Download Patch area, substrate depth, and richness affect giving

Oikos 118: 17211731, 2009
doi: 10.1111/j.1600-0706.2008.17473.x,
# 2009 The Authors. Journal compilation # 2009 Oikos
Subject Editor: Thomas Valone. Accepted 7 May 2008
Patch area, substrate depth, and richness affect giving-up densities:
a test with mourning doves and cottontail rabbits
Mohammad A. Abu Baker and Joel S. Brown
M. A. Abu Baker ([email protected]) and J. S. Brown, Dept of Biological Sciences, Univ. of Illinois at Chicago, 845 W. Taylor St.
(M/C 066), Chicago, IL 60607, USA.
We compared the foraging behavior of mourning doves Zenaida macroura and cottontail rabbits Sylvilagus floridanus in
patches that varied in initial food abundance, surface area and substrate depth. We measured giving-up densities (GUD),
food harvest and proportion of food harvested to investigate their ability to respond to characteristics of resource patches.
GUDs have been analyzed in three ways: grams of per patch, grams per unit surface area (GUDAREA), and grams per unit
volume of sand (GUDVOL).
Mourning doves and cottontails exhibited similar responses to resource density and sand depth. Both foragers detected
and responded to variation in initial food abundance. The proportion of food harvested from a patch increased from
40.7, 43.8 to 48.3% (for the doves) and 34.9, 35.8 to 38.4% (for the rabbits) in patches of low, medium and high initial
food abundance, respectively. Deeper substrates reduced the foragers’ encounter probability with food, decreased patch
quality and resulted in higher GUDs (60% higher in the deepest relative to shallowest substrate) and lower harvests. A
significant interaction between initial food abundance and substrate depth showed that both species were willing to dig
deeper in patches with higher resource density. Patch size (surface area) had no effect on food harvest or the proportion of
food harvested. Consequently, GUDAREA and GUDVOL increased in patches with a smaller surface area. Smaller patches
appeared to hamper the dove’s and cottontail’s movement across the surface.
Our results revealed that mourning doves and cottontails forage under imperfect information. Both species were able to
respond to patch properties by biasing their feeding efforts toward rich and easy opportunities, however, mourning doves
were more efficient at food harvesting.
The interaction of patch area, volume and food abundance directly influenced food harvest. Such resource characters
occur under natural situations where food varies in abundance, area of distribution, and accessibility.
Food harvest represents an interplay between resource
characteristics and the animals’ ability to respond to these
characteristics. Diet choice, habitat selection and patch use
are the three main contexts of foraging theory aimed at how
feeding animals exploit opportunities and avoid hazards
(Stephens et al. 2007). Patch use theory considers how
much effort a forager should devote to depleting the
resources of a localized area before moving on in search
of a new ‘patch’ (Charnov 1976, Stephens and Krebs 1986).
Patch use applies to circumstances where foragers detect and
bias their efforts towards spatial aggregations of resources. A
forager may increase its benefits from the degree of
aggregation and its ability to detect and respond to these
aggregations (Brown 2000). Foragers should travel through
poor patches and harvest rich ones in order to maximize
their fitness rewards (Stephens and Krebs 1986). These
rewards may take the form of energy, safety (Sih 1980,
Brown and Kotler 2004), trace nutrients (Pulliam 1975),
and/or variance of intake rates (Caraco 1980).
Several patch characteristics are known to influence
resource harvest and forager effort (see Meyer and Valone
1999 for an example with multiple foraging costs). First and
foremost is initial food abundance. Foragers should aim to
harvest more from rich patches than poor. Yet, information
constraints may cause foragers to overutilize poor patches
while underutilizing rich patches (Valone and Brown 1989,
Valone 2006). Other patch characteristics include the type
of food (Brown and Morgan 1995), the type of substrate
from which the forager must detect and extract resources
(Price and Heinz 1984, Price and Podolsky 1989, Kotler et
al. 2001), climate (Kilpatrick 2003) and predation risk
(Brown et al. 1988). Less investigated, yet of likely
importance are substrate depth (Nolet et al. 2006), and
patch area (Schmidt and Brown 1996). Furthermore, what
happens when several factors simultaneously influence the
properties of a single patch? Here, we investigate simultaneously three of these important factors: initial food
abundance, substrate depth, and patch area. We show
how several factors acting together yield a more sophisticated and diverse set of predictions. The actual response of
the foragers then yields insights into how they assess and
respond to resource heterogeneity. We investigate changes
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in giving-up density (GUD), cumulative harvest, and
proportion of food harvested from patches that vary in
elements that create diminishing returns in natural situations, namely: area, substrate depth and initial food
abundance.
Foraging strategies and sensory perceptions such as visual,
olfactory and tactile cues allow for varying degrees of
information acquisition. Foragers use this information to
assess and respond to heterogeneity in prey abundance,
patch size and volume. For instance, the long beaks of storks,
the long-mobile snouts of elephant shrews, olfactory sense of
kangaroo rats and digging abilities of gerbils may allow them
to forage deeper in substrates while de-emphasizing the role
of vision. Whereas diurnal seed-eating birds may rely on
vision to find seeds, enhancing seed harvest from the surface
at the expense of seeds deeper in the substrate (Kotler and
Brown 1999, Vander Wall et al. 2003, Skinner and
Chimimba 2005).
Varying patch attributes has been used to investigate
environmental features that influence a forager’s patch use
behavior. Using behavioral titration approaches from
foraging theory, one can better elucidate how habitat
heterogeneity at both the macro- and micro-scales may
influence resource exploitation and reveal mechanistic bases
of patch use, diet choice, community organization and
species coexistence (Moermond 1986, 1990, Brown 1989,
Brown et al. 1994, Kotler and Blaustein 1995, Whelan
2001, Shochat et al. 2004). Diet choice can also be affected
by the distribution and abundance of different foods
(Brown and Morgan 1995). Fox squirrels were partially
selective on the food with higher initial abundance when
presented apart, while the higher encounter probability of
peanuts increased their selectivity at low quitting harvest
rates and the preference of sunflower seeds increased their
selectivity at high quitting harvest rates (Brown and Morgan
1995).
Studies on the effects of patch characteristics on foraging
behavior generally vary just initial prey abundance. Exceptions include studies that vary predation risk by placing
food patches in safe or risky habitats (Brown and Kotler
2004), or by changing the distribution of food within an
experimental food patch (e.g. micropatch partitioning,
Schmidt and Brown 1996). The relationship between
harvest and time spent exploiting a depletable food patch
(gain curve) directly affect the forager’s patch departure. A
gain curve emerges as an interaction between structural
resource properties, the abundance and distribution of
food within the patch, the forager’s sensory abilities and
mechanics of patch exploitation (Olsson et al. 2001, 2002).
When changing patch characteristics such as initial prey
abundance or within patch resource distributions, the
forager experiences a change in its gain curve that should
influence how long and how thoroughly the forager uses the
patch (Olsson et al. 2001, 2002).
As might be expected, increasing the initial prey
abundance elevates the gain curve (Olsson et al. 2001) and
increases the amount of food harvested before the patch is
abandoned. In general, both the amount of food harvested
and the giving up density increase with increasing initial prey
abundance (Valone and Brown 1989, Morgan et al. 1997).
Furthermore, as an indication of patch assessment by the
forager, the proportion of food harvested generally increases
1722
with initial food density. The failure to equalize GUDs
seems to result from imperfect patch assessment (Olsson
et al. 1999) or a gain curve in which the per time encounter
probability changes with patch depletion (the gain curve
deviates from the ideal of random search see Olsson et al.
2002 for an example with starlings).
Foraging behavior is also influenced by the substrate
from which an animal feeds. Price and Podolsky (1989) and
Price and Hienz (1984) showed how coarser substrates than
sand reduce the harvest rates of desert granivores. Furthermore, adding gravel and small rocks to the surface of a
patch increased the GUD relative to their absence (Kotler
and Brown 1999). Davidson and Morris (2001) reported
on increased GUDs in fine sand due to its higher bulk
densities compared to coarse sand. Such a result is
consistent with quitting harvest rate rules under elevated
costs of foraging (Davidson and Morris 2001). Under
natural and experimental conditions, foraging behavior of
warblers gleaning insects appeared to be strongly influenced
by fine-scale foliage structure, mainly: the species of leaf,
accessibility to perches, and the leaf surface qualities
(Whelan 1989, 2001).
Often, giving-up density is used as a surrogate for
quitting harvest rate. However, when patches vary in
characteristics such as area, volume, and substrate depth
the simple notion of a giving-up density can be expressed in
different ways. Most studies present giving-up densities as
grams of food remaining per patch, where other patch
characteristics remain constant across experimental food
patches. But when patches vary in surface area, would it
be more appropriate to express giving-up densities as per
unit surface area, or as GUDs per unit volume when
patches vary in substrate depth? In fact, measuring GUDs
per patch, GUDs per unit area, and GUDs per unit volume
from patches that vary in surface area and in substrate
volume provides different and complementary ways of
viewing attributes of patch use under natural situations. We
used these metrics to examine and compare foraging
behavior and patch assessment by mourning doves and
cottontails for patches varying in depth, area and initial prey
abundance.
We measured the giving-up-densities (grams of food
remaining per patch) of mourning doves and cottontails in
experimental food patches. We studied the effect of patch
characteristics on foraging to reveal factors influencing
quitting harvest rates. We explored the reaction of two
very different species to the same patch properties to test for
characteristics of resource patches to which foragers can
respond and whether these characteristics are general or
species specific, and to evaluated patch design for measuring
GUDs. In what follows we develop testable predictions
from foraging theory. We then present our study methods
for measuring the giving-up densities of doves and then
cottontails from patches that varied with respect to initial
food density, surface area and sand depth, and then present
the results. Predictions and results are couched in terms of
how patch characteristics and the forager’s patch use
strategies may influence the amount of food harvested,
proportion of food harvested, GUD per patch, GUD per
unit surface area (GUDAREA), and GUD per unit volume of
sand (GUDVOL).
Predictions
In order to increase energy benefits and reduce effort,
foragers should bias their efforts towards patches with
smaller areas (higher concentration of food per unit area),
shallower substrates (greater ease of food encounter) and
higher total resource abundance (for a fixed area and
substrate depth). The model of Morgan et al. (1997) on the
effect of spatial scale on the functional response (food
harvest as a function of initial food abundance) of fox
squirrels, predicts that increasing patch richness should
increase proportion of food harvested. Here we consider
within-environment effects of increasing patch richness by
varying independently three properties of patch quality:
initial food abundance (traditional sense of patch richness),
patch size, and substrate depth.
Effect of initial food abundance (IPA)
If the foragers are able to detect and respond to the initial
abundance of food within the patch, they should bias their
efforts towards patches with higher initial resource abundances. The size of this bias and its effect on GUDs and the
proportions of food harvested depend on the forager’s
ability to accurately assess patch quality. At one extreme the
forager may be ‘prescient’ (sensu Valone and Brown 1989)
and able to use sensory cues such as vision and olfaction to
accurately estimate patch quality. As it forages, its estimate
of remaining density is simply the difference between its
initial estimate and its cumulative harvest from the patch.
Such a forager should leave each patch at the same quitting
harvest rate which under random search yields the same
GUD independent of initial food abundance. At the other
extreme, the forager may be unable to make any assessment
of current patch quality. Such a forager should devote the
same amount of search time to each patch resulting in the
same proportions of food harvested regardless of initial food
abundance. In between is the ‘ordinary’ forager that has
imperfect information, but which gains some insights into
patch quality as it forages the patch. Such a forager (e.g.
Bayesian) will not leave each patch at the same quitting
harvest rate (GUDs will often increase with initial food
abundance see Olsson and Brown 2006) but it will favor
rich patches with more search time (the proportion of food
harvested will also increase with initial food abundance).
Our data revealed (see results) that both mourning doves
and cottontails forage under imperfect information. Their
GUD, food harvest and proportion of food harvested all
increased significantly with initial prey abundance. This
knowledge about their patch use becomes essential in
establishing the next two sets of predictions.
Effect of substrate depth
When holding depth or patch area fixed, there are no
ambiguities regarding the units of initial prey abundance
and GUD they are simply grams per tray. However, in
considering the effects of substrate depth, GUD and initial
prey abundance can be treated as either grams per patch
(controlling for patch area) or grams per unit volume of
substrate. We will reserve ‘GUD’ for grams per patch, and
‘GUDVOL’ when referring to grams per unit volume.
(a) More and deeper substrate should reduce harvest
rates for any remaining amount of food both because of the
greater volume of substrate and the encumbrance of having
to dig deeper. Shallow patches should be in all ways more
favorable than deeper patches. Hence, we expect giving-up
densities, food harvest and the proportions of food
harvested to vary as follows:
GUD1:5
cm BGUD3:0 cm BGUD4:5 cm
food harvest1:5
cm food
harvest3:0
cm food
harvest4:5
cm
proportion of food harvested1.5 cm proportion of food
harvested3.0 cm proportion of food harvested4.5 cm
(b) When evaluated as GUDVOL (food remaining per
unit substrate volume) there is now the confounding effect
of initial prey abundance per unit volume declining with
depth. An initial abundance of say 2 g per patch represents
only one third as much food per unit volume when
comparing a depth of 4.5 cm with 1.5 cm. From the results
of prediction 1 we know that GUD increases with initial
prey abundance and hence we can expect the same effect to
carry over for GUDVOL in response to initial prey
abundance per unit volume:
GUDVOL; 1:5 cm GUDVOL; 3:0 cm GUDVOL; 4:5 cm
This prediction presupposes that depth provides little
encumbrance to foraging. However, if the forager is either
unable or unwilling to forage to the depth of the deepest
trays, or if the forager’s encounter probability with deeper
seeds is substantially lower than on shallower seeds, then
substrate volume will have a disproportionate effect on
GUDs and:
Food harvest1:5 cm Food harvest3:0 cm Food harvest4:5 cm
3GUD1:5 cm B2GUD3:0 cm B GUD4:5 cm
GUDVOL; 1:5 cm BGUDVOL; 3:0 cm B GUDVOL; 4:5 cm
These predictions examine how GUDs change with substrate volume for a fixed initial abundance of food within
the entire patch. Which of the alternative predictions holds
for how GUDVOL changes with substrate depth indicates
the degree to which depth itself is a large encumbrance to
the forager. One can use the switch point in this relationship as a gauge for when depth becomes troublesome to a
forager.
(c) We can evaluate the effect of depth on GUDVOL by
fixing the initial prey abundance per unit volume. This can
be done by using the three treatment combinations of A
(1.5 cm depth and 2 g initial prey abundance), B (3 cm
depth and 4 g) and C (4.5 cm depth and 6 g). We expect
the shallow trays to offer a more favorable encounter
probability on seeds because as substrate depth and volume
increases there is the encumbrance of having to dig more
and deeper in search of food items. We expect that
GUDVOL will increase with depth:
GUDVOL; 1:5 cm BGUDVOL; 3:0 cm B GUDVOL; 4:5 cm
We test this prediction by only considering the treatments shown by the shaded boxes in Table 1.
1723
resource density
8
6.25
5.128
4
3.158
2.575
2.667
2.069
1.714
sand volume
0.75
0.96
1.17
1.5
1.9
2.33
2.25
2.9
3.5
GUDsmall tray B GUDmedium tray BGUDlarge tray
Food harvestsmall tray Food harvestmedium tray
Food harvestlarge tray
Proportion of food harvestedsmall tray
Proportion of food harvestedmedium tray
small
medium
large
small
medium
large
small
medium
large
Proportion of food harvestedlarge
tray
However, there is a confounding effect when evaluating
giving-up density per unit area (GUDAREA). For a given
initial food abundance the patch richness per unit area goes
up in smaller areas. Since GUDs increase with initial prey
abundance this effect should manifest as:
GUDAREA;
5.333
4.167
3.419
2.667
2.105
1.717
1.778
1.379
1.143
resource density
tray size
6 gram
Like the effects of depth, we expect smaller patches to offer
more favorable encounter probabilities as the seeds are now
concentrated into a smaller area. Hence:
small tray GUDAREA; medium tray
GUDAREA; large
tray
0.75
0.96
1.17
1.5
1.9
2.33
2.25
2.9
3.5
small
medium
large
small
medium
large
small
medium
large
2.667
2.083
1.709
1.333
1.053
0.858
0.889
0.69
0.571
(C) 4.5 cm
(B) 3.0 cm
small
medium
large
small
medium
large
small
medium
large
(A) 1.5 cm
0.75
0.96
1.17
1.5
1.9
2.33
2.25
2.9
3.5
sand volume
sand volume
tray size
Depth
2 gram
resource density
tray size
4 gram
Material and methods
IPA
Table 1. The experimental layout of food patches used at each site. The 27 artificial food patches established into three stations (A, B and C) of nine trays each.
1724
Effect of patch size (area)
Experiments on mourning doves were conducted in two
residential backyards of Oak Park, a suburb of the Chicago
Metropolitan Area, Illinois, USA. As food, we used
commercially available millet seeds. Following periods of
pre-baiting and acclimation, data were collected for nine
days within each backyard between 18 December 2005 and
10 April 2006. Days were not necessarily consecutive and
were spaced to correspond with favorable weather. First one
yard and then the other were sampled.
Each yard contained a community of seed-eating birds.
Based on direct observations, up to 12 mourning doves
Zenaida macroura, six European collared doves Streptopelia
decaocto (just in the first yard) and ca 25 house sparrows
Passer montanus used these trays (in the second yard
sparrows could number beyond 50). Based on direct
observations, mourning doves contributed to the bulk of
foraging and essentially all of the foraging beyond a certain
point. More so than the sparrows, mourning doves were
willing to dig deeper into the substrate by swishing their
beaks back and forth through the sand.
For experiments on the eastern cottontail, we used the
same patches but for food we used commercial alfalfa
pellets. We selected three sites spaced ca 30 m apart at the
greenhouse compound of the Univ. of Illinois at Chicago.
Eighteen days of data (six days per site) were collected
intermittently from 22 May 2006 until 4 August 2006.
Cottontails were the only foragers within these trays and the
total number of cottontails at the compound appeared to
range from ca 1015 individuals.
Each of the five sites (two backyards for doves and three
greenhouse sites for cottontails) received 27 artificial food
patches arranged as three stations of nine trays (Table 1).
The 27 food patches represented all combinations of three
trays sizes (circular, plastic trays of 27, 32 and 36 cm in
diameter), three substrate depths (1.5, 3 and 4.5 cm depth),
Results
The experiments yielded a total of 486 data points from
each species (doves: 2 sites 9 days per site 27 trays per
day; cottontails: 3 sites 6 days per site 27 trays per day).
GUD data were log-transformed both to reduce heteroscadisticity (correlation between mean GUD and variance)
and to remove problems associated with evaluating the
variance of data created by taking the ratio of two variables.
We used the general linear model of SYSTAT 10 to test for
differences in the dependent variables (GUD, food harvest,
proportion of food harvested, GUDAREA and GUDVOL)
separately against the independent variables patch depth,
initial food abundance, tray size and species. Two-way and
three-way interactions between the independent variables
were also incorporated in the analyses (Appendix 1). We
conducted separate analyses on the different independent
variables. We feel this successfully identifies the roles of
patch characteristics and the forager’s patch use strategy in
influencing these related but complementary metrics of
patch use.
Effect of initial food abundance
GUD, food harvest and the proportion of food harvested all
increased significantly with the initial food abundance.
Mean giving-up densities (in grams) ranged between 1.19,
2.25 and 3.10 (for the doves) and 5.86, 11.57 and 16.63
(for cottontails) for patches of low, medium and high initial
food abundance, respectively. Both doves and cottontails
were able to bias their efforts towards the richer patches.
The proportion of food harvested from a patch increased
from 40.7, 43.8 to 48.3% (for the doves) and 34.9, 35.8 to
38.4% (for the rabbits) in patches of low, medium and high
initial food abundance, respectively (Fig. 1, Appendix 1).
Both doves and cottontails responded somewhat similarly to
7
Mourning doves
Grams of food
6
Giving-up densities
Food harvest
5
4
3
2
1
0
0
2
4
6
8
Initial abundance of food
30
Cottontails
Grams of food
and three initial food abundances (2, 4 and 6 g of millet per
patch for doves, and 9, 18 and 27 g of pellets per patch for
rabbits), (Table 1). The nine trays of a station were
randomly arranged next to each other in a circle. On a
given day, each station received either all of the low depth,
medium depth or high depth trays. Within a ring all nine
combinations of tray size and initial food density were
present. Over a three day period, the three substrate depths
were rotated as a 33 latin square design across the three
stations. For doves the latin square was repeated three times
for each site generating a total of nine days per site. For
cottontails the latin square was repeated twice for a total of
six days per site.
Prior to a day (from mourning doves) or night (from
cottontails) of data collection, trays were filled with food
mixed thoroughly into the sifted sand substrate (commercial bank sand). For doves, trays were established between
07:00 and 08:00, left out all day, and then the remaining
seeds were sieved from each tray between 16:00 and 18:00
h. For cottontails, trays were established around noon and
then left for 24 h prior to sieving out the remaining food.
The bulk of cottontail foraging occurred at night with a
peak of activity just after dusk.
Giving-up densities
Food harvest
20
10
0
0
9
18
27
36
Initial abundance of food
Figure 1. Mean giving-up densities and amounts of food
harvested by mourning doves and cottontails were significantly
higher in patches with high initial abundance of food.
changes in initial food abundance, however, mourning
doves harvested a higher proportion of food from patches
than did the cottontails.
Effect of substrate depth
GUD, food harvest and the proportion of food harvested all
varied significantly with substrate depth (F2,458 138.8,
108.4 and 142.4 for the doves and F2,459 30.18, 20.19
and 26.77 for the cottontails respectively with pB0.001 for
all three variables). Mean giving-up-densities increased from
1.4 and 9.9 g in shallow patches to 2.8 and 12.7 g in
patches of the deepest substrate for mourning doves and
cottontails respectively (Fig. 2). Foraging of both species
was negatively influenced by increasing patch depth as food
harvest from deep patches decreased by both species. In
deep patches, mourning doves showed lower foraging
efficiencies than cottontails as their proportions of food
harvested went through a sharper decline from 64.2% in
shallow patches to 27.9% in deep ones. This decline ranged
between 45.2% and 28.9% for the cottontails.
Our results showed a significant increase in food harvest
with depth when opportunities for easy harvest of food were
available (i.e. shallow patches). Patch depth showed a
significant interaction with initial food abundance for
1725
6
(a)
5
4
3
2
1
0
0.0
1.5
3.0
4.5
Giving-up density per unit volume
Giving-up density in grams of food
(a)
6.0
8
7
6
5
4
3
2
1
0
0.0
1.5
(b)
30
20
10
0
0.0
1.5
3.0
4.5
6.0
Giving-up density per unit volume
Giving-up density in grams of food
Patch depth
(b)
3.0
4.5
6.0
4.5
6.0
Patch depth
40
30
20
10
0
0.0
1.5
3.0
Patch depth
Patch depth
Figure 2. Mean giving-up densities of mourning doves (a) and
cottontails (b) increased significantly with substrate depth. Boxes
show the range in which 50% of the values fall. The whiskers show
the range of observed values that fall within 1.5the spreads of
50% of the values. x are the outside values that fall beyond 1.5 the spread of 50% of the values.
Figure 3. Mean giving-up densities per unit volume of sand
decreased significantly with patch depth for mourning doves (a)
and cottontails (b). Boxes show the range in which 50% of the
values fall. The whiskers show the range of observed values that fall
within 1.5 the spreads of 50% of the values. x, o are the outside
and far outside values that fall beyond 1.5the spread of 50% of
the values and 3 the spread of the values respectively.
mourning doves with respect to food harvest (i.e. effect of
depth was greatest at low initial food abundance and less so
at high initial food abundance) but not with the proportion
harvested (F4,458 8.24, pB0.001; F4,458 0.7, p 0.589
respectively). In contrary, patch depth and initial food
abundance had no significant interactions in the cottontail
data.
Giving-up densities per unit volume of sand exhibited
significant differences with respect to all main effects of
depth, tray area and initial food abundance for both species
(Appendix 1). A significant decrease in GUDVOL with depth
was reported (Fig. 3), with data ranging between 1.6 and
5.9 g l1 in shallow patches to 1.1 and 2.6 g l1 in deep
patches for mourning doves and cottontails respectively
(F2,458 14.05 and F2,459 86.34, pB0.001). GUDVOL
was also significantly lower in large trays (1.1 and 1.3 g l1)
than in small ones (1.5 and 8.8 g l1 for mourning doves
and cottontails respectively) (F2,458 14.93 and F2,459 522.6, pB0.001).
For our final comparison of depth effects, we used
different depths of sand, but with the same initial food
abundance per unit volume for all trays of a given size
(equal ‘standardized’ resource density, see treatments shown
in grey in Table 1). Both species exhibited lower GUDs
(standardized GUDs) per volume of sand in shallow patches
(Fig. 4). Standardized GUDs decreased from 1.39 and
7.49 g l1 in small trays to 0.97 and 1.1 g l1 in large trays
for mourning doves and cottontails respectively.
1726
Effect of patch area
There was no significant effect of patch size on giving-up
densities, amounts of food harvested or the proportion of
food harvested (F2,459 0.22, p0.8 and F2,459 0.182,
p0.83 and F2,459 0.1, p 0.9 respectively) for cottontails. However, mourning doves had significantly different
GUDs (but not food harvest or proportion harvested)
between patches of different sizes (F2,458 4.83, p B0.05
and F2,458 1.73, p0.18 and F2,458 1.58, p 0.21
respectively). Mean giving-up densities (in grams) ranged
between 2.087, 2.176 and 2.271 (for mourning doves)
and 11.46, 11.21 and 11.38 (for cottontails) for patches
(a)
2
1
0
0.0
1.5
3.0
4.5
6
Giving-up density in grams of food
3
Giving-up density per unit volume
(a)
5
4
3
2
1
0
6.0
large
(b)
15
10
5
0
0.0
1.5
3.0
medium
small
Patch area
4.5
Giving-up density in grams of food
(b)
Giving-up density per unit volume
Patch depth
30
20
10
6.0
0
large
medium
small
Patch area
Patch depth
Figure 4. Mean giving-up densities per unit volume from patches
of standardized resource abundance increased with depth for
mourning doves (a) and cottontails (b). Boxes show the range in
which 50% of the values fall. The whiskers show the range of
observed values that fall within 1.5 the spreads of 50% of the
values. * are the outside values that fall beyond 1.5the spread of
50% of the values.
Figure 5. Patch area had no effect on the giving-up densities of
mourning doves (a) and cottontail rabbits (b). There was no
significant increase in food harvest from smaller food patches.
Boxes show the range in which 50% of the values fall. The
whiskers show the range of observed values that fall within 1.5 the spreads of 50% of the values.
of small, medium and large area, respectively. While
cottontails had a slight decrease in mean GUDs throughout
the three patch areas, mean GUDs of mourning doves
increased between small and large patches (Fig. 5).
However, when GUDs were measured per unit area of
the food patches (GUDAREA), they were significantly lower
in large (22.33 and 24.87 g m2) than small (36.48 and
44.54 g m2) trays for mourning doves and cottontails
respectively (Fig. 6).
The interaction effect of patch size and initial food
abundance were significant with respect to GUDAREA for
both species (Appendix 1). GUDAREA was significantly
lower in smaller patches through the different initial food
abundances (F4,458 2.59, p B0.05 and F4,459 10.46,
pB0.001). Additionally, mourning doves had significant
interactions of patch depth with both patch area and initial
food abundance with respect to GUDAREA. This suggests an
increase in the negative influence of small patches on
foraging efficiency with depth and low initial food
abundance (Appendix 1).
Discussion
Initial prey abundance, substrate depth and patch area all
influenced the patch use behavior of mourning doves and
cottontail rabbits. Both species biased their efforts towards
individual patches of higher resource density and shallow
patches with easier opportunities for food harvest. More
food and a higher proportion of food were harvested from
patches with higher initial abundances (Fig. 1). As expected,
deeper substrate reduced the foragers’ encounter probability
with food (as they required more bulk volume of sand,
which in turn reduced resource density, Table 1), decreased
patch quality and resulted in higher GUDs and lower
harvests (Fig. 2). Contrary to our prediction, patch size
had no effect on food harvest or the proportion of food
harvested by both species. However, mourning doves
had significantly lower GUDs in smaller patches. Yet,
GUDAREA and GUDVOL increased for both species in
patches with a smaller surface area or shallow depth.
1727
120
Giving-up density per unit area
(a)
100
80
60
40
20
0
large
medium small
Patch area
120
Giving-up density per unit area
(b)
100
80
60
40
20
0
large
medium
small
Patch area
Figure 6. Mourning doves (a) and cottontails (b) had higher
GUDAREA in smaller trays due to the increase in patch richness
with small patch areas. Boxes show the range in which 50% of the
values fall. The whiskers show the range of observed values that fall
within 1.5the spreads of 50% of the values.
Despite being very different taxa foraging for quite
different foods, the mourning doves and cottontails
exhibited some similar responses and small differences.
The increased substrate depth affected mourning doves
more than cottontails. Forager size and foraging technique
likely explain this. Based on direct observations, both
species explore the substrate by alternating bouts of
churning the substrate followed by the harvest of freshly
exposed food items. Mourning doves do this by swishing
their beaks sideways through the sand. To access deeper
seeds, the dove must partially plunge its head into the sand.
The rabbits shovel backwards with their forepaws leaving
larger and deeper disturbances than the doves. Hence, the
GUDs of doves nearly doubled in going from 1.5 cm of
sand to 4.5 cm. Whereas this increase in depth caused less
than a 50% increase in the GUDs of cottontails.
In the present study, we used greater volumes of sand to
increase substrate depth and vary the ease of encounter to
prey between the different patches. The foragers took more
advantage of shallow patches by increasing their food
harvest compared to deep ones (Fig. 2, 3, GUDVOL with
standardized initial food abundance); the effect of deep
patches was magnified with decreasing patch area and initial
food abundance (Appendix 1). However, for a given initial
1728
prey abundance, GUDVOL decreased with depth through
the different patches, indicating that both the mourning
doves and cottontails forage under imperfect information,
as they use information acquired while exploiting the
patches. This effect on GUDVOL came about via a decline
in initial food abundance per unit volume as more sand was
added to the patch.
In the present study, mourning doves’ food harvest
exhibited a significant interaction between patch depth and
initial food abundance. In deep patches (4.5 cm of sand),
the doves increased their food harvest from 0.52, 1.03 to
1.94 g at low, medium and high initial food abundance
respectively. This shows that the foragers were willing to dig
deeper and more thoroughly in patches of higher resource
density hence, increasing the available food motivated more
intense patch use. The doves are able to choose, up to a
point, how deep to dig and this depth will increase with
initial food abundance. Gawlik (2002) manipulated fish
density and water depth (i.e. prey accessibility) in artificial
ponds accessible to eight species of free-ranging wading
birds. Foraging birds increased their GUDs with increasing
water depth and had an upper threshold for water depth
beyond which they appeared unable to forage. A similar
relationship between elevated GUDs and food accessibility
was reported in a swan-pond system (Nolet et al. 2001,
2006) where GUDs on benthic tubers increased with water
depth. In the swan-pond system, accessibility was more
important than differences in energetic costs of foraging.
Accessibility to resources determined by foliage structure
also affects avian foraging behavior by influencing encounter rates with prey, prey accessibility, and energetic costs of
attacking and capturing prey (Greenberg and Gradwohl
1980, Robinson and Holmes 1982, Schmidt 1998, Whelan
1989, 2001).
We selected a mammalian and an avian forager as they
offered wide opportunities for diverse foraging performances due to different sensory and locomotory modes.
Thus, their similar responses to resource density and patch
depth emerged from very different ways of foraging and
perhaps sensing and collecting food. Mourning doves
appeared to be more efficient foragers, harvesting a greater
fraction of food from the patches than cottontails. Food
quality, background availability of food, and experience
with this sort of foraging may all have been more favorable
for the mourning doves. Doves in these yards were already
well familiar with concentrations of millet seeds from bird
feeders; seeds are probably at low background abundance in
the surrounding lawns, and uncovering buried seeds is
probably part of doves’ normal foraging repertoire. Cottontails were foraging for a novel food (alfalfa pellets) against a
background of potentially equal forage in the lawn, and
digging may not be part of a cottontail’s normal foraging
behavior. Experience and memory of patch distribution
(pre-harvest information) played an important role in
allowing northern bobwhites to selectively exploit patches
high in resources (Kohlmann and Risenhoover 1998).
When exploiting novel, but predictable patches, Vásquez
et al. (2006) showed that degus Octodon degus made more
accurate assessments of patch quality after two weeks of
foraging from paired patches of poor and rich resource
densities. This pattern was observed consistently from day
15 to day 21 and agrees with a prescient foraging strategy
(Valone and Brown 1989). Vásquez et al. (2006) suggests
that the Bayesian behavior observed in previous patch
assessment studies could result from short-term evaluations
and/or lack of resource predictability (Valone and Brown
1989, Olsson et al. 1999).
Contrary to previous studies where mourning doves
followed a fixed time patch exploitation strategy (Valone
and Brown 1989, Hayslette and Mirarchi 2002), our results
showed the doves discriminating appropriately between rich
and poor patches. Our patches were smaller and generally
offered more striking contrasts in area, depth and initial
prey abundance than those used by Valone and Brown
(1989) in the Sonoran Desert of Arizona. Alternatively the
schedule of daily offering the same mourning doves the
same suite of patch choices may have honed their ability
and/or willingness to discriminate between patches (Valone
and Brown 1989, Vásquez et al. 2006). Conditioning and
memory may have played a role. The foragers may use the
daily renewal of patches to improve their ‘within-day’ patch
assessment and exploitation abilities (Vásquez et al. 2006).
Contrary to our predictions, patches with smaller area
had higher GUDAREA and GUDVOL. A part of this increase
likely is the effect of increased initial food abundance per
unit area as tray size declines. However, the foraging mode
and the physical effect of foraging while standing in the
food patch also contributed to the increased GUDAREA and
GUDVOL in smaller patches. Our results demonstrate that
while both species were willing to dig deeper in large
patches, those patches were easier to manage than their
equivalent size of small-sized patches. GUDs throughout all
patches from mourning doves (regardless of resource
density or depth) have shown a slight increase with patch
area (2.087 g in small to 2.27 g in large patches) suggesting
the doves taking some benefit from higher encounter
probability in smaller patches. Perhaps placing our trays
in close proximity caused some assessment ambiguities that
caused doves and cottontails alike to fail to distinguish
patches of different sizes. Kohlmann and Risenhoover
(1998) found that northern bobwhites Colinus virginianus
were able to distinguish among patches of different quality
when the patches were spaced 1.5 m a part, but failed to do
so when they were 0 or 3 m apart. Given our foragers’
ability to distinguish initial food abundance and depth we
find it unlikely that they were unable to detect the area of
these raised plastic trays with distinct rims and boundaries.
More likely, the way the doves and cottontails stand in the
trays while foraging obliterated any advantage to having a
smaller tray. This behavior may have obstructed access to
areas of the patch directly underfoot creating blind spots
that would have increased proportionately as patch size
declined. Smaller trays may exacerbate this blind spot and
cancel any advantages gained from having to search a
smaller area. We may have gotten quite different results had
we buried the trays flush with the surrounding lawn.
Curiously, with the surface of the food patches being
higher than the ground (since we placed the trays directly
on the ground), we never observed doves or cottontails
harvesting food while standing outside of the patches.
Environmental heterogeneity and patchiness represent
both challenge and opportunity for foragers. If the forager
can detect and respond to this heterogeneity then it can
either harvest more in the same amount of time or spend
less effort harvesting a given amount of food. Actually
knowing what a free-ranging animal can and cannot assess is
hard to achieve through direct observations, or within its
uncontrolled environment. Here we let animals reveal their
abilities through artificial food patches placed within their
environment. Such patches can be and have been used to
examine predation risk, diet preferences, habitat selection
and habitat quality (Brown 1988, Kotler and Brown 1988).
When using artificial food patches patch characters such as
substrate selection, patch area and depth are important
properties for establishing a useful tool for challenging the
forager to reveal its perceptions.
We combined standard methods of measuring giving-up
densities from food patches with new metrics (GUDAREA
and GUDVOL) in patches that vary in surface area, substrate
volume and initial resource abundance. We examined and
compared these metrics on the foraging performance of two
different foragers. Both doves and rabbits harvested a higher
proportion of food and biased their feeding efforts towards
rich patches and patches with shallow substrates. The
similar results exhibited by doves and cottontails suggest
that behavioral titrations can be a general and useful tool for
assessing an animal’s perceptions of heterogeneous environments and resources. The predictions and different GUD
metrics should prove useful when developing appropriate
artificial food patches for new taxa. It may be useful to first
expose the study animals to a battery of patch types that
vary in size, initial food abundance, and substrate. Furthermore, varying these patch characteristics may reveal those
factors that most influence the forager’s efficiency. For
research on animals foraging from natural food patches, this
research suggests that clear measures of patch area and patch
‘depth’ may be important. Measures of food availability and
harvest per patch, per unit area, and per unit volume may
provide complementary information on the animal’s foraging responses and even its niche. The alternate hypotheses
and predictions for how initial prey abundance, patch area
and substrate depth should influence patch use behaviors
apply equally to free-ranging and captive animals, and to
experimental as well as natural food patches.
Acknowledgements We thank Thomas Halfpenny from Chicago,
Illinois for allowing us to work in his backyard. We also thank
C. Whelan and S. Emerson for providing comments on earlier
versions of the manuscript, and K. Schmidt for initiating
discussions at ESA, 2006. We thank T. Valone, D. Morris and
B. Kotler for comments that greatly improved the manuscript.
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Appendix 1. The effects of initial abundance of food, substrate
depth and patch size on the giving-up-densities (in log scale),
amount harvested and the proportion of food harvested by mourning
doves and cottontail rabbits (IPA, initial prey abundance). *pB0.05,
**pB0.01, ***pB0.001.
Mourning doves
Source
DF
Depth
IPA
Traysize
Yard
Traysizedepth
IPAdepth
IPAtraysize
IPAtraysizedepth
Error
LGUD
2
2
2
1
4
4
4
8
458
Depth
IPA
Traysize
Yard
Traysizedepth
IPAdepth
IPAtraysize
IPAtraysizedepth
Error
Mean-square
Food harvest
2
2
2
1
4
4
4
8
458
39.396
32.857
1.371
0.009
0.595
0.234
0.063
0.056
0.284
138.823***
115.780***
4.833**
0.033
2.097
0.826
0.224
0.196
86.290
176.939
1.379
0.882
0.275
6.556
0.316
0.119
0.796
108.421***
222.319***
1.733
1.108
0.346
8.238***
0.397
0.149
Proportion of food harvested
Depth
2
5.500
IPA
2
0.240
Traysize
2
0.061
Yard
1
0.097
Traysizedepth
4
0.018
IPAdepth
4
0.027
IPAtraysize
4
0.010
IPAtraysizedepth
8
0.007
Error
458
0.039
Depth
IPA
Traysize
Yard
Traysizedepth
IPAdepth
IPAtraysize
IPAtraysizedepth
Error
GUDAREA
2
15628.812
2
25382.309
2
8401.663
1
178.323
4
723.585
4
1179.823
4
408.472
8
72.872
458
157.975
Depth
IPA
Traysize
Yard
Traysizedepth
IPAdepth
IPAtraysize
IPAtraysizedepth
Error
GUDVOL
2
2
2
1
4
4
4
8
458
Yard
Depth
Traysize
Traysizedepth
Error
F-ratio
10.186
56.000
10.827
0.637
0.100
0.539
0.471
0.048
0.725
GUDVOL standardized
1
0.040
2
6.947
2
3.742
4
0.230
152
0.221
142.386***
6.209**
1.581
2.522
0.453
0.704
0.270
0.181
98.932***
160.673***
53.183***
1.129
4.580***
7.468***
2.586*
0.461
IPA traysizedepth
Error
8
459
0.073
0.180
0.403
Food harvest
2
310.548
2
2124.294
2
2.794
4
9.960
4
15.103
4
2.476
8
2.146
459
15.384
20.187***
138.089***
0.182
0.647
0.982
0.161
0.140
Proportion of food harvested
Depth
2
1.100
IPA
2
0.055
Traysize
2
0.004
Traysizedepth
4
0.041
IPA depth
4
0.028
IPA traysize
4
0.006
IPA traysizedepth
8
0.007
Error
459
0.041
26.767***
1.333
0.102
0.999
0.685
0.141
0.160
Depth
IPA
Traysize
Traysizedepth
IPA depth
IPA traysize
IPA traysizedepth
Error
GUDAREA
2
2994.821
2
41213.132
2
16413.621
4
307.758
4
129.227
4
1461.951
8
20.528
459
139.762
21.428***
294.881***
117.440***
2.202
0.925
10.460***
0.147
Depth
IPA
Traysize
Traysizedepth
IPA depth
IPA traysize
IPA traysizedepth
Error
GUDVOL
2
2
2
4
4
4
8
459
86.341***
118.091***
522.624***
28.126***
9.973***
45.432***
4.144***
Depth
IPA
Traysize
Traysizedepth
IPA depth
IPA traysize
IPA traysizedepth
Error
Depth
Traysize
Traysizedepth
Error
466.115
637.520
2821.403
151.837
53.840
245.269
22.372
5.399
GUDVOL standardized
2
16.306
2
672.583
4
8.864
151
1.881
8.668***
357.533***
4.712***
14.046***
77.222***
14.929***
0.879
0.138
0.744
0.650
0.066
0.179
31.413***
16.919***
1.038
Cottontails
Depth
IPA
Traysize
Traysizedepth
IPAdepth
IPAtraysize
LGUD
2
2
2
4
4
4
5.445
45.713
0.039
0.160
0.117
0.060
30.176***
253.320***
0.218
0.887
0.650
0.333
1731