Journal of Animal Ecology (1983), 52, 829-836

HONEY BEE FORAGING ECOLOGY:OPTIMALDIET,

MINIMALUNCERTAINTYOR INDIVIDUAL CONSTANCY?
BY HARRINGTON WELLS AND PATRICK H. WELLS

Faculty of Natural Sciences, Universityof Tulsa, Tulsa, Oklahoma 74104 and

Departmentof Biology, Occidental College, Los Angeles, California 90041

SUMMARY

(1) Experiments using honey bees and artificial flower patches were designed to test
three alternativeforagingecology models: optimal diet, minimaluncertainty,and individual
constancy. Honey bee responses to a mixed colour flower patch and to flower morph
associated differencesin rewardquantity, quality, and frequencywere measured.
(2) Each honey bee visiting a patch of randomlydistributedblue and yellow flowers was
constant to one colour, even though that behaviourwas suboptimal.
(3) When reward quantity was unequal between the two flower morphs each bee was
constant to one colour, even though that behaviouroften resultedin suboptimalreward.
(4) When reward quality was unequal between the two colour morphs each bee was
constant to one colour, even though that behaviouroften resultedin suboptimalreward.
(5) When reward frequency was higher in one flower morph than in the other each bee
was constant to one colour, even though that behaviouroften failed to maximize rewardor
minimizeuncertainty.
(6) Although each of our experiments had the potential to refute the individual
constancy model of honey bee foraging ecology, none did. Optimal diet and minimal
uncertainty theories failed to predict honey bee foraging behaviour and, under the
conditions definedby our experiments,are refuted.

INTRODUCTION

Three distinct predictive models of foraging ecology have been developed: one based on
optimal diet theory, one on minimizinguncertainty,and one on individualconstancy. The
foraging patterns expected according to these theories differ in many circumstances and,
since the predictionsare quantitative,experimentalobservationsmay be tested against each
hypothesis.
Optimal diet theory predicts the behaviour which should maximize joules gained per
joule expended in searching for food. This entails obtaining the greatest reward while
travelling the shorter distance. Food is a requirement for survival and reproduction.
Therefore, optimal diet behaviour should be favoured by natural selection. Predictions of
the optimal diet theory are, in fact, observed in the foraging patterns of some pollinators
(Pulliam 1975; Oster & Heinrich 1976; Pyke 1978, 1979; Waddington & Holden 1979).
However, optimal diet behaviour is not always the observed feeding pattern of insects
(Griffiths 1981).
Minimal uncertainty theory describes the foraging pattern which maximizes the
probability of obtaining a reward, but the average reward may not be maximized. An
evolutionary advantage of minimizinguncertaintycan occur when reward frequencies are
0021-8790/83/1000-0829$02.00 ? 1983 British Ecological Society

829

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830 Honey beeforaging ecology
extremely variable so that food on a regular basis is of primary importance to assure
reproductionand survival. Observations of some foraging behaviours agree only with the
minimal uncertaintytheory (Thompson, Vertinsky & Krebs 1974; Caraco 1980; Caraco,
Martindale& Whitham 1980; Real 1980, 1981).
Individual constancy theory predicts that each individual of a species will forage
selectively on one flower type in a polymorphic plant population, even when rewardis not
maximized or when uncertaintyis not minimized. Some field observations (Hanson et al.
1964) and experimental studies (Wells, Wells & Smith 1981) support the individual
constancy model. Experimentshave shown that bees become attached to colour rather
than position of flower or geometry of flower patch, and the genetic consequences for
angiosperms when the individually constant forager is a pollinator, have been examined
(Wells 1983; Wells, Wells & Smith 1983).
Artificial flower patches offer the possibility of critically analysing a wide variety of
foraging systems because they allow strict experimental controls to be implemented on
floral rewards, attractant stimuli, and floral distributions, as well as on the types and
numbers of foragers. This study, through the use of artificial flower patches, seeks an
answer to the question: do honey bees forage as predicted by the optimal diet theory, as
expected by the minimal uncertainty theory, or according to the individual constancy
model? The experiments are crucial (Hempel 1966) and are scientific in the Popperian
sense (Popper 1957) in that any possible result cannot support all three theories and must
be regardedas a refutationof some of them.
The present study tests the predictive value of three foraging ecology theories for the
honey bee-plant system. It has four sections (i) How will individual honey bees forage
when all flower morphs have identical rewards? (ii) What will be the pattern of individual
honey bee foraging when reward quantities differ between flower morphs? (iii) Will
individual honey bees forage in an optimal diet fashion when reward qualities differ
between flower morphs? (iv) Will individual honey bees forage in a manner so as to
minimize the uncertaintyof finding a reward when the frequency of empty flowers differs
between flower morphs?

METHODS

The artificialflower patch design of Wells et al. (1981) was used. Two types of flowers in
equal numbers and randomly distributed existed in each experiment. Flowers were
plexiglass squares (yellow or blue), painted on the bottom side. Each flower was on a
pedicel. Honey bees, Apis mellifera L., from a twenty-framehive were trained to fly 60 m
to a clear watch glass containing 1.25 M sucrose. The watch glass was removed replaced
with an artificial flower patch, and the bees chose what types of flowers to visit. In all
experiments, flowers that contained reward were refilled as emptied, and random
arrangements of flowers on the grids were changed periodically so that flower position
would not become a factor.

Experimentswith identical rewards in allflower morphs

Bees were trained to a watch glass of sugar solution. The watch glass was removed and
replaced with a grid containingeighty flowers (forty blue, forty yellow), each with 2.5 P1of
1.25 Msucrose. Data on four bees were recorded.

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 H. WELLSAND P. H. WELLS 831
Experimentsusing diferent rewardquantities
Grids having thirty-six flowers (eighteen blue, eighteen yellow) were used. Bees were
trained to a watch glass of sugar solution. The watch glass was replaced by a grid which
had yellow flowers with 2.5 1lof 1-25 M sucrose and blue flowers with 20 ul of 1.25 M
sucrose. Data on four bees were collected the first day. The second day the reciprocal
experimentwas performedby using grids where blue flowers had 2.5 #1 and yellow flowers
20 #1 of 1 25 Msucrose. Three of the Day 1 bees continuedto visit the grids on Day 2, and
data on eight additionalbees were recorded. Optimal diet theory predicts that bees should
visit flowers offeringthe greatervolume of reward.

Experiments using differentrewardqualities

We did two experiments which offered bees the opportunity to choose a high energy
reward over a lower quality solution, as they should according to optimal diet theory. In
the first of these, five honey bees were trained to a watch glass containing 1.25 ul sucrose.
The watch glass was then replacedwith a thirty-sixflower grid containingequal numbersof
yellow and blue flowers. Each flower had 10 #1 of sucrose solution, but the quality (sugar
concentration)was varied as follows: Days 1-4 had equal molarities (1-5 M)of rewardin
each colour: on Days 5, 6, 8, and 10 yellow flower rewardquality was greater (2-5 M)than
blue (0.75 M);on days 7 and 9 blue flower reward quality was greater (2-5 M)than yellow
(0-75 M).
On Day 11 the second experiment was started, in which three bees from the first
experiment and four newly recruited bees were used. Day 11 had both yellow and blue
flowers with 10 ul of 1.5 Msucrose. Data were collected for four additionaldays with blue
flowers having 10 1of 2.5 Mand yellow flowers having 10 1of 0.75 Msucrose.

Experimentsusing differentrewardfrequencies
Artificialflower patches containing sixty-fourflowers (thirty-twoblue, thrity-twoyellow)
were used. Bees were trained to a watch glass containing 1.25 Msucrose. The watch glass
was removed and replaced with a grid in which 2/3 of the blue flowers were empty and 1/3
of the blue flowers had 20 p1 of 1.25 M sucrose. Yellow flowers all had 20 1lof 1.25 M
sucrose. Data were recordedon five bees for 2 days, then for an additional2 days with only
1/3 yellow flowers, but all blues, provisioned. Both optimal diet and minimal uncertainty
theories of pollination ecology predict that bees should visit flowers of the colour in which
all flowers providedreward.
Chi-squarestatistics were used to test the data for departuresfrom predicted.Bees were
tested for random visitation to flowers of different colours and for sameness of foraging
behaviour (test of homogeneity)in each experiment. The multinomial General Exact test
(Wells & King 1980) was used to test for a change in behaviourof individualbees.

RESULTS AND DISCUSSION

Experiments with identical rewards in allflowers of both colour morphs
Data are summarized in Table 1. Bees did not forage randomly (x2 = 410, d.f. = 4,
P < 0.005) or homogeneously (Z2 = 410, d.f. = 3, P < 0.005). Individual bees were
constant to colour, consistently flying over flowers of one colour to reach others having the
colour to which they were attached. Thus, the bees were individuallyconstant and did not
forage as predictedby optimal diet theory. More energy than necessary was used to obtain
a given reward.

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832 Honey beeforaging ecology
Experimentsusing differentrewardquantities
Table 2 reports observed foraging behaviour when the two flower types had unequal
quantities of reward. No bee that foraged on both days changed foraging behaviour
(General Exact Test, P > 0-1, Wells & King 1980), even though yellow flowers had the
lesser reward quantity on the first day, and the blue flowers had it the second day.
Therefore, data for both days were lumped for further testing. Bees did not forage
randomly (X2= 1036, d.f. = 12, P < 0.001) or homogeneously (X2= 1032, d.f. = 11, P <
0.001). In fact, the bees were so constant to colour that only one honey bee visited both
types of flowers. That bee first visited one yellow flower containing 20 1u of 1.25 Msucrose,
and subsequentlyvisited twenty blue flowers each containingonly 2.5 #1 of 1.25 Msucrose.
Therefore bees did not show optimal diet behaviour when reward quantities differed.
Instead, individual bees remained constant to a flower morphology, with most bees not
even testing both types of flowers; the bee which did test flowers of both colours did not
continue to visit the type with the greaterreward.

Experimentsusing differentrewardqualities
Table 3 contains the results of the first experimentusing a variation in reward quality.
Initial control days established individual forager preferences. Then sugar concentrations
were varied such that one of the flower types on a given day would offer a greaterreward.
Four of the five bees were constant to a colour over the entire 10 days. These bees
obviously did not forage homogeneously as a group, nor did individuals switch flower

TABLE1. Patternsof honeybee foragingon a patchcontainingfortyblueandforty

yellowflowers,with2.5 ul of 1 25 Msucroseperflower
Flowersvisited
Beeno. Blue Yellow
1 0 140
2 103 0
3 0 84
4 83 0

TABLE2. Honey bee foragingpatternswhen differentflowercolours contained

differentrewardquantities
Flowersvisited
Day I Day 2
Blue Yellow Blue Yellow Total
Beeno. 20 #1 2-5 #1 2-5 #1 20 ,l Blue Yellow
1 0 96 0 34 0 130
2 0 72 0 21 0 93
3 13 0 176 0 189 0
4 0 114 - * 0 114
5 149 0 149 0
6 111 0 111 0
7 116 0 116 0
8 0 44 0 44
9 40 O 40 0
10 22 0 22 0
11 20 1 20 1
12 0 7 0 7
* Did not return.

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TABLE 3. Honey bee foraging patterns when different flower colours contained different reward qualities?Fir
quality; 10 #1lrewardper flower. B = blue, Y = yellow, with experimentday above and sucros
Flowersvisited
Days 1 2 3 4 5 6 7 8
B Y B Y B Y B Y B Y B Y B Y B Y
Beeno. 1.5 1.5 1.5 1-5 1-5 1-5 1.5 1.5 0.75 2.5 0-75 2.5 2.5 0.75 0.75 2.5 2
1 10 0 6 0 13 0 11 0 11 0 12 0 8 0 7 0
2 0 9 0 10 0 10 0 12 0 11 0 8 0 1
3 0 10 0 8 0 15 0 8 4 10 0 14 9 9 6 9
4 1 5 0 18 0 15 0 20 0 17 0 18 0 16 0 17
5 6 0 11 0 10 0 10 0 13 0 12 0 11 0

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834 Honey beeforaging ecology
morphologies. Two bees were constant to yellow flowers and two to blue flowers. Only one
'mistake'was made by a bee, and it was on an initialday when no differenceexisted. These
bees did not forage in an optimal diet manner and, since they did not taste both qualities,
their behaviourdid not allow that option.
Bee no. 3 did sample both flower types. Bee no. 3 was completely constant to yellow
flowers the first 4 days but on Days 5, 7, and 8 extensively visited both types of flowers.
On these days the bee's behaviour appeared to be random (X2= 1.72, d.f. = 1, P > 0.1)
rather than optimal. Also, behaviour on Day 5 was not significantlydifferentfrom that on
Day 7 (X2= 1.7, d.f. = 1, P > 0.1), or Day 7 from Day 8 (2 = 0.36, d.f. = 1, P > 0.1).
Since the greater reward on Days 5 and 8 was on yellow flowers, and on Day 7 on blue
flowers, a change in behaviour would be expected according to the optimal diet theory. It
was not observed. Finally, even though bee no. 3 was constant to yellow flowers on Days 6
and 9; on Day 9, optimal diet theory would predictconstancy should be to blue flowers.
During the second experiment on reward quality, the same difference in molarity was
maintained for 4 days. This sustained option did not result in honey bees foraging in an
optimal diet manner (Table 4). Both old and new bees were constant to colour, but some
bees to yellow flowers and some to blue flowers. In fact, only 1.3% of the flowers visited
were 'mistakes' (not to the flower colour to which a bee was constant). Bee no. 3, which
foraged randomly on 3 days in the first experimentbecame constant in the second, to the
flower colour with lower food quality (yellow), after it had sampled the higher quality food
on Day 12.
Therefore,no evidence was found that honey bees will forage in an optimal diet manner
when food quality differs in two flower types. It appears that the majority of bees were
constant to a flower type to the degreethat exposure to the rewardsof both types of flowers
rarely occurred. However, even when both flower types were sampled there was no
evidence to support the idea that honey bees would forage in an optimal diet patternwhen
food quality differencesexist.

Experimentsusing differentrewardfrequencies
Table 5 contains the observed data. Honey bees did not forage randomly (X2= 403, d.f.
= 5, P < 0.001) or homogeneously as a group (X2= 460, d.f. = 4, P < 0.001). Contraryto
the prediction of minimal uncertaintytheory, the bees remained constant to flower colour
(some to blue and some to yellow), regardless of the frequency of reward. Only two bees

TABLE4. Honey bee foragingbehaviourwhendifferentflowercolourscontained

differentrewardqualities.Secondexperiment:consistentdifferencein quality;10 #l
rewardper flower.B = blue,Y = yellow,withexperimentday aboveand sucrose
molaritybelow
Flowersvisited
Days 11 12 13 14 15
B Y B Y B Y B Y B Y Total
Beeno. 1.5 1.5 2.5 0.75 2.5 0.75 2.5 0.75 2.5 0.75 B Y
3* 1 12 1 8 0 10 0 8 0 10 2 48
4* 1 13 0 19 0 15 0 18 0 14 1 79
5* 9 0 7 0 9 0 11 0 11 0 47 0
6 10 0 10 0 13 0 11 0 12 0 56 0
7 13 0 11 0 8 0 -- 11 0 43 0
8 2 0 11 1 13 0 14 1 10 0 50 2
9 0 3 0 15 0 12 0 14 0 14 0 58
* Bees3, 4, and5 respectivelyfromTable3.

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 H. WELLSANDP. H. WELLS 835
TABLE 5. Honey bee flower visitationwhen differentflower colours contained
rewardsat differentfrequencies.Days 1 and2 all yellowwithreward,1/3 bluewith
reward.Days 3 and 4 all blue with reward,1/3 yellowwith reward.+ indicates
visitsto flowerwithreward;- visitsto emptyflowers
Flowersvisited
Day 1 Day2 Day3 Day4 Total
Beeno. Y B+ B- Y B+ B- Y+ Y- B Y+ Y- B Y B
1 0 6 17 1 22 16 0 0 5 0 0 32 1 98
2 0 14 2 0 37 51 0 0 12 - - 0 116
3 18 0 0 7 0 0 23 12 18 25 19 0 104 18
4 0 17 13 0 35 29 - - 0 0 14 0 108
5 - 0 35 25 0 0 57 0 0 6 0 123

sampled both flower morphs, but neither switched to the colour flower with highest
frequency of reward. Thus, behaviour did not often allow the option to maximize the
probabilityof obtaining a reward (in this case, minimizinguncertainty also is optimal diet
behaviour). Even when mistakes did occur and both flower colours were visited, the bees
did not use the informationto optimize, or to minimizeuncertainty.
Each of the four experimentaldesigns we used had the potential of refuting alternative
models of honey bee foraging ecology under specifiedtest conditions. Results of each type
of experimentare contrary to predictionsof optimal diet theory, and in the test of minimal
uncertainty, that model also failed as a predictive tool. Results of all four types of
experimentsare consistent with the predictionsof the individualconstancy model of honey
bee-plant ecological interaction.

ACKNOWLEDGMENTS

We thank Dr Adrian Wenner for critically reviewing the manuscript; David Kayne,
Timothy Sutherlandand Grace Yasuda for their valuabletechnical assistance.

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(Received 13 September 1982)

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