Behavioral Ecology Vol. 12 No. 2: 219-226
© 2001 International Society for Behavioral Ecology
Harvest rates and foraging strategies in Negev Desert gerbils
a Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel b Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, 84990 Israel
Address correspondence to O. Ovadia, who is now at Yale University, School of Forestry and Environmental Studies, 370 Prospect Street, New Haven, Connecticut 06511, USA. E-mail: ofer.ovadia{at}yale.edu .
Received 17 February 1999; revised 13 November 1999; accepted 4 September 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We examined the foraging strategy and quantified the foraging traits of two nocturnal rodent species, Allenby's gerbil (Gerbillus allenbyi) and the greater Egyptian sand gerbil (Gerbillus pyramidum). In the laboratory, both species used two distinct foraging strategies: either they immediately consumed seeds found in a patch (seed tray); or they collected and delivered the seeds to their nest box for later consumption. Moreover, we found a transition in foraging strategy among individual G. allenbyi under laboratory conditions; they all began by consuming the seeds on the tray and, after 7 days on average, switched to the collecting strategy. By contrast, in the field both species used only one foraging strategy; they collected and delivered the seeds to their burrow or to surface caches for later consumption. Furthermore, G. allenbyi and G. pyramidum collected seeds at significantly higher rates in the field than in the laboratory because the seed encounter rates for both species were higher in the field. This suggests that in natural conditions, probably involving predation risk and competitive pressure, gerbils must respond in two ways: (1) they must choose a foraging strategy that reduces predation risk by minimizing time spent feeding outside their burrows; and (2) they must forage more efficiently. In the field, seed handling time of the larger species, G. pyramidum, was shorter than that of the smaller one, G. allenbyi. This difference may give G. pyramidum an advantage when resource levels are high and when most of a forager's time is spent handling seeds rather than searching for more seeds. Additionally, our field study showed that the seed encounter rate of G. allenbyi was higher than that of G. pyramidum. This difference may give G. allenbyi an advantage when resource levels are low and when searching occupies most of the forager's time. The different advantages that each species has over the other, under different conditions, may well be factors promoting their coexistence over a wide range of resource densities.
Key words: coexistence, encounter rate, foraging strategy, functional response, handling time, harvest rate.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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It is becoming increasingly accepted that behavior can play an important role in determining the structure and the function of complex ecological communities (e.g., Fryxell and Lundberg, 1998
; Hassell and May,
1985; Sutherland,
1996). One fundamental and essential behavior for all animals is
foraging. Indeed, foraging theory was developed about 30 years ago to
understand community structure and function, and since then numerous aspects
of foraging behavior have been investigated
(Emlen, 1966;
MacArthur and Pianka, 1966;
Perry and Pianka, 1997;
Stephens and Krebs, 1986). Two
major focuses of foraging theory are foraging strategies (e.g., patch quitting
rules and diet selection) and foraging traits (e.g., handling time, encounter
rate and nutritional demands) (Stephens
and Krebs, 1986).
In many cases, an individual can use a wide range of foraging strategies.
Moreover, an individual may switch its foraging strategy in response to
environmental changes. Such adaptive foraging behavior is very important
because it can affect population persistence
(Henein et al., 1998),
interactions between species
(Hambäck and
Ekerholm, 1997; Holt,
1984; Holt and Kotler,
1987; Werner,
1992; Werner and Hall,
1989), and stability of the system
(Fryxell, 1997;
Schmitz et al., 1997).
Foraging traits, such as handling time and encounter rate, are the basic
elements of any foraging model that describes the interaction between a
consumer and its resources (Holling,
1959). Measuring foraging traits of different species allows
comparison between different patch use and diet selection strategies
(Brown and Mitchell, 1989).
Moreover, interspecific differences in foraging traits and consequently in
harvest rate, may be the basis for the coexistence between species in a
community (e.g., Armstrong and McGehee,
1980; Brown, 1989;
Kotler and Brown, 1988;
Vincent et al., 1996;
Waltman, 1983). For example,
coexistence between species might be due to differences in their harvest rates
while foraging on different substrates
(Hughes et al., 1995;
Price and Heinz, 1984), at
different resource densities (Brown,
1989), or under different levels of predation risk
(Kotler et al., 1994).
In order to understand the behavioral mechanisms that promote coexistence between two nocturnal gerbil species, Allenby's gerbil (Gerbillus allenbyi) and the greater Egyptian sand gerbil (Gerbillus pyramidum), we studied their foraging strategies and quantified their foraging traits under different environmental conditions: a laboratory and a field setting. The foraging strategies on which we focused were: (1) immediate feeding in a patch (on-patch consumption), and (2) collecting in a patch and caching the food for later consumption. The foraging traits were seed handling time and seed encounter rate.
Natural history
G. allenbyi and G. pyramidum occur sympatrically in a
wide range of sandy habitats in the Western Negev Desert
(Abramsky et al., 1985a). The
smaller species, G. allenbyi (mean mass = 26 g), occurs mostly in
stabilized sands and semi-stabilized dunes with relatively dense vegetation
cover (Abramsky et al., 1985b).
The larger species, G. pyramidum (mean mass = 40 g), occurs mostly in
shifting and semi-stabilized dunes with more sparse vegetation cover
(Abramsky et al., 1985b). The
two gerbil species are similar in their general ecology; they are both
solitary burrow dwellers that forage nocturnally for seeds, which constitute
large proportions of their diets (Bar et
al., 1984). Although individual G. allenbyi and G.
pyramidum do not have cheek pouches, they carry seeds in their mouth and
deliver them to surface caches or to their burrows for later consumption
(Ovadia, 1999). Individuals of
both species typically block their burrow entrance with sand
(Ovadia, 1999). We assume that
this behavior may reduce predation risk by snakes and protect stored seeds
from theft. Direct observations have shown that individual G.
allenbyi and G. pyramidum aggressively defend food sources, and
these aggressive interactions include chases and attempts at physical contact
(Ovadia, 1999).
The effect of the three major predators, owls, snakes, and foxes, on the
behavior of G. allenbyi and G. pyramidum was investigated
intensively. In the presence of owls, both species forage less and avoid the
open microhabitat (Abramsky et al.,
1996; Kotler et al.,
1991,
1992). In contrast, when
snakes are present both are active mainly in the open microhabitat (Kotler et
al., 1992,
1993a,c).
Finally, in the presence of foxes, the two gerbil species reduce their
foraging activity, but there is no difference in foraging effort between
under-bush and open microhabitats (Ovadia,
1999). Synthesizing the above results reveals that predation risk
is not creating an axis of environmental heterogeneity along which the two
gerbil species may coexist (Brown et al.,
1994b; Kotler et al.,
1994).
Field experiments have shown that individual G. allenbyi and
G. pyramidum compete strongly with each other
(Abramsky and Pinshow, 1989;
Abramsky et al., 1991,
1992,
1994;
Mitchell et al., 1990). The
larger species, G. pyramidum, excludes the more efficient forager
(Brown et al., 1994a;
Kotler et al., 1993b), G.
allenbyi, from the best habitat
(Abramsky et al., 1990;
Ziv et al., 1993) and from the
early part of the night (Kotler et al.,
1993d; Ziv et al.,
1993). Thus, ecologists suggested that coexistence between the two
species is due to a trade-off between the dominance of G. pyramidum
versus the foraging efficiency of G. allenbyi
(Kotler et al., 1993d;
Ziv et al., 1993). Here, we
define foraging efficiency as the ratio of harvest rate to foraging costs (see
Brown, 1988).
Testing for species-specific foraging traits that may mediate coexistence,
Kotler and Brown (1990)
measured the harvest rate of G. pyramidum and G. allenbyi.
However, their study was done under laboratory conditions and they did not
consider the potential use of more than one foraging strategy: specifically
(1) immediate feeding in a patch; and (2) collecting in a patch and caching
the food for later consumption. It is possible that each foraging strategy may
be associated with specific foraging traits. Therefore, the quantification of
the frequency of each strategy in the population and the detection of
strategy-specific foraging traits may have important implications regarding
the coexistence of the two gerbil species. Furthermore, we believe that
extrapolating foraging data obtained in the laboratory to animals under
natural conditions may be problematic and therefore we suggest that laboratory
studies be complemented with field studies. In this study we measured the
strategy-specific foraging traits of gerbils under both laboratory conditions
and in the field.
Predictions
In accordance with the natural history of the species and in light of the
goals of the present study, we predicted that:
- In the field gerbils will use mainly the collecting and caching strategy
which minimizes exposure to predators.
- Gerbils will face diminishing returns in their resource intake as a result
of the seed distribution and depletion and the cost associated with
harvesting.
- The harvest rates of gerbils in the field will be higher than those in the
laboratory, because gerbils should compensate for the additional costs that
they experience when foraging in the presence of their competitors and
predators.
- Foraging traits will differ between the two gerbil species, both under
laboratory conditions and in the field. The larger species, G.
pyramidum, which is active during the first part of the night when
resource density is high (Kotler et al.,
1993d; Ziv et al.,
1993), will have shorter handling times. The smaller species,
G. allenbyi, the more efficient forager
(Brown et al., 1994a), will
have higher seed encounter rates.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Measuring foraging traits
Holling (1959
) developed
the first equations describing foraging behavior as a function of handling
time and encounter rate (Holling's disc equation). However, using the
Holling's disc equation for experimental data may be problematic because it
models feeding rate at unchanging resource density, and most experiments allow
depletion of the resource by the consumer (e.g.,
Carter et al., 1984;
Collins et al., 1981;
Livdahl, 1979;
McArdle and Lawton, 1979;
Thompson, 1975,
1978). An integrated form of
the Holling's disc equation, the random predator equation, has been developed
for modeling the functional response of consumers experiencing diminishing
returns in their resource intake as a result of the resource depletion
(Rogers, 1972;
Royama, 1971). The linearized
form of this equation (Rogers,
1972), has been recommended
(Southwood, 1978), and used in
many empirical studies (e.g., Carter et
al., 1984; Collins et al.,
1981; Thompson,
1975).
Kotler and Brown (1990)
suggested a similar integrated linearized form for estimating encounter rate
(a, in units of s-1) and handling time (h, in
units of s/g) of gerbils foraging on depletable seed patches, from their total
foraging time and the amount of food they harvested in a patch:
 | (1) |
Kotler and Brown (1990)
developed Equation 1 based on the natural history of G. allenbyi and
G. pyramidum. The similar linearized form proposed by Rogers
(1972) has been criticized for
inaccuracy when tested with a simulated data set
(Juliano and Williams, 1987).
However, we have used Equation 1 for our experiments because it was developed
specifically to fit both the gerbil system and the kind of data we collected
during this study.
Field study
The field site was located in the Holot Mashabim Nature Reserve
(31°01' N, 34°45' E), situated in the Haluza region, 35 km
south of Beer Sheva, Israel. Sandy areas at the study site can be classified
into two habitat types based on mobility of the sand and on the dominant
perennial plant species. The two habitat types are semi-stabilized dunes and
stabilized sands (Danin,
1978). Average annual precipitation at the site is 108 mm.
Rainfall is limited to winter, and dew forms on approximately 250 nights per
year.
We used one 1-ha plot enclosed with rodent-proof fences to measure the harvest rates of the two gerbil species. The 1-ha plot contained similar proportions of the two major habitat types, semi-stabilized dunes and stabilized sand. Direct observation and sand tracking suggest that these fences did not effect the activity of mammalian predators. Data collected from live trapping in control plots of the same size over the past 15 years indicate that the average density of G. allenbyi and G. pyramidum is 10.75 ± 1.41 and 2.18 ± 0.51 individuals/ha, respectively (Abramsky Z, unpublished data).
We did two field experiments with each gerbil species. Each experiment
lasted 12 nights and was scheduled so that foraging measurements occurred on
moonless nights. We used the following experimental protocol. For six
consecutive nights, we trapped and removed all the rodents from the enclosed
plot. Thereafter, we released six naive gerbils of a single species into the
plot and let them habituate to their new surroundings for two nights. During
each of the following three nights we ran one to three foraging sessions. We
began each foraging session by placing six seed trays (60 x 45 x
2.5 cm deep) in an open area (
1 m from shrubs). The distance between
adjacent seed trays was 1 m. Each seed tray was filled with 3 dm2
of sifted sand into which 3 g of millet seeds were thoroughly mixed. We
videotaped the foraging sessions using two thermal imaging cameras (an
Infracam and a Radiometer-IR-760, both by Inframetrics Inc.). We stopped
foraging sessions after different time intervals to obtain data spread over
the entire range of patch depletion. At the end of each session, we removed
the seed trays and sifted the sand to recover the remaining millet seeds. For
each session we recorded the total time that gerbils spent foraging in each
tray (t in s) and the mass of the seeds remaining in the tray (final
mass, or Nf, in g). Because the initial mass
(No) of seeds on each tray was 3 g, the amount of seeds
harvested was the difference between the initial and final masses (3 -
Nf). At the end of each experiment we opened gates in the
fences of the enclosed plot for two weeks so that animal and resource
densities could attain similar levels outside and inside the plots.
Data from livetrapping and sand tracking stations suggest that on average
an individual G. allenbyi or G. pyramidum covers a minimum
area of 20 x 20 m per night (Brown
et al., 1994a). Furthermore, in most foraging sessions we were
able to observe three to six gerbils simultaneously foraging on different seed
trays. Thus, we believe that during each experiment almost all individuals in
the enclosure contributed to the data set.
Laboratory study
We captured six individuals of each gerbil species at the field study site
and brought them to the laboratory. We built six 0.7 x 3 m adjacent
arenas. We placed a nest box on one side of the arena and a metal seed tray
(60 x 45 x 2.5 cm) on the other. Using one species at a time, we
introduced one animal into each of the six adjacent arenas and allowed them 2
days for habituation. For the next several nights, we conducted on average 12
foraging sessions. At the beginning of each foraging session, we introduced a
single seed tray into each arena. Again, each seed tray contained 3
dm2 of sifted sand into which 3 g of millet seeds were thoroughly
mixed. By direct observation and using six stopwatches, we measured the time
that each of the six gerbils spent foraging for seeds. We stopped the foraging
sessions after various time intervals to obtain data spread over the entire
range of patch depletion, removed the seed trays, and sifted the sand to
recover the remaining millet seeds. The data from a session consisted of the
time spent foraging by a gerbil within its seed tray, the mass of the seeds
that it collected or consumed, and the final mass of seeds left in its
tray.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Foraging strategies: laboratory and field studies
A notable finding of the laboratory experiments was that both species had two distinct foraging strategies: either they consumed seeds immediately on the tray, or they collected and delivered the seeds to their nest box for later consumption (Figure 1 and Table 1). Moreover, we found a transition in foraging strategy among individual G. allenbyi; they all began with the on-tray consumption strategy and after a few days switched to the collecting strategy (Figure 2). Such pattern was not found among individual G. pyramidum.
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By contrast, in the field both species used only one foraging strategy:
They collected and delivered the seeds to their burrow or to surface caches
for later consumption (Figure 3
and Table 1). In a separate
field experiment, a similar pattern was found. Gerbils ate seeds in the patch
in less than 1% of the foraging bouts, and in 99% they collected and delivered
seeds to their burrows or to surface caches for later consumption
(Ovadia, 1999).
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Harvest rates: laboratory study
We used Equation 1 to do a multiple regression analyses and found that
under laboratory conditions the harvest-rate curves of the two gerbil species
fit a type II functional response as described by Holling
(1959) (see
Figure 1 and
Table 1). The slopes of the
harvest rate curves decrease as the time spent foraging increases
(Figure 1), implying that
gerbils experience diminishing returns from their harvest as they spend more
time foraging (Charnov,
1976).
We did analyses of covariance to test for the effect of foraging strategy on harvest rates of the two gerbil species. We treated time spent foraging in a patch as the dependent variable, ln (No/Nf) and (No-Nf) as covariates, and foraging strategy as an independent categorical variable. The effect of foraging strategy on the harvest rates of G. allenbyi and G. pyramidum was highly significant (F = 33.75; df = 1,52; p <.001 and F = 45.29; df = 1,38; p <.001, respectively), with both species harvesting faster when collecting the seeds for later consumption. These differences may be due to differences in seed handling time, seed encounter rate, or both. The multiple regression analyses provided the values of seed encounter rate and seed handling time for each species (Figure 4a,b and Table 1). For both species, seed handling time was shorter and seed encounter rate was higher when collecting seeds than when consuming seeds in the tray (Figure 4a,b and Table 1). To test whether these differences are significant, we added the interaction terms between foraging strategy and the covariates into our models. The interaction between the foraging strategy and seed handling time of G. allenbyi and G. pyramidum was not significant (F = 0.997; df = 1,50; p =.323 and F = 0.849; df = 1.36; p =.363, respectively). Hence, neither species had significantly different seed handling times when using different foraging strategies (Figure 4b and Table 1). The interaction between the foraging strategy and seed encounter rate of G. allenbyi and G. pyramidum also was not significant (F = 0.322; df = 1,50; p =.573 and F = 0.927; df = 1,36; p =.342, respectively). It follows that neither species had significantly different seed encounter rates when using different foraging strategies (Figure 4a and Table 1). We could not relate the differences in harvest rates between the two foraging strategies to seed encounter rate or to seed handling time in either species.
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We did not find significant differences in harvest rates between the two species when they consumed seeds in the tray (F = 2.08; df = 1,55; p =.155). However, when they collected seeds for later consumption, we were able to detect significant interspecific differences; G. pyramidum harvested seeds at a higher rate than G. allenbyi (F = 50.12; df = 1,35; p <.001). We could not relate this interspecific effect to differences in seed handling time (Figure 4b and Table 1) or in seed encounter rate (Figure 4a and Table 1) between the two gerbil species (F = 0.608; df = 1,33; p =.441 and F = 0.353; df = 1,33; p =.557, respectively). Instead, these differences may be the result of the combined effect of seed handling time and seed encounter rate.
Harvest rates: field study
We found that in the field the harvest rate curves of the two gerbil
species fitted a type II functional response curve
(Holling, 1959; see
Figure 3 and
Table 1). As in the laboratory
situation, the slopes of the harvest rate curves decrease as the time spent
foraging increases (Figure 3),
again suggesting that gerbils experienced diminishing returns from their
harvest as they spend more time foraging
(Charnov, 1976).
We found a significant difference in harvest rates between the two species, with G. pyramidum harvesting seeds at a higher rate than G. allenbyi (F = 8.625; df = 1,120; p =.004). Seed handling time of G. pyramidum (154.91 s/g) was significantly shorter than that of G. allenbyi (380.67 s/g) (F = 6.81; df = 1,118; p =.01; Figure 4b, Table 1). Thus, when both species forage in rich patches, G. pyramidum will have an advantage over G. allenbyi. Seed encounter rate of G. allenbyi (5.9 x 10-3 s-1) was significantly higher than that of G. pyramidum (2.4 x 10-3 s-1) (F = 5.867; df = 1,118; p =.017; Figure 4a and Table 1). Thus, when food density in patches is very low, G. allenbyi will have an advantage over G. pyramidum.
Harvest rates: comparison between the laboratory and the field
studies
We tested for differences in the harvest rates between the field and the
laboratory experiments. The results showed that, when collecting seeds for
later consumption, both G. allenbyi and G. pyramidum
harvested seeds at significantly higher rate in the field than under
laboratory conditions (F = 77.045; df = 1,95; p <.001 and
F = 8.04; df = 1,60; p =.006, respectively;
Figure 5). We found that for
both species, seed handling time was similar and seed encounter rate was
higher in the field than in the laboratory
(Figure 4a,b and
Table 1). For G.
pyramidum, we did not find significant differences in seed encounter rate
between the field and the laboratory (F = 1.15; df = 1,58; p
=.288; Figure 4a). However,
seed encounter rate of G. allenbyi was significantly higher in the
field (5.9 x 10-3 s-1) than in the laboratory
(1.58 x 10-3 s-1) (F = 13.83; df = 1,93;
p <.001; Figure
4a).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Foraging strategies and foraging traits are two of the major focuses of optimal foraging theory (Stephens and Krebs, 1986
). The interaction between each one of them and
environmental heterogeneity may have important ramifications for the
understanding of population and community patterns and processes (e.g.,
Hambäck and
Ekerholm, 1997; Henein et al.,
1998; Holt and Kotler,
1987; Kotler and Brown,
1988; Werner,
1992). We found that under laboratory conditions, both G. allenbyi and G. pyramidum used two distinct foraging strategies; either they immediately consumed seeds on the provided seed trays, or they collected the seeds for later consumption. Additionally, individual G. allenbyi began with the on-tray consumption strategy and then switched to the collecting strategy (Figure 2). However, in the field both species used only one foraging strategy. They collected seeds on trays and delivered them to their burrow or to surface caches for later consumption. Why, in the field, do gerbils rarely eat seeds where they find them?
Our preliminary experiments show that in smaller arenas gerbils primarily used the on-tray consumption strategy. This suggests that the distance between a food patch and an individual burrow may affect foraging strategy. During the laboratory study, the distance between the food patch and the nest box did not change, and gerbils used both foraging strategies. Moreover, in each of the four field experiments (two for each species), few individuals located their burrows adjacent to the seed trays (less than 1 m), and none fed on the seed trays. Thus, although distance may be an important factor, it seems that this was not the main factor motivating gerbils in the field to use the collecting strategy exclusively.
Gerbils in the field are subjected to conflicting pressures imposed by
abiotic and biotic factors. For example, predation risk may compel gerbils to
minimize the time that they spend foraging outside their burrows, while
competition may encourage them to stay longer in patches and to defend them
from other gerbils. Calculations based on field data have shown that predation
risk amounts to 91% of the total foraging cost
(Brown et al., 1994b).
Moreover, predation risk causes gerbils to reduce their activity
(Abramsky et al., 1996; Kotler
et al., 1991,
1992,
1993a,
c) and, under high predation
pressure, the strong competition between the two gerbil species almost
disappears (Abramsky et al.,
1998). Therefore, it is likely that predation risk has a strong
effect on gerbil foraging strategy. Indeed, the results of our field study
show that gerbils chose a foraging strategy that reduces predation risk by
minimizing the time spent feeding outside their burrows.
G. allenbyi and G. pyramidum harvested seeds at
significantly higher rates in the field than in the laboratory
(Figure 5). This difference was
due to the increased seed encounter rate
(Figure 4a and
Table 1) and suggests that
under natural conditions—which probably include predation risk and
competition pressure—gerbils not only change their foraging strategy,
but also forage more efficiently. The ability of individuals to adaptively
switch their foraging strategy or to change their harvest rates may have
substantial implications on both the population and the community levels
(e.g., Fryxell, 1997;
Hambäck and
Ekerholm, 1997; Henein et al.,
1998; Holt, 1984;
Holt and Kotler, 1987;
Schmitz et al., 1997;
Werner, 1992).
Kotler and Brown (1990)
measured the values of seed handling time and seed encounter rate for the two
gerbil species under laboratory conditions. Their estimated seed handling
times of G. allenbyi and G. pyramidum were 939.3 s/g and
534.9 s/g, respectively (Kotler and Brown,
1990). Their estimated seed encounter rates of G.
allenbyi and G. pyramidum were 2.09 x 10-3
s-1 and 1.62 x 10-3 s-1, respectively
(Kotler and Brown, 1990).
Laboratory seed handling time and seed encounter rate measured by Kotler and
Brown (1990) were close to the
laboratory values we measured for gerbils consuming seeds in trays
(Table 1). The arena used by
Kotler and Brown in their laboratory study (70 x 55 cm) was smaller than
the arena that we used (70 x 300 cm). Since our preliminary experiments
showed that, in the smaller arenas, gerbils primarily used the on-tray
consumption strategy, we suggest that in the Kotler and Brown experiment,
gerbils most often fed on the seed trays.
In the field the two species demonstrate a significant difference in
harvest rates, with G. pyramidum harvesting seeds at a higher rate
than G. allenbyi (Figure
3). In addition, our field study supports Kotler and Brown's
(1990) conclusions regarding
seed handling time. G. pyramidum's seed handling time (154.91 s/g)
was significantly shorter than that of G. allenbyi (380.67 s/g)
(Figure 4b and
Table 1). This difference may
give G. pyramidum a foraging advantage over G. allenbyi in
rich patches: G. pyramidum will collect more seeds per unit time.
Moreover, we found that in the field, seed encounter rate of G.
allenbyi (5.9 x 10-3 s-1) was significantly
higher than that of G. pyramidum (2.4 x 10-3
s-1) (Figure 4a and
Table 1). Thus, when patch food
density has been lowered, G. allenbyi will have an advantage over
G. pyramidum: it will be able to find and collect more seeds per unit
time of search.
Previous studies have shown that the larger species, G. pyramidum,
excludes the smaller species, G. allenbyi, both from the preferred
habitat (Abramsky et al., 1990;
Ziv et al., 1993) and from
favored activity h (Kotler et al.,
1993d; Ziv et al.,
1993). Brown et al.
(1994a) found that the giving
up density of G. allenbyi is lower than that of G.
pyramidum. Based on these results, ecologists suggested that coexistence
between the two species is based on a trade-off between dominance of G.
pyramidum and foraging efficiency of G. allenbyi
(Brown et al., 1994a;
Kotler et al., 1993d;
Ziv et al., 1993). This
trade-off occurs along an axis of environmental heterogeneity comprised of
spatial and temporal variability in resource abundance
(Ben-Natan, 1999).
Our study demonstrates that the interspecific differences in foraging traits may be sufficient to promote coexistence between the two species. At the beginning of the night, when resource density in patches is high and the forager spends most of its time handling seeds, G. pyramidum is more efficient due its shorter handling time. Later in the night, when resource density in patches is low and the forager spends most of its time searching for seeds, G. allenbyi is more efficient due to its higher encounter rate. Therefore, we suggest that coexistence between the gerbil species is sustained by several related mechanisms operating along the same axis of environmental heterogeneity.
Vincent et al. (1996)
developed a theoretical model to explore how trade-off in conversion
efficiency, handling time, and encounter rate effect coexistence between
species. One important outcome of this model is that a difference in encounter
rate between species may support coexistence over a wide range of
environmental heterogeneity. Although Vincent et al.
(1996) deal with different
situations, our results lend credence to their theoretical study concerning
the importance of encounter rate in promoting species coexistence. The
relative advantage in encounter rate of the subordinate species, G.
allenbyi, over G. pyramidum, allows it to exploit resource
patches that are not profitable for the dominant species. This advantage may
permit species coexistence over a wide range of resource densities.
Finally, we showed that there are substantial differences in foraging strategies and foraging traits between laboratory and field experiments. Thus, we suggest that, in order to effectively test foraging theories, laboratory experiments should be run in conjunction with field studies, where animals are exposed to real ecological pressures.
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ACKNOWLEDGEMENTS |
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We thank Gideon Wasserberg, Gil Ben-Natan, Eyal Shochat, and Ido Tsorim for discussion and comments on the manuscript. We also thank John Fryxell and an anonymous reviewer for their helpful suggestions and comments. Finally, we thank Oswald Schmitz and Illisa Kelman for their help revising the manuscript. Field research was supported by the Israel Science Foundation (founded by the Israel Academy of Sciences and Humanities) grant number 169/95.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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