place pattern of food availability: a comparison between an insectivorous and a granivorous weaver species ( Ploceus hicolor and Euplrctes hordeaceus). Behav. Ecol. Sociobiol., 31: 9-15. Gallistel, CR., 1990. The Organization of Learning. MIT Press, Cambridge, MA. Gibbon, J., 1991. Origins of scalar timing theory. Learn. Motiv., 22: 3-38. Giraldeau, L. and Lefebvre, L., 1987. Scrounging prevents cultural transmission of food-finding behaviour in pigeons. Anim. Behav., 35: 387-394. Kamil, A.C., 1978. Systematic foraging by a nectar-feeding bird, the amakihi (Loxops cYrerz.s). J. Comp. Physiol. Psychol., 92: 388-396. Mistleberger, R.E., 1994. Circadian food-anticipatory activity: Forma1 models and physiological mechanism. Neurosci. Biobehav. Rev., 18: 171-195. Mistleberger, R.E. and Rusak, B., 1994. Circadian rhythms in mammals: Formal properties and environmental influences. In: M.H. Kryger, T. Roth and W.C. Dement (Editors), Principles and Practice of Sleep Medicine, 2nd Edition, W.B. Saunders, Philadelphia, PA, pp. 277-285. Phillips, D.L., Rautenberg, W., Rashotte, M.E. and Stephan, F.K., 1993. Evidence for a separate food entrained oscillator in the pigeon. Physiol. Behav., 53: I 105-l I 13. Rijnsdorp, A., Daan, S. and Dijkstra, C., 1981. Hunting in the kestrel, F&a tinnunculus, and the adaptive significance of daily habits. Oceologia, 50: 391-406. Saksida, L.M. and Wilkie, D.M., 1995. Time-of-day discrimination by pigeons, Colunzba licicc. Anim. Learn. Behav., 22: 143-154. Wilkie, D.M., 1995. Time-place learning. New Directions in Psychol. Sci., 4: 85-89. Wilkie, D.M. and Willson, R.J., 1992. Time-place learning by pigeons, Columba liriu. J. Exp. Anal. Behav.. 57: 145-158. Wilkie, D.M., Saksida, L.M., Samson, P. and Lee. A., 1994. Properties of time-place learning in pigeons, Columba li~ia. Behav. Process., 31: 39-56.
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(I 996) 77-88
Field observations of time-place behaviour in scavenging birds Donald M. Wilkie *, Jason A.R. Carr, Amy Siegenthaler, Matthew Kwok Department
of Psychology,
The Uniaersity ofBritish Accepted
Birgit Lenger, Michael Liu,
Columbia, Vancouver, BC, V6T 124, Canada
I I March
1996
Abstract Encoding the spatial location and the time at which significant biological events occur is thought to be a fundamental way in which one form of memory is organized in animals (Gallistel, 1990, The Organization of Learning. MIT Press, Cambridge, MA). If this is true, one would expect to find evidence of this process in a wide variety of animals and in a wide number of situations. We report field observations of scavenging birds at two outdoor locations at which people tend to congregate and eat food, primarily around midday. Scavenging birds appeared to anticipate this peak in food availability and arrived at these locations before the number of people was at a maximum; time of day, not the absolute number of people, was the best predictor of the number of birds at both sites. At a third location where food is not consumed this relationship was not observed. Taken together these observations support the notion that animals represent the spatial and temporal characteristics of biologically important events and use this knowledge to forage efficiently. Kewords:
Time-place behaviour; Anticipation; Anticipatory flocking; Scavenging birds
1. Introduction Gallistel (1990) hypothesized that time-place learning might be a fundamental way in which one form of memory is organized in the brains of animals. His basic notion is that whenever a biologically significant event occurs, animals encode both the time and the spatial location at which it occurred. Such time-place memory codes can be used by animals to guide their behaviour. For example, if a forager regularly finds food at place 1 at time 1 and at place 2 at time 2, its foraging behavior could be optimized by visiting the appropriate place at the appropriate time. This hypothesis assumes that animals are orientated in time and form spatial cognitive maps, processes clearly demonstrated by vast literatures (e.g., Aschoff, 1989; Gallistel, 1990; Gibbon, 1991).
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Time-place learning in avian species has been demonstrated in the laboratory. Biebach et al. (1989) published the first laboratory experiment. In their experiment, garden warblers (Sylvia borin) were tested in a Skinner box consisting of a central living area connected to four compartments or ‘rooms’, each containing a grain dispenser. Each day the birds were tested for 12 h. Each feeder was unlocked (making grain available) for a 3-h period each day. For example, the sequence of food availability for a particular bird might be as follows: Room 1, 0600-0900; Room 2, 0900- 1200; Room 3, 1200- 1500; and Room 4, 1500- 1800 h. The birds had to spend 280 s in the living area during each trial before the doors to the four rooms were opened. At each door opening a record was kept of which room was entered. The birds quickly learned to enter the correct room at the correct time in the 12-h session, suggesting that the birds had learned a time-place association. This was demonstrated convincingly in test sessions in which all four feeders were unlocked for the full 12-h period, making food available for visits to any room at any time. Under these conditions the birds continued to visit the correct room at the appropriate time. This demonstrates that cues from an armed feeder were not responsible for guiding the birds to the correct room. Because the birds were rewarded no matter which room choice they made, the time-of-day signal clearly over rode any tendency to repeat a reinforced choice. The effects of a variety of manipulations of the 1ight:dark cycle under which the subjects lived suggested that their time-place behaviour was controlled by the phase angle of a light-entrained circadian oscillator (Biebach et al., 1991). Our laboratory has also demonstrated time-place learning, using pigeons (Columba Zivia). In one of our first experiments (Wilkie and Willson, 1992) pigeons were tested in a transparent square Plexiglas chamber that sat on a table top in a well-lit test room. Several distal visual cues were available to the pigeons (concrete pillar, door, window, etc.). Each wall of the chamber contained a pecking key (transilluminated by red light during test sessions) and a grain dispenser. Sessions lasted 60 min and were divided into four 1%min periods during which pecking a particular key produced grain rewards on a variable-interval schedule. As in the study with garden warblers, the pigeons learned to visit and peck the correct key at the correct time. Later work (Wilkie et al., 1994) suggested that, in the pigeon, time-place behaviour over a 1 h period is subserved by an interval timer that has stopwatch-like properties. In another experiment (Saksida and Wilkie, 1995) pigeons received two brief (17 min) sessions each day, one in the morning between 0900 and 1000 and a second in the afternoon between 1530 and 1630. In both sessions pigeons were tested in a clear Plexiglas box, again located on a tabletop in a well lit room that provided several distal spatial cues. In both sessions all four keys were illuminated but only one (e.g., Key 2) provided food in the morning session and another (e.g., Key 4) provided food in the afternoon. To gauge the pigeons’ expectations of where food would be available all sessions began with a brief period during which the location of pecks were recorded but no food was delivered. The subjects again provided evidence of time-place learning, as they initially pecked the key that would provide food later in the session and rarely pecked the two keys that never produced food. Control procedures (e.g., using only morning or afternoon sessions) ruled out the possibility that subjects had learned an alternation strategy rather than a time-place association. Other tests suggested that the pigeons, like the garden warblers, were basing their time-place behaviour on the phase of an endogenous circadian oscillator. It thus appears that pigeons use two different timing systems in these types of tasks; an interval timer for short periods and a phase timer for longer periods (cf., Wilkie, 1995). Three field studies have confirmed that birds appear to be able to adjust their behaviour to match
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temporal and spatial patterns of food availability thereby confirming the ecological validity of these laboratory studies. Kamil (1978) studied a nectar-feeding bird, the amakihi ( LLUO~Ssirens). He found that once these birds deplete a flower cluster of its nectar they tend to wait for about an hour before revisiting; thus, the primary pattern of visitation was temporal one. Avoidance of depleted clusters was not due to physical differences between visited and unvisited flowers or any obvious spatial pattern of revisitation. Kamil (1978) also remarked on the promise of field studies. He suggested that field studies may reveal the role of learned behaviours in an animal’s biological success. This may be especially evident in the study of foraging behaviour as an animal may be able to greatly improve its foraging efficiency by learning about the spatial and temporal distributions of its food and modifying its behaviour accordingly (see Aschoff, 1989 and Daan and Aschoff, 1982 for similar discussions). In a second field study Rijnsdorp et al. (1981) studied the daily activity patterns of kestrels (Fulco tinnunculus) and their main prey, the common vole (Microtus arualis). Voles live in underground burrows and during daylight they tend to forage on the surface approximately every 2 h. Rijnsdorp et al. (1981) found that kestrel flight-hunting coincided with these peaks in vole surface activity. It appears that the kestrels restricted their flight-hunting to the times-of-day in which a high yield would be expected. Additionally, many kestrels exhibited idiosyncratic daily patterns of activity (e.g., hunt in one location in the morning and in another in the afternoon). However, these habits were modified by daily experience; observations and field experiments revealed that if a bird was successful hunting in an area it tended to return to the same area 24 h later. The authors estimated that by restricting her flight-hunting to times of high potential yield, one kestrel saved lo-22% in her total flight-hunting time. A third study (Daan and Koene, 198 l), suggests that wading oystercatchers ( Huemutopus ostrulegus) anticipate mollusc availability on tidal mudflats. Mollusc close their valves shortly after water run off to prevent desiccation and predation. This makes the timing of foraging bouts by oystercatchers critical. Daan and Koene studied a flock of oystercatchers which formed roosting gatherings in the inland fields of an island. These inland fields were separated from the water by a high dike which provided a visual barrier. Every 5 min during daylight hours field observers recorded the number of birds in the roost and on the mudflats. Daan and Koene found that at approximately the time that the musselbeds became exposed by the retreating tide the birds flew from the island, over the dikes and to the musselbed. When the tide was early, the birds were late and vice versa. It therefore appears that the birds based their departures on an endogenous timing mechanism and not on stimuli directly associated with the state of the mudflats. In the present report additional field evidence of time-place behaviour in birds is presented. Amakihis, kestrels and oystercatchers are specialized foragers as they eat a restricted range of food whose availability clearly varies on a temporal basis. In the present paper we present data on generalist foragers: scavengers, such as pigeons, gulls (Lurus sp.), starlings fSturnu.s rdguris~ and crows (Corcus caurinus) at three busy outdoor locations. Evidence of time-place behavior in generalist foragers would be important as it would suggest that this ability is not an adaptive specialization that has evolved only in specialist foragers with a restricted diet but rather is a capability demonstrated by a wide range of animals. There are two possible mechanisms which could account for a regular pattern of arrivals and departures of scavenging birds at the locations studied. One possibility is that birds’ behaviour is based on the status of an endogenous timing mechanism. In the present context, scavenging birds may visit each location on the basis of the phase angle of an endogenous oscillator or once some interval
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timer attained some value. A second possibility is that birds’ behaviour is controlled by external, periodic, environmental events. As the presence of people is directly related to food availability at the test sites, the birds may visit these sites when large numbers of people are present. This latter form of temporal regulation of behaviour does not require any form of endogenous timing system. We attempted to distinguish between these two alternatives with a regression analysis in which the number of people present and the time-of-day were used to predict the number of birds at the field locations. We hypothesized that if the birds had learned a time-place relationship (1) they would arrive at a site around the same time every day in anticipation of the people and food; and (2) that time would be a better predictor of the numbers of birds at the sites than would be the exact numbers of people on any given day.
2. Materials and methods 2.1. Site I One part of the study was carried out at Granville Island in Vancouver (British Columbia, Canada). Granville Island is located on False Creek between the Burrard and Granville Street bridges. It was once a marshy tidal flat, but it is now a successful waterfront redevelopment project occupying about 35 acres of land. Granville Island attracts about 8 million visitors annually with its many theatres, shops and restaurants. One of the most popular venues is the Public Market which houses 47 merchants including bakeries, butchers, fresh produce shops, confectioneries and fast-food outlets. Thus, the Public Market is a place where many people go to purchase and consume food. Just outside of the Market is an outdoor seating area, a photograph of which is shown in Fig. 1. This area can seat about 150 people at tables and benches. This was the area in which observations were made. The total observation area measured about 345 m*.
Fig. I. Photograph market.
of the Granville Island Site. The depicted
area is a waterside
deck immediately
adjacent to a public
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A variety of birds are found in this area. The most abundant species are pigeons, seagulls, starlings and crows. Some of these birds appear to nest under the two bridges mentioned above. In the daytime, many of them are found either roosting on the nearby rooftops and awnings or foraging on the ground for food. Many of the visitors to the market bring seeds specifically to feed the birds but the birds have also been observed to consume a variety of foods dropped by people eating there. Food left or brought by people seems to be the main food source for these birds. A record was made of the number of birds and people in the square from October 4, 1994 to March 24, 1995, using hand tally counters. A total of 43 trips were made to the Market during this time period, producing a total of 240 counts. An effort was made to cover the majority of the daylight hours. During this period of time, sunrise varied from 6:17 a.m. in October to 6:06 a.m. in March and sunset varied from 5:45 p.m. in October to 6:32 p.m. in March (all times given are Standard Time). Counts were taken at 20-min intervals; at each time, the total number of birds, the total number of people and an estimate of the number of feedings were noted. Both birds on the ground and the rooftops and awnings were counted. As well, both people sitting in the area and walking through the area were counted. Observations were always made from exactly the same location. 2.2. Site 2 Nearly identical procedures were used at the second site, a 245 square meter concrete plaza adjacent to UBC’s Student Union Building (S.U.B.). This building contains a video arcade, computer facilities and several commercial operations such as travel agencies. It also contains many restaurants, with combined seating for over 1000 people. The plaza (see Fig. 2) was near one of the two main entrances to the building and contains many benches that students use as a meeting area. The main difference in procedure from that employed at Site 1 was that only birds on the ground were counted (this turned out to be an important variation). Species of birds frequenting this area were similar to
Fig. 2. Photograph of the Student Union Building Site. The depicted area is a plaza immediately entrances to this building that houses many establishments providing food and drink.
adjacent to one of the main
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Fig. 3. Photograph of the control, Parkade site. The depicted area are grassy fields, graveled parking areas, roadways and sidewalks adjacent to a large car parking structure.
those at Site 1, with the addition of sparrows (Melospiza occasions, between October 4, 1984 and March 24, 1995. 2.3. Control
melodia).
Data were collected
at 476
site
Control data were also taken from an area of the UBC campus in which people do not regularly go to consume food. Data were taken on a total of 16 different days between March 7, 1995 and February 8, 1995. Observations were made from a window on the third floor of the UBC Psychology building which overlooks a campus road, and is situated across the street from a six storey parkade and open parking lot (Fig. 3). The total area within view measured about 55 000 ml. As with the other sites, the number of birds, number of people and number of feedings were counted at 20-min intervals and an attempt was made to cover the majority of daylight hours. 2.4. Obsercers Two observers recorded data at all three sites. Some observations were made simultaneously by the observers to permit an estimation of inter-observer reliability. At the Parkade site the Pearson I^ was 0.89 for number of people and 0.95 for the number of birds. The corresponding values at the other two sites were: S.U.B 0.998, 0.992, Granville Island 0.942, 0.998. 2.5. Data analysis Observed numbers of people and birds were aggregated over observers and days to get a single average number of birds and people at each of the temporal intervals. These averaged counts were used, along with the temporal data, in correlation and regression analyses. Because the average counts of birds and people were not linear with respect to time at the two experimental sites, data were
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Granvlile kiana 250 I(4
Tme
of Day
S U.B
3o/(b) I
__
brds
----kvb 3
3o(c) 20 -
4 10 -
Fig. 4. Numbers of birds and people at various times over the course of days at (a> Granville Island, (b) Student Union Building and Cc) the control Parkade site. A box is drawn around the peak in the number of birds and people in (a) and (b) to illustrate the main finding that birds seem to anticipate the peak in human food dispersal activities.
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analyzed separately for mornings (when the counts of birds and people increased) (when the counts of birds and people decreased).
and afternoons
3. Results 3.1. Incidences of eating behaviour At all three sites a record was kept of the number of birds that were observed to eat food. At the Parkade site no instances of eating were observed. Eating was frequently observed at Granville Island: averaged across all of the observation periods, 17.3 birds were seen to eat at each time period. The corresponding number for the S.U.B. site was 0.24 (i.e., one instance in every four observations at each time-of-day). The different criteria for counting birds at the latter two sites probably explains the difference in the number of observed incidents of eating. At the Granville Island site all birds were counted while at the S.U.B. site only birds on the ground were counted. A bird that found food and flew off to eat it elsewhere was not counted at the S.U.B. but was counted at Granville Island. In any case, these data establish that birds eat scavenged food at the test sites but not at the control site. 3.2. Temporal distribution
of birds and people
The distributions of the average number of birds and people over the course of a day at the three sites are shown in Fig. 4. At the control (Parkade) site most birds were seen in the earliest part of the day. The number of people peaked somewhat later and did not change in any systematic manner over the course of the remaining part of the day. The pattern of bird and people counts was much different at the two test sites. At the S.U.B. and at Granville Island the number of people increased throughout
Table I Pearson correlation
coefficients
CT)
Granville Island morning people time
birds 0.674 0.886
people 0.908
Student Union Building morning people time
birds 0.676 0.907
people
birds 0.022 - 0.620
people
0.817
Parkade all day people time
-0.130
afternoon birds 0.76 I - 0.907
afternoon birds 0.307 - 0.843
people - 0.780
people -0.617
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the morning, peaked at around midday, and declined in the afternoon. There are some differences in the shapes of these distributions; most notably the distribution obtained at the S.U.B has fuller tails and a sharper peak than the same distribution for Granville Island. At both test sites the number of birds, like the number of people, increased during the morning, peaked around midday, and declined during the afternoon. However, the peaks of the bird distributions lie earlier in the day than the people distributions; the number of birds at both the S.U.B. and Granville Island was nearly at a maximum one to two hours before the number of people tended to peak. While the number of birds at the S.U.B. tended to peak at midday, there was a decrease in the number of birds at the S.U.B. just as the number
Granville Island pm
Granvllle Island am
Stw 1
SUB
step 1
Time
am
Step 2 - TIM
T,me
Step 2 - Tlnw d bxde
SU.B pm
8 Peas
Fig. 5. Results of the stepwise multiple regression in which birds was the dependent variable, and time of day and numbers of people were predictors. The data were analyzed separately for mornings and afternoons. In all cases time-of-day was included in the regression in the first step and was associated with rather large values of r-squared. In two of the four cases, the mean number of people contributed additional, independent, predictive power and therefore was included in the second step of the stepwise regression.
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of people reached a maximum. Because only birds on the ground were counted at this site, this decrease may reflect competition between people and birds for space on the ground. 3.3. Statistical analyses Because the distributions of birds and people over a day at the two test sites was non-linear, data for morning and afternoon were analyzed separately. Table 1 shows the Pearson correlation coefficients between the number of birds, number of people and time of day. For the Parkade site there was a modest but significant ( P < 0.05) negative correlation between birds and time, reflecting the fact that the number of birds observed at this site decreased over the day. The correlations amongst the other variables were close to zero and did not approach statistical significance. At the two test sites there was a significant ( P < 0.0 1) and moderately strong positive relationship between the number of birds and number of people. There was a significant (P < 0.01) and even stronger correlation between the number of birds and time of day. Stepwise multiple regression was also performed on the three variables for both test sites, with the data again being divided into morning and afternoon observations. The number of birds was the dependent variable and the mean number of people present and the time-of-day served as predictor variables. The results of this analysis are shown in Fig. 5, which shows the value of the r2 (times 100%) for each step of the regression. The absence of a bar indicates that no factor was added in the second step. The time-of-day was included first in the regression equation in all cases, with quite large associated r’ values. This indicates that in all cases time-of-day was a better predictor of the number of birds than was the mean number of people at the field sites. In two of the four cases, the mean number of people was added in the second step. This indicates that the mean number of people at the test sites provides an additional, independent, improvement in predicting number of the regression equation. The additional predictive gain in including people was quite modest.
4. Discussion Clear evidence of time-place behaviour was found. At both sites birds appeared to anticipate reoccurring peaks in human activity, part of which was deliberate or accidental food distribution. The apparent anticipation of peaks of human activity at both test sites is an important observation suggesting that the scavenging birds were using time of day as a stimulus rather than using the number of people as an environmental stimulus predictive of food. This finding extends the findings of Daan and Koene (1981) in their study of foraging oystercatchers. They found that these birds’ foraging flights from their inland roost to the musselbeds were controlled by the expected time of low tide and not simply by the visual sighting of the mussels; the birds appeared before the musselbeds were usable on days when the ebb tide was late and sat in their roosts until the appropriate time on days when the tide was early. The overall pattern of bird activity at both sites was similar despite differences in how birds were counted at the two sites and despite considerable differences in the environment at the two sites - a waterside public market and a meeting location in the centre of a large university campus. Although we did not systematically record the species of birds at either site, casual observation revealed that
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pigeons, gulls, crows, starlings and sparrows were the most common. The observation of time-place behaviour in these scavenging birds is important in demonstrating the generality of this behaviour across a range of species. Although time-place behaviour has been observed in laboratory pigeons (e.g., Saksida and Wilkie, 19951 the present observations constitute the first field confirmation of this behaviour in non-specialist foragers. This finding is important in that it gives additional credence to Gallistel’s (1990) thesis that time-place memory coding is a fundamental mechanism in the organization of one type of animal memory. Although we have no direct evidence that the time-place behaviour observed in the scavenging birds was in fact learned, the fact the human food-activity has occurred at the two test sites for only approximately 20 years argues against the notion that time-place behaviours are inherited behaviour patterns that have evolved in environments in which resources vary with temporal and spatial regularities. Also the fact that laboratory animals learn arbitrary, artificial time-place associations suggests that time-place learning might be a very general and flexible process - one capable of optimizing behaviour in the face of changing patterns of temporal and spatial regularities in the environment. There is other work, however, which suggests that an animal’s proficiency at time-place learning may be predictively related to its foraging ecology. Falk et al. (1992) examined insectivorous ( Ploceus bicolor) and granivorous (Euplectes hordeaceus) weaver species using the same experimental chambers and procedure as Biebach et al. (1989) that we described earlier. These authors reasoned that as the granivorous species eats mainly seeds. which have no regular daily pattern of availability, they might have a lower tendency to acquire time-place behaviour when compared to insectivorous weavers. The granivorous birds acquired the task faster than the insectivorous birds but both species learnt to visit each location at the correct point in a daily session. Both types of birds appeared to use an endogenous timing mechanism to track the location of food as their pattern of room visits was maintained by both species when all compartments provided food for an entire test day. However, a photoperiod phase advance produced an immediate and dramatic deterioration of the granivorous birds’ time-place behaviour (they appeared to enter rooms at random) whereas the insectivorous birds maintained the order and duration of their room visits but they entered each room approximately 2 h early on the test day. Falk et al. concluded that this, and other related differences between the behaviour of these species in this task, reflect a predisposition towards this form of learning in the insectivorous species. Our data are not inconsistent with their conclusions as both the insectivorous and granivorous species displayed time-place learning. Instead, it appears that a great variety of organisms are capable of time-place learning, but there may be quantitative differences in the robustness of this form of learning in animals which may be predictively related to their foraging ecology. The laboratory work reviewed above suggests that birds use phase timers when required to anticipate environmental regularities in food availability with a period of several hours. It therefore seems unlikely that the birds observed in the present study used a stopwatch-like internal clock to control their arrivals and departures from our field sites (see Wilkie, 1995). The most likely candidate is phase timing subserved by one, or many endogenous circadian oscillators (Gallistel, 19901. A wide variety of physiological and behavioural circadian rhythms are driven by photoperiod (in mammals, see Mistleberger and Rusak (19941; in birds, see Binkley (199011, or meal-entrained endogenous oscillators (in mammals, see Mistleberger (1994); in birds, see Phillips et al. (1993)). Thus the birds may have learned to visit the food patches when some endogenous oscillator, or group of oscillators,
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attain a certain phase angle. whether each individual bird some others might simply behavioural strategies while (e.g., Giraldeau and Lefebvre,
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One question left unanswered by the present results is the question of made use of a timer. Perhaps some birds time the arrival at a site but ‘join the crowd’. Evidence that individual birds may use different foraging has been reported in the literature on observational learning 1987).
Acknowledgements This research was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). J.A.R.C. was supported by a Sir Dudley Spurling Scholarship.
References Aschoff, J., 1989. Temporal orientation: Circadian clocks in animals and humans. Anim. Behav., 37: 881-896. Biebach, H., Gordijn, M. and Krebs, J., 1989. Time-place learning by garden warblers, Sv/t)ia h-in. Anim. Behav., 37: 353-360. Biebach, H., Falk, H. and Krebs, J., 1991. The effect of constant light and phase shifts on a learned time-place association in garden warblers (Sylvia borin): Hourglass or circadian clock? J. Biol. Rhythms, 6: 353-365. Binkley, S., 1990. The Clockwork Sparrow: Time, Clocks, and Calendars in Biological Organisms. Prentice-Hall, Englewood Cliffs, NJ. Daan, S. and Aschoff, J., 1982. Circadian contributions to survival. In: J. Aschoff, S. Daan and G.A. Groos (Editors), Vertebrate Circadian Systems: Structure and Physiology. Springer-Verlag, New York, NY. Daan, S. and Koene, P., 1981. On the timing of foraging flights by oystercatchers, Huematopus ostrultyys, on tidal mudflats. Neth. J. Sea Res., 15: l-22. Falk, H., Biebach, H. and Krebs, J.R., 1992. Learning a time-place pattern of food availability: a comparison between an insectivorous and a granivorous weaver species ( Ploceus hicolor and Euplrctes hordeaceus). Behav. Ecol. Sociobiol., 31: 9-15. Gallistel, CR., 1990. The Organization of Learning. MIT Press, Cambridge, MA. Gibbon, J., 1991. Origins of scalar timing theory. Learn. Motiv., 22: 3-38. Giraldeau, L. and Lefebvre, L., 1987. Scrounging prevents cultural transmission of food-finding behaviour in pigeons. Anim. Behav., 35: 387-394. Kamil, A.C., 1978. Systematic foraging by a nectar-feeding bird, the amakihi (Loxops cYrerz.s). J. Comp. Physiol. Psychol., 92: 388-396. Mistleberger, R.E., 1994. Circadian food-anticipatory activity: Forma1 models and physiological mechanism. Neurosci. Biobehav. Rev., 18: 171-195. Mistleberger, R.E. and Rusak, B., 1994. Circadian rhythms in mammals: Formal properties and environmental influences. In: M.H. Kryger, T. Roth and W.C. Dement (Editors), Principles and Practice of Sleep Medicine, 2nd Edition, W.B. Saunders, Philadelphia, PA, pp. 277-285. Phillips, D.L., Rautenberg, W., Rashotte, M.E. and Stephan, F.K., 1993. Evidence for a separate food entrained oscillator in the pigeon. Physiol. Behav., 53: I 105-l I 13. Rijnsdorp, A., Daan, S. and Dijkstra, C., 1981. Hunting in the kestrel, F&a tinnunculus, and the adaptive significance of daily habits. Oceologia, 50: 391-406. Saksida, L.M. and Wilkie, D.M., 1995. Time-of-day discrimination by pigeons, Colunzba licicc. Anim. Learn. Behav., 22: 143-154. Wilkie, D.M., 1995. Time-place learning. New Directions in Psychol. Sci., 4: 85-89. Wilkie, D.M. and Willson, R.J., 1992. Time-place learning by pigeons, Columba liriu. J. Exp. Anal. Behav.. 57: 145-158. Wilkie, D.M., Saksida, L.M., Samson, P. and Lee. A., 1994. Properties of time-place learning in pigeons, Columba li~ia. Behav. Process., 31: 39-56.
