Flower Constancy: Definition, Cause, and Measurement
Nickolas M. Waser
The American Naturalist, Vol. 127, No. 5. (May, 1986), pp. 593-603.
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Vol. 127, No. 5
The American Naturalist
May 1986
FLOWER CONSTANCY: DEFINITION, CAUSE, AND MEASUREMENT
N I C K O L M.
A ~ WASER
Department of Biology. University of California, Riverside. Cal~fornia93521
Slrbr~ittedMro.c.11 9 , 1985: Acc.eptccl Scpter~ihcr13. 1985
Pollinating animals sometimes restrict their visits to flowers of a single species
or morph within a species, even when rewarding alternative flowers must be
bypassed in the process. The tendency to specialize in this way, common in some
social bees, has been referred to asflower cotlJtancy (Plateau 1901; Clements and
Long 1923; Grant 1950; Free 1966, 19700; Levin and Anderson 1970). The striking
features of constancy are that individual pollinators, even members of the same
bee colony, specialize on different flower types, and each may switch its specialty
from time to time (Grant 1950; Free 1966; Heinrich 1976, 19790; Wells and Wells
1983; Wells et al. 1983). These features indicate that flowcrs passed over by an
individual at a given time are indeed rewarding, since they are acceptable to
conspecific individuals or to the same individual at another time.
It is useful to distinguish constancy from two other kinds of specialization that
might occur when there is access to several flower types. A pollinator may
specialize because it has fixed floral affinities, as do oligotropic or oligolectic
solitary bees (see Faegri and van der Pijl 1979; Schemske 1983). 1 refer to :his as
$xed preference. Alternatively, a species without fixed affinities may speci- I'ize on
flowers that are abundant and rewarding. Such behavior is predicted by simple
optimal-diet theory (e.g., MacArthur and Pianka 1966). It should occi~rwhen the
most rewarding flowers are sufficiently abundant and superior that the highest
reward-intake rate is achieved by skipping inferior flowers, even though this
elevates travel costs relative to a generalized diet. I refer to this as lrrbile pr.c.f>r.ence. There is good evidence that pollinators such as bumblebees and temperate
hummingbirds choose flowers partly on the basis of the energetic value of rewards
the flowers contain (Heinrich 1976; Pleasants 1981; Gass and Montgomerie 1981;
Pyke 1981; Waser 19836).
Some workers have equated constancy with fixed preference (Grant 1950;
Linsley and MacSwain 1958; Faegri and van der Pijl 1979), others with labile
preference (see below), but I advocate reserving the term for a third kind of
specialization (see also Bateman 1951; Levin and Anderson 1970; Wells and Wells
1983). Suppose that a pollinator can remember how to recognize or manipulate
only one or a small number of flower types or requires a long time to learn to
recognize or manipulate each type. Such behavioral constraints favor specializaAm. Nat. 1986. Vol. 127. pp. 593-603. S 1986 by The U n ~ v s ~ h of
~ t Ch~cago.
y 0003-0147.'86.'2705-0008$02.00 A l l rlphtr lsaelvsd
5 94
T H E AMERICAN NATURALIST
tion because they elevate mean handling time per flower when several types are
visited. By skipping all but one or a few types the pollinator saves handling costs,
since it does not invest in further learning or successive relearning. Skipping is the
best strategy if reduced handling time more than offsets increased travel costs
(McNair 1981; Stanton 1984).
In this view constancy derives from something intrinsic in the pollinator,
namely, limitations of its nervous system. Fixed preference also derives from
intrinsic physiological and morphological limitations, but labile preference derives
from something largely extrinsic to the pollinator, namely, abundances of flowers
and the rewards they contain.
Unless the three kinds of specialization occur in some combination (which is
not unlikely), each should be distinguishable by its behavioral "signature" (see
also Wells et al. 1983). With constancy, the specialty should differ among
conspecific individuals depending on the sequence of acceptable flowers each has
encountered, since encounter history could determine which type is learned first
(see Heinrich 19796). Moreover, the behavior should occur even when available
flower types all offer similar, energetically acceptable rewards (as defined operationally in the first paragraph of this paper), that is, when simple diet theory
predicts generalization. With fixed preference, conspecifics should have concordant and unchanging specialties. With labile preference, individuals should have
concordant specialties that change predictably according to floral abundances and
rewards, and specialization should occur only when rewards differ substantially
among flowers (see MacArthur and Pianka 1966).
After elaborating on memory and learning constraints that may cause constancy, I discuss definitions of constancy and preference in terms of flower-toflower movements, a corresponding quantitative constancy index, and suitable
empirical measures of pollinator behavior. I cite some experimental evidence
suggesting that constancy is indeed caused by behavioral constraints, and I
mention recent examples of confusion between constancy and preference and
some possible consequences of each behavior for plant reproduction.
BEHAVIORAL CONSTRAINTS THAT FAVOR CONSTANCY
Darwin seems to have been the first to propose that behavioral constraints are
involved in constancy:
That insects should visit the flowers of the same species for as long as they can. is of great
importance to the plant. as it favours the cross-fertilisation of distinct individuals of the same species;
but no one will suppose that insects act in this manner for the good of the plant. The cause probably
lies in insects being thus enabled to work quicker: they have just learned how to stand in the best
position on the flower, and how far and in what direction to insert their proboscides. (1876. p. 419.)
Here Darwin refers to morphological differences among flowers, but the idea
can be extended to differences in other traits involved in flower recognition or
manipulation, such as color, odor, or the type of floral reward (e.g., nectar vs.
pollen). There is good evidence for constancy based solely on color (for reviews,
see Waser 1983u,b).
I have alluded to two kinds of behavioral constraint that favor constancy (cf.
Pietrewicz and Kamil 1981). One possibility, the "memory hypothesis," is that
FLOWER CONSTANCY
595
pollinators are limited in their ability to remember simultaneously how to recognize or manipulate more than a few flower types. This is similar to one view of the
search image (Dawkins 1971; Pietrewicz and Kamil 1981; Stanton 1984). Another
possibility, the "learning hypothesis," is that pollinators require a substantial
time to learn to recognize and handle each type.
Most discussion of what causes constancy (Heinrich 1976, 19796; Laverty 1980)
invokes the learning hypothesis, and it is certain that learning to deal with flowers
takes time. There is also evidence, however, that bees (Kugler 1943; Heinrich et
al. 1977; Gould 1985), butterflies (Stanton 1984), and birds (Cowie and Krebs
1979; Pietrewicz and Kamil 1981) have short "memory windows" (Krebs et al.
1981). This is just the constraint required by the memory hypothesis. It means that
information, for example about how to manipulate one flower type, can be lost
because it is replaced by information about a new flower type or sin~plybecause
time has passed.
There is another reason to suspect that memory constraints are important for
constancy. With large memory capacity all flower types could be learned eventually. The total time required to learn five types (for example) should be on the
order of hours at most, judging from learning experiments with hummingbirds and
bees (Weaver 1956; Menzel et al. 1974; Heinrich 1976, 19796; Heinrich et al. 1977;
Goldsmith and Goldsmith 1979; Laverty 1980; Waser 19836). This is much shorter
than the expected pollinator life span (weeks to years; Heinrich 1 9 7 9 ~Calder
;
et
al. 1983) or the flowering of plants (usually weeks; Waser 1978 and references
therein). A pollinator with a large memory should not be constant if it experiences
flower types for a period much longer than that needed for learning. since the
learning investment for each type would be made only once and amply repaid by
savings in travel costs over a long period.
The memory and learning hypotheses are not mutually exclusive. Indeed. the
latter can be considered a special case of the former, in which a flower type must
be learned only once rather than relearned continually. In some cases, the two
hypotheses do yield different predictions. For example. if initial learning alone is
involved, pollinators that encounter several flower types should become less
constant and increasingly proficient at using all types. If limited memory is
involved, pollinators should not become less constant, and if there is any variation, the least constant individuals should be least proficient and forage most
slowly (see also Stanton 1984).
Some predictions are shared by the two hypotheses, at least when one is dealing
with naive pollinators. For example, constancy should decrease as travel costs
increase and outweigh the extra learning cost associated with inconstant foraging.
Thus, constancy should depend on flower density (for a hint of this, see Grant
1949, p. 89; Brown and Clegg 1984). In addition, constancy should increase as a
visitor encounters flowers that are increasingly dissimilar in morphology or color.
This last prediction is upheld by the experimental results discussed later.
Specialization should be discernible in pollinator movements between flowers
or plants. Imagine the simplest situation in which a pollinator at each of two flower
T H E AMERICAN NATURALIST
FIG. 1.-Notation used in Bateman's index and table 2 for the frequencies of all possible
transitions between flowers of two types. 1 and 2. Constant transitions are those within types.
i.e., A and D. Inconstant transitions are those between types. i.e.. B and C .
types has certain probabilities of next visiting type 1 and type 2. Actual movements can be cast into a matrix of transition frequencies (fig. I ) that reflects these
probabilities, and the sequence of visits can be thought of as a Markov process
(Straw 1972).
Bateman (1951) proposed a constancy index that depends on the tendency for
all transitions to occur between like flowers (see also Levin and Anderson 1970;
Straw 1972). A pollinator leaving any flower has equal access to flowers of types 1
and 2. When transition frequencies are known (see fig. l), Bateman's index is
CONS =
[(AD)'!?
-
(BC)l'?]/ [(AD)[!"
(BC)'!?] .
Ranging from - 1 (complete inconstancy; all transitions between unlike flowers)
to 0 (random transitions) to + 1 (complete constancy; all transitions between like
flowers), this index is identical to Yule's (1912) "measure of colligation" for the
analysis of contingency tables (discussed further in Bateman 1951; see also Fisher
and Bailey 1949).
The index has the interesting property of being insensitive to changes in transition frequencies A and C by a constant multiple, that is, to a fixed change in the
probability of approaching flower type 1 regardless of the current flower. A
reasonable interpretation is that this change represents increased preference for
type 1. By this definition, Bateman's index is insensitive to preference changes; it
is altered only by unequal changes in transition frequencies between like and
unlike flowers in the same row or column. If A increases proportionately more
than C , for example, CONS will increase. An interpretation is that the chance of
visiting type 1 is greater if the pollinator is already at that type. This behavior is in
accordance with constancy; thus, the index seems reasonable.
A broader definition of preference involves any change in total transitions to
one or another flower type (i.e., in the column totals of fig. 1; Fisher and Bailey
1949, p. 227; Levin and Anderson 1970; Chesson 1983), rather than a strictly
proportional change in each column element. I will not pursue different definitions
further, but I use the ratio of column totals to estimate preference in an example
mentioned later.
FLOWER CONSTANCY
597
EMPIRICAL MEASUREMENT OF CONSTANCY
To measure constancy quantitatively requires information about movements
between flowers that can be evaluated with an index such as Bateman's. This
information cannot be gleaned from the purity of pollen loads carried by pollinators, a traditional constancy measure (Clements and Long 1923; Linsley and
MacSwain 1958; Free 1963, 1970h; Kislev et al. 1972; Grace and Nelson 1981).
Such an indirect measure does not take into account floral availabilities and thus
does not serve even to demonstrate specialization, much less to distinguish among
the various kinds. For example, a pure load may mean simply that the pollinator
foraged in an area containing only one flower type or that it visited several types
but actively collected pollen from only one (Free 19700).
Observing pollinator movements in nature (Bennett 1883; Christy 1883; Plateau
1901; McNaughton and Harper 1960; Heinrich 1976) is an obvious, direct way of
assessing choice, but there is a drawback. Given highly nonrandom spatial mixing
of flower types and complex pollinator movements, it is difficult to generate
accurate expectations of encounter frequencies with different flowers (see Stanton
1984). Known encounter rates are needed if one hopes to ascribe a positive value
of Bateman's index to something other than a patchy distribution of plant species.
Field observations may suffice to infer the presence of constancy, however (e.g.,
Stucky 1984).
One way to measure constancy quantitatively is to control flower availabilities
experimentally. This approach was pioneered by Clements and Long (1923), who
presented pollinators with "bouquets" of different flowers (see also Jones 1978;
Thomson 1981). Others have arranged artificial flowers into regular arrays and
exposed them to pollinators in the laboratory (Manning 1957; Waddington and
Holden 1979; Real 1981; Wells et al. 1983). Large arrays allow the availabilities of
flowers to be controlled and all types of movements between the flowers to be
scored simultaneously, thus generating results appropriate for quantitative indexes of constancy and preference.
A R R A Y EXPERIMENTS
I have conducted several array experiments in the field to-test the prediction
derived above that constancy increases as a visitor encounters increasingly dissimilar flowers. Each array contained two flower types (table 1). In each experiment there were two or three arrays that differed in how distinct their constituent
flowers were in color andlor morphology (table 2, "Major Differences" column).
Good arguments can be made that my ranking of how strongly pairs of flowers
differed was consistent with what a bee would experience.
In April 1979 1 scored visits of nectar-collecting solitary bees (Diadasiu sp.;
Anthophoridae) to annual wild flowers in Organ Pipe Cactus National Monument,
Arizona. There were two arrays separated by 2 m, each of which measured 1 m by
1 m and contained 100 vases, spaced 10 cm apart, in which 50 flowers of two
species were alternated. The flowers were species visited naturally by the bees in
adjacent areas.
TABLE l
P L , ~ NUSED
T ~ I N ARRAY
EXPERIMENTS
Site o r
Source
Arizona
Costa
Rica
Species
Morphology'
Color
Hriplopclpplrs spinlilosis
Gaillardia ciriionica
Clzrietznctis stei,ioides
Digitalis purplrreri
Fllc.Iisicr cirhoreacens
Agercltirla sp.
composite. disk and ray
composite, disk and ray
composite, disk only
broad tube
narrow tube
composite. disk only
small. short petals
large, longer petals
yellow
yellow
white
purple or white
purple
white
dark yellow+
pale yellow
" "Disk
and ray" refers to floret type. t These are flower colors, but vegetation color also differed within each Brnssic.a species TABLE 2
Hs
+ Ga
36
19
18
25
.24
None
12
9.2 fl
61
4
4
30
.83
C
12
9.3 fl
Dp(purple) + Dp(white)
vs.
Dp(purple) + FA
or VS.
Dp(white) + A sp.
141
104
105
125
.I2
C
39
13.3 inf
139
47
42
31
.19
M
23
12.3 inf
117
14
14
72
.74
M
30
8.3 inf
+ Bn(yellow)
or
Bo(red) + Bo(green)
72
29
33
51
.32
C
26
NA
55
6
9
17
.62
C
26
NA
Bol
185
14
15
87
.80
C+M
26
NA
+ Bn(yellow)
VS.
Bn + Bo#
23
7
7
7
.29
C
8
NA
44
3
4
2
.46
C+M
8
NA
VS.
Cs
+
Ga
Bn(white)
vs.
Bn
Bn(white)
+
' Abbreviations for species names: H s . Hnplopclppus spinlrlosis; Ga. Gnillclrdiri ariioriiccl: Cs,
Ch~enclctisstevioides; Dp, Digitcilis plrrplrrecl: Fa, Flcchsicl rirhorrscrns: A sp.. Agercitina sp.: Bn.
Brcissicci nriplrs: Bo, Brua~iccioleraceel. Digitalis prrtplrreci had two flower colors and Brrissiccl spp.
had several vegetation colors: these are specified in parentheses.
t Species listed first in a mixture is "type 1" (see fig. 1 ) in calculations of transition frequencies.
j: Major characteristics (M = morphology. C = color) distinguishing flowers in an array. $ Mean number of flowers (fl) in inflorescences (inf) visited if known. This comparison involved honeybees. # This comparison involved solitary bees. '
FLOWER CONSTANCY
599
In March 1981 1 observed nectar-collecting bumblebees, Bornbus ephippiut~ls,
at Cerro de la Muerte, Costa Rica. There were three arrays spaced 3 m apart; each
measured 60 cm by 40 cm and contained 24 vases, spaced 10 cm apart, in which 12
inflorescences of two species were alternated. I pruned inflorescences to produce
floral "flags" of about the same size ( 5 flowers of Digitulis prirprirea, 10 flowers or
heads of other species). I scored movements between inflorescences, since each
contained several flowers. Again, the flowers were species visited naturally by the
bees in adjacent areas.
Finally, I analyzed two experiments from Bateman (1951), in which honeybees
and unidentified solitary bees visited mustards in a garden. Bateman did not
specify interplant spacing or whether bees collected nectar or pollen. Only movements between plants were considered.
In all pairwise comparisons of arrays exposed simultaneously to pollinators,
constancy was greater in the array containing flowers of dissimilar color andlor
morphology than in the array containing more-similar flowers (table 2; N = 6,
one-tailed sign test, P = .016). This is the result predicted if the behavior is caused
by memory or learning constraints.
DISCUSSION
Given the widespread interest in constancy among crop scientists and ecologists, it is surprising that the five studies cited earlier and a few noted by Clements
and Long (1923) appear to be the only attempts to measure constancy using direct
behavioral observation in the field. Array experiments are equally rare; those
discussed here, few as they are, are all that I know of.
Arrays allow the simultaneous scoring of all possible transitions between flower
types whose accessibility is controlled, exactly what is required for an index such
as Bateman's. It is more difficult to score all transitions or to achieve controlled
accessibility with artificial bouquets, and bouquet studies to date do not provide
information suitable for measuring constancy quantitatively. For example, Jones
(1978) used bouquets in a way that allowed for all possible transitions between
flowers, but not at one time and place. Thomson (1981) constructed bouquets of
several species, presented them to bumblebees naturally foraging at flowers of one
species, and considered movements onto that species in the bouquet to represent
constancy. He scored only certain transitions, however, corresponding to one
row of figure 1. Since either constancy or preference will influence row elements,
the behavior Thomson recorded cannot be unambiguously ascribed to constancy.
Constancy and labile preference have not been distinguished in several recent
laboratory studies. Bumblebee choice based on reward quality is called constancy
by Heinrich et al. (1977). Waddington and Holden's (1979) constancy model and
test also involved preference for a superior reward. Laboratory studies have not
been designed to measure constancy quantitatively, although some have certainly
demonstrated that it occurs (Wells and Wells 1983; Wells et al. 1983).
Distinguishing constancy from preference is of value if one is interested in plant
reproduction. It has been argued that plants can compete for pollination by the
usurpation of pollinator visits or through interspecific pollen transfer (Waser
600
T H E AMERICAN NATURALIST
19830; Campbell and Motten 1985). Interspecific pollen transfer might lead to
stigma clogging, disruption by foreign pollen, or the loss of pollen deposited on
foreign flowers, each of which could reduce fitness. The potential for each mechanism of interaction can be inferred from records of pollinator movements. For
example, Delphinilltn nelsonii and Ipotnopsis aggregata compete for hummingbird pollination, and hummingbirds visiting arrays (Waser 1978) show constancy
of only 0.04 according to Bateman's index. Hummingbirds also show moderate
preference: the ratio of total transitions to each type (Chesson 1983) is 1.57 in
favor of I. aggregata. Thus, both species might suffer from interspecific pollen
transfer, and D. rielsonii might suffer more because I. aggregata is more attractive, a conclusion supported by observations in natural populations and experiments (Waser 1978; Kohn and Waser 1985; R . Mitchell, pers. comm.).
I hope to have demonstrated the value of attempting to define constancy in
more mechanistic and quantitative terms and the value of attempting to formulate
testable hypotheses about why foragers exhibit such behavior. The experimental
evidence at hand is consistent with the hypothesis that constancy is related to
limited ability to learn or remember how to recognize several flower types at once
or how to deal with them efficiently. Thus, the evidence suggests that constancy is
not a highly evolved adaptation as has been implied in the pollination literature
(Grant 1949, 1950; Levin 1978; Faegri and van der Pijl 1979); rather, it represents
an imperfect adaptation attributable to behavioral constraints.
SUMMARY
A pollinator that restricts its visits to one flower type, even when other rewarding types are accessible, can be said to exhibit flower constancy. This usage
distinguishes constancy from fixed preference or labile preference for the most
rewarding flower type; I discuss a quantitative constancy index that is insensitive
to preference changes. Because a constant visitor avoids flowers with acceptable
rewards, the behavior is inefficient unless there are constraints such as an inability
to learn quickly or to remember simultaneously how to deal with many flower
types. If such constraints are the basis for constancy, it should be most pronounced when flowers in a mixture differ strongly in morphology or color. I
observed bees foraging in outdoor flower arrays and found that constancy always
increased with increasing differences among flower types; similar results can be
gleaned from one other study. The available experimental evidence thus suggests
that constancy reflects behavioral constraints.
ACKNOWLEDGMENTS
For comments and ideas I thank W. S . Armbruster, D. Campbell, P. Feinsinger,
A. Montalvo, C . Osenberg, and especially my most thoughtful and constant critic,
M. Price. She and students from two graduate classes helped in the field, and
National Science Foundation grants DEB 81-02774 and BSR 83-13522 provided
financial support.
FLOWER CONSTANCY
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