Research article

Density-dependent habitat selection in migratory

passerines during stopover: what causes the deviation

from IFD?

E. SHOCHAT1,2,*, Z. ABRAMSKY1,2, B. PINSHOW1,2

and M.E.A. WHITEHOUSE2

1Department of Life Sciences, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva 84105,

Israel; 2Mitrani Department for Desert Ecology, Jacob Blaustein Institute for Desert Research, Ben-

Gurion University of the Negev, Midreshet Ben-Gurion 84990, Israel

(*author for correspondence, address: Center for Environmental Studies, Arizona State University,

P.O. Box 873211, Tempe, AZ 85287-3211, USA, e-mail: eyal.shochat@asu.edu)

Received 21 June 2001; accepted 14 June 2002

Co-ordinating editor: P. Lundberg

Abstract. We studied the distribution of migratory warblers (genus: Sylvia) in poor and high

quality habitat patches at a stopover site in the northern Negev, Israel. The purpose of our study

was to test predictions based on the ideal free distribution (IFD) model by using a natural eco-

system which has a high turnover of individuals moving between unfamiliar foraging patches. We

trapped birds in two groves of Pistacia atlantica embedded within a coniferous forest. The fruit-

density ratio between these groves was 45:1. We compared bird density, body condition and habitat

matching (the ratio between bird density and resource density) at the two sites. To analyse the data

we integrated two approaches to density-dependent habitat selection: the isodar method and the

habitat matching rule. As predicted by the IFD model, we found that habitat suitability decreased

with bird density with a high correlation between warbler densities in the two habitat patches.

Contrary to IFD predictions, warbler density in the poor patch was higher than expected by the

habitat-matching rule. This habitat under-matching, had a cost: in the rich habitat the average

energy gain per individual bird was higher than in the poor habitat. Further analysis suggests that

the apparent habitat under-matching is not due to interference or differences in warbler competitive

abilities. Therefore, we suggest that this migratory bird community is not at equilibrium because

the birds possess imperfect knowledge of resource distribution. We propose that this lack of

knowledge leads to free, but not ideal distributions of migrant birds in unfamiliar stopover sites.

Key words: density dependence, habitat matching, habitat selection, ideal free distribution, non-

equilibrium, stopover

Introduction

The ideal free distribution (IFD) model (Fretwell and Lucas, 1969) describes an

evolutionary stable strategy for the distribution of organisms across habitats or

resource patches that maximizes individual fitness or payoff. It assumes that

Evolutionary Ecology 16: 469–488, 2002.� 2002 Kluwer Academic Publishers. Printed in the Netherlands.

competition increases as more individuals compete for resources in a given

patch. Consequently, it would pay for some of the competitors to move to a less

profitable habitat or patch. In such a patch the accompanying lower level of

competition would compensate for the lower resource density. The process of

density-dependent habitat selection thereby results in equal fitness of foragers

across all patches. The concept of density-dependent habitat selection has

provided major advances in ecological studies and has given the impetus for

further theoretical developments (Fretwell, 1972; Morris, 1987, 1988, 1989;

Milinski and Parker, 1991). However, while many studies claimed to support

the IFD model, it has been criticized, as many organisms from different taxa

deviate from its predictions (for review see Kennedy and Gray, 1993).

Two approaches to study the density-dependent habitat selection are the

isodar method and the habitat-matching rule. The first, the isodar method, is

based only on density surveys. The original isodar theory, applied to IFD, was

developed to overcome the problem that fitness is impossible to measure in

most cases (Morris, 1987). It assumed that animals are ideally and freely dis-

tributed in two habitats that differ in resource density, and therefore that

animal densities in the two habitats are highly correlated. The regression line

that describes the relationship between the density of individuals in two ad-

jacent habitats is a line of equal fitness (an ‘isodar’ sensu Morris, 1987, 1988).

The intercept and the slope of the isodar are the estimators of the quantitative

and the qualitative differences between the habitats (Morris, 1987, 1988).

The second approach, the resource-matching rule (Parker, 1978) rephrased

as the habitat-matching rule (Pulliam and Caraco, 1984), is based on habitat or

patch quality in terms of resource distribution across habitats/patches. If fit-

ness or payoff is equal across habitats or patches and among all individuals,

then the distribution of the resources in the environment must correlate with

the distribution of consumers. The result is that the ratio of consumers across

habitats/patches should match the ratio of resources.

The application of the IFD model to short term studies that measured in-

stant payoff across resource patches led to misconceptions of the IFD (Treg-

enza, 1994). A basic assumption of the habitat-matching rule that has been

repeatedly ignored is that habitat matching is only expected when there is

‘continuous resource input’ (Morris, 1994; Tregenza, 1994; Sutherland, 1996).

In this situation resources that are repeatedly added to the environment are

immediately consumed by foraging individuals (Parker, 1978). But even under

experimental conditions of continuous resource input, an under-matching be-

tween the densities of the resources and the consumers in two foraging patches

of different qualities has been reported (e.g. Gray, 1994; Gray and Kennedy,

1994; Kennedy, et al., 1994). It is apparent from these studies that, even under

simplified conditions, some basic assumptions of the IFD theory are violated.

These violations include unequal competitive abilities of the foragers (Parker

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and Sutherland, 1986; Houston and McNamara, 1988), interference (Suther-

land, 1983), and imperfect knowledge of resource distribution (Abrahams,

1986). Kennedy and Gray (1993) also suggested that travel costs may cause

deviations from the IFD (but see Astrom, 1994).

There are two additional assumptions that are often violated by foraging

animals. One is that individuals are ideal, i.e. possess perfect information about

the amount of resources in the environment. The second is that they are free to

select where to forage in order to maximize their fitness. The first assumption

of complete knowledge of the neighbourhood is permissible when individuals

live at one site all their lives and when habitats are adjoining, at least at the

scale of the organism studied. However, it is readily violated when animals are

exploiting an unfamiliar habitat. Abrahams (1986) showed in a simulation

model (the perceptual limit model) that imperfect knowledge can affect animal

distribution in two or more habitats. The model predicts an increase in habitat

under-matching as the population grows, since more foragers allocate them-

selves randomly between sites. In Abrahams’ model, consumer densities always

under-match the resources since individuals over exploit the poor habitat.

Can an IFD be achieved in an unfamiliar environment, and can it be main-

tained as new individuals keep arriving and departing? This question is of par-

ticular relevance to migrating birds during their brief stopovers to rest, forage,

and replenish fat reserves, suggesting that migrating birds may provide a good

system to test Abrahams (1986) perceptual limit model. Firstly, migrating birds

arriving at unfamiliar foraging habitats may not be able to assess differences

between them. They may not posses any knowledge about resource distribution

across the habitats, and they do not have time to gain sufficient knowledge.

Secondly, bird densities at a habitat can change rapidly. Migration waves of

different populations, or even changes in weather conditions, may cause dra-

matic changes in bird densities at the same site within days or even hours.

Thirdly, the rapid turnover of individuals prevents pseudoreplication. Many

studies on IFD used the same individuals at different resource densities. As

shown byMilinsky (1994) past experiencemay bias habitat use by individuals, or

affect movement between patches. The high turnover of individuals at stopover

sites enables quick, repeated sampling at the same stopover site of completely

new individuals. This can be easily confirmed by marking individual birds.

Most importantly, the payoff of foraging on different patches can be mea-

sured. Density-dependent habitat selection should work in the short term just

as it does in the long term because there must be a connection between im-

mediate rewards and the long-term fitness of individuals (Kennedy and Gray,

1993). Therefore, though fitness is hard to measure, any of its short-term

components, like changes in body mass or fat stores, would be appropriate.

This is especially true for migratory birds. According to the optimal migration

theory there is a major importance for food-rich stopover site selection in order

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to minimise predation risk and to maximise the speed of migration and energy

economy during migration (Alerstam and Lindstrom, 1990). High fat deposi-

tion rate is especially important in our case since for many migrants, the

northern Negev represents the last opportunity to refuel before crossing the

Saharan desert. On their southbound migration, birds that do not manage to

store enough fat may not complete their journey and perish. Therefore, rapid

fat deposition has an important role in natural selection (Alerstam, 1990).

We studied habitat selection among migratory passerines during autumn

migration in two stopover sites. These sites were Pistachio groves that differ in

fruit density. It has been shown that fruits, rather than insects, are often the

main source for fat gain in passerines during migration (Fry et al., 1970; Izhaki,

1986). Our goal was to test whether habitat selection by ‘naive’ warblers is a

density-dependent process, in which birds trade-off between food density and

competition. According to the perceptual limit model predictions (Abrahams,

1986) we hypothesized that bird distribution would be free but non-ideal. This

may emerge from imperfect knowledge about the environment due to insuffi-

cient time to gain that knowledge. Consequently, we predicted that: (1) the poor

habitat would be over-exploited and (2) deviations from habitat matching

would increase with bird density. We also tested a second hypothesis, that over-

exploitation of the poor habitat has a cost (fitness in the poor habitat should be

lower than in the rich one). We predicted that the overall average body con-

dition in the poor habitat would be lower than in the rich one, due to a lower

energy gain. This important outcome of over-exploitation has not been inves-

tigated in any of the continuous input studies.

Methods

Study area

Our study was done in the Lahav forest, northern Negev, Israel. The mostly

coniferous Lahav forest has been planted by the Jewish National Fund since

1956 in a semi-arid zone about 10–20 km north of Beer-Sheva. During the last

15 years broad-leaf groves were planted, mainly in the southern part of Lahav

woods. These included several Pistachio orchards that yield fruit during the

autumn, and therefore serve as an important habitat for migratory passerines

during stopover (Sapir, 2001). We studied habitat selection in two Atlantic Pis-

tachio (Pistacia atlantica) groves surrounded by coniferous lots. Both Pistachio

stands were planted in 1981, and are of the same size (about 4 ha). The distance

between them is about 1 km. For an unknown reason, the trees in one grove, plot

20, were rich in fruits during the study period, while those in plot 19 bore very few

fruits. Hereafter, we define these groves as the rich habitat and the poor habitat.

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Studied species

From among the large variety of passerine species captured, we concentrated

on two groups: warblers of the genus Sylvia, and chats (family: Turdidae).

Although both groups are known to be mostly insectivores, analysis of drop-

pings and observations on feeding birds (Sapir, 1999, 2001) revealed that

during stopover, warblers fed mainly on Pistachio berries, while chats fed

mainly on insects. Since we did not quantify insect density, we were unable to

correlate resource densities and chat densities.

Bird sampling

In autumn 1995 we sampled birds using mist nets in the rich habitat. Mist

netting was conducted on 19 days between 17/8 and 18/11. In Autumn 1996

birds were sampled in the rich habitat for 19 days between 27/7 and 30/11. In

15 out of the 19 days (between 5/8 and 9/11) birds were also sampled in plot 19

(the poor habitat). In each plot, 96 m of mist net were opened from first light

for 4 h. Birds were collected every 30 min. For each bird we recorded species,

wing length (an estimator for body size), body mass, and fat score on a scale of

0–5. According to the sampling method, all densities are given as (number of

birds)/(96 m mist net · 4 h).

Resource density

We estimated fruit density by counting the number of fruiting trees in each

plot, assuming that variation between trees was not different between plots.

There were 179 fruiting trees in the rich habitat and only four in the poor

habitat. These numbers were constant between years and throughout Autumn

1996. Therefore, the resource ratio between the two plots was 45:1 in favour of

the rich plot. A more precise estimation of fruit density in autumn 1998 also

confirmed this resource ratio (Sapir, 2001). Kennedy and Gray (1993), and

Kennedy et al. (1994) noted that in order to detect deviations from habitat

matching, several resource ratios between two habitats should be used, in-

cluding extreme differences between food density in the two habitats. In our

two sites, however, we had to deal with a given permanent situation.

Evaluating body condition

Usually energy gain is evaluated in birds by measuring changes in the body

mass of recaptured individuals. However, the number of birds we recaptured

during 15 sampling periods was too low for statistical analysis. Therefore we

evaluated body condition by using two methods. First, we measured fat score

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(from 0 to 5) for each bird captured by checking the amount of fat present in

the sternum fat reserves.

Next, we regressed body mass vs. wing length for each species and used the

residuals of the regression to indicate body condition for each individual. We

defined the ‘body condition index’ of an individual as the residual value of its

body mass divided by the expected value (obtained from the regression). We

found that the residuals were highly correlated with the fat score (For Black-

cap, the most common species n ¼ 94, r ¼ 0:74, p < 0:001), indicating that

after removing the effect of body size, higher body mass is largely the result of

increased fat storage. However, since the fat score is measured on an arbitrary

scale (0–5) it is not normally distributed. In contrast, the normal distribution of

the calculated body condition index makes this method appropriate for sta-

tistical analysis. We plotted (for each day) the average value of the body

condition index against density (suitability lines, Fretwell and Lucas, 1969).

Habitat selection

We used the isodar method (Morris, 1987) to evaluate quantitative and qual-

itative differences between the two groves. We further tested whether habitat

matching best fit the predictions of a continuous input or a consumer-resource

model (i.e., a situation where consumers forage over a very large scale, and

resource renewal may exceed the intake rate of single individuals). In partic-

ular, Morris (1994) suggested that the consumer-resource model would yield a

linear isodar on an arithmetic scale, whereas the continuous input yields a

linear isodar on a logarithmic scale.

Statistical analysis

Linear regressions were applied to data which were normally distributed. We

followed Dixon (1950 in: Sokal and Rohlf, 1981) to detect and remove outliers.

Results

During our census, we recorded nine species of Sylvia warblers (common and

scientific names are given in Appendix 1) of which three species were wide-

spread: Lesser Whitethroat, Blackcap and Orphean Warbler (Appendix 1). In

1995 bird densities in the rich habitat were much higher than in 1996 (Table 1,

n ¼ 19, t ¼ 4:073, p ¼ 0:001). Among the warblers – Blackcap, Lesser White-

throat and Common Whitethroat were significantly more abundant in 1995.

There were no significant differences in the densities of Orphean Warbler be-

tween years.

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In 1996, the total bird species densities in the rich habitat were significantly

higher than in the food-poor one (Table 1, n ¼ 15, t ¼ 5:293, p < 0:001). In the

food-rich habitat all three widespread species of warblers were significantly

more common than in the food-poor habitat. We tested whether the differences

in bird densities were due to differences in fruit densities between the rich and

the poor plot.

Temporal migration patterns

Five common species of chats stop over in Lahav woods during autumn:

Rufous Bush Robin, Black-eared Wheatear, Common Redstart, Robin and

Black Redstart (scientific names are given in Appendix 1). We excluded chats

from the habitat selection data analysis for two reasons. First, analysis of feces

showed that the diet of those species that were present at very high densities in

the groves, consisted mainly of insects (Sapir, 2001). Furthermore, direct ob-

servations revealed that all of them are highly territorial (Sapir, 2001). During

stopover, inter- and intra-specific aggressive encounters were frequently seen.

These negative interactions suggested that in general, chats were not free to

select their habitat.

It is hard to asses whether the seasonal partitioning of the chats at the study

site (Fig. 1a) is a result of different distances of the breeding and/or wintering

grounds from the study site, or a direct result of competition (e.g. Abramsky

and Safriel, 1980). The negative relationship between the two most com-

mon chats during the short period of overlap (Common Redstart density¼95.2 � 64 · [log] Black-eared Wheatear density, n ¼ 9, r2 ¼ 0:73, p ¼ 0:024)

suggests that aggressive interactions may explain to some extent the observed

pattern.

Table 1. The number of sampling days and bird densities in stop over sites in Lahav woods during

autumn 1995 and autumn 1996. The number of birds includes all species trapped.

1995 1996 1996

Habitat Rich Rich Poor

Sampling days 19 19 15

Period 17/8–23/11 27/7–30/11 5/8–9/11

Birds/day (SE) 82.0±(7.61) 46.4±(5.24) 11.0±(1.12)

t-test Between years (Rich habitat) Between habitats (1996)

n 19 15

t 4.073 5.293

p =0.001 <0.001

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In contrast with chats, warblers fed mainly on fruits and occasionally on

insects. Moreover, they seldom showed aggressive behaviour (Sapir, 1999,

2001). Often, a few individuals of the same or different species were seen

feeding on the same branch. Unlike the chats, the migration waves of the two

most common warblers, Lesser Whitethroat and Blackcap, overlapped. The

migration waves of these two species also coincided with those of Orphean

Warbler during early migration (Fig. 1b). The densities of Blackcap and Lesser

Whitethroat were positively correlated (Blackcap density ¼ 6.93 + 0.77 ·Lesser Whitethroat density, n ¼ 18, r2 ¼ 0:66, p < 0:01).

These differences in migration patterns between chats and warblers are im-

portant since they suggest that warblers do not interfere with each other.

Therefore, rather than interference competition, it is more likely that warblers

Figure 1. Changes in species densities with time in the food-rich Pistachio grove in the Lahav forest

during autumn 1995 for (a) five common species of chats (family: Turdidae) and (b) three common

species of Warblers (genus: Sylvia). Similar patterns were observed in autumn 1996.

476

experience scramble competition (where all individuals have an equal chance of

acquiring food, and obtaining food depends largely on order of arrival at the

resource; Nicholson, 1954). In other words, warbler distribution seems to be

free. The question is whether it is ideal.

Habitat selection

The simultaneous migration of Sylvids, the lack of interference and the

similar diet of the species studied, suggested that density-dependent habitat

selection should be studied at the genus, rather than at the species level. That

is, if density-dependent habitat selection exists, newly arriving individuals

selecting a habitat should consider the number of all Sylvids in the habitat,

rather than just the density of their own species. Because we did not notice

any inter- or intra-specific negative interactions between warblers, we con-

cluded that scramble competition is more likely in warblers than interference

competition. Therefore, we calculated a ‘guild’ isodar and suitability lines for

the whole Sylvia genus, rather than for each species on its own. Previous

studies on migratory warblers (reviewed by Hutto, 1985) have also shown a

high correlation between resources and bird ‘guild density’ rather then a

single species.

Suitability

To test whether habitat selection was density dependent, we calculated habitat

suitability by regressing bird body condition against bird density. In 1995 we

found a significant negative correlation between Sylvid densities and the av-

erage body condition of the birds in the rich plot (linear regression, n ¼ 19,

r ¼ �0:47, p ¼ 0:022) (Shochat, 1999). In 1996 we sampled birds in both the

rich and the poor habitats. Expected body mass and average fat score of

Sylvids decreased as density increased in both plots, while the regression lines

diverged (Fig. 2a). This indicated that the density-dependent effect is stronger

in the poor plot. The fit of the suitability line in the rich habitat is low

(r2 ¼ 0:195), suggesting that body condition is also affected by other factors,

not only competition.

Under IFD, one would expect that on any given day the average body

condition of birds in the two habitats would be equal. Therefore, connecting

densities of the same day on the suitability lines of the two habitats should yield

lines parallel to the x axis. However, in 12 cases, the average body condition in

the rich plot was higher than in the poor plot (Fig. 2b, paired t-test, n ¼ 13,

t ¼ 4:46, p ¼ 0:001), suggesting that indeed, distribution was not ideal-free.

The opposite trend was observed only on 1 day, when densities and sample

sizes were low.

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Isodars

Quantitative and qualitative differences between habitats can be detected by

the isodar method (Morris, 1988; Ovadia and Abramsky, 1995). We found a

very high correlation between the density of Sylvids in the rich and the poor

habitat (Fig. 3a). The quantitative difference between the plots (intercept) is

about five birds/(96 m net · 4 h). This means that according to the regression

model the first bird entered the poor habitat when there were five birds already

in the rich one. The slope of the isodar, about 2.5, reflects the divergence of the

Figure 2. (a) The relations between body condition index and warbler densities (suitability lines

sensu Fretwell and Lucas 1969) in both food-rich and food-poor groves in autumn 1996. The

average body condition of warblers decreased as their density increased in both groves. The two

suitability lines diverge, suggesting that in the food-poor grove, any new individual entering has a

higher negative effect on other individual’s energy gain, compared with the food-rich grove. (b) The

same data as in 2a, with lines connecting data that were collected on the same day in the two groves.

On all but 1 day the average body condition was higher at the food-rich patch. Two points are

missing for the food-poor plot, one with no warblers trapped (seven warblers in the food-rich

patch), and another removed as an outlier (11 warblers in the food-poor patch and 37 in the food-

rich patch).

478

suitability lines in the two habitats. It indicates that for each five birds that

enter the rich habitat, two birds enter the poor habitat. By using the equations

of the suitability lines (y ¼ 1:06� 0:002x and y ¼ 1:01� 0:007x for the rich

and the poor habitat respectively), we calculated the expected densities of

warblers in the poor plot under IFD (Fig. 3a). According to this calculation

birds should start to use the poor habitat when the overall density is much

higher (about 25 birds in the rich plot instead of five, as indicated by the

intercepts of the expected isodar and the observed pattern).

To evaluate whether fruit distribution in the study site follows a continuous

input situation, we compared the shape of the ‘density correlation’ line on an

arithmetic scale (Fig. 3a) with that on a logarithmic scale (Fig. 3b). If input of

resources is continuous, an isodar should be linear on a logarithmic scale

Figure 3. (a) Following the isodar method there is a high positive correlation between the densities

of warblers in the two plantations. The intercept indicates the average total density in which

individuals start to occupy the poor habitat. The slope indicates the divergence shown in 2a. The

expected isodar under IFD is also shown, suggesting that the observed line is not a line of equal

energy gain (see text for more details). (b) The same correlation between warbler densities in the

two plantations on a logarithmic scale. Correlations on both arithmetic and logarithmic scales are

high, with a better fit (r2) on the logarithmic scale. This may suggest that fruits ripen according to

the continuous input, rather than the consumer-resource model.

479

(Morris, 1994). When we plotted the warbler density in the rich plot against the

warbler density in the poor plot, the fit (r2) of the regression line on logarithmic

scale was better than on the arithmetic scale (Fig. 3). This trend did not change

after removing Sardinian Warbler densities (a resident species in the Lahav

area which may bias in density measures by having a high site fidelity, data not

shown). The better fit on logarithmic scale may suggest continuous input (i.e.,

fruits ripen and are eaten by birds immediately). Note however that both

regression lines in Figure 3 yield a very high fit (r2) and that the differences

between the r2 of the two regression lines are small so that this suggestion is

only weakly supported by the data (see Discussion).

Resource matching

As mentioned earlier, the ratio between fruit densities in the two groves was

45:1 (log ratio ¼ 1.65). Under an IFD, the ratio of resources per individuals in

the two habitats should be equal. Subsequently, based on predictions of the

resource-matching rule, we tested whether the average ratio between warbler

densities was equal to the ratio between resources. We assumed that the two

groves did not differ in predation risk, and that birds were distributed ac-

cording to food abundance. This assumption is supported by a long-term study

on bird abundance in the studied groves (Sapir, 2001).

In contrast to the habitat-matching rule predictions, we found that on all

15 days, the ratio between warbler densities (0:58� 0:13) was lower than

the ratio between resources, indicating habitat under-matching (CI0:001;13 ¼0:53� 0:99). Thus it appears that the poor habitat was over-exploited (more

individuals than expected by IFD). Consequently, we hypothesized that there

must be a cost for over-exploitation.

We tested whether there was a cost to over-exploitation of the poor habitat

by comparing the average body condition of birds on each day between the two

habitats. We found that the average body condition index of warblers in the

food-poor plot (1.02) was significantly lower than in the food-rich plot (0.97)

(ANOVA, n ¼ 15, r2 ¼ 0:418, p ¼ 0:024), suggesting that average energy gain

in this habitat was lower.

The observed habitat under-matching pattern could be a consequence of

unequal competitive abilities since the different species of warblers differ sig-

nificantly in body size. Therefore, in order to compensate for a possible bias of

unequal competitive abilities, one should consider biomass rather than densi-

ties when checking if consumers match resources. In order to ascertain whether

differences in competitive abilities may have caused the deviation from IFD, we

calculated the total bird body mass ratio between the rich and the poor habitats

for each day. We then tested whether the values matched the resource ratio

between the habitats. We used here the expected body mass of each individual

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which was calculated by regressing the body mass against wing length and not

the observed mass values, since the observed values are affected by density

and by habitat. This compensation for body mass did not change the ob-

served pattern of habitat under-matching when comparing the densities

(CI0:001;13 ¼ 0:53� 0:23).

One of the predictions of the perceptual limit model (Abrahams, 1986) is

that deviations from IFD should increase with total consumer density. When

we plotted the deviations from habitat matching against densities, we found

a significant positive relationship (linear regression, r2 ¼ 0:249, p ¼ 0:035;

Fig. 4a). To test whether this was caused by differences in competitive abilities,

we also used the deviations from habitat matching that were calculated by

using body mass instead of densities. As shown in Figure 5b, not only did the

observed pattern persist, the fit (r2) of the regression line is higher. It indicates

Figure 4. (a) The deviations from IFD increase with density, as predicted by the perceptual limit

model (Abrahams, 1986). The deviations were calculated using warbler densities. (b) When the

deviations were calculated using warbler body mass instead of warbler density, linear regression

yielded an even better fit. Therefore, taking into account unequal competitive abilities did not

compensate for the deviations from IFD.

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that after taking into account the competitive abilities of each species there is

still an increase in deviations from IFD with an increase in density.

Discussion

In this study we tested whether (1) there is a density-dependent process of habitat

selection among migratory passerines during stopover, and (2) whether imper-

fect knowledge of resource distribution leads to deviations from IFD as sug-

gested by Abrahams (1986). We found that at any given time there were more

birds in the rich habitat than the poor habitat. Yet the distribution of birds was

not ideal free; habitat under-matching (the poor habitat was over-exploited) was

evident. The degree of under-matching may be even greater than we estimated.

When calculating the ratio between resource densities at the two sites we did not

take into account rapid fruit depletion in the poor habitat. It may result in an

even higher resource density ratio than we reported. Still, the habitat under-

matching led to a fitness cost in the poor habitat, where the average body con-

dition of the birds was worse than that of birds in the rich habitat.

Can these deviations from the IFD be explained? The habitat matching rule is

only expected when resource input to the environment is continuous. In the

absence of a continuous input situation, the habitat matching rule is violated no

matter how the birds are distributed (Tregenza, 1994; Sutherland, 1996). Fol-

lowing Morris (1994) our results suggest that there is a continuous input of fruit

in the Pistachio groves (Fig. 3). However, since the correlation between warbler

densities in the two groves was highly linear on both arithmetic and logarithmic

scale, this interpretation should be made with caution. It seems that it is difficult

to obtain a clear separation between continuous input and resource–consumer

situations by this method. Morris (1994) also used isodars to study rodent dis-

tribution and he too found small differences between isodars that were plotted

on arithmetic and logarithmic scales. However the continuous input of re-

sources, which is an excellent experimental variable to use in the study of animal

distribution among foraging patches, is a rare situation in nature (Morris, 1994;

Tregenza, 1994; Sutherland, 1996). Moreover, in the Pistachio groves in Lahav

woods, the dynamics of fruit ripening is slow and continuous throughout the

autumn, unlike in a continuous input situation (Sapir, 1999, 2001). Therefore, it

is likely that fruit ripening dynamics and their consumption by warblers may be

more closely approximated by the consumer–resource model (Morris, 1994).

Since fruit renewal at the rich habitat exceeds the intake rate by warblers it

violates the IFD assumption of a continuous input of resources.

Can the lack of resource-matching between the two groves be explained by

the lack of continuous input of fruits in the Lahav Pistachio groves? To address

this question, animal distribution under different situations should be com-

482

pared. Tregenza (1994) explained how interference influences the directions of

deviations from habitat matching. According to him, high interference should

lead to over-exploitation of the poor habitat, whereas low interference will

cause under-exploitation of the poor habitat. When there is no interference

competition and no continuous input of resources, foragers may not enter the

poor habitat even when densities are high, since they are free to enter the rich

habitat (Tregenza, 1994). As we found no evidence of interference competition

in this study, we would expect most birds to use only the rich habitat at low

bird densities, while at very high densities the birds should under-exploit the

poor habitat. The results, however, show that at any population density there

is always an over-exploitation of the poor habitat. Consequently the lack of

continuous input is not sufficient to explain the deviations from IFD.

Since there is no interference, the question should be whether there is

competition at all. In other words: is there a density-dependent habitat selec-

tion process in the Lahav woods? The results support the idea that habitat

selection during migration is density dependent: as density increases, there is a

decline in average body condition (Fig. 2). These differences should be inter-

preted with caution, since fat storage may represent fat depositions in remote

sites north of ours. However, data from other sites in the study area, from both

spring and autumn indicate that in most cases body condition is negatively

correlated with density (Sapir, 2001; Shochat, unpublished). Specifically in this

study, we had no reason to assume that factors that bias body condition will

behave differently in the two groves. Therefore, it appears that density has a

strong effect, which concurs with other studies on different bird species at

stopover sites (e.g. Hansson and Petterson, 1989; Moore and Yong, 1991). We

also found a strong link between densities in the two habitats (Fig. 3), despite

the distance between them. In addition to the very high correlation, the slope of

the isodar in Figure 3 indicates the divergence of the suitability lines in

Figure 2, and exemplifies the strength of the isodar method as a tool to assess

qualitative differences between different habitats (Ovadia and Abramsky,

1995). However, the regression line that describes this correlation is not an IFD

isodar since each point on the line always represents lower fat gain in the poor

habitat. Such a linear relationship between densities is possible not only when

fitness in the two studied habitats is equal, but also in cases where fitness, or

energy gain, in one habitat is linearly correlated with fitness/gain values in the

other habitat (Morris, 1994).

In this study we applied for the first time a ‘guild’ isodar (Fig. 3). Following

Hutto (1985), who found a pattern of habitat matching only when he used the

densities of all warbler species and compared it with insect density, we suggest

that when there is no interference, this can be done also when plotting an

isodar and when species with a similar diet coexist in the same space at the

same time. Such a case can also agree with the ‘shared habitat preference’

483

(Pimm et al., 1985) where all species show the same primary and secondary

habitat preference. Regelmann (1984) and Houston and McNamara (1988)

showed that after all the large individuals or good competitors distributed

themselves ideally in two habitats, smaller individuals or bad competitors can

in turn distribute themselves according to the densities of the large ones. This

may be the case whether interference is taking place or not.

The deviations from IFD found here are not the result of interference. Two

alternative explanations for the deviations can be either unequal competitive

abilities (such as those that occur during scramble competition; Parker and

Sutherland, 1986; Houston and McNamara, 1988) or imperfect knowledge of

resource distribution (the perceptual limit model; Abrahams, 1986). Separating

these two models is difficult. The perceptual limit model (Abrahams, 1986) has

two major predictions. One is that the bias in densities will always be towards

the poor habitat. The second prediction is that an increase in the overall density

should increase the degree of under-matching, because more and more indi-

viduals will randomly select where to go. In contrast, Parker and Sutherland

(1986) showed how competitive abilities can be matched to the food input ratio,

by either density under- or over-matching. Houston and McNamara (1988)

further developed this model and demonstrated that in most cases of unequal

competitive abilities the overall distribution of consumers will under-match the

input ratio. According to their model, the degree of under-matching should be

higher at high overall consumer density. Therefore these two models (perceptual

limit and different competitive abilities) have more or less the same predictions.

The systematic bias we found towards the poor habitat and the tendency of

the deviations to increase with total bird density (Fig. 4) agree with the per-

ceptual constraint model of imperfect knowledge (Abrahams, 1986). Though

there are differences in scramble competitive abilities between the warblers,

especially of different species, we found no evidence that the habitat under-

matching pattern was a result of these differences. However, imperfect

knowledge of the environment is more than the inability to evaluate slight

differences between patches of different resource densities. That is, individuals

in a new environment simply may not know their choices beyond their visual

horizon. How this fact affects their ability to discriminate between patches of

slightly different qualities remains unclear. The increase in deviations from IFD

as density increases (Fig. 4) may suggest a link between these two aspects of

imperfect knowledge: the perceptual limit (Abrahams, 1986) and the simple

lack of knowledge on where the food patches are, suggested here. At this stage

we have no idea how these are connected.

How would the distance between the two study plots lead to habitat under-

matching? Density-dependent habitat selection requires a choice between two

or more habitats. Most studies on IFD were conducted in two adjacent

patches. However, if each habitat patch is at equilibrium with its nearest

484

neighbour, one should expect an IFD and habitat matching across all patches

on a larger scale. This may be true in a landscape where all patches are suitable

for the individuals, although these patches may differ in quality. However,

when the area between two suitable patches is hostile, namely, the patches are

to some extent isolated islands, the densities of consumers in these patches may

under-match resource distributions. In our study, a local resource peak in the

environment may have led to the observed under-matching. Birds that landed

near the poor habitat may have stayed in it because the whole area around it

was completely hostile, and chances of moving to the rich habitat remained low

since it was not in sight. Regelmann (1984) also considered travel cost effects.

Though it did not affect the final distribution which appeared to be ideal free, it

affected switching rate of fish between two food patches. He also found dif-

ferences in switching rates between good and bad competitors.

In conclusion, our work indicates that equilibrium, as it is defined by the

IFD model (no individual gain by switching patch), is not likely to develop in

the short term in stopover sites of migrating birds. In the long term it is not

clear whether differences in body condition between habitat patches of different

qualities affect their total fitness. However, high fat depositions are crucial for a

successful journey to migrate over harsh conditions, i.e. the crossing of the

Saharan desert. Since body condition significantly differed between the two

habitat patches we studied, a direct effect on bird inclusive fitness is possible. In

terms of immediate pay-off, the results suggest that an IFD cannot be achieved

in an unfamiliar environment, and cannot be maintained as new individuals

keep arriving and departing. Yet, food density can be a good estimator of

migratory bird density. Furthermore, bird densities across habitat patches may

be highly correlated (even though the birds are not ideally distributed) yielding

a very high-fit isodar. Altogether, confirmation of an IFD may not only require

the study of animal distribution, but also research on body condition/fitness,

and on the distribution of resources. Among migratory passerines, we detected

an under-matching situation, resulting in a cost to birds in the fruit-poor

habitat. The resource under-matching appeared to be the result of imperfect

knowledge about the distribution of food patches. This suggests that temporal

communities formed during stop over are not ideally distributed. Such com-

munities may always be on the verge of, but never at equilibrium, since by the

time it takes a transient population to explore its environment, it would need to

move on and then would be replaced by another naive group.

Acknowledgements

Financial support for this research was provided by the Jewish National Fund.

We thank Ido Tsurim, Nir Sapir and Yoni Witztum for their assistance in the

485

field. We also thank Douglas Morris and Niclas Jonzen for comments that

greatly improved the manuscript. This is publication number 343 of the Mit-

rani Department of Desert Ecology.

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Common and Latin names of migrant warblers of the genus Sylvia and chats (family: Turdidae)

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