Bumblebee Response to Variation in Nectar Availability
Author(s): John M. Pleasants
Source: Ecology, Vol. 62, No. 6 (Dec., 1981), pp. 1648-1661
Published by: Ecological Society of America
Stable URL: http://www.jstor.org/stable/1941519
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Ecology, 62(6), 1981, pp. 1648-1661
© 1981 by the Ecological Society of America
BUMBLEBEE
RESPONSE
TO VARIATION
IN NECTAR
AVAILABILITY1
JOHN M. PLEASANTS
Department of Botany, Iowa State University, Ames, Iowa 50011 USA
Abstract. I examined the response of bumblebees to two kinds of spatial variation and two kinds
of temporal variation in nectar levels. The spatial variation involved differences in reward value
among plant species and differences in nectar availability among patches of flowers of a single species.
The temporal variation involved changes in nectar availability over a season and between years. In
all cases the response of bees was measured by differences in bee density or abundance.
The response of bees to different plant species was determined by the density of foraging bees on
the flowers of each species at a given time (bee: flower ratio = B/F). I examined several groups of
plant species whose members overlapped in their flowering periods and in their bumblebee visitors.
Within a group, the relative magnitudes of the B/F's for species indicate the degree to which their
flowers are preferred by bees. If bees are optimal foragers, preference should reflect the per-flower
reward value of species. I characterized the potential reward value of species by their nectar production rates (NPR's). The bees' preference for species was found to be very similar to the relative
magnitudes of their NPR's. I also considered whether including the time and energy costs of foraging
on the different species would produce a better predictor of preference. While these factors did affect
the absolute reward value of species they did not influence their reward value relative to one another.
Foraging costs are most likely to have no effect on preference when species have similar floral
morphologies.
To assess the response of bees to differences in patch quality I bagged some of the inflorescences
in an experimental patch. Following this reduction in the number of flowers, the number of bees in
the patch decreased proportionately, producing a B/F very similar to that of a control patch. When
the bagging was removed the number of bees increased such that the B/F was again similar to that
of the control patch. In general these results provide further support for optimal foraging in bumblebees.
I examined the response of bees to temporal variation in nectar levels to determine whether
resource limitation for bumblebees changed over time. Seasonal changes in the abundances of three
bumblebee species were compared with seasonal changes in the total nectar production by the plants
each bee visited. Preference factors were used to convert floral production to nectar production. In
general, seasonal production and utilization were closely matched, indicating no major change in
nectar resource limitation. The cumulative numbers of bees seen during each of two summer seasons
(1974 and 1975) were very similar. This indicates that the resource base, which had not changed
between years, was capable of supporting only a limited number of bees. During 1975 a natural
species removal experiment occurred which allowed an assessment of competition among bees. Apis
mellifera, which had been well represented in 1974, was absent. The bumblebees of short and medium
tongue length with which honeybees overlapped in resource use exhibited competitive release. Their
abundances increased in 1975 resulting in near-perfect density compensation.
Key wvords: bumblebees; competitive release; density compensation; nectar production rate;
optimal foraging; pollinators; preference.
INTRODUCTION
A currently active area of inquiry in ecology is concerned with whether animals forage in a manner which
optimizes their energy intake rate (see reviews by
Schoener 1971 and Pyke et al. 1977). Three important
aspects of this question are which types of food items
to eat (optimal diet), whether to stay in one patch or
move to another (optimal patch choice), and how to
move between resource points (optimal movement
patterns). Some answers to these questions can be
obtained by observing animals in choice situations,
i.e., where there is some variation in the types of food
items, quality of patches, or reward value of resource
points available. One animal group which has received
a good deal of attention with regard to optimal foraging
is bumblebees. This is because there is less difficulty
Manuscript received 20 June 1980; revised and accepted
12 December 1980.
with bees in quantifying the reward value and spatial
distribution of the resources they use (nectar) and in
observing their foraging behavior. Most of the work
done on bumblebees has been directed at optimal
movement patterns (Pyke 1978b, c, d, Heinrich 1979a,
Zimmerman 1979), while little work has been done on
the first two aspects of the question. In this paper I
explore these two aspects of optimal foraging by examining the response of bumblebees to two types of
variation in nectar resources: differences among plant
species in nectar rewards and differences in nectar
availability between patches of flowers of a single
species. If bumblebees forage in an efficient, optimal
manner we would expect them to forage more heavily
on species which provide a greater energetic reward.
The primary factor influencing the reward value of a
species is its nectar production rate (NPR). Therefore,
species whose flowers have higher NPR's should be
more attractive to bees and should be preferred by
December 1981
BEE RESPONSE TO NECTAR AVAILABILITY
them. This preference will be manifested in a higher
number of foraging bees relative to the available number of flowers (bee: flower ratio = B/F). We would
also expect optimally foraging bees to concentrate
their foraging activity in patches of flowers which provide the greatest reward. Rather than looking at the
behavior of individual bees, which has been the most
common approach in these kinds of studies, I have
examined the collective response of bees by measuring
differences in bee density on flowers.
A second major question, also involving the response of bees to variation in resource levels, is
whether the degree of resource limitation for bees
changes over time. The degree of resource limitation
will determine the strength of selection pressures for
competitive displacement and resource partitioning
among bumblebee species. It will also affect selection
for adaptations to increase foraging efficiency. Resource limitation was studied by examining the response of bees to variation in total plant nectar production over a season and variation in nectar
production and availability between years. Response
was measured by changes in bee abundance.
The plant species involved in this study grow in
mountain meadow habitats. The pollinator fauna of
these communities is dominated by bumblebees (responsible for >70% of all observed insect pollinator
visits; Pleasants 1977). Several studies have shown
that in bumblebee communities there is a partitioning
of plant resources (Heinrich 1976b, Inouye 1976,
Pleasants 1977, 1980). Partitioning results from different bumblebee species foraging on different plant
species. In general, coexisting bumblebee species fall
into different tongue length classes (short, medium,
long) and the average corolla depth of flowers they
visit is similar to worker bee tongue length (Inouye
1976, Pleasants 1980). These displacement patterns are
good inferential evidence that competition among
bumblebees for nectar resources is important, implying that nectar is a limiting resource. This is further
corroborated by the increasing wealth of evidence on
bee behavioral adaptations and foraging strategies
which serve to maximize energetic returns. Because
of the association between a particular bumblebee and
a set of plant species, each meadow plant community
can be divided into several guilds of plant species
(Pleasants 1977, 1980). The members of a particular
guild all receive the largest proportion of their pollinator visits from the same bumblebee species. In general, guild members avoid competition for pollinators
by having blooming periods which show a regular temporal segregation over the summer season (Pleasants
1977, 1980).
METHODS
In this study I used data on plants and bumblebee
pollinators collected primarily from two study sites.
The sites, numbered 1 and 2, are located on the west-
1649
ern slope of the Rocky Mountains in the Gunnison
National Forest near Crested Butte, Colorado and are
at elevations of 2590 and 2743 m, respectively. The
sites consist of 0.6 and 2.4 ha of meadow surrounded
by aspen trees. A third site, Site 3 (3040 m), is a meadow surrounded by Engelmann spruce.
To examine the response of bumblebees to variation
among plant species in nectar production, I compared
the nectar production rates of four groups of species
with the degree of preference shown towards them by
bumblebees. Nectar sugar production rates were determined for noncomposite species by bagging inflorescences and marking flowers that were just about to
open. I then removed and measured the volume of
nectar which had accumulated during the life-span of
the flower using a capillary tube (5, 10, or 25 /xL). The
sugar concentration of the nectar was measured with
a hand-held Bausch and Lomb temperature-compensated refractometer. The total sugar produced per
flower was divided by flower longevity so that nectar
production rate (NPR) was expressed on a 24-h basis.
There was no indication for any of the species studied
that NPR was influenced by the presence of accumulated nectar (J. Pleasants, personal observation). I examined 20-50 flowers for each species. Nectar sugar
production by composites (family Asteraceae) was
measured in a different manner because I was unable
to extract the small amount of nectar from the florets
using a capillary tube. Composite florets remained
open for 2 d. During day I they were in the male (pollen-shedding) phase and on day 2 they were in the
female condition (style branches separated). Flower
heads were bagged for I d and the nectar accumulation
in both male and female phase florets was sampled
(the nectar in female phase florets represents only I
d of production because virtually all of the nectar production from the previous day was removed [J. Pleasants, personal observation]). The amount of nectar
sugar in florets was measured by flushing them with
3 ,uL of distilled water using a 10- tL syringe equipped
with a Chaney adapter (Hamilton Corporation, Reno,
Nevada). The resulting solution was removed with
either the syringe or a 5-,uL capillary tube and placed
in a refractometer to determine percent sugar. The
average of male and female floret sugar production
was used to get a daily rate.
The preference for a species was measured by the
number of bee visitors per flower (BIF). BIF is equivalent to a snapshot census of bees on flowers. It is the
number of bees seen on flowers during a 1-2 min scan
of a patch of flowers divided by the number of flowers
in the patch. Each bee in the patch is counted only
once. The differences in preference shown towards
two or more species within a group were expressed on
a relative scale. The most preferred species (highest
BIF in the group) was given a preference rating of
1.00. The preference rating for each of the other
species was related to this standard by dividing its BIF
1650
JOHN M. PLEASANTS
by that of the most preferred species. Relative preference was calculated at several times during the flowering period of each species and then averaged over
all times. The following pairs of species were examined. At Site 2 there are two legume species, Lathyrus
leucanthus and Vicia americana, which have extensive temporal and spatial overlap and receive the majority of their visits from Bombus appositus (Pleasants
1980). In 1975 the number of bumblebees on each of
these species was sampled at four different times during their blooming period. On the same day a portion
of the meadow was sampled by transect and quadrat
to estimate the relative number of open flowers for
each species. While this did not allow me to calculate
the actual BIF for each species it did give an indication
of the relative preference for each species. At Site 2,
an 8 m x 8 m patch of Agastache urticifjlia (Lamiaceae) and a 9 m x 7 m patch of Polemonium foliosissimun (Polemoniaceae) were monitored over a 15d period in 1978. These species are visited by both
Bombus bijfirius and B. flaviJfrons. On five different
days during this period the number of bees in each of
these patches was recorded at midmorning, late morning, and early afternoon. The number of flowers open
on each census day in each patch was obtained by
extrapolation from a flowering curve based on several
flower censuses made during this period. At Site 3,
two 8 m x 8 m patches containing both Delphinium
barbevi (Ranunculaceae) and Corydalis caseana (Fumariaceae) were monitored over a 15-d period in 1978.
These species are visited by B. flavifrons and B. appositus. During this period five bee censuses were
made. Each census was made sometime between 0930
and 1200. The number of open flowers of each species
was counted in the patches after each census. A group
of five composite species was studied at Site 2 in 1978.
These species have broadly overlapping blooming periods and are visited primarily by B. biiarius with B.
flavlifJronsas a minor visitor to two of them. In four 10
m x 10 m patches the number of bees on each species
was monitored two to three times during the day at
four times over a 15-d period. On each census day the
number of flower heads with open florets was counted
and the number of open florets per flower head (from
a sample of 20-40 flower heads) was estimated.
To estimate the costs of foraging in these species
I timed bees foraging on flowers. Two stopwatches
were used, one to record the total period of observation and the other to record handling time. For species
with inflorescences that required bees to fly between
adjacent flowers, handling time was equal to the time
spent in flowers. For species with inflorescences that
allowed bees to walk between adjacent flowers, handling time included in-flower time and walking time.
Travel time (either between flowers or inflorescences)
was equal to the difference between total time and
handling time. Handling and travel time were expressed on a per-flower basis by dividing by the num-
Ecology, Vol. 62, No. 6
ber of flowers visited. Bees were observed for a minimum of 20 visits per foraging bout. Data on 200-1000
flower visits were obtained for each plant species.
I conducted resource reduction experiments in the
summer of 1978 on two species, Agastache urticiiolia
(at Site 2) and Delphinium barbeyi (at Site 3). For each
species I delineated two patches consisting of numerous inflorescences, within a large stand. Patches were
10 m x 10 m and were 3-5 m apart. The number of
open flowers in each patch was counted. The two
patches were designed to contain approximately equal
numbers of flowers. On the day of the experiment I
censused each patch for the number of bees visiting
flowers of the subject species. The number of flowers
was reduced in one patch (experimental) at = 1100 by
placing nylon netting (bridal veil) over a number of
inflorescences. The number of flowers under the bagging was counted. After 0.5-1 h I recensused the experimental and control patches. The bagging remained
on the inflorescences for -24 h. Prior to removing the
bagging I censused each patch. I then removed the
bagging and censused again. The bee densities reported here are an average of several censuses that were
made at different times shortly before and after treatments.
In determining the response of bumblebees to seasonal changes in nectar availability I focused on Bornbus bifarius at Site I and B. bifirius and B. flavifrons
at Site 2. These bees were chosen because of the large
amount of data on their activity and on the floral resource production of the species they visited. The data
were collected during the months of June through August 1975. The change in abundance of each bee
species over the season was compared with the change
in nectar production by the species they visited. A
measure of bumblebee abundance was obtained from
60-90 min censuses made every 5-6 d at each site.
The census consisted of a slow walk by two observers
3-5 m apart along a fixed route through the meadow.
Bees seen on flowers were identified (conspicuous differences in thoracic and abdominal markings made
field identification of bumblebees possible) and the
plant species was recorded as well as whether the bee
was collecting pollen or nectar. To control for any
diurnal changes in bumblebee activity, censuses were
always conducted at the same time of day (between
1000 and 1200). The abundance results have been standardized to the average number of bees seen per 30
min of census time. To assess nectar availability I first
determined the daily number of open flowers for each
species by multiplying the proportion of its flowers
open on a particular day (from flowering curves) by
the total number of flowers it produced (per square
metre) over its blooming period (see Pleasants 1980
for details). For species in the Asteraceae the number
of flower heads with open florets was used instead of
the number of open flowers. As discussed below, the
preference of bumblebees for foraging on different
December 1981
I ABLE
BEE RESPONSETO NECTAR AVAILABILITY
1651
1. Comparison of relative reward value of plant species and degree to which they are preferred by bees.
1
/ L
2
4
Average
5
6
(B/F) x
100
Relative
reward
value
Relative
attractiveness
(preferencerating)
no. per
visitors
per flower
Sugar
nectar concenflower-' tration
Species
3
mg sugar
per flower*
(24 h)-'
(%)
1.96
0.46
41
16
0.804
0.074
2.13t
0.16t
0.092
2.92
0.71
46
40
1.330
0.280
0.624
0.073
0.210
1.000
0.138
0.38
0.59
48
36
0.182
0.214
0.468
0.410
0.851
1.000
1.000
0.900
Group 1
Vicia americana
Lathvrus leuc(anthus
1.000
1.000
0.075
Group2
Delphinium barbevi
Corxvdalisca.seana
1.000
Group3
Agaastache urti(cifolia
Poleimonium Joliosissimum
per
per
per
per
per
per
florett
head§
floret
floret
head
floret
head
.301
.330
.106
.083
.024
15.77
9.04
2.27
.85
.27
.274
.328
.063
.085
.012
0.91
1.00
0.32
0.25
0.07
1.00
0.57
0.14
0.05
0.02
0.84
1.00
0.39
0.35
0.09
1.00
0.62
0.19
0.08
0.02
per
Group4
Rudbeckia montana (R.m.)
Helianthella quinquenervis
(H.(q.)
Helenium hoopesii (H.h.)
Vig,iiera nmulltiflora(V.m.)
Erigeron speciosus (E.s.)
' Column I x Column2.
t Only an index.
t For Rudbchkia montana and Helianthella quinquenervis this is an average of first-day (d phase) and second-day (D
phase) NPR for florets. These are the only composites with nectar production on the second day and where second day
florets are visited by bees.
§ Based on the following average number of florets per head: R. m. 52.4 (d + Y), H. q. 27.4 (d + Y), H. h. 21.4 (d),
V. im. 10.2 (d), E. s. 11.1 (d).
species seems to be a good indicator of their potential
reward value (nectar production rate). To convert the
number of open flowers for a species visited by a particular bumblebee into the amount of nectar it represented to that bee, the number of open flowers was
multiplied by the species' preference rating. Preference ratings were calculated in the following manner:
On each day that the pollinator census was made the
number of bumblebees of a particular species seen on
each plant species was recorded. This number was
divided by the estimate of the number of open flowers
of the species giving a BIF value. Standardized preference ratings were obtained from B/F's as described
earlier. The preference rating for each species is an
average of its rating for each census time. To estimate
the total amount of nectar available to a particular
bumblebee species on a given day I used the formula
E
summers of 1974 and 1975. As an estimate of the total
number of bees seen during each summer I used the
area under the curves of bee abundance plotted against
time (see Figs. 6 and 7). Since I spent a shorter period
of time at the study sites in 1975, I used the area under
an equivalent portion of the 1974 curve (marked by
arrows in Figs. 6 and 7) to make the 1975 bumblebee
abundance estimates comparable to those for 1974. By
knowing what species were in bloom and the stage of
their blooming at the conclusion of my stay in 1975,
I could determine the same point in time in 1974. This
means that fewer calendar days were under consideration in 1975. This is because the flowering season
in 1975, although delayed at the start, proceeded more
rapidly than in 1974, with species' blooming periods
being as much as 5-7 d ahead of 1974 after an equal
number of calendar days.
Pin;, where p, is the standardized preference shown
shown by that bumblebee species for plant species i,
ni is the number of flowers of species i open on that
day, and s represents the entire set of plant species
visited by that bumblebee.
To determine the year-to-year response of bumblebees to differences in nectar availability I used data
on bee abundances and floral production from the
RESULTS
Response
AND DISCUSSION
to differences
among species
I examined four groups of species to determine if
the preference shown by bees towards the members
of each group was related to their reward value. Each
group was composed of species which had rather
broad overlap in their time of flowering and species of
1652
JOHN M. PLEASANTS
Ecology, Vol. 62, No. 6
TABLE2. Estimatesof foragingrewardand costs.
2
I
Time per flower (s)
Plantspecies
Handling* Travelingt
Group 2
Delphinium barbevi
Corvdalis caseana
Average
interval
between
successive
visits to
a flower
4
5
6
Cost
(Cost/
reward)
Net energy
intake rate
3
(s)t
Average
reward/
per
flower
(J)§
x100
(J/s)¶
.080
.193
31
33
.0632
.1113
(J)
1.86
1.01
1.72
444
4904
.254
.590
1.67
2.89
0.10
1.33
378
1032
.030
.017
.095
.059
56
57
.0075
.0096
.119
.0038
.0038
.0033
.0046
.0054
3.2
4.3
4.8
12.3
6.4
.0912
.0828
1.76
Group3
Agastache urticifolia
Polemonium foliosissimum
Group4
1.24
Rudbc'kia montana
Helianthella quinquenervis
Helenium hoopcsii
Viguicra munltiflora
Erigeron speciosus
0.96
0.86
0.79
0.81
.023
.044
.054
.118
.138
922
612
1451
1068
7900
.087
.066
.038
.082
.0690
.0368
.0803
* Th; for Agastache urticifoliaand all composites this includes nonflighttravel time between flowers on an inflorescence.
t T,; based on average flighttime between flowers and between inflorescencesper flower (= total flighttime per inflorescence/averagenumberof flowers visited per inflorescence).
t (FIB)(Th + T,).
§ SJ, = column 2 x NPR x J,; NPR (mg sugar/s)from Table 1, assumingthat 24-hrnectar accumulationwas produced
over a 10-h daylight period; J, = 15.48 J/mg (IJ = .239 cal).
ThJh + TtJ,; based on 0.034 J g- .s--' for handling and nonflight travel, 0.435 J-g-
. s-
for flight (Pyke 1978a); worker
body mass B. appositus 0.28g, B. flavifrons 0.13g, B. bifarius0.06g (Pyke 1978a). The body mass used to calculate cost is
a weightedaveragebased on frequencyof visits to a plant species by differentbumblebees.Thermoregulationcosts are not
included.
11(Column3 - column 4)/(T,,+ T,).
bumblebee visitors. The potential reward value of
species was measured by their nectar production
rates. Preference was measured by the number of bees
per flower (B/F) on a species. Preference in this paper
refers to how a population of foraging bees is dispersed
over the available flowers of the various plant species
at some point in time. It does not imply anything about
the frequency of visitation by individual bees to various species during a foraging trip (cf. Heinrich 1979b).
The results (Table 1) show a fairly close correspondence between the relative reward value of flowers
(column 5) and the relative number of bees seen on
them (column 6). Heinrich (1976b) presents similar
evidence for five species in a Maine bog.
I investigated whether the slight deviations between
some of the values in columns 5 and 6 could be explained by considering other factors which might influence a species' reward value. The precise definition
of reward value is the net energy intake rate a bee
experiences while foraging on a species. The general
expression for net energy intake rate is
EIT =
C
T
(1)
where G = the energetic gain from a flower (energy
from nectar sugar), C = the energetic cost involved
in obtaining the nectar (energy expended in handling
a flower and traveling to the next), and T = the time
required to obtain the nectar (handling and traveling
time per flower). NPR only affects G. Does a consideration of the time and energy costs of foraging change
the reward value from that based on NPR alone'? A
more detailed version of Eq. 1 can be written (simplified from Pyke 1978a) as follows:
EIT=
SJ, - (ThJh + T,J,)
Th + Tt
(2)
where S = average standing crop of nectar sugar per
flower in milligrams, J,, = joules per milligram nectar
sugar, Th = average handling time per flower, T =
average traveling time per flower (includes a withininflorescence and between-inflorescence component),
Jh = cost of handling per unit time (joules per second), and Jt = cost of traveling per unit time (joules
per second). S will be equal to the average time interval between successive visits to a flower times the
rate of nectar production. It can be shown that the
average intervisit interval is equal to the reciprocal of
the number of bees foraging per flower (FIB) multiplied by the time per flower (Th + T,). Thus
S = (F/B)(Th + T,)NPR.
(3)
When the energetic costs of foraging (ThJh + TtJt) are
small relative to the energetic gain (SJ), the cost com-
1653
BEE RESPONSE TO NECTAR AVAILABILITY
December 1981
5 *25
v-
o 4
.,...
1O
I
3
3
.,
I|
I |
|I
a
_1
1
E
C
E
unbagged
C
bagged
bagged
DAY 1
C
E
E
C
unbagged
DAY 2
FIG. 1. Agastache urticifolia resource reduction experiment. E = experimental patch, C = control patch. On day I some
inflorescences were bagged in the experimental patch to reduce nectar availability. On day 2 the bagging was removed. Bee
numbers were censused in control and experimental patches before and after each treatment on each day.
ponent can be ignored, making the net energy intake
rate approximately equal to the gross energy intake
rate.
E/T
ers can be visited does not affect reward value (contra
Heinrich 1979b). For example, consider a species with
a given number of bees foraging on it and with a given
time per flower (Th + T,). What would happen to the
reward value of this species (E/T) if flowers could be
visited twice as rapidly [(Th + T,)/2]? It would mean
that the average intervisit interval would be halved
and therefore the average standing crop of nectar
would be half of what it was before. Bees would spend
(F/B)(T, + T,)NPR J,,
(T,, + T,)
SJ,,
T, + T,
NPR J,.
=FIB
(4)
Note that the handling and traveling time terms cancel
out. What this indicates is that the rate at which flow-
3
30 [
25
a)
c
0
-0
2 ° 20
0
-o
0
In
a)
15
0
a)
-0
_0
>
0
1
) 10
aQ
a)
-0 5
C
E
E
unbagged
bagged
DAY 1
FIG. 2.
C
C
E
E
bagged
C
unbagged
DAY 2
Delphinium barbeyi resource reduction experiment. Details as in Fig. 1.
1654
JOHN M. PLEASANTS
Ecology, Vol. 62, No. 6
TABLE3. Preference ratings for plant species. All plant species in the family Asteraceae except: Polemronium (Polemoniaceae). Hvdrophvylum (Hydrophyllaceae), Agastache (Lamiaceae), Geranium (Geraniaceae), and Vicia (Fabaceae). Preference factors for composites measured per head.
Site 2
Site 1
Visited by: Bombus biflarius*
Preference
Plant species
factor
Rudbeckia montana
Helenium hoopesii
Vi,guier mulzIltif(ioru
Geranium Jremontii
HydrophylvlumfJndleri
Erigeron speciiosus
1.00
0.50
0.10
0.08
0.03
0.02
Bombus bifarius
Site 2
Bombus flavifrons
Plant species
Preference
factor
Rudbeckia montana
Hvdrophyllumrfndleri
Wyethia amplexicaulis
Helianthella quinquenervis
Helenium hoopesii
Viguiera mulhltiflora
Polemonium Joliosissimum
Erigeron speciosus
1.00
0.66
0.49
0.46
0.21
0.10
0.03
0.02
Plant species
Preference
factor
Hydrophyllum fendleri
Wyethia amplexic'aulis
Agastache urticifJlia
Vicia americana
Helianthella quinquenervis
Polemonium foliosissimum
Rudbeckia montana
1.00
0.59
0.09
0.04
0.03
0.03
0.01
' See Pleasants (1980) for data on the extent to which plant species are shared with another bumblebees species.
half as much time per flower as before and receive half
as much reward; thus the E/T would not change.
What then is the relationship between preference
(BIF) and NPR? If bees are foraging optimally and
basing their choice of forage species on energy intake
rate, then, when all bees have made their choice, the
reward value of all plant species should be equal (see
General Discussion). For two species with equal reward values
(F/B),NPR,J,
= (F/B)NPRJ,,,
(5)
where subscripts refer to species 1 and 2, respectively.
After rearrangement Eq. 4 becomes
(BIF),
(BIF)2
_ NPR1
NPR2
(Table 2) show that the net energy intake rate is very
similar for the species within each group. This is what
optimal foraging would predict and is what was assumed to occur so as to set up Eq. 5. The results also
show that for the five composites in Group 4, foraging
costs are a small percentage of the reward obtained,
justifying the approximation in Eq. 4. For the pairs of
species in Groups 3 and 4 foraging costs are more
significant. In addition these costs are probably underestimates because energy expenditures for thermoregulation, which are difficult to estimate (Pyke 1980), are
not included. However, in both groups energy expenditures are the same percentage of gain for each member. This is also true for the composites in Group 4,
the species in Group 1, and the two species examined
by Pyke (1980). Consequently, Eq. 1 can be rewritten
(B F) /(B F)2 is the bees' relative preference for
E/T =
, where p is the proportionality constant
T
for
NPR
the
relative
is
and
I
NPR,/NPR2
species
relating cost to gain. For two species with the same
species 1. Thus, theoretically, preference should only
when bee foraging has equalized reward values (see
p,
be a function of NPR.
General
Discussion),
This conclusion is based on the assumption that enG1 - pG1 _ G2 - pG2
ergy costs of foraging are negligible compared to enT,
T,
ergy gain. Is this the case? One would expect that
the
term
for
After rearrangement
cancels, indicating
p
since bumblebee workers are not foraging only
themselves, they would have to maintain a sizeable that once again the relative reward value of two
profit margin. In the few studies where cost as well as species is a function of their gross energy intake rate
gain was measured, the cost as a percentage of the and thus their NPR's alone, as in Eq. 6. Why should
gain varied with time of day, season, and year, and the cost percentage be so similar within each group'?
with ambient temperature (Heinrich 1975a, Pyke One way this can occur is if the floral morphologies
1978&, 1980). In some cases the costs were significant. of the species in the group are similar, such that hanFor the two species examined by Pyke (1980) costs dling and traveling times are similar. In fact it can be
averaged =34% of the gain, a value too large to be shown that foraging costs can be ignored whenever
ignored. I estimated gain and cost for the species in traveling (or handling) time per flower is the same proTable 1. 1 was not able to measure directly the gain portion of total time per flower for both species. Each
for these species because I did not measure the stand- of the groups in Table 1 is composed of species with
ing crops of nectar. Except for the species in Group similar floral morphologies except Group 3. A. urtiI standing crops were too small to be measured by cifolia has small flowers which are densely arranged
extraction with capillary tubes. However I did esti- on a spike allowing bees to walk between them. P.
mate standing crop using Eq. 3. Lathyrus and Vicia foliosissimum inflorescences are composed of numerwere not included in this analysis because BIF values ous clusters of two to three flowers which are not arfor them were only indices. First of all, the results ranged in any regular fashion. Bees must fly between
BEE RESPONSE TO NECTAR AVAILABILITY
Decenmber 1981
wards them. I then considered whether the rate at
which flowers could be visited (Th + T,) and the costs
of foraging should be included along with NPR to provide a more precise measure of reward value. Time
and energy costs of foraging cancelled out when comparing species. Thus, although time and energy costs
do affect the absolute reward value of a species, they
do not affect its reward value relative to another
species. Only NPR differences influence reward value
and consequently determine preference.
Variation in patch quality
5(
LJ
HZ
4r
0
rl(,
LJ -
-
/
G
LU
·/
/
LU
20/
Resource
I
0-
/
2
28
JUNE
FIG. 3.
/
/
l
/
/
B biforius
1
1
8
18
JULY
1
7
AUGUST
28
1655
Comparison of seasonal change in total available
nectarproductionby plant species visited by B. bifariuswith
seasonal change in B. bifjrius abundance.
clusters. Because flying costs are 13 times greater than
nonflight costs (see footnote", Table 2), the lower
energetic cost of foraging on A. urticifjolia flowers may
explain why it is slightly more preferred than expected
based on NPR alone (Table 1). Despite the difference
in floral morphology for these two species the cost is
the same proportion of the gain for both (Table 2),
indicating that NPR alone is still the dominant influence on preference. Whether the similarity in cost percentage among species visited by the same bees is a
general pattern, regardless of floral morphology, remains to be seen.
To summarize, in trying to characterize the reward
values of species I initially considered only the relative
magnitude of their NPR's, which is related to the gross
energy intake rate. This was found to be closely correlated with the relative preference shown by bees to-
To understand how bees respond to patches of flowers that differ in reward expectations I experimentally
reduced the number of flowers within one of two
patches of Agastache urticijolia at Site 2 and of Delphinium barbeyi at Site 3. The numbers of bees in the
experimental patch and in the control patch were censused before and after the reduction. The results are
shown in Figs. 1 and 2. Immediately after the resource
reduction the bees in the experimental patch experienced a reduced average reward per flower because
of the now higher BIF ratio. According to optimal foraging theory (Charnov 1976, Pyke et al. 1977) a bee
should leave a patch when the reward expectation falls
below the expectation from other patches. Whether or
not bees are responding in this manner will be most
apparent when the BIF ratio is examined. Under the
null hypothesis we would expect no change in the bee
density in the patch following bagging of inflorescences. This would be manifested by a higher ratio of
bees to available (unbagged) flowers relative to the
control patch. The percent increase in BIF would be
equal to the percent decrease in the number of flowers
in the patch. If bees forage optimally we would expect
bee density to decrease in the experimental patch such
that the BIF remains similar to that for the control
patch. To evaluate the effect of bagging I have com-
50
(I-)
SITE 2
uJ
SITE 2
D
z 40-
40-
2
0
r1r)
(I-)
30-
30-
/
\
cnI
L-J
D
m 20-
/
20/
B tlavifrons
biforius
*14
w
0
0Resource
LLi
10.
/
I
D
z
30
JUNE
I-.'
_ I
10
20
JULY
I
1
30
9
AUGUST
-_-
·
30
JUNE
~l
mw
10
I
I
I
I
20
30
9
JULY
AUGUST
FI;. 4. Comparisons of seasonal change in total available nectar production by the plant species visited by B. hifjrius
or B. flaviiJrons and the seasonal change in the abundance of B. bifjrius or B. flavifrons.
JOHN M. PLEASANTS
1656
Ecology, Vol. 62, No. 6
the behavior of individual bees in the patch. They
stayed longer in flowers and on inflorescences (J.
*
Pleasants, personal observation; also see Heinrich
·S
u
1979a and Inouye 1978 for similar observations).
z
30<
One feature of Fig. 2 that deserves comment is the
markedly
higher BIF for both experimental and con* zr
D~
<
*trol
patches on the 2nd d of the experiment. This was
20probably due to the fact that the experiment was con'
near the end of the flowering season (18 and 19
eeducted
,,
when the blooming of most species was endcnJ
*August)
Q
had nowhere else to go. In fact, the numand
bees
ing
10ber of open flowers in the control patch declined by
50% from the 1st d of the experiment to the
·~*~~
~~~~almost
J ^~~~second.
LJ[~
~~ Despite the overall higher bee densities and
thus the lower average profit margin on the 2nd d, the
10
30
20
40
BF's for both patches remained similar. This does not
RESOURCE
ABUNDANCE
imply that the bees' method of choosing acceptable
FIG. 5. Correlationbetween amount of nectar resource foraging locations has changed, but only that their noavailableand bee abundance.Data points from census times tion of what was an acceptable reward had been low40-
in Figs. 3 and 4. r = .92, P < .001.
ered.
Seasonal variation in nectar availability
pared the BIF for the experimental patch after treatment with the BIF for the control patch at that time.
I have not compared the after-treatment BIF with the
before-treatment B/F because some of the differences
between these two could be due to diurnal fluctuations
in bee density unrelated to the experiment. For Agastache urti('iolia the available resource was reduced
by 31.7% in the experimental patch. As predicted, the
BIF ratio remained similar to that for the control
patch, being only 4.7% higher. For Delphinium barbeyi the results were somewhat equivocal. The number of flowers was reduced by 48.2% in the experimental patch. However, in this case the BIF
increased, being 22.4% higher than the control patch.
This is still a smaller increase than would be expected
under the null hypothesis, indicating some movement
of bees from the patch.
The experimental design also made it possible to
test the response of bees to resource augmentation.
When the bagging was removed, the nectar which had
accumulated in the bagged inflorescences over the previous day became available. Under the null hypothesis
we would expect no change in bee density following
removal of the bagging, which would result in a lower
BIF ratio. For Agastache urticijolia the available
number of flowers increased by 31.7% as a result of
removing the bagging. Thirty minutes later, when the
patch was censused, the BIF was already back to within control levels (only 8.9% lower than the control).
For Delphinium barbeyi the available flowers were increased by 48.2% but the BIF (after 30 min) was within
4.3% of control levels. There was no indication that
the accumulated nectar caused the BIF to overshoot
control levels. This suggests that the accumulated nectar was rather quickly depleted, returning the system
to a steady state. Although the BIF was unaffected,
the accumulated nectar did have a noticeable effect on
To examine the response of bumblebees to seasonal
changes in nectar availability I focused on individual
bumblebee species and the nectar production by the
guild of plant species each visited. The response of a
bumblebee species was measured by the change in its
abundance over the summer (utilization curve). The
seasonal change in the amount of resource available
to that bumblebee (production curve) was obtained by
summing the daily number of open flowers of each
species weighted by its nectar production rate per
flower. The results of a previous section indicated that
the degree to which plant species are preferred is a
fairly accurate predictor of their relative nectar production rates. Therefore, I employed preference as a
weighting factor to convert the floral production of a
species into its nectar resource equivalent. Although
this would appear to be a very indirect way of determining the reward value of flowers there are two reasons why it might be better than using nectar production rates. First, as mentioned above, the reward value
of a species may be influenced by its floral arrangement and each guild includes species which differ in
this regard. The effect of this variable is difficult to
measure but it appears that preference may take it into
account. Second, the actual reward value of a plant
species to one particular bumblebee species is influenced by the number of bees of other species foraging
on it. Although most plant species have only one major
bumblebee visitor, many of them are visited to a small
extent (<30% of all visits), and a few are visited to a
larger extent (>30% but <50%) by a second bumblebee species (Pleasants 1980). Using NPR's alone to
estimate reward ignores the losses to other bees but
preference would be expected to incorporate this factor.
One other important point must be made to justify
using preference to determine nectar production. At
BEE RESPONSETO NECTAR AVAILABILITY
December 1981
1974
& biforius
B. flavifrons
Apis mellifera
--
-
B. occidentalis
30-
(Curve)
Total bees
1
SITESITE
1657
(Uppe
(Curve)
1/)
LU
D
z
20-
oC)
cn
LJ
LJ
10-
30
20
June
10
20
July
30
9
19
August
20
June
July
August
FIG.6. Changein the abundanceof bee species over time in 1974.The arrow marksthe point in the 1974 season that is
equivalentto the end of the 1975study period.
first glance it would appear that using preference as a
weighting factor would necessarily cause a match between resource abundance and bee abundance because preference is based on the number of bees per
flower. However, circularity is avoided because preference is based on the relative B/F's among species.
Although BIF itself is clearly influenced by the abundance of bees, this influence is removed when the B/F
for each species is standardized by dividing it by the
largest BIF value among species. For example, suppose we found that the floral abundances of two
species did not change from one census time to the
next. Suppose also that the overall abundance of bees
on these two species doubled over this same period.
Then the absolute BIF for each species would be twice
as large for the second census. However, the relative
BIF will not change. When the number of flowers is
weighted by preference it will indicate equal amounts
of resource for the two census periods despite a doubling of bee abundance. Thus bee abundance and the
estimate of nectar production are independent of one
another. All that is assumed here is that the degree to
which one species is preferred over the other is not
influenced by total bee abundance (see General Discussion).
The preference ratings for the species visited by B.
bifarius at Site 1, by B. bifarius at Site 2, and by B.
flavifrons at Site 2 are shown in Table 3. Utilization
and production curves are shown in Figs. 3 and 4.
What is important is the shape of the production curve
relative to the shape of the utilization curve. There is
no a priori criterion for determining the scale of these
two curves. This is because the curves are not absolute measures of production or utilization but merely
indicate change over time. A scaling factor was chosen
for the production curve which facilitated comparison
with the utilization curve. There is rather close agreement between seasonal production and utilization for
all three cases. There is a significant correlation (r =
.92) between the number of bumblebees present on
census days and the estimate of the amount of nectar
available to those bees (Fig. 5). The fact that the
bee: resource ratio is relatively constant throughout
the summer indicates that, in general, the degree of
resource limitation for bees does not change over time.
Thus the intensity of inter- and intraspecific competition among bumblebees for nectar resources changed
little throughout the season. Despite the constancy of
resource limitation within a site over time, sites can
differ in the degree of their resource limitation. Comparing plant species found at both Sites 1 and 2, the
average BIF was 2.6 times greater at Site 1, indicating
that bees there were receiving less than half the profits
per flower. A possible explanation for this is discussed
below.
The value of using preference ratings to take into
account the nectar production lost to other bumblebee
species is illustrated by the ratings for the plants visited by B. bifarius at Site 2. The factors for the members of the Asteraceae can be compared with the preference factors (per head) in Table 1 for these same
species based on visits by all bees. The values for
Helenium, Viguiera, and Erigeron are higher in Table
3. This is because the standard species, Rudbeckia,
unlike these three species, is also visited by B. flavifrons. Thus its reward value to B. bifarius is lowered,
making the value of the three species relatively higher.
The value for Helianthella, on the other hand, is lower
in Table 3. This species is also visited by B. flavifrons,
but more so than Rudbeckia (Pleasants 1980), which
lowers its relative value to B. bifarius.
Variation between years
If bumblebees are resource limited we would expect
that the cumulative seasonal production of nectar
would support only a limited number of bees. When
total nectar production is similar for two different
years we would expect that the total number of bees
1658
JOHN M. PLEASANTS
......
bifarius
1975 1975B.B
j flavifrons
Apis mellifera
50 SITE 1
Ecology, Vol. 62, No. 6
- -.
Total bees
Projected
40 LJ
I-
7z
O
30 -
20 -
if)
o
LU
LU
r'
10
-
II
1
10
20
July
FIG. 7.
I
30
II·
I
9
August
July
August
Change in the abundance of bee species over time, 1975.
seen in the 2 yr would also be similar. The abundances had the greatest diet overlap were B. bifarius and B.
of each plant species were very similar for the sum- flavifrons. B. flavifrons is a medium-tongued bumblemers of 1974 and 1975 (r = .88, P < .001) and hence bee while the other three species are short tongued
the amount of available resource was constant for (Macior 1974). At Site 1, 8 out of the 10 plant species
those 2 yr. In comparing bumblebee abundances for visited by B. bifarius and 4 out of 10 visited by B.
these 2 yr I used the combined seasonal abundances flavifrons were also visited by honeybees. At Site 2,
of species with short and medium tongue length. These all 11 species visited by B. bifarius and 7 out of the
10 visited by B. flavifrons were also visited by honspecies are B. bifarius, B. flavifrons, B. occidentalis,
and the honeybee, Apis mellifera. Season totals for eybees. B. occidentalis visited 9 out of the 10 species
bee abundance were obtained from the area under the used by B. bifarius and 3 out of the 10 used by B.
curves in Figs. 6 and 7. Fig. 8 shows that the total flavifrons at Site 1. B. occidentalis also used all 11
number of bees seen at each site did not change from species visited by B. bifarius and 5 out of the 10 used
1974 to 1975. This supports the idea that a similar by B. flavifrons at Site 2. As Fig. 8 shows, B. bifarius
amount of resource supports a similar number of bees.
and B. flavifrons appear to have undergone competiA particularly significant feature of Fig. 8 is that the tive release in 1975. Increases in numbers such as this,
contribution of certain species to the total bee abun- termed density compensation, are often observed for
dance changed markedly between 1974 and 1975. The species on islands where competitors are missing
numbers of B. bifarius and B. flavifrons seen in 1975 (Mac Arthur et al. 1972, Yeaton 1974). The presence
were greater than for 1974 and compensated for the of density compensation in this pollinator system inlow numbers of B. occidentalis and Apis mellifera dicates that bees do have a competitive effect on one
seen in 1975. The reason these latter two species had another by depleting a limited supply of resources.
such low numbers was probably because they were Competitive release between bumblebee species has
more vulnerable to the severe winter of 1974-1975. also been observed in a short-term species-removal
For B. occidentalis the reduction might have been be- experiment (Inouye 1978).
cause the queens of this species have much shallower
overwintering hibernaculae than other bumblebees
GENERALDISCUSSION
(Hobbs 1968). The fall of 1974 was characterized both
Nature of the response to variation
by freezing temperatures and little insulating snowfall
The
is
not
which
For
native,
previous sections showed the responses by
Apis mellifera,
(Inouye 1976).
the reduction may have been due to inability to main- bumblebees to four kinds of variation in nectar availtain hives over the winter. In 1975, with honeybees
ability: among species, among patches of flowers withand B. occidentalis virtually absent, the floral re- in a population, over a season, and between years.
sources usually taken by these two species were avail- What are the mechanisms that produce these reable to B. bifarius and B. flavifrons. This situation sponses?
thus provided a natural species removal experiment to
The dynamics of the response of bees to variation
test whether pollinators that use similar resources are in nectar availability among species can be better
in competition with one another. The pollinator
understood by referring to a conceptual model. The
model is a more formal development and a graphic
species with which B. occidentalis and A. mellifera
BEE RESPONSETO NECTAR AVAILABILITY
December 1981
SITE 2
SITE 1
700-
B. occidentalis
::::-l Apis mellifera
K'\\ B.Ibifarius
B. flavifrons
1659
RA
t
600 -
500
-
ILJ
ULJ
.
49
....... ::
::6: 1::'
::::6
:::::::
LU
\
66
:110
'372
400 -
406
:44 7
0
o
-*u
300 -
::::
::::::
D
z
c
Qr
D
\\
301<
d
200 -
196
100-
=176
...
136
70
1974
1975
1974
1975
FIG. 8. Comparison of total number of bees and composition of bee fauna for species of short and medium tongue
length in 1974 and 1975.
representation of an explanation given by Heinrich
(1976a). The form of the model is borrowed from Fretwell (1972), who used it to explain the successive colonization of optimal and suboptimal habitats by birds.
Consider four plant species, A, B, C, and D, in a simplified system where nectar secretion begins in the
morning and the rate remains constant throughout the
day. Points RA, RB, Rc, and RI (see Fig. 9) refer to
the potential reward value (nectar sugar intake rate)
of each species as foraging begins in the morning, and
are indicative of each species' NPR. The curves extending downward from each of these points indicate
the decline in the actual reward value of each species
as the number of bees foraging on it increases. I will
assume, as discussed above, that the costs of foraging
do not influence reward value. I will also assume, although this is not essential, that bees remain constant
once they have chosen which species to forage on. As
the first bumblebees begin to visit flowers in this meadow they should choose to forage on the species which
provides the highest reward (species A). As more bees
arrive in the meadow the number of bees on species
A increases and consequently its expected reward value decreases. Eventually the expected reward from
species A will decrease to a level equal to that of a
second, as yet unvisited species (species B; point RB
in Fig. 9). Additional bees entering the meadow will
find both species equally profitable and will be just as
likely to choose to forage on one as the other. With
the continued influx of bees to the system, the number
of visitors on both A and B increases and the reward
c
b
a
NUMBEROF VISITORS PERFLOWER
FIG.9. Model showing the relationshipbetween the nectar productionrates of species A, B, C, D and the number
of bees foragingon them per flower. RA, RB, RC, and RD
are the potential reward values of species A, B, C, and D
beforebees beginforaging,andare indicativeof each species'
nectar production rate. The curves A, B, C, D show the
decline in each species' rewardvalue as the numberof bees
foragingon it increases. The intersectionsof the horizontal
lines and curves A, B, C, D indicatepoints where the reward
value of species is the same. Points a, b, c are the B/F values
when the numberof bees in the meadow has stabilized;the
reward value of all three species is then the same (=R).
Species D does not receive visits in this scheme.
expectation of both of these species becomes reduced
until a third species (species C) has equal reward value
(point RC) and begins to attract visitors. When no
more bees enter the meadow the system reaches a
steady state. At this equilibrium point the flowers of
all species will have the same reward value (R) and
standing crops of nectar will not change. It should be
noted however, that each species may have a different
standing crop of nectar at this point. The standing crop
will depend upon how rapidly flowers can be visited
(see earlier discussion). A species with a greater traveling and handling time per flower will have a larger
standing crop. The shapes of the curves in Fig. 9 come
from assuming that the lag time between successive
visits to a flower is a function of the reciprocal of the
number of bees foraging per flower, as discussed earlier. With curves of this shape the relative attractiveness of species (based on their B/F's, a, b, c, and d
in Fig. 9) does not change with overall bee densities
(i.e. with position of the equilibrium value R) and always corresponds to the relative magnitude of NPR's
(RA, RB, RC, and RD). In Fig. 9, RD is lower than R,
meaning that species D will not be visited. Actually,
because of the accumulation of nectar in its flowers,
the reward value of species D may later in the day
equal or exceed that of other species, at which point
it will receive visits. To incorporate this effect into the
model would require a third axis, a time axis, showing
1660
JOHN M. PLEASANTS
the rise in a species' reward value prior to visitation.
This would lower the BIF when a higher ranking
species would be perceived by bees as being equal to
a lower ranking one. However, it will not affect the
eventual relative B/F's among species.
Although Fig. 9 is primarily of heuristic value, it
does have some testable features. It predicts that at
equilibrium, species should have a similar reward value. Heinrich (1976a, 1979b) and Pyke (1980) provide
some support for this as do the estimates of reward
value for the pairs or groups of species in Table 2. It
also predicts that when R is sufficiently lowered, due
to a high overall abundance of bees, some species, not
previously visited, should begin to receive visits. This
is illustrated by bumblebee utilization of Geranium
fremontii (Geraniaceae), a species found at both Sites
1 and 2. Geranium produces a small amount of dilute
nectar (Watt et al. 1974) and is mainly visited by flies.
At Site 1, where bumblebee density is higher and flowers receive two to three times as many visits, Geranium is visited by B. bifarius and B. flavifrons. At Site
2, where the species is equally abundant, I have never
observed bumblebees foraging on it. Another feature
of the model is the successive colonization of species
with different NPR. This has been observed in a field
experiment (Heinrich 1979b). However, it will probably not be observed under natural conditions since
it appears that a bee's decision about which species
to forage on is not made on a daily basis. A bee's
specialization for a certain species is often remembered and carried over to successive days (Free 1970,
Heinrich 1976a). However, there is evidence that despite this constancy there is low-level visitation to other species (Heinrich's majoring and minoring, 1976a,
1979b). This has been interpreted in part as a periodic
assessment of the floral environment to determine if
the species currently being visited is the most profitable.
In contrast to the relatively long-lasting decision as
to which species to forage on, a bee's choice of whether to remain in a patch (or on an inflorescence) appears
to be part of a continual decision-making process. This
is some evidence that a decision is made after each
flower visited (Pyke 1978d). How this decision is made
is not precisely known but it is thought to involve an
assessment of the average reward expectation for a
species in the area in which the bee is foraging. When
flowers in a patch are encountered which have rewards
less than this standard, bees will leave the patch. Such
behavior will be optimal when the reward values of
neighboring inflorescences in a patch are correlated
(hot or cold spots, Pleasants and Zimmerman 1979).
This does appear to be the case in the few species
examined to date (Pleasants and Zimmerman 1979, M.
Zimmerman, personal communication). Considering
the inflorescence as a patch, there also appears to be
a correlation between the reward value of neighboring
flowers for many species (Pyke 1978c, J. Pleasants and
M. Zimmerman, personal observation).
Ecology, Vol. 62, No. 6
There are two possible explanations for the seasonal
tracking of resource levels by bumblebees as seen in
Figs. 3 and 4. One, it could represent a population size
(numerical) response to changes in resource levels.
Two, it could be a facultative response in foraging
activity to changes in resource availability. Explanation 1 implies that increases in nectar production bring
about worker production. While this is probably generally true, the appearance of new workers is not instantaneous. It takes 21-30 d for an adult worker to
develop from an egg (Hobbs 1968). It is possible that
the appearance of new workers could be timed to coincide with anticipated future resource levels. However, the shape of the bumblebee abundance curve is
very different at Sites 1 and 2 for B. bifarius. If the
numerical response is a programmed feature of the
biology of this species we would expect similar responses. Also, the production of workers can only account for increases in bumblebee abundance and cannot explain the midseason decrease in bee abundance
observed at Site 1. The response suggested by explanation 2 may be of two forms. Bumblebee hives have
a division of labor such that some bees are engaged in
foraging while others are involved in nest maintenance
and brood care (Free and Butler 1959). This suggests
the possibility that bees normally involved in nest
maintenance might be pressed into foraging service
when available resources increase or foragers might
remain in the hive when resources decrease. The
available evidence actually indicates that bumblebee
foraging activity might operate contrary to what I have
just described. When nectar in the hive honeypot is
augmented experimentally (simulating increased resource availability) fewer workers leave the nest to
forage (Brian 1954). On the other hand, when colony
resources are reduced experimentally (Brian 1954) or
when nectar input to the hive is reduced because foragers are removed (Inouye 1978), more bees, including
house bees, begin to forage. These experimental conditions are rather drastic but do suggest that the
changes in bee abundance seen in Figs. 3 and 4 are
not regulated entirely by the number of foragers sent
from the hive. It must be remembered that bumblebees
are solitary foragers and do not recruit other individuals to nectar sources as do honeybees. A second,
more likely form of facultative response involves
changes in the dispersion of bees over the meadow.
My census route covered only the main part of the
meadows where flowers were most dense. There were
also flowers near the margins of the meadow and scattered under trees. All else being equal, bees should
prefer to forage in the central area. As the density of
bees increases, their average profit will decrease and
additional bees may begin to visit more peripheral
areas. The successive colonization would be similar
to that modeled by Fig. 9. Plants in marginal areas
may therefore act as a buffer zone, receiving visits
when resource levels get too low in the central area,
but receiving few visits when resource levels are high.
BEE RESPONSE TO NECTAR AVAILABILITY
December 1981
This will tend to keep the ratio of bees to available
resource in the central area relatively constant over
time. The higher overall bee: resource ratio I observed at Site 1 may be due to the fact that the meadow
is much smaller than Site 2 (0.6 vs. 2.4 ha) and more
isolated. At Site 1 bees may be forced to continue
foraging in the central area because they have nowhere
else to go.
A numerical response is the most plausible explanation for the competitive release and density compensation observed when comparing bumblebee abundances over 2 yr (Fig. 8). In this case the additional
nectar resources available in 1975, due to the absence
of Apis Imtellijera,allowed the populations of B. bifarius and B. flavifrons to increase over 1974 levels.
In general the fine-scale match-up between bee abundance and nectar level differences among species or
patches would appear to involve foraging adaptations
which maximize net energy returns. The coarse tuning
of bumblebee abundance to seasonal or yearly nectar
production levels probably involves both a foraging
activity and a bee population growth response.
ACKNOWLEDGMENTS
Part of this research comes from my Ph.D. work at the
University of California, Los Angeles (UCLA). I would like
to thank my thesis readers, Henry Hespenheide and Lynn
Carpenter, and especially my advisor Martin Cody. This part
of the research was supported by a grant from Sigma Xi and
from the Stephen A. Vavra fund at UCLA for botanical research. The rest of the work was done while at Washington
University in St. Louis. I would like to thank the following
people for comments on earlier drafts or for advice and suggestions: Mike Zimmerman, David Inouye, Graham Pyke,
Peter Raven, and Owen Sexton. I would particularly like to
thank my wife, Barbara, for assistance in the field and suggestions on improving the manuscript.
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