Bee Foraging Ranges and Their Relationship To Body Size
Bee Foraging Ranges and Their Relationship To Body Size
Bee Foraging Ranges and Their Relationship To Body Size
DOI 10.1007/s00442-007-0752-9
Received: 3 April 2007 / Revised: 3 April 2007 / Accepted: 4 April 2007 / Published online: 5 May 2007
© Springer-Verlag 2007
Abstract Bees are the most important pollinator taxon; to the diVerent techniques that have been used to assess for-
therefore, understanding the scale at which they forage has aging distance. The equations we present can be used to
important ecological implications and conservation appli- predict foraging distances for many bee species, based on a
cations. The foraging ranges for most bee species are simple measurement of body size.
unknown. Foraging distance information is critical for
understanding the scale at which bee populations respond Keywords Body size · Foraging distance · Apoidea ·
to the landscape, assessing the role of bee pollinators in Bee · Pollination
aVecting plant population structure, planning conservation
strategies for plants, and designing bee habitat refugia that
maintain pollination function for wild and crop plants. We Introduction
used data from 96 records of 62 bee species to determine
whether body size predicts foraging distance. We regressed The distance over which animals forage can strongly aVect
maximum and typical foraging distances on body size and their population dynamics, genetic structure, and life his-
found highly signiWcant and explanatory nonlinear relation- tory; it can also aVect these same traits in organisms with
ships. We used a second data set to: (1) compare observed which they interact. As such, foraging distance is a critical
reports of foraging distance to the distances predicted by component for understanding the persistence of populations
our regression equations and (2) assess the biases inherent and species interactions. Foraging distance also inXuences
the spatial characteristics of many community interactions
that have ecosystem-level consequences, such as predation,
parasitism, nutrient transfer, seed dispersal, and pollination
Communicated by Richard Karban.
(Holling 1992; Ritchie and OlV 1999; Roland and Taylor
Electronic supplementary material The online version of this 1997).
article (doi:10.1007/s00442-007-0752-9) contains supplementary Bees are the primary pollinators for most ecological
material, which is available to authorized users. regions of the world (Axelrod 1960; Bawa 1990). Their for-
aging distance strongly inXuences the sexual reproduction
S. S. Greenleaf (&)
Department of Plant Pathology, University of California, of most Xowering plants and can determine the genetic
One Shields Avenue, Davis, CA 95616, USA structure of plant populations (Campbell 1985; Waser et al.
e-mail: [email protected] 1996). For example, pollinators may not visit small or iso-
lated plant populations, leading to plant reproductive failure
N. M. Williams
Department of Biology, Bryn Mawr College, (Cunningham 2000; Lennartsson 2002). Conversely, long-
101 N. Merion Ave, Bryn Mawr, PA 19010, USA distance foraging, even by introduced species, may rescue
mating in otherwise doomed plants within habitat
R. Winfree · C. Kremen fragments (Dick 2001).
Department of Environmental Science, Policy and Management,
University of California, 137 Mulford Hall, Bee foraging distance also aVects agricultural produc-
Berkeley, CA 94720, USA tion. Animal pollination is required to produce 15–30% of
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590 Oecologia (2007) 153:589–596
the US human food supply (McGregor 1976), while 75% of We measure body size using intertegular span, which is a
107 fruit, nut, and vegetable crops that collectively make up robust estimator of body mass (Cane 1987). Rather than
40% of the global plant-food supply beneWt from animal constraining the body size–foraging distance relationship to
pollination (Klein et al. 2006). Crop pollination is enhanced a linear form, as was done in previous studies, we use a
by bees that depend on natural habitats (Greenleaf and power function, and determine not only the strength of the
Kremen 2006a, 2006b; Klein et al. 2003a, 2003b; Kremen relationship but also its shape. We develop a predictive
et al. 2004, 2002; Ricketts 2004). Many wild bees that pol- relationship between body size and foraging distance. We
linate crops nest in natural habitats and forage on crops then use a second data set to compare observed foraging
within their daily travel distance (Ricketts 2004). Foraging distances to the distances predicted from body size and to
distance therefore determines the spatial scale at which test biases in Weld methods that have been used to measure
wild bees can provide pollination services to crops (Kre- bee foraging distance.
men 2005).
Foraging distance has been shown to increase with body
size for various taxa. For example, for some vertebrate Methods
groups, body size is predictive of home range, a metric that
is closely related to foraging distance. For many verte- We reviewed 96 published records of foraging distances
brates, body size and home range area scale according to for 62 bee species from six families (Andrenidae, Apidae,
the function: range = Y0Mb, where Y0 is a constant, M is Colletidae, Halictidae, Megachilidae, and Melittidae). We
body mass, and b is a scaling exponent (Haskell et al. divided these data into two categories: (1) records that
2002). The form of this relationship varies among studies allow for an estimate of maximum foraging distance and
and taxa, and it may be linear or either an increasing or (2) records reporting an observed foraging distance with no
decreasing nonlinear function (e.g., Harestad and Bunnell information on how it relates to maximum foraging dis-
1979; McNab 1963; Milton and May 1976; Schoener 1968; tance. We considered only those records in the Wrst cate-
Turner et al. 1969). Theoretical explanations for the rela- gory for inclusion in the regression analyses of foraging
tionship between body size and foraging distance continue distance on body size. Records that were not used in regres-
to be debated (e.g., Haskell et al. 2002; Jetz et al. 2004; sion analysis were included in our comparison of observed
Kelt and Van Vuren 2001; Makarieva et al. 2005). Evi- and predicted foraging distances and in comparing the
dence suggests that foraging range may increase with body biases in various methods.
size for four insect parasitoid species (Roland and Taylor
1997), but the relationship between body size and home Records of estimated maximum foraging distance
range or foraging distance remains largely undescribed for
most invertebrate taxa. Records that estimated maximum foraging distance used
Three published studies have described relationships three diVerent methodologies: homing, feeder training, and
between bee body size and foraging distance. First, Van bee dance interpretation. In homing research, bees are cap-
Nieuwstadt and Iraheta (1996) described a linear relation- tured at the nest and released at various distances from the
ship between head width and foraging distance for four spe- nest to determine how many bees return from various dis-
cies of stingless bees (Tribe: Meliponini). Head width, tances (e.g., Fabre 1914; see Table S1). In order to produce
however, may not vary predictably with body size across a standardized measure among records, we performed
genera, and families (Cane 1987); thus, these results cannot logistic regressions on the raw data from 15 species to gen-
be generalized to other bee taxa. Second, Gathmann and erate the predicted distance for return of 90% of individuals
Tscharntke (2002) analyzed data from 11 records of 21 sol- (hereafter “maximum homing distance”) and 50% of indi-
itary bee species and found a linear relationship between viduals (hereafter “typical homing distance”). Records that
body length, and foraging distance (r2 = 0.47). The rela- did not provide data on the number of bees released and
tively low predictive power of this relationship may have proportion returned at various distances were excluded
been due to the choice of body length as a measure of bee from regression analyses but were included in our other
size and the lack of consistency in Weld and statistical tech- analyses.
niques between datasets. A third study observed that among In the feeder training technique (e.g., Van Nieuwstadt
four Bombus species, those with larger wingspans were and Iraheta 1996; see Table S2), artiWcial feeders are set
estimated to have larger foraging ranges, but the relation- out near the nest. After a learning period, the feeders are
ship between body size and foraging range was not investi- moved to successively larger distances from the nest until
gated mathematically (Westphal et al. 2006). bees no longer forage at them. The maximum distance at
Here, we re-examine the relationship between body size which bees forage at artiWcial feeders reXects the maxi-
and foraging distance, using data from six families of bee. mum distance at which it is energetically proWtable to
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Oecologia (2007) 153:589–596 591
forage at an artiWcial feeder and will depend on the avail- estimated maximum foraging distance. The maximum for-
ability of alternative resources. For feeder training results aging distance may be greater than the observed distance
we were unable to obtain the original data; therefore, we because the nest may not be located midway between
used the maximum foraging distance estimate reported in where the sisters were collected.
the original studies (hereafter maximum feeder training In the pollen mapping technique (e.g., Packer 1970; see
distance), rather than a maximum predicted foraging dis- Table S3), pollen taken from the nest is identiWed, a Xoral
tance from logistic regression, as above. Some researchers resources map is made, and distance is estimated between
also reported the distance at which bees stopped recruiting the nest and the Xowers from which pollen was collected.
foragers to the artiWcial feeder (hereafter maximum com- This method assumes bees travel to the nearest patch of a
munication distance). given pollen resource; thus, as reported in the literature,
The bee dance interpretation technique (e.g., Beekman pollen mapping measures the minimum foraging distance
and Ratnieks 2000) determines the distance of actual forag- for a particular Xoral resource.
ing trips under natural conditions and can therefore be used In the nest–forager association technique (e.g., Robert-
to measure both typical and maximum foraging distance. It son 1966; see Table S3), nest sites and foraging bees of a
is limited to bees having a dance language and has been particular species are located and the distance between
used to study foraging distance for only four Apis species them is measured. This technique has the potential to mea-
(Dyer and Seeley 1991). We did not analyze data from sure actual foraging distance and could therefore be used to
these four species because the sample size would have been estimate maximum and typical distances. However, the
too small for meaningful statistical analysis. Additionally, research we reviewed did not use marked individuals, and it
we did not review the extensive data on Apis mellifera for- was not clear that all nests in the area had been located.
aging distance that has been collected using the bee dance Thus, the observed foragers may have been from an undis-
interpretation technique, because our focus is on interspe- covered nest.
ciWc, not intraspeciWc, variation. The nest–plant association technique (e.g., Westrich
1996; see Table S3) is only suited for oligolectic bees. Like
Records of observed foraging distance but not maximum the pollen-mapping method, this technique identiWes the
foraging distance distance between the nest site and the nearest Xowers on
which the bees are observed. It shows that the bees forage
Records that reported observed foraging distance but not at least that distance but does not measure maximum or typ-
maximum foraging distance were those using a variety of ical foraging distance.
techniques: mark–recapture, genetic analysis, pollen map- Harmonic radar has been used to track bumble bee for-
ping, nest–forager association, nest–plant association, aging trips (Osborne et al. 1999). This technique had the
harmonic radar, and nest site addition. In the mark–recap- advantage of recording actual foraging trips and therefore
ture technique, bees are marked at the nest and located had the potential for determining maximum and typical
while foraging (e.g., Kapyla 1978; see Table S3). This foraging distances. However, many of the bees that were
method has the advantage of directly observing the dis- observed Xew beyond the radar’s range of 600 m and/or
tance of actual foraging trips. However, search area were lost as they Xew behind physical barriers such as
expands as the square of the distance from the nest, so the hedges.
number of marked bees in the landscape is quickly In the nest site addition method (Gathmann and Tscharn-
diluted. Most of the data we found were not obtained with tke 2002), nest boxes are placed at diVerent distances from
equal sample eVort per unit area and the number of recap- Xowers. If bees nest successfully in boxes located some dis-
tured bees was too small to rarify the data to correct for tance from the nearest Xowers, then one can conclude that
unequal sample eVort (e.g., Walther-Hellwig and Frankl bees forage at least that far.
2000). Without suYcient sample eVort near the outer edge
of the foraging range, it is not possible to determine maxi- Measuring body size
mum foraging distance, and unequal search eVort at diVer-
ent distances precludes the determination of typical For all species for which we found foraging distance data,
foraging distance. we assessed body size by measuring the distance between
In the genetic analysis approach (Darvill et al. 2004; the wing bases, intertegular (IT) span, on a sample of 5–10
Knight et al. 2005; see Table S3), foraging social bees are individuals, using a dissecting microscope and calibrated
collected along a transect across a landscape, and tested to ocular micrometer (Tables S1–S3). IT span measures the
determine which bees are sisters (i.e., are foraging from the thorax, which contains the Xight muscles, and is empiri-
same nest). One-half of the distance between the locations cally related to dry body mass: IT span = 0.77(mass)0.405
where a pair of sisters was collected is the minimum (R2 = 0.96; mass in mg and IT in mm; Cane 1987).
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592 Oecologia (2007) 153:589–596
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Oecologia (2007) 153:589–596 593
Table 1 Parameters (mean § 95% conWdence levels) describing relationship between the log of intertegular (IT) span (X) and the log of foraging
distance (Y) according to the function log Y = log a + b log X
Dependent variable n log a b R2 F
Maximum homing distance (km) 16 ¡1.363 § 0.517 3.366 § 1.084 0.776 45.02
Typical homing distance (km) 16 ¡1.643 § 0.582 3.242 § 1.218 0.718 33.05
Maximum feeder training distance (km) 17 ¡0.760 § 0.412 2.313 § 1.155 0.548 18.20
Maximum communication distance (km) 13 ¡0.993 § 0.521 2.788 § 1.314 0.665 21.80
All P values <0.001
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594 Oecologia (2007) 153:589–596
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Oecologia (2007) 153:589–596 595
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