ELSEVIER Behaviouml Processes 39 (1997) 149-159

B HAVIOURAL
6 ROCESSES
Searching in patches by European starlings, Sturnus vulgaris
Sasha R.X. Dal1 *, Innes C. Cuthill
Behavioural Biology Group, School of Biological Sciences, Ukersity of Bristol Woodland Road, Bristol BS8 I UC. I/. K.
Received 25 January 1996; revised 22 July 1996; accepted 23 July 1996
Abstract
Despite the importance of within-patch search for predicting optimal patch-leaving strategy, little experimen-
tal effort has been devoted to the study of this foraging behaviour. In addition, predators strategic responses to
variability in features like the within-patch distribution of prey can have important consequences for their
dietary decisions. We therefore analyse the search paths of European starlings, Sfurnus vulgaris, foraging
individually in artificial patches that vary in the spatial distribution of buried prey in an outdoor aviary. The
results demonstrate that the birds are searching differently depending on the order in which the experimental
patch-types are experienced. We speculate that where the spatial predictability of prey is initially high the birds
adopt a fixed search rule that results in area-concentrated starch once a prey item is found, and performs well
for both distributions encountered. However, where the predictability is initially low a more flexible strategy is
adopted that results in increased area-concentrated search with experience of a patch type, independent of the
actual within-patch distribution of prey. These findings suggest that starlings can use distinct strategies for
different prey types, but they are classifying these types on subjective criteria that are difficult to predict from a
priori reasoning. 0 1997 Elsevier Science B.V.
Keywords: Search strategy; Prey distribution; Area-concentrated search: Patch use
1. Introduction
One of the main problems that have concerned students of foraging behaviour is the efficient
exploitation of patches of prey (e.g. Chamov, 1976; Parker and Stuart, 1976; reviewed in Stephens
and Krebs, 1986). If patches are clearly delimited then optimal foraging theorists have reasoned that
the crucial decision that a forager has to make is when to leave one patch and move on to another.
The marginal value theorem (MVT; Chamov, 1976; Parker and Stuart, 1976) is an influential
theoretical treatment of this problem that has inspired a large body of research (Stephens and Krebs,
* Corresponding author. Tel: + 44-117-9289000 ext. 3998; fax: + 44- 117-9257374; e-mail: sasha.dall@bristol.ac.uk.
0376-6357/97/Sl7.00 Copyright Q 1997 Elsevier Science B.V. All rights reserved
PfI SO376-6357(96)00053-8
1986). The main prediction of the MVT is that predators should leave a patch when the expected net
rate of intake falls below the average for the habitat as a whole. This applies with a variety of
within-patch energy gain functions, but the main predictions of the MVT have been based on the
assumption of patch depression (Chamov et al., 1976). This phenomenon, where the instantaneous net
rate of energy intake (prey capture rate) is negatively related to patch residence time, can occur for a
variety of reasons: either due to the search strategy of the predator within a patch (i.e. it occurs when
a predator revisits parts of the patch repeatedly), the response of prey to the presence of the predator
(i.e. where the prey make themselves more difficult to capture when a predator is detected), or both
(Chamov et al., 1976). In the case of a predator loading prey for return to central nest or burrow,
deceleration of gain rate can occur due to increasing difficulty in loading items (Orians and Pearson,
1979; Giraldeau and Kramer, 1982; but see Cuthill and Kacelnik, 1990). Where prey cannot or do not
respond to predators (e.g. for relatively sessile, unresponsive prey) the patch gain function will
primarily be determined by the searching behaviour of the predator (Stephens and Krebs, 1986).
Therefore, when a predator should leave patches of unreactive prey will crucially depend on its
within-patch searching behaviour.
Random within-patch search has been commonly assumed and is necessary for the form of patch
depression that generates the biologically interesting predictions of the MVT for unresponsive prey.
This is because a random forager will frequently revisit parts of the patch that have already been
depleted and thus its instantaneous rate of intake will be depressed with the time it spends in the
patch. Despite the dependence of the MVT predictions for unresponsive prey on this crucial predatory
behaviour, very little experimental effort has been committed to qualifying the assumption of random
within-patch search (but see e.g. Smith and Dawkins, 1971; Smith and Sweatman, 1974; Smith,
1974a; Smith, 1974b; Zach and Falls, 1975; Zach and Falls, 1979, for detailed work on general search
in patchy environments). Indeed, when Baum (1987) looked at the gain functions of pigeons foraging
on artificial patches in the laboratory, he found little evidence for negative acceleration. It was
therefore concluded that the birds were foraging systematically in the experimental set up, and it was
reasoned that this should be expected since any appropriate, systematic adjustment of search
behaviour would be more efficient than behaving randomly (Baum, 1987).
Maintaining a range of within-patch search strategies can be adaptive when a range of prey types
(sensu Stephens and Krebs, 1986) are to be exploited (i.e. for generalist predators). Different prey will
respond to different environmental factors and so will be likely to be distributed differently, even
within clearly defined patches. Thus what will be an adaptive foraging strategy for one prey type
might not be adaptive for others. Indeed, theoretical investigations looking at the effects of varying
the distributions of the number of prey per patch have shown that different distributions require very
different patch leaving rules for optimal exploitation (Green, 1987; Iwasa et al., 1981). The predicted
effects of varying the spatial distribution of prey within a patch per se, however, are less well
understood. Nevertheless, establishing how a generalist predator can respond to variation that might
be experienced with different prey types will have important implications for the trade-offs underlying
its day-to-day dietary decisions (Dal1 and Cuthill, submitted).
This study therefore attempts to investigate the ability of a generalist predator, the European
starling (Sturnus uulgaris), to adapt its search behaviour to variation in the spatial distribution of prey
within patches. The search task that the birds in our experiment face is an abstraction of one that is
commonly encountered by starlings in the wild when they are foraging terrestrially on topsoil
invertebrates (Tinbergen, 198 1) whose exact position is uncertain prior to sampling (because they are
S.R. X. Dull, C. Cuthill / Behm iourul Processes 39 f 1997) IJ9- I59 151
buried). Since this is a situation where systematic search will be relatively difficult, the results will
have important implications for the range of situations for which the MVT can be used to predict
patch-use. In addition, the extent to which the manipulations affect the starlings search behaviour
will provide insights into how this species deals with the costs of generalising.
2. Materials and methods
2. I, Subjects
Foraging trials were performed on 24 wild-caught, juvenile European starlings, Stumus uulgaris, of
undetermined sex between the 29th of September, 1993 and the 8th of May, 1994. The birds were
selected from a pool which had been captured during the summer (from July to August, 1993) and
housed in outdoor aviaries (at Langford, UK) in flocks of 20 to 30 birds. Both during this post-capture
phase and between trials in the experimental period, the birds had access to ad libitum food (turkey
starter crumbs) and water (for bathing and/or drinking) in 3 m X 2 m X 2 m enclosures.
2.2. Experimental arena
The foraging trials were carried out in a visually isolated pen near the aviary that the starlings were
housed in. The floor of the arena had been filled to a depth of approximately 0.05 m with coarse
builders sand and perches placed symmetrically at various heights. Food was exclusively located
within a patch delineated by a 0.25 m2 metal grid that rested on the surface of the substrate during
the trials. Parts of the substrate had been covered so as to leave a 1 X 1.5 m area of sand exposed
(thus allowing six non-overlapping placements of the 0.25 m* grid). A video camera (Sony
CCD-TR707E with wide angle attachment) had been fitted in the centre of the roof so as to allow a
complete view of the sand floor area.
2.3. Procedure
The experiment was a repeated-measures design, with each starling experiencing a series of trials,
one per day, in one of two experimental patch treatments, before switching to the other. Prey within
a patch were either:
1. dispersed (distributed uniformly with a mean of 0.5 prey per cell on a 0.25 m2 grid divided by
string into 100, 0.025 m* cells), or
2. clumped (according to a negative binomial distribution with the same mean, s = 1.6 and
k = 0.218 on the same grid).
Prior to the experiment the birds were randomly allocated to two groups of 12 individuals
according to the order in which they experienced the different patch treatments. The food items were
mealworms, larvae of the yellow flour beetle (Tenebrio molitor), that had been frozen and freshly
thawed on the day of each trial so as to render them immobile. After being buried according to the
patch treatment, the sand was smoothed over in order to eliminate any visual cues the birds might use
to locate individual prey items.
For each bird on each trial, the position of the patch was randomly allocated to one of the six
IS2 S.R.X. Dull. .C. Curhill / Behu~wurtrl Proce.wes 39 f 1997) 149-159
possible placings (q.v.1 and two mealworms placed randomly on the surface of the patch to focus the
attention of the birds on this area. Before a trial each bird was deprived of food for approximately 15
min and each trial lasted 30 min or until the starling had done a total of 5 min cumulative probing
(Tinbergen, 1981). The behaviour was recorded on 8 mm video cassette and viewed on a remote
monitor during the trial. The time of day that each bird was tested was randomised between
successive trials and the patch treatments were only switched over when the bird had done a total of
four trials with at least 2 min of cumulative probe foraging in each. However, not all of the birds
achieved this criterion for switching between treatments and so had to be dropped from the analysis.
As a result only 12 birds are included, with eight having experienced the dispersed treatment first and
four having experienced the clumped treatment first.
2.4. Video analysis
Since the primary goal of this study was to investigate within-patch search strategies, the video
camera was placed so as to obtain the most relevant field of view for this purpose. By doing this,
however, the ability to recognise actual capture events was sacrificed because all footage was hence
taken from above the foraging birds and European starlings do not show distinct head-up swallowing
or handling of prey. For this reason there are no data from which to construct the individual gain
curves.
The first and last trials of each treatment block were analysed, enabling the effect of experience to
be investigated along with any effects of treatment. For these trials, the original search footage was
discretised by recording the position of the head of a foraging starling every 2 seconds. A starling was
classified as foraging if it was walking slowly over the sand arena and frequently moving its head
downwards, either because it was probing (Tinbergen, 198 1) or inspecting the substrate carefully. The
time unit used for discretisation is essentially arbitrary, and searching animals can adjust either their
speed (e.g. orthokinesis), the amount of turning that they do (e.g. klinokinesis), or both (Benhamou,
1992). In order to analyse the effects of treatment on these two components of search separately, the
sinuosity index (Bovet and Benhamou, 1988) for each of the trials was calculated in addition to the
Euclidean distances moved each time step (search speed). The former involved rediscretising each
search path so that the position of a birds head every unit length (rather than time) was obtained and
calculating sinuosity from the resultant distribution of changes in direction over a trial, using the
methods described by Bovet and Benhamou (1988). The step length used for the rediscretisation was
0.05 m.
3. Results
3.1. Multivariate analysis
Since the temporal and spatial components of a search path cannot be considered as totally
independent variables, a multivariate analysis was carried out with trial sinuosity, the mean search
speed per trial and its variance as variates, in order to adjust the family-wise error rates appropriately
(Sokal and Rohlf, 1995). The data were analysed using a mixed-model multivariate analysis of
variance (MANOVA) with order (treatment block 1 versus treatment block 2) as a between-subjects
S.R.X. Dull. .C. Cuthill/ Behariorrrul Processes 39 (1997) 149-159
153
factor, and treatment (clumped versus dispersed) and trial (the first trial of the treatment block versus
the last (fourth) trial) as within-subjects factors. In order to control for the effects of foraging bout
iength, the mean number of position recordings in a search path per trial was included as a covariate.
The latter was found to have a significant effect (Wilks A = 0.427, F3,23 = 10.296, P < 0.001) and a
significant three-way interaction between order, treatment and trial emerged (Wilks A = 0.716,
FJ _ = 3.045, P = 0.049). To interpret this result, the equivalent univariate analyses were performed
separately to discover for which of the variates the interaction between factors had an effect.
3.2. Unic;ariate analyses
With the mean sinuosity index as a variate, and controlling for bout length as before, the equivalent
mixed-model analysis of variance (ANOVA) demonstrated that the three-way interaction was
significant (F,.?, = 8.39, P = 0.008). In addition, sinuosity was significantly positively related to the
mean bout length (slope = 0.002, t = 4.84, P < 0.001). With the mean search speed as the variate,
again the interaction between the factors was significant ( F1,25 = 4.69, P = 0.04), but mean search
speed was found to be significantly negatively related to bout length (slope = - 0.112, t = -4.86,
P < 0.001). For the variance in search speed, however, there was no significant interaction between
the order in which the treatments were presented, the treatment presented and how much experience
the birds had with the treatment (F,,,, = 0.12, P = 0.735). The search speed variance was also found
to be negatively related to the mean length of search path (slope = - 1 .Ol 1, t = - 4.21, P < 0.001).
Following from the above results, and in order to interpret the meaning of the three-way
interaction, the three-way ANOVAs for mean sinuosity and mean search speed were split into
separate repeated-measures ANOVAs that included the only the birds that had experienced the
treatments in the same order. Thus for each variate for which the three-way interaction was
significant, two separate ANOVAs were performed to investigate the effects of treatment and trial,
and their interaction.
3.3. The three-way interaction and sinuosity
For the eight birds that had been presented with dispersed treatment first, the appropriate
repeated-measures ANOVA demonstrated that treatment had a significant effect on how sinuous the
search paths were (F,,, = 10.9, P = 0.013), however trial did not have a significant effect (F,,, = 0.06,
P = 0.818) and there was no significant interaction between the factors (F,,, = 0.18, P = 0.689). Fig.
1 illustrates these results and shows that, where birds experienced the dispersed treatment first, their
search paths were significantly more sinuous when prey were clumped in a patch than when they were
dispersed. This effect was not mediated by experience, indicating that learning is not involved in this
response to the within-patch distribution of prey (i.e. a fixed search rule was used).
However, it can also be seen from Fig. 1 that, for the birds that experienced the clumped treatment
first, the effects of treatment and treatment experience were markedly different. Indeed, from the
appropriate ANOVA, this time there was no effect of treatment (F,, = 2.13, P = 0.241) but a
significant effect of trial (F,., = 10.82, P = 0.046). Again the interaction was not significant
(F,,? = 5.28, P = 0.148). F ig. 1 shows that, for birds that experienced prey that were clumped within
a patch first, the search paths were significantly less sinuous at the beginning of a treatment block
than at the end, regardless of the within-patch prey distribution. Thus, it appears that these birds
154 S.R.X. Dull. .C. Curhrll/ Behucioural Processes 39 (1997) 149-159
0.45 -
n Clumped First
q Dispersed First
Clumped 1 Clumped 4 Dlrpcr~sd 1 Diaperted 4
Treatment and Trial Number
Fig. 1. The mean sinuosity index per trial (rad cm - I2 + s e m.), at the beginning (first trial) and end (fourth trial) of each .
treatment block, for starlings that experienced the two treatment distributions in different orders (dispersed first versus
clumped first).
respond to the different within-patch prey distributions by turning more with experience (i.e. a more
flexible search rule was used), but that this response is a general one and not affected by the actual
prey distribution.
3.4. The three-way interaction and search speed
Fig. 2 illustrates that the various effects on mean search speed are equivalent but in the opposite
direction to those reported above for sinuosity. Indeed the results of the repeated-measures ANOVAs
demonstrate that, for birds experiencing dispersed first, again treatment has a significant effect
(F,,, = 12.35, P = 0.011, but not trial (F,, = 2.29, P = 0.174) and there is no significant interaction
(F,,, = 0.55, P = 0.485). Also, for the birds experiencing the other order (clumped first), again
treatment had no effect (F,,, = 1.95, P = 0.257), with trial having a significant effect (F,,, = 30.66,
P = 0.012) and the interaction between treatment and trial not being significant (F,., = 0.14,
P = 0.741). So, these results (Fig. 2) indicate that, where the birds are turning more, they are also
moving slower. Therefore the birds move slower for clumped prey than dispersed when the dispersed
treatment is experienced first, and this is not affected by experience. On the other hand, when
S.R.X. Dull. .C. Curhill /Behcr~~iorrral Processes 39 (1997) 149-159 155
13 -
l Clumped First
H Dispersed First
Clomped 1 Clumped 4 DI8peraed I Dhperaed 4
Treatment and Trial Number
Fig. 2. The mean search speeds per trial (cm s- + s.e.m.1, at the beginning (first trial) and end (fourth trial) of each
treatment block, of the birds that experienced the two treatment distributions in different orders (dispersed first versus
clumped first).
clumped prey are experienced first, the birds slow down with more experience of a particular
treatment, but this effect of experience is not affected by treatment.
4. Discussion
In summary, the starlings in our experimental set up appear to use markedly different search
strategies dependent on which of the within-patch distributions of prey are experienced first. This has
generated the observed three-way interaction between the effects of the order in which the treatments
are experienced, the actual treatment experienced and how much experience the birds have had on the
treatment. The results indicate that, if the prey are dispersed within a patch when the experimental set
up is first encountered, then starlings use a fixed rule (i.e. that is unaffected by experience of our
manipulations) that results in moving relatively slowly and turning more when the prey are clumped
within a patch. On the other hand, when prey are clumped within a patch on first encounter, the
starlings appear to use a more flexible rule (i.e. that is mediated by experience of some aspect of our
manipulations) that means that starlings start on a particular prey distribution by moving relatively
quickly and turning relatively little. They then slow down (show orthokinesis) and turn more (show
156 S.R.X. Dull, .C. Curhill/ Beha~iorrrul Processes 39 (1997) 149-159
klinokinesis) with experience of the patch type. When following this strategy these starlings do not
appear to show distribution-specific search (Figs. 1 and 2).
There are a number of important implications of these results. At a general level, it appears that
starlings can use quite different within-patch search strategies under different circumstances. At first
glance, this is not totally surprising since European starlings are very generalist feeders, exploiting a
wide range of food and habitat types (Feare, 1984; Tinbergen, 1981). Intuitively, then, one might
expect a range of search strategies to be used. It is difficult to predict a priori, however, whether the
best thing to do as a generalist is to have a range of specific rules for each resource type, or whether a
general rule that does well enough on average will suffice. This will only be established by assessing
how different the specific strategic requirements are for the different resource types, how much using
one strategy will interfere with the foragers ability to use an alternative, and how costly this
interference will be. The results of such assessments will have important implications for both the
value of having a range of specific rules (sensu the value of information; Stephens, 1989) and the
associated costs (see Dal1 and Cuthill, submitted).
The results of this experiment suggest that starlings may utilise a repertoire of different strategies in
different contexts. This is a valid generalisation since prey that are found in similar habitats but are
just distributed differently (i.e. the situation that the set up here was meant to simulate) will be most
likely to be those for which the value of having a repertoire will be out-weighed by the associated
costs. The costs are likely to be high because, with few or no cues as to when to expect a certain type
of prey, chances are that a specific rule for one type will drastically reduce the ability to exploit
another. If context specific-search strategies are used in such instances then it is likely that there will
be other distinct strategies that will be used in contexts where there are fewer potential costs. For
instance, when European starlings are foraging for fruit in orchards (Feare, 1984; Tinbergen, 198 1)
the resultant lost opportunities to exploit top soil invertebrates are less likely to be important for
moment-by-moment decision making.
What is less clear is why these starlings responded strongly to the order of experiencing the
different prey manipulations, and not very strongly (if at all) to the actual within-patch prey
distributions presented. One possibility is that the first experimental distribution experienced deter-
mined how spatially predictable the experimental food source (i.e. patch) was perceived, and that
this determined the search rule used. Thus, experiencing the clumped treatment first might have
caused the birds to perceive the experimental patch as providing a relatively unpredictable supply of
food in space. This could be because, although the numbers of prey per cell in the patch were
determined according to a negative binomial distribution (q.u.), which cells contained which numbers
of prey were determined randomly at the beginning of each trial (i.e. there was a high variance in
intake per unit area). In addition, although finding a prey item in this treatment means that there is a
high probability that further prey will be found in the same cell, captures provide less information
than in the dispersed treatment because the location of prey in space is stochastic rather than
deterministic. Thus, if the birds are using local cues (e.g. the frame) to monitor spatial position, they
could perceive the clumped treatment as more unpredictable than the dispersed treatment. Where food
is relatively unpredictable in space, it might be best to search so as to cover as much of the potential
food source as possible when you have relatively little experience of a situation, and to concentrate
search more as you acquire information about where prey are likely to occur. For such a scenario, the
starlings presumably perceived a change in the set-up between treatment blocks but reacted as if the
food source had become less predictable again (hence the lack of significant treatment effects for
S.R.X. Dull. .C. Cuthill /Behacioural Prwesses 3Y (1997) 149-1.59 157
these birds). Perhaps following a relatively capture-independent search rule upon encountering the
dispersed treatment meant that a high enough level of unpredictability was perceived to warrant the
continued use of the rule.
When the food source is considered relatively predictable in space, as it might have been where the
dispersed treatment was experienced first, the best thing to do might be to follow a fixed search rule.
A rule that could have generated the observed search patterns might be: when a prey item is found,
slow down (show orthokinesis) and turn more (show klinokinesis) for a certain period of time (or area
searched), otherwise move quickly and turn less. Indeed, such rules have been suggested to account
for the commonly observed phenomenon of area-concentrated search (Benhamou, 1992). Because this
rule was being used when the clumped treatment was first experienced, and such a rule will perform
well for aggregated prey distributions (Benhamou, 19921, perhaps the food source was still perceived
as predictable enough to warrant the maintenance of such a rule.
If the starlings in our set up are responding to the spatial predictability of the experimental food
source (patch) in the way suggested above, then perhaps for the general foraging task investigated
(foraging for top soil invertebrates (Feare, 1984; Tinbergen, 198 1)) resource types (sensu Stephens
and Krebs, 1986) are defined by their spatial predictability. It may be that starlings define particular
areas of grassland as types on the basis of their spatial predictability (relative to local cues) and use
relevant search strategies when foraging on them. If this is the case then the importance of
understanding how animals categorise their worlds for the relevant application of much foraging
theoretical work cannot be emphasised enough. Also since theoretical findings indicate that general
search strategies for continuously patchy environments need not be distribution-specific in order to be
generally effective (Benhamou, 19921, perhaps it is not surprising that the search behaviour shown by
the starlings here was not sensitive to experience of this prey characteristic. Prey that can only be
detected at relatively short distances (as they were here) are likely to be perceived as continuously
distributed (Arditi and Dacorogna, 1988; Benhamou, 19921, even when confined to obviously
delimited regions of the habitat. Little can be speculated from our results, however, regarding the
timescale over which such search rules may be utilised by starlings in the wild. Further investigation
is necessary for both confirmation of the existence of such rules and insight into the ecological
timescale over which they are implemented.
The implications of these findings for the prevalence of random within-patch search are less
extensive. At first glance, perhaps the predictions of the marginal value theorem (MVT; Chamov,
1976; Parker and Stuart, 1976) are pertinent to this type of patch use problem for European starlings
since clear, systematic search within patches was not observed. Little can be concluded, however, due
to the lack of gain functions for the birds foraging in the artificial patches. Indeed, even search paths
that appear to contain a large random component have been known to generate strikingly linear gain
functions for house sparrows (Getty, personal communication). Also for other patch types (e.g. trees
containing insect larvae) presumably systematic search will be easier and the probability of revisiting
depleted sections of a patch minimised. Where the resultant gain functions are linear other factors
may be more important in determining patch-use strategy (e.g. obtaining information; Beachly et al.,
1995).
In conclusion, it is hoped that these findings have at least highlighted the importance of the detailed
investigation of generalist foragers responses to manipulations of potential prey type characteristics
such as spatial distribution. Not only have such investigations got important implications for the
determinants of diet width and its dynamics (Dal1 and Cuthill, submitted), but they can also provide
insights into the factors that are used in the functional categorisation of such foragers niches. Such
understanding has profound implications for the application of much of the widely accepted foraging
theory. In addition, the difficulty in qualifying the assumptions underlying this theory has been
highlighted by our discussion, with, specifically, both observed gain functions and quantified search
paths indicated as necessary to qualify the generality of patch depression and random search for the
relevance of the MVT.
Acknowledgements
We are grateful to Simon Benhamou for detailed comments on an earlier version of this
manuscript, and to Tom Getty for discussing his unpublished work with us. SRXD was supported by
a Natural Environment Research Council (NERC) research studentship.
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