Foraging in a complex naturalistic environment: capacity of spatial working memory in flower bats
1 Department of Biology, University of Munich, 82152
München-Martinsried, Germany
2 Max-Planck Institute for Ornithology, 82319 Seewiesen, Germany
* Author for correspondence (e-mail: winter{at}zi.biologie.uni-muenchen.de)
Accepted 30 November 2004
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Summary |
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Key words: spatial memory, orientation, cognition, foraging, bats
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Introduction |
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Within the natural environment, typical mammal or bird foraging excursions
will normally consist of multiple locations to be visited in sequence rather
than just being directed towards a single goal. To prepare such sequences,
cognitive mechanisms may enable animals to identify spatial locations of
interest and chain them into a visitation sequence. Beyond coding spatial
coordinates there must therefore be an association of the places with the
resources they offer and thus of an individual's past experience with those
places. This information must exist over several temporal scales, since an
animal must be able to distinguish places both by their general, long-term
utility (i.e. food productivity) and by their short-term utility (i.e. their
visitation history). Accordingly, rats remember their feeding activity at
specific places in spatial working memory, which allows them to avoid
productive sites after having emptied them of food
(Roberts, 1984).
Simple but otherwise successful behaviour paradigms for spatial memory
ability (water maze, radial arm maze) do not suffice to investigate strategies
of exploiting naturalistically complex, temporally dynamic spaces. Most
importantly, laboratory environments with only a few potential goals and the
inability to change attributes dynamically may not be adequate to challenge
complex behaviours that possibly involve behavioural planning. In addition,
the efficient behavioural testing of animals in dynamic and complex
environments under minimal disturbance is hardly possible without automated
methods for objective behavioural data recording (e.g. Gass,
1977,
1978
;
Young et al., 1993
;
Mauck and Dehnhardt, 1997
;
Tsibulsky and O'Gower, 2002
;
Fry et al., 2000
;
Taylor et al., 2002
;
Kao et al., 1995
;
Gerhardt et al., 1998
;
Hagstrum et al., 1996
). We
developed a novel automated experimental system for the simulation of a
complex naturalistic environment with dynamic food availability for sequential
behaviour experiments with multiple individuals. In the present study we used
it to examine how flower-visiting bats acquire a spatial win-shift task in a
64-feeder environment.
Neotropical flower bats (Glossophaginae, Phyllostomidae) exploit an
ecological environment characterised by spatially predictable feeding sites
(flowers) with a resource (nectar) of temporally dynamic availability
(Winter and von Helversen,
2001). Previous work has shown that once the spatial location of a
flower is known, Glossophaga primarily uses spatial memory to
relocate such food targets (Thiele and
Winter, 2004
). In addition, the hippocampus of nectar-feeding
glossophagine bats is 50100% larger in size than the
carnivorous/insectivorous members of the same family (Phyllostomidae;
Baron et al., 1996
; U. Kaupert
and Y. Winter, unpublished). This may indicate a specialized cognitive
adaptation to a trophic niche where the predictability of both spatial
location and the dynamics of food resource availability (flower nectar)
challenge an animal to optimise foraging trajectories. This raises questions
about behavioural competences gained from hippocampal enlargement and of the
trade-offs involved. We designed the present study to estimate the capacity of
spatial working memory for this mammalian spatial memory specialist. We
presented single bats of the species Glossophaga soricina with a
64-feeder win-shift foraging task at a vertically oriented array of feeders
inspired by the experimental design of Sutherland and Gass (1996). Feeders
gave only single rewards so that bats had to remember the spatial distribution
of their own previous foraging activity within the current bout of foraging to
forage efficiently.
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Materials and methods |
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Individual cages are equipped with feeders, a remote surveillance system and computer-controlled doors. This allows for the automatic release of an animal from its cage to the room containing the experimental feeder array and its subsequent return to its cage, followed by resetting the array and release of the next animal. With this system animals can alternately search for food independently in the same array for given time intervals without the presence of test personnel.
Cage and feeder system
Feeders can be adjusted to supply variable amounts of a liquid (e.g. water
or sugar water). For detection and timing of visits each feeder
(Fig. 1) has an infrared diode
and light sensor at its front edge. For our experiments with hover-feeding
bats, this sensor determines the time and duration of a feeding event with 1
ms resolution. An outer ring of PVC masks the wiring and provides a uniform
outer appearance, both visually and echo acoustically. The supply of sugar
water is controlled by a pinch valve at each feeder and a single electronic
pump for the feeder system that holds the sugar water in a gas-tight injector.
Food is delivered only after arrival, so that an animal cannot sense its
presence beforehand.
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Feeders can present three different types of stimuli. A green LED can serve as a visual stimulus. An odour current controlled by a pinch valve can be issued from a 1 mm hole as an olfactory stimulus. A motorised swivel arm can present shapes offering visual or echo-reflecting stimuli. For the experiment reported here, no stimuli were activated and all feeders were of the same external appearance and were programmed identically.
Individual cages each contain two feeders, a resting place connected to an electronic balance that detects presence and monitors body weight, an infrared (IR) sensitive video camera for observation and motion detection, and an IR lamp (860 nm) for illumination. Animals cannot see the feeder array from the cage with sidewalls that are opaque PVC, but external light can enter through the roof and back wall that are transparent Perspex. Cages are accessible through a Perspex door (Fig. 2) and have an additional motor-operated guillotine door that serves as an entry hatch.
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The perch hangs from an electronic balance (Scout SR2020; VWR-Merck Biosciences, Ismaning, Germany) connected to a PC, which registers the presence and weight of the bat to 10 mg resolution. A small roof over the perch provides shade from daylight. Individual cameras can be selectively connected to a motion alarm via a camera switch for detection of movement in the cage.
The electric door and the supervision system make it possible automatically to lock an animal in or out. When an animal has completed a trial, the cage door is opened and the motion sensor of the video camera activated. When an activity signal is received from within the cage (feeder, balance, or motion alarm), the door is closed. When a further activity signal is received from within the cage after the door has been closed, the enclosing process is completed and the door of the next cage will be opened. While doors close slowly to prevent injury, these agile fliers may still escape through the moving door. A mechanical flight barrier erected within the cage prevents such escapes.
Sixty-four identical feeders (self-built) are mounted in an array of eight by eight with a distance of 25 cm between feeders (horizontal and vertical) on an aluminium stand with a PVC blind to shield backside cables and tubing. The frame is tilted 15° forward to prevent liquid from dropping onto feeders below during cleaning. The vertical arrangement of feeders leads to a hydrostatic pressure difference between horizontal rows of feeders. We compensate for this through pressure adjustment, which is essential for achieving identical feed volume at all 64 feeders. Pressure regulation is achieved in two steps. During operation, the tubing system is under slight positive pressure. The pressure in the tube system is adjusted to normal for the specific height of the visited feeder before a reward is given. This occurs through the brief opening of an overflow valve at the same height as the visited feeder. This delays liquid delivery by 180 ms. During the subsequent opening of a feeder valve no elastic or hydrostatic pressure is on the system and only the food pump causes liquid flow. After delivery of each unit of liquid, the pump again sets the whole tubing system under slight positive pressure. Calibrations confirmed that by this measure all feeders gave identical reward volumes without measurable systematic error.
The computer controls the 650 TTL-data links connected via four I/O-interfaces with 192 TTL I/O-lines each and the serial data lines from the balance that are connected to an 8-port RS-232 card (Fig. 3). DC electricity is supplied from outside the experimental room to exclude transformer noise and also the zero noise computer without fans provides no acoustical landmark.
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Operation
Automated tests can be conducted on six animals simultaneously, with
individuals being active in the test arena alternately. Animals can be
released to the feeder array in any order. Feeders at the array can be
programmed to be active at the same time or in succession, and a feeder's
condition can be signalled by stimuli of the different sensory modalities. The
spatial distribution of rewarding and non-rewarding feeders is freely
adjustable and can be different for particular individuals. Trial duration may
depend on a fixed time interval or on the number of feeder visits and can be
adapted individually. Practical operation is illustrated in
Fig. 4. After acclimatisation
in the cages to get used to feeders, stimuli and the environment, one animal
at a time is released for an experimental trial to the feeder array. For
experiments with Glossophaga soricina we found it optimal to have
only three animals flying alternately so that each can have 20 trials at the
feeder array in one night's work (Fig.
4). At the beginning of the night the animals have half an hour to
drink nectar from the cage feeders (nectar-feeding bats respond better after
initial feeding and rehydration before trials are started). The computer
activates the feeder array and deactivates rewards in the first cage. The
trapdoor is then opened electronically and the animal leaves the cage. The
cage door is closed behind the animal after its first visit to a feeder in the
array, and the animal can visit feeders in any sequence for the duration of
the trial. After this time the computer reopens the cage door, which by its
noise signals the end of a trial, switches off the feeder array and switches
on the cage feeders. After re-entry into the cage and electronic detection
(balance, video motion alarm, or visit to a feeder) the door is closed. When
the animal is locked in, the next door is opened and the next bat can visit
the feeder array.
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Subjects and experimental procedure
In the present study we used the 64-feeder system to estimate the capacity
of spatial working memory in a nectar-feeding bat, by presenting single bats
with a win-shift foraging task at the vertically oriented array of feeders.
Experimental subjects were 17 adult male Glossophaga soricina Pallas
(Phyllostomidae, Glossphaginae) bred in captivity. One individual with few
visits during some trials was excluded from some of the analyses. After
transfer from the animal facility, bats could accustom themselves to their
individual cages and feeders for 1 day. This was the only pre-training of the
animals before data collection began. Thus each bat was experimentally
naïve on first confrontation with the feeder array. Starting on day 2,
they were released individually to feed at the array, where each feeder gave a
single reward on the first visit (10 µl of 17% wt/wt;
Bolten et al., 1979, containing
sucrose, fructose and glucose in equal parts as typical for nectar from bat
pollinated flowers; Baker and Baker,
1990
). Bats spontaneously probed feeders on their first visit to
the array and readily alternated between cage and feeder array. Each trial
lasted until 64 visits to feeders had been made or 5 min had passed since the
first visit to a feeder, whichever came first. Bats were free to revisit
feeders at will, but for efficient feeding, they had to learn to visit feeders
only once (win-shift behaviour). In general, bats trained quickly to this
protocol and we had few problems running three animals per night.
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Results |
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Movement within array
Bats made on average 37.3 feeder visits (±2.3 S.D., range
1564) during 5 min trials (after trial 10) and emptied 28.6
(±1.5 S.D.) of the feeders. Bats often visited feeders in an
uninterrupted sequence of visits at the array. They also often briefly circled
through the room between visits, especially after they had received a reward.
Generally, the next feeder was usually not adjacent to the previous one
(Fig. 6A). On average, the next
feeder visited after a reward was 4.6 feeder positions away (= 4.6x25
cm). After an unrewarding visit, the distribution was bimodal with peaks at
distances of two and five feeders from the previous one
(Fig. 6A). Thus, bats did not
move through the array by applying the simple search rule of systematically
visiting adjacent feeders but instead tended to jump between non-adjacent
positions that were more than half the width of the array apart. This is an
important result.
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The direction of movement between successively visited feeders was significantly non-random. Of the eight rows of feeders available for each visit (12.5% random chance of selecting a specific row), bats tended to stay within the same row visited previously. After an unrewarding visit, bats next chose the same row in 41% of choices (S.D. 12%, N=16), more often than expected if they had selected rows by chance (t=9.9, d.f.=15, P<0.001). After a reward, the frequency was 29% (S.D. 5.7%, N=16), also significantly more often than expected by chance (t=11.9, d.f.=15, P<0.001). In addition, bats were less likely to remain within the same row after receiving a reward than after not receiving a reward from a visit (paired-t=4.86, d.f.=15, P<0.001). Bats avoided moving vertically up or down (only 5% of choices) but rather moved diagonally in changing horizontal rows. The proportion for a single feeder to be the next visited was 4.5% for each of the seven feeders in the same row, 0.8% for each feeder in the same column, and 1.5% for each of the 49 feeders from a different row and column. Taken together, bats had clear biases in moving through the array but did not seem to apply a simple or stereotypic search rule.
Temporal sequence of visits
The temporal sequence of visits was characterised by median time intervals
between successive visits of 1.2 s(N=1009) after non-rewarded, and
2.5 s (N=3501) after rewarded visits
(Fig. 6B). Thus, visits within
sequences followed in quick succession, especially when no reward was
obtained. The bimodality in interval durations reflects the bats' tendency to
circle the room after receiving a reward rather than visiting the next feeder
directly. Feeder visits lasted between 500 ms (non-rewarded) and 800 ms
(rewarded, modal values), reflecting the time needed to ingest the reward.
Win-stay and win-shift
Initially, bats tended to revisit in the same trial feeders from which they
had received rewards (win-stay) so that on average 42% of all feeder visits
were revisits during the very first trial (or 34% during the first three
trials; Fig. 7A). However, bats
learnt rapidly that rewards were given only once and adjusted their behaviour.
After trial 10, the frequency of revisits was significantly below expectation
assuming random choice of feeders. We obtained this result by computing for
each visit to a feeder the number of currently empty feeders divided by 64,
which gives the chance probability of revisiting. For each individual we
calculated the mean of these data over all visits from all trials included.
For the same visits we determined the proportion of revisits actually made. To
have comparable data, this analysis was restricted to the first 20 visits of
trials. We compared individually expected with individually observed revisits
using paired t-tests and the results are shown in
Fig. 7A. During trials
13, revisits occurred significantly more often than expected by chance
(paired t-test, t=5.4, d.f.=14, P<0.001). There
was no significant difference from chance expectation during trials 410
(paired t-test, t=0.5, d.f.=15, not significant), while
during trials 1120 revisits occurred significantly less often than
expected by chance (paired t-test, t =2.8, d.f.=15,
P=0.014).
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In the previous analysis we calculated the mean over the entire set of trials. For the following we considered performance within a trial. Within trials, bats revisited feeders significantly less often than expected from chance performance up to the 25th visit during a trial (Fig. 7B). This was determined by using the same data as above. However, instead of averaging over entire trials we averaged for each individual over successive blocks of five visits within trials. This gave us a pair of measured and expected values for each individual for each block of five-visit intervals during a trial. Up to the 25th visit during a trial bat performance exceeded chance level (Wilcoxon test, Zs>2.1, Ns=16, Ps<0.05).
In addition, it was interesting to note that if individuals were split equally into high and low performers (an artificial distinction, since distribution of performance between individuals was continuous) then the high group initially revisited feeders during a single trial at 40% the rate expected from chance and remained below 80% of chance level up to the 45th visit during a trial. The low performers, conversely, revisited feeders at a rate of 80% (and above) of chance level from the very beginning of a single trial. Thus, individuals during our study performed unequally and may have differed in the behavioural mechanisms applied during the task.
Evidence for scent cues?
If bats were leaving some scent cue by themselves then the ability to avoid
previously visited feeders would not be an effect of memory but of sensory
discrimination. Our general observations speak against this possibility. Bats
hover in the air while feeding and only the tongue and frontal head make
contact with the feeder. After habituation to feeders we normally did not
observe inspection behaviour that would be required for olfactory sampling.
Instead, bats approached chosen feeders directly and without hesitation.
Nevertheless, to examine further the possibility of putative olfactory cues we
performed the following analysis. It is unlikely that a hypothetical olfactory
cue would be individual-specific. If scent-marking behaviour had evolved, bats
in nature should not only avoid flowers visited by themselves but also every
flower visited recently by any other bat. Refill intervals in natural flowers
often range from 20 min to about 1 h (von
Helversen, 1993; Winter and
von Helversen, 2001
; von
Helversen and Winter, 2003
) so a scent mark should persist over
such a time interval in order to be useful.
During our experiments groups of three bats used the same array in an uninterrupted nightly cycle so different individuals fed from the array in repeated succession. Thus, if scent cues influenced feeder visitation we should expect feeder visits by any bat to influence the choice behaviour of its immediate successor at the array. We analysed our data for evidence of such an effect. We determined for each feeder for each trial if it had been visited in the preceding trial (always a different individual). This gave us four groups of feeders: feeders visited or not during the preceding trial and feeders visited or not during the succeeding trial. We then asked if the probability of visiting a feeder was affected by previous visitation by another individual. To exclude the potential effect of scent decay we only included pairs of trials separated by a maximum time span of 20 min between visits by the two individuals. Analysis was restricted to data after trial 10 and, within individual data sets, to feeders visited at least three times during trials 1120. The results of our analysis did not produce any evidence for an influence of scent cues. The ratio of visits to feeders that had or had not been visited by the previous bat was 1.02 (±0.18 S.D.). This was not significantly different from 1.0, the ratio expected for random choice between feeders that had been either visited or not visited by the predecessor (t-test, t=0.425, d.f.=10, P=0.68). Scent cues do not appear to have influenced feeder choice during our experiments.
Recency and working memory capacity
If bats had selected feeders at random then revisits should have followed
the current ratio between emptied and full feeders. The results in
Fig. 7 and the analysis given
above show that bats avoided revisits. Since bats did not appear to have used
a simple rule of movement at the array they must have remembered the positions
of feeders emptied in order to avoid those positions during later visits
during the same trial (spatial working memory;
Olton and Samuelson, 1976).
This memory must have formed rapidly as feeder visits lasted only 0.8 s
(hovering duration) to 2 s (time span to next visit;
Fig. 6).
If bats did remember feeders visited then it might be expected that feeders
emptied recently are better remembered and more successfully avoided than
those feeders emptied longer ago (recency effect). After a visit to a feeder a
bat has n opportunities during the next n visits of a trial
to revisit this particular feeder. Accordingly, there are n1
opportunities to return two or more visits later to an emptied feeder, and
n2 opportunities to return three or more visits later during
each sequence of n visits following the first visit and so on. We
calculated the number of opportunities that each bat had for each length of
inter-visit interval from the number of visits made during each trial. We then
summed the number of revisits and the number of opportunities over blocks of
five inter-visit interval lengths and calculated the percentage of
opportunities taken by each bat for each block of intervisit intervals
(Shettleworth and Krebs,
1982). We performed these calculations separately for the initial
trials 13 and the later trials 11 to 20
(Fig. 8A). A consequence of the
initial win-stay strategy was a strong tendency in trials 13 to revisit
feeders that had recently been emptied. So there were many revisits during
short intervisit intervals during those trials. By trials 1120, this
win-stay effect was no longer detectable. Surprisingly, however, was the flat
continuation of the curve in Fig.
8A. In general, recent events are often remembered better than
events from longer ago, the so-called recency effect
(Shettleworth, 1998
). For our
data, we had expected that for visits to feeders that had occurred longer ago
(long inter-visit interval) bats would eventually show disproportionately
higher rates of revisitation errors, indicating that they were forgetting
their initial visit. However, the expected increase in the number of errors
after long intervisit intervals is not apparent in the data
(Fig. 8A). This differs from
the findings of other authors performing similar experiments with other
organisms (Fig. 8B,
Discussion).
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Discussion |
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The smooth operation of experiments with this set up depends not only on technology, but also on cooperation by the animals. An animal that delays its return to the cage will, in consequence, set back the experiment for all other animals. During our experiments some groups of three bats completed a series of 20 interleaved trials in 7 h, while others required as much as 12 h because some individuals returned late. Preliminary experiments taught us that reward quantity in the cages and the feeder array must be well balanced for smooth operation (as described in the Materials and methods section) as bats may otherwise prefer to remain in one of the experimental compartments (cage or feeder array). The system described here can easily be adapted for other animal taxa without major changes to the basic principle of operation. The hanging perch for bats may be replaced by an erect perch for birds. For mice, we have used feeders as quantitative water dispensers (Y.W., unpublished). The system is a dependable means to effect completely automated data collection in behavioural tests on a wide variety of animals.
Spatial working memory
To maximize their rate of food intake while foraging or maximize their
foraging efficiency, bats had to avoid the positions of feeders already
emptied, as feeders gave only a single reward during a trial. Food was only
delivered after arrival so bats could not sense its presence beforehand. Two
lines of evidence support the idea that bats during our experiments remembered
the spatial positions where they had fed. Initially, bats revisited emptied
feeders significantly more often than expected under random choice (win-stay
behaviour; Fig. 7A, trials
13). Many of these revisits occurred after 510 intermittent
visits to other feeders rather than directly following the initial visit. This
is apparent from Fig. 8A where
the rate of revisits during trials 13 was still higher even after
510 intervening visits to other feeders. This provides first evidence
that bats must have remembered the spatial positions visited recently. This
result cannot be explained by a simple movement pattern. A forager using
area-restricted search remains in the vicinity of a good location. The bats,
however, tended to jump between positions within the feeder array, often
moving more than half its width between successive visits
(Fig. 6A). Furthermore, these
distances were larger after a reward than after an unsuccessful visit.
Area-restricted search predicts the opposite.
Bats changed their behaviour from win-stay to win-shift within 410
trials (Figs
7A,8A).
Thereafter they significantly avoided emptied feeders
(Fig. 7B). However, did bats
avoid empty feeders by remembering their spatial locations? At the 64-feeder
array, bats could have easily obtained a high rate of success if they had
systematically emptied feeders starting at one corner and going up- or
downwards in rows, using thigmotactic or chaining behaviour. This, however, is
not what they did. On average, the next feeder visited was 4.6 feeder
positions away from the previous one (Fig.
6A). Thus, bats did not move through the array by applying the
simple search rule of systematically visiting adjacent feeders but instead
tended to move across large gaps of, on average, half the extent of the total
feeder array. This is strong evidence that bats remembered the spatial
locations visited and therefore possess a well-developed spatial working
memory. This conclusion is further corroborated by our failure to find
evidence for scent cues influencing feeder choice. During our experiments the
same array was used by several bats in an uninterrupted nightly cycle so
different individuals fed from the array in repeated succession. Thus if scent
cues had influenced feeder visitation we should expect feeder visits by a bat
to influence the choice behaviour of its immediate successor at the array. Our
analysis did not produce any such evidence. While data on movement patterns
within natural inflorescences are still scant, observations of Glossophaga
commissarisi during inspection flights between adjacent inflorescences of
a rainforest vine also did not indicate systematic movement between adjacent
neighbours (von Helversen and von
Helversen, 2003).
Previous authors have tried to show the use of spatial working memory by
examining data for an effect of recency. If locations of emptied feeding sites
are remembered, then one might expect that recently experienced feeding sites
are better remembered and more successfully avoided than those emptied longer
ago (recency effect; Shettleworth,
1998). Two examples from the literature are seed-storing marsh
tits that remembered the sites of food recovery
(Shettleworth and Krebs, 1982
)
and hummingbirds remembering the positions of feeders already emptied
(Sutherland, 1986
). In the
marsh tit study, the percentage of `revisit opportunities taken' (see
Materials and methods; Fig. 8B)
was below 1%, but rose to significantly higher values when more than 29 visits
had passed since initial seed recovery
(Shettleworth and Krebs,
1982
). Similarly, the rate of `revisit opportunities taken' by
hummingbirds was initially between 2 to 5%, but rose to values between 10% to
30% after 2030 intervening visits to other feeders
(Fig. 8B). Thus, in both bird
species spatial working memory is of sufficient capacity to remember the sites
of feeding actions visited about 30 visits earlier.
In the present study, a recency effect was not apparent up to the 45th
visit during trials (Fig. 8B).
By comparison, the marsh tits were actually doing slightly better than the
bats (lower proportion of revisit opportunities taken,
Fig. 8A,B) but only until about
30 visits. However, one should note that, even within a species, the
quantitative characteristics of memory should vary with the details of what is
remembered. For instance, spacing between feeders
(Brown, 1994), the numerical
size of the array, whether feeders are arranged in three dimensions or two (as
here), or the actual time interval that has passed (in this study always below
five minutes), etc. While the bat curve remained flat in our experiment
(Fig. 8A) we do not know if and
under which conditions it would eventually rise. So the change in pattern
within the bat data from trials 13 to 1120 is perhaps of equal
interest as the difference from the two sets of bird data.
Olton (1977) suggested that
rats can hold visits to 2530 different arms in their spatial working
memory based on work in a 17-arm maze, and Roberts
(1979
) reported good
performance in a hierarchical maze with 32 different locations (8 arms that
continue in two successive bifurcations). The present data indicate that
nectar-feeding bats at least match the performance reported for rats and they
suggest the possibility that the spatial working memory capacity of these
flower-visiting specialists may surpass that of rats.
From an ecological point of view, a well-developed spatial working memory
would be expected for a nectar-feeding flower visitor
(Cole et al., 1982;
Armstrong et al., 1987
). Since
the nectar of flowers is often replenished rapidly, individual flowers are
worth revisiting but only after a sufficient time interval has elapsed. This
creates the need to remember past actions of flower visitation in order to
space visits adequately. The natural problem faced by the bats is, thus, not
only spatial but also temporal. It is worth noting that within the speciose
family of neotropical phyllostomid bats, the volume of the hippocampus is
greatly enlarged in the nectar-feeders, surpassing the volume of closely
related but insect-feeding species by 50100% (U. Kaupert and V. Winter,
unpublished). This indicates a neural adaptation to a trophic niche where
spatiotemporal dynamics maintain resources (flower nectar) in continuous but
tractable change and where behavioural optimisation should depend on rapid
spatial learning and memory.
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Acknowledgments |
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Footnotes |
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