Bee Flowers: A Hypothesis on Flower Variety and Blooming Times

Bee Flowers: A Hypothesis on Flower Variety and Blooming TimesAuthor(s): Bernd HeinrichSource: Evolution, Vol. 29, No. 2 (Jun., 1975), pp. 325-334Published by: Society for the Study of EvolutionStable URL: http://www.jstor.org/stable/2407220 .

Accessed: 03/09/2013 15:38

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

Society for the Study of Evolution is collaborating with JSTOR to digitize, preserve and extend access toEvolution.

http://www.jstor.org

This content downloaded from 129.128.216.34 on Tue, 3 Sep 2013 15:38:52 PMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=ssevol

http://www.jstor.org/stable/2407220?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


BEE FLOWERS: A HYPOTHESIS ON FLOWER VARIETY AND BLOOMING TIMES

BERND HEINRICH

Division of Entomology and Parasitology, University of California, Berkeley, California 94720

Received June 3, 1974

In arctic (Kevan, 1972), temperate (Lovell, 1903), and tropical regions, the flowers of different species of plants in a given habitat at any one time usually exhibit a variety of colors, scents, morphologies, and blooming times. Bees are the primary pollinators of many of them (Baker and Hurd, 1968). Adaptations of given species of plants to specific pollinators (MMuller, 1881; Knuth, 1909; van der Pijl, 1961; van der Pijl and Dodson, 1966; Grant and Grant, 1965; Faegri and van der Pijl, 1971), to an array of generalized pollinators, or to differences in pollinator behavior (Macior, 1970, 1971) probably do not account for all of the extraordinary array of forms, colors and scents of the bee-pollinated flowers in a given habitat. Those commonly visited by bumblebees alone may be white, red, yellow, purple, ultraviolet, green, or blotched and streaked with a variety of colors. The flowers may be zygomorphic (Werth, 1949), platform- shape, or equipped with varying numbers of lobed and unlobed petals.

The key to the evolution of different types of flowers is usually considered to reside in the preferences and the flower- constancy of the pollinators. The flower- constancy of bees, and its probable impact on plant speciation has been discussed (Grant, 1949; Grant, 1950; Manning, 1956a; Free, 1966). However, little is known about the selective pressures producing the variety of flowers upon which flower-constancy is based.

It is rarely possible to witness selection, but inferences of differential selection ex- erted by pollinators can sometimes be made from careful studies of the interactions of flower-visitors and plants in a given area. The studies of Clarkia bees of the western

United States (MacSwain et al., 1973) and of bumblebees on Pedicularis in the Rocky Mountains (Macior, 1970, 1971) serve as good examples. It is necessary to deter- mine what affects flower choice and flower fidelity of the foragers in the presence of numerous species of sympatric plants.

This paper concerns the functional significance in the variety and in the assort- ment of flowers visited primarily by bumblebees in one habitat in Maine. The observations from this area may serve as a model applicable to other plant assemblages and pollinators.

METHODS

Observations were made in a bog containing native plants in which the most common flower visitors were native bees. The bog contained areas of heath, open areas of sphagnum moss and marsh flats. In Maine, solitary bees and bumblebees are by far the most common visitors to most flowers, although the imported Apis mellifera is abundant in some localities. The solitary bees are abundant in spring, while bumblebees are the most common visitors in late summer and fall. (Heinrich, unpub.) Other observations were made in a hay- field with non-native plants, where the bees were in the presence of an artifactual arrangement of plants.

The times of flowering were derived from observations during the spring and summer of 1972 and the summer and fall of 1973, according to the method of Anderson and Hubricht (1940). The flowering times during the 10 weeks in which the observations overlapped were similar. Most of the species grow in patches, but in scoring flowering time, the presence of flowering individuals within the entire habitat was used,

EVOLUTION 29:325-334. June 1975 325



326 B. HEINRICH

Aster novoe-ong//oe

Spfraea /i/o/01 /\hm

Zmpallens

5 meters

S5o/io/ago cancdensis ~ t

Chte/oner glabrG

FIG. 1. Foraging path of a Bombus vagans worker visiting five species of flowers in 18 minutes. It spent most of its time appearing to search for the blossoms of Chelone hidden in foliage. Few, if any, of these blossoms in the area were not visited. Some were visited several times in close succession. The bee hesitated before landing on the Aster and Impatiens blossoms.

rather than the presence of flowering within a particular plot or patch. Voucher speci- mens of the plants are deposited in the herbarium at the University of California, Berkeley.

RESULTS AND DISCUSSION

Intraspecific Variability and 'Flower-visitor Fidelity

The search-behavior of most animals involves search-images (Tinbergen, 1960). Given equal food reward per prey item, animals generally search for the most abundant morph. As a result, the rate of food retrieval is density dependent. In the case of predator-prey interactions, the rarer prey is captured at a lower rate than that pre- dicted by its frequency (Popham, 1941). Conversely, in pollinator-flower relationships, infrequent variants of a species are at a "minority disadvantage" with respect to pollination (Levin, 1972a).

Like predators, bees and other pollinators acquire a search image during foraging. Bumblebees are conditioned rapidly, and

search for flowers with the features they as- sociated with food rewards (Kugler, 1934; Manning, 1956b). Initially the bees may visit numerous species of plants (Hobbs, 1962) on a foraging trip (Fig. 1), but they eventually restrict their foraging to specific ones (Fig. 2).

The eventual flower-choice of the bees is related to the amount of food reward that the flowers yield. The bees forage where they make the most profit (Hobbs, 1962), provided they can distinguish one species from another. (The most rewarding flowers are not necessarily the ones of greatest food production. Profit is also related to the number of other bees already foraging from the flowers, and on how well the foragers have learned to manipulate the flowers.) The search image, and conse- quently the flower fidelity, should be sharp- ened if the flowers are sufficiently distinctive, and if the identifying features are uniform and unvarying. However, if the flowers offer no food rewards, and if they rely on inexperienced foragers for pollination, then uniformity of features should lead to rapid identification, and rapid ex- clusion.

In the Maine bog I observed only one flower species, the orchid Calopogon pulchellus (Salisb.) R. Br., with conspicuous variability of color in the visible portion of the spectrum. Unlike most other flowers C. pulchellus provides no food rewards to the pollinators, relying entirely on deceit to attract pollinators.'

Bumblebees visiting the widely scattered flowers of C. pulchellus stopped also at Pogonia ophioglossoides (L.) Ker., another showy orchid, and Kalmia angustifolia L. which was also in bloom in the area. A total of 14 bumblebees (4 species) observed in two afternoons visited a total of 75

1 The flower has a lip crested with yellow hairs superficially resembling anthers (the lip is upper- most rather than ventral as in most orchids). Bumblebees, and skippers (Hesperidae) probed among these hairs with their probosci. I found no nectar in any of the 30 flowers from which I attempted to extract nectar with 1 Iul capillary tubes.



BEE FLOWERS 327

BEE# I mN

FIG. 2. Foraging paths of a Bombus fervidus worker. Designations of flowers as in Fig. 1. ()=a foraging trip of 29.5 minutes on Aug. 19. Two other foraging paths of the same bee (not plotted) were observed on the same day. During the total time that the bee was observed while on the three foraging trips (65.3 minutes) it visited 620 flowers of Aster and 24 of Impatiens. (Other B. fervidus in the same area visited nearly exclusively the Impatiens.) On Aug. 25 the same bee was followed for 33.0 minutes

( .It now visited 307 flowers of Aster and no Impatiens, even though Impatiens was then as common as before.

blossoms of C. pulchellus. The bees ap- peared to be passing through the area hur- riedly since they did not remain for more than several minutes and sampled only a few of the available flowers. Presumably they had not yet established a specific foraging area and flower preferences (see Fig. 1 ).2 Since the non-rewarding flowers are visited primarily by unconditioned pollinators, it is probable that the flower's ability to deceive is increased by its variability in color. The highest number of these non-rewarding flowers visited by a bee without stopping at other flowers was 17. The more dissimilar are the non- rewarding flowers, the longer it should take pollinators to learn to avoid the species.

Pogonia blooms at the same time and in the same places as Calopogon. The pink Pogonia blossoms contain nectar, and flower variability is not conspicuous. The bumblebees visiting the Calopogon also visited the Pogonia. Since the bees visited both species of orchids, they received at least some food

2 Bumblebees with established foraging preferences may visit thousands of blossoms in an area, remaining during a single foraging trip for an hour or more in a small area (Heinrich, unpub.).

rewards while foraging in the area. The simultaneous bloom of the two species could have selective value if the combined flowers provide sufficient visual stimuli to attract the pollinators, and if the food rewards of the one retain the unconditioned pollinators long enough to pollinate the non-rewarding flowers.

Color and Form Variety Between Species It is probable that at least two opposing

selective pressures are operating simultaneously to affect flower morphology. On the one hand the flowers of a given species must conform in various ways to the re- quirements of its pollinators. For example, both honeybees and bumblebees have spon- taneous form- and color-preferences (Zerr- hahn, 1933; Kugler, 1934) and learn to associate some signals with food more quickly than others (Menzel, 1968; Kris- ton, 1973). The insects discover those food sources first which are advertised by the most "conspicuous" flower signals (Lovell, 1919), and which are not hidden. On the other hand, the "preferred" signals and flower morphologies are not necessarily the most favorable for cross-pollination. The



328 B. HEINRICH

flowers of a given species are no longer "conspicuous" when they are like those of a neighbor. The more they are like their neighbor, the more the foragers stray, usually at an energetic cost to themselves. For example, honeybees visit the flowers of a nectarless variety of muskmelon, Cucumis melo, but only if they occur intermingled with flowers bearing nectar (Bohn and Davis, 1964). The more unlike the neigh- boring flowers, the more it pays the bees to specialize and the more the plants can rely on flower-faithful foragers.

Honeybees (v. Frisch, 1914) and bumblebees (Kugler, 1934) can be trained to associate a variety of scents, colors, and geometric patterns with food. In experimental situations their ability to choose the "correct" symbol or constellation of stimuli (the one(s) to which they have been conditioned) in large measure depends on how much these differ from the others which are concurrently available.

In the field the scents, colors, and geometric patterns (Leppik, 1956) of flowers are also token stimuli symbolizing food, and the juxtaposition of different flower signals (either different colors, scents, and shapes or constellations of these stimuli) in any one habitat affects the bees' fidelity and hence their pollination efficiency (Levin, 1972a, 1972b). Muller (1881) noted that different species of bee-flowers blooming at the same time and place in the Alps differed widely in color. Similarly, different species of Pedicularis pollinated by bumblebees and blooming together on Mt. Rainier have different reflectances (Macior, 1973). As many as seven species of bee pollinated Clarkia may grow on the same hillside at the Sierra foothills of Cali- fornia, and although these plants appear to be very similar vegetatively, the species are sharply defined by differences in flower color, petal markings, and petal size and lobing patterns (Lewis, 1953; MacSwain et al., 1973). The UV absorption patterns of "yellow" composite flowers blooming concurrently in Florida indicate that the flowers that to us appear to be similar, are different to the bees (Eisner et al., 1969).

Kevan (1972) writes that "To insects, the high arctic flowers of the different species have more distinctive colors and color patterns, and there are more different colors and color patterns, than there are to humans."

Competition for the available pollinators by the different species of plants should favor making the rarer flowers more rewarding. Overcoming the "minority disadvantage" would also necessitate adver- tising the presence of this reward with signals different from the less rewarding flowers. Kauffeld and Sorensen (1971) have shown that the attractiveness of different clones of alfalfa is closely related to nectar production, and unrelated to flower color and aroma, even though the bees orient to the flowers primarily by color at a distance and aroma at close range. Only when the bees perceive a difference in a flower species from the others is it advan- tageous for that flower to produce more nectar and compete with the others for the pollinators. The greater the variety of the flowers in a community the less likely that the pollinators will roam and the better are the chances that pollen will be deposited from one flower to another of the same species. In turn, the differences between simultaneously blooming species promoting individual bee forager fidelity, may preadapt the flowers for pollination by some other pollinator species, and initiate adaptive radiation. For example, orange flowers could attract hummingbirds as well as bees. If pollinated by the birds they could evolve to become red.

Apparent "straying" of bees was observed in a field containing two non-native flowers (one orange, one yellow) in simultaneous bloom, Hieracium aurantiacum L. and H. pratense Tausch. In this natural experiment (but ecologically unnatural flower arrangemnent) the bees distinguish between these morphologically similar flowers and establish individual foraging preferences (Table 1). However, some of the bumblebees on the orange flowers frequently landed on the yellow (and vice versa), frequently leaving them immedi-



BEE FLOWERS 329

TABLE 1. The numbers and kinds of flowers visited by 12 insects in a field of Hieracium pratense and H. aurantiacum during portions of their foraging trips. The morphologically similar flowers, which were blooming simultaneously, occurred in approximately equal proportions at an average density (total) of 100 per square meter. Numbers indicate the flowers of each species visited during the foraging trip.

Number of flowers visited

(yellow) (orange) Foragers H. pratense H. aurantiacum

Bombus vagans 17 73 if if 16 337 if ft 170 14 if If O 146

B. terricola 162 0 if if 0 35 if if t78 0

B. ternarius 0 189 Apis mellifera 142 0

if if 0 183 Syrphid fly 49 0

if if 37 12

ately without stopping to probe for nectar, as if becoming aware of their "mistake" only at very close range. Similar behavior on non-native flowers was also observed in a field containing the yellow composite Leontodon autumnalis L. and the buttercup Ranunculus acris L. The "approach-avoid- ance" behavior of the bees on these non- native flowers are cited to point out possible straying of a pollen vector in relation to the juxtaposition of superficially similar flowers. Inconstancy, as that cited above, results in wastage of nectar and pollen for the plants, and reduction of profit to the bees. If the plant species produce sterile hybrids, the penalty to them of the bees' straying would be more severe, since they would be removed from the reproducing population. For example, Lewis (1961) observed that although Clarkia lingulata and C. biloba (which can interbreed and produce sterile hybrids) may grow in adjacent colonies, in experimental mixed populations one is eventually eliminated, possibly because of infi- delity of the pollinators.

A long-term evolutionary response

whereby hybridization is reduced is charac- ter displacement, which has been observed in butterfly pollinated Phlox (Levin and Kerster, 1967; Levin and Schahl, 1970). Other options that accentuate contrasts and thus reduce pollinator straying include shifts of blooming time, or changes of habitat. While selective pressures for the above would be expected to be particularly severe where the production of hybrids is possible, they need not be restricted to potentially interbreeding populations.

In the bog with native plants, the flowers blooming in any one place and time are different from each other (Fig. 3). Despite the large variety of flowers, the diversity of pollinators required for pollination appears to be low. Except for a few Lepidoptera on Cephalanthus, and Diptera and Coleoptera on Spiraea, the flower visitors other than bees are relatively few (Heinrich, unpub.). It is well-recognized that social bees do not have specific bee-flower relationships; the bees visit whatever flowers are available that provide access to the nectar or pollen (Kugler, 1934; Manning, 1956b; Brian, 1957). There is some separation in the flowers visited by "short-tongued" and "long-tongued" bumblebees. However, the diversity of flower types is probably not explicable in terms of adaptation to specific pollinators alone, since the bees are for the most part similar to each other while the flowers vary widely.

Morphology, like color and scent, may be another feature increasing the bee's fidelity. For example, although the large zygomorphic flowers of Chelone glabra L. (Fig. 3) produce relatively large amounts of nectar, in central Maine they are visited exclusively by Bombus vagans and B. fervidus, and only by those specific individuals which have learned to enter the blossoms. The "closed" corolla excludes most of those bees which have not specialized. However, those bees which enter, and which have been rewarded with ample nectar, search widely for other flowers of the same type. If the morphology of the blossoms of the relatively widely spaced plants did not act



330 B. HEINRICH

A D C D C D ABCD ABCD

Scutellaria Chelone Caooo -v fkg (Labiatae) N (Scrophulariaceae) Calopogon EQgonla

QN (Orchidaceae) D (Orchidaceae)N ABCD AABCD ABD C D

-4-

Nymphaea (Nymphaeaceae) Rhododendron Solix Cephalanthus P (Ericaceae) NP (Salicaceae) NP (Rubiaceae) Nt

A B C D ABD A B A B C D AB

Led urn Voccinium ~~~~Pontederia (Va cciniaceae)- (pontederiaceae)

(, | Rosa(Rosaceae)P (Ericaceae) N Gaylussacia NP N ABC A B C D Vaccinium CD

Spiroec @ A9k. (Vacciniaceae)N (Rosaceae) PN Andromeda

Solidago | Kalmia Senecio Chamaedaphne

(Compositae) N (Ericaceae) N P Aster ( Ericaceae) N (Compositae)NP Iris (Iridaceae) N

FIG. 3. The morphological types of native flowers visited by bumblebees in a bog. The most common visitors are indicated by letters in upper left. A = Bombus terricola Kirby, B = B. ternarius Say, C = B. vagans F. Smith, D = B. fervidus Fabricius. Some flowers of different families have similar external floral morphology, while in others of the same family the external flower morphology varies widely. N and P indicate nectar and/or pollen, the primary food reward of the flowers.

to exclude some bees, there would be little nectar remaining, and potentially faithful bees might be less inclined to specialize on the relatively sparsely distributed blossoms. Similarly, I conclude that flower signals act at the level of the individual flower visitor, to exclude as much as to attract. Whole populations (species) are excluded from some plant species when the flower signals, and the flower morphology, becomes more and more diversified and devi- ant from the ancestral types. The specificity thus becomes built-in. Scent, like length of corolla tubes, may sort out and exclude different flower visitors, yielding flower-faithful foragers. Dodson et al. (1969) find that males of many Euglossine bees in the Neotropics are strongly attracted to 1,8-cineol found in more than 70% of 150 species of orchids analyzed. Yet the bees are highly species-specific.

The specificity may be due to repellent scents, for adding some of the 50 other scents of orchids to 1,8-cineol results in a drastic reduction in the number of Euglos- sine species attracted.

There is obviously a limit to the variety of visual signals of flowers that a given group of pollinators, like bees, can attend to before straying is inevitable. The greater the number of plant species in a habitat, as in the tropics, the greater should be the selective pressures for flowers to deviate from the "conventional" bee-pollinated ancestral types. Herein may lie part of the answer to the numerous bizarre types of pollination mechanisms of tropical flowers based on species-specific foragers, the great reliance on scent as a major alterna- tive long-distance signalling mode, and the sometimes precise partitioning of seasonal or diurnal blooming times (van der Pijl and



BEE FLOWERS 331

26w 25

24 23 w

2 1B

5 20 p

18 w 4 1 7 P

16 P

14 B_1 2 13 R

10 w 3 9 W

8 w

2 6 8

2 w

20 25 30 5 10 1520 25 31 5 10 15 20 2530 5 10 15 20 25 31 5 10 15 20 25 31 5 10 1520 2530 5 lOIS APRIL M AY JUNE JULY AUGUST SEPTEMBER OCTOBER

FIG. 4. Flowering times of the native plants frequently visited by bumblebees in a bog. Included are different types of bog habitat so that many of the simultaneously blooming flowers were not necessarily side by side. Asterisk= flowers provide pollen only. Matched pairs of numbers at left indicate flowers of nearly identical or similar appearance. Others differ widely in morphology. Letters at right indicate flower color. B= blue, L = lavender, P = pink, R = red, W = white, Y = yellow. Species are coded by numbers appearing near mid-point on graph of flowering time. 1, Salix discolor, Muhl.; 2, Chamae- daphne calyculata (L.) Moench.; 3, Salix sericea Marsh; 4, Rhododendron canadense L. (Torr.); 5, An- dromeda glaucophylla Link; 6, Kalmia polifolia Wang; 7, Vaccinium corymbosum L.; 8, Nymphaea dorata Ait.; 9, Gaylussacia buccata (Wang) K. Koch; 10, Ledum groenlandicum Oeder; 11, Iris versi- color L.; 12, Vaccinium Oxycoccus L.; 13, Kalmia angustifolia L.; 14, Scutellaria epilobifolia A. Hamil- ton (?) ; 15, Calapogon puichellus (Salisb.) R. Br.; 16, Pogonia ophioglossoides (L.) Ker.; 19, Rosa carolina L.; 20, Rosa blanda Ait.; 21, Pontederia cordata L.; 22, Spiraea tomentosa L.; 23, Cephalanthus occidentalis L.; 24, Solidago uliginosa Nutt.; 25, Aster novae-an gliae L.; 26, Chelone glabra L. Species 6, 9, 14, 15, 16, 19, 20, and 26 were relatively rare.

Dodson, 1966). In addition, if the need for variety for the sake of forager-fidelity has been a potent selective pressure, then it should also have resulted in adaptive radiation leading to reliance on pollinators other than the ancestral bee pollinators.

Phenology, Mimicry and Food Rewards If variety of form and color of flowers

occurring in a habitat at any one time is of significance to the reproductive biology of the plants, then several mechanisms whereby such variety could be constructed and maintained are possible.

The simplest mechanism may be a di- vergence in blooming time of the competing species of similar appearance. In a relatively stable (excluding possible succession) habitat such as a bog inhabited by native plants, the time of flowering of the various

species extends from early spring until fall (Fig. 4). In this habitat the two species of Salix (discolor and sericea), two species of Kalmia (angustifolia and polifolia), and two species of Vaccinium (macrocarpon and Oxycoccus), having nearly identical blossoms, have separate blooming times, thus tending to accentuate differences between the flowers occurring in this habitat at any one time. However, two species (Rosa blanda and R. carolina), both of which are relatively rare, bloom at about the same time of year.

Macior (1971) suggests that mimicry among some of the rarer flowers in the Rocky Mountains is a mechanism whereby the population size of a flower type is retained high enough for the bumblebee pollinators to retain an interest in it-and make foraging on such flowers worthwhile.



332 B. HEINRICH

TABLE 2. The delay in blooming time, and the nectar reward, of one plant with respect to another of similar appearance in the same habitat. Eight sets of similar flowers are compared.

Flowering delay (days) of Nr. 2 and ,l nectar 3 in relation X mg

to Nr. 1 X Range N sugar Difference

I 1 Aster novae-angliae L. - 0.042 (0-0.44) 30 0.021 - 2 Aster simplex Willd. (?) 31 0.040 (0-0.41) 25 0.018 -14%

II 1 Vaccinium Oxycoccus L. - 0.487 (0-1.19) 30 0.133 - 2 Vaccinium macrocarpon Ait. 15 0.023 (0-0.187) 43 0.0047 -96%

1 Prunus pensylvanica L.f. - 0.179 (0-0.625) 50 0.042 - III 2 Prunus virginiana L. 5 0.008 (0-0.0156) 132 0.001 -98%

3 Prunus serotina Ehrh. 15 0.064 (0-0.094) 33 0.022 -48%

IV 1 Rubus allegheniensis Porter - 1.21 (0-3.98) 25 0.25 - 2 Rubus setosus Bigel ( ?) 23 - (Trace) 25 _ -100%

1 Salix discolor Muhl. - 2.16 (0.54-3.34) 51 1.44 - V 2 Salix sericea Marsh. 16 4.59 (3.10-4.40) 31 0.43 -70%

1 Solidago canadensis L. - 0.005 (0-0.031) 30 0.0024 - V 2 Solidago rugosa Mill. 35 0.006 (0-0.031) 28 0.0045 +87%

1 Vaccinium corymbosum L. - 4.75 (1.96-5.40) 12 0.86 - VI 2 Gaylussacia buccata (Wang.) K. Koch 11 2.54 (0.97-5.60) 27 0.30 -65% 1 Viburnum lentago L. - 0.062 (0-0.625) 34 0.0038 -

2 Viburnum acerifolium L. 5 - (Trace) 25 - -100% 1 Refers to whole catkins, having approximately 200 nectar-bearing flowers.

On the other hand, the staggering blooms of different flowers in any one ecosystem is thought to have evolved in relation to a reduction in competition between the plants for the pollinators. This hypothesis, proposed by Robertson (1895, 1924) has cur- rently received more detailed attention (Mosquin, 1971; Heinrich and Raven, 1972; Frankie et al., 1973; Stiles, 1974).

The food rewards may be another factor along with the flower signals affecting the selective pressures on blooming time. The pollinators would probably discriminate between two similar, but not identical, simultaneously blooming flowers if one of them is more common or provides greater food reward. The species discriminated against may thus be eliminated or become autoga- mous. However, its chances of being pollinated would be greater if it blooms slightly after the similar one of high food production, because the pollinators would already be conditioned to a similar search image. The amounts of sugar per flower in several

flowers of similar appearance in Maine tends to support this hypothesis. The second flower to bloom tends to have less nectar than the first of similar appearance (Table 2). The second flower may thus deriye some benefit by being similar to the first if it is visited by pollinators that have as long a memory as honeybees. Honeybees are reported to have a long-term memory lasting one month (Menzel, 1968). When the insects learn new signals they do not necessarily forget old ones but merely sup- press them in their memory (Kolterman, 1969).

The establishment of similarity between flowers of different species through time and at different locations, and variety at any one time and place, could involve several selective pressures operating simultaneously. On the one hand, a rewarding flower may diverge either in blooming time or flower signal and, thereby, "escape" a non-rewarding one. Being unable to "escape" a floral mimic in space, the reward-



BEE FLOWERS 333

ing flower could bloom before the non- rewarding, and escape it in time. As a result of such interactions flower-convergence could be evolving at the same evolutionary time that flower diversity, at any one seasonal time, is retained or accentu- ated. It must be stressed that this discussion is restricted to the external features of flowers-color, scent, morphology. (The hypothesis would predict some degree of convergence in food rewards of flowers pollinated by the same group of pollinators at the same time that flowering times and token stimuli may be diverging.)

These results and suggestions must be interpreted with great caution, for the nectar rewards are in most cases so minute that it is often difficult to measure them accurately, and there is now evidence that more than just sugars and water may be provided (Baker and Baker, 1973). Sec- ondly, little can be said about the selective pressure for specific flower signals and their arrangement in time in a habitat until it is shown which animals are the primary pollinators. Lastly, and perhaps more im- portant, as Macior (1971) has pointed out, the key to an understanding of the selective pressures will reside in more careful analy- sis of the foraging behavior.

SUMMARY

The external features of flowers of the different species of native plants in a Maine bog vary greatly. However, almost all of these diverse flowers are visited primarily by the same species of native bees. An explanation for the variety of flower colors, shapes, and scents may be related to addi- tional factors besides adaptation to specific pollinators. It is proposed that a first requirement for an efficient pollination system with many species of plants in a habitat is flower fidelity by individual pollinators. Such fidelity is observed in bumblebees. Individual bees of a species are well-known to be conditioned to forage from any of a great variety of morphological types of flowers. However, the fidelity breaks down if the flowers blooming at any

one time are not sufficiently different from each other. The simultaneous flowering of common species may result in a diversity of flower types, while sequential flowering or rareness, may result in flower similarity, or convergence. On the other hand, flowers should evolve to reduce their variability within the species. Those flowers which do not provide food would be at a selective advantage by being variable in appearance, or by mimicking another flower and blooming slightly after it.

ACKNOWLEDGMENTS

I thank Herbert G. Baker, Robert K. Colwell, Leslie K. Johnson, Paul Opler, and Peter H. Raven for helpful comments and criticisms on a draft of the manuscript. This study was supported in part by Na- tional Science Foundation Grant GB-3 1542.

LITERATURE CITED

ANDERSON, E., AND L. HUBRICHT. 1940. A method for describing and comparing blooming seasons. Bull. Tor. Bot. Club 67:639-648.

BAKER, H. G., AND P. D. HURD. 1968. Intra- floral ecology. Ann Rev. Ent. 13:385-413.

BAKER, H. G., AND I. BAKER. 1973. Some anth- ecological aspects of the evolution of nectar- producing flowers, particularly amino acid production in nectar, p. 242-264. In V. H. Heywood (ed.), Taxonomy and ecology. Proc. of an Int. Symp. Academic Press, New York.

BOHN, G. W., AND G. N. DAVIS. 1964. Insect pollination is necessary for the production of muskmelons (Cucumis melo v. veticulatus). J. Apic. Res. 3:61-63.

BRIAN, A. D. 1957. Differences in the flowers visited by four species of bumblebees and their causes. J. Anim. Ecol. 26:71-98.

DODSON, C. H., R. L. DRESSLER, H. G. HILLS, R. M. ADAMS, AND N. H. WILLIAMS. 1969. Bio- logically active compounds in orchid fragrances. Science 164:1243-1249.

EISNER, T., R. E. SILBERGLIED, D. ANESHANSLEY, J. E. CARREL, AND H. C. HOWLAND. 1969. Ultraviolet video-viewing: the television cam- era as an insect eye. Science 166: 1172-1174.

FAEGRI, K., AND L. VAN DER PIJL. 1971. The principles of pollination ecology. 2nd ed., Ox- ford, Pergamon Press.

FRANKIE, G. W., H. G. BAKER, AND P. A. OPLER. 1973. Tropical plant phenology: applications for studies in community ecology. In H. Lieth (ed.), Phenology and seasonal modeling. Ber- lin, Springer-Verlag.



334 B. HEINRICH

FREE, J. B. 1966. The foraging behavior of bees and its effect on the isolation and speciation of plants. In J. G. Hawkes (ed.), Reproductive biology of vascular plants. London, Pergamon Press.

FRISCH, K. v. 1914. Der Farbensinn und For- mensinn der Bienen. Zool. Jahrb. (Physiol.). 35:1-188.

GRANT, V. 1949. Pollination systems as isolating mechanisms in angiosperms. Evolution 3: 82-97. . 1950. The flower constancy of bees. Bot.

Rev. 16:379-398. GRANT, V., AND K. A. GRANT. 1965. Flower pol-

lination in the Phlox family. New York, Columbia University Press.

HEINRICH, B., AND P. A. RAVEN. 1972. Ener- getics and pollination ecology. Science 176: 597-602.

HOBBS, G. A. 1962. Further studies on food- gathering behavior of bumblebees (Hymenop- tera: Apidae). Can. Ent. 94:538-541.

KAUFFELD, N. M., AND E. L. SORENSEN. 1971. Interrelations of honeybee preference of Alfalfa clones and flower color, aroma, nectar volume, and sugar concentration. Kansas Agric. Expt. Station. Res. Publ. 163.

KEVAN, P. G. 1972. Floral colors in the high Arctic with reference to insect-flower relations and pollination. Can. J. Bot. 50:2289-2316.

KNUTH, P. 1909. Handbook of flower pollination V. 1. Translated by J. R. Ainsworth. Clasendon Press. Oxford.

KOLTERMAN, R. 1969. Lern- und Vergessens- prozesse bei der Honigbiene-angezeigt anhand von Duftdressuren. Z. vergl. Physiol. 63:310- 334.

KRISTON, I. 1973. Die Bewertung von Duft- und Farbsignalen als Orientierungshilfen an der Futterquelle durch Apis mellifera L. J. comp. Physiol. 84:77-94.

KUGLER, H. 1934. Bliitenokologische Untersuch- ungen mit Hummeln VII Die Anlockung von "Neulingen" durch Bliiten. Planta 23:692-714.

LEPPIK, E. E. 1956. The form and function of numeral patterns in flowers. Amer. J. Bot. 43:445-455.

LEVIN, D. A. 1972a. Low frequency disadvantage in the exploitation of pollinators by corolla variants in Phlox. Amer. Natur. 106:453-460. . 1972b. Pollen exchange as a function of

species proximity in Phlox. Evolution 26:251- 258.

LEVIN, D. A., AND H. W. KERSTER. 1967. Natural selection for reproductive isolation in Phlox. Evolution 21:679-687.

LEVIN, D. A., AND B. A. SCHAAL. 1970. Corolla color as an inhibitor of interspecific hybridization in Phlox. Amer. Natur. 104:273-283.

LEWIS, H. 1953. The mechanism of evolution in the genus Clarkia. Evolution 7:1-20.

* 1961. Experimental sympatric populations of Clarkia. Amer. Natur. 95:155-168.

LOVELL, J. H. 1903. The colors of northern gamopetalous flowers. Amer. Natur. 37:365- 384; 443-479.

1919. The flower and the bee. Constable. London.

MACIOR, L. 1970. The pollination ecology of Pedicularis in Colorado. Amer. J. Bot. 57: 7 16-726. . 1971. Coevolution of plants and animals

-systematic insights from plant-insect interactions. Taxon 20:17-28. . 1973. The pollination ecology of Pedicu-

laris on Mount Rainier. Amer. J. Bot. 60: 863-871.

MACSWAIN, J. W., P. H. RAVEN, AND R. W. THORP.

1973. Comparative behavior of bees and Ona- graceae. IV. Clarkia bees of the western United States. Univ. Cal. Publs. Ent. 70:1-80.

MANNING, A. 1956a. Some evolutionary aspects of flower constancy of bees. Proc. R. Phys. Soc. 25:67-71. . 1956b. Some aspects of foraging behav-

iour of bumblebees. Behaviour 9:164-201. MENZEL, R. 1968. Das Gedachtnis der Honig-

biene fur Spektralfarben. I. Kurzzeitiges und langzeitiges Behalten. Z. Vergl. Phys. 60:82- 102.

MOSQUIN, T. 1971. Competition for pollinators as a stimulus for the evolution of flowering time. Oikos 22:398-402.

MULLER, H. 1881. Alpenblumen. Engelmann. Leipzig.

PIJL, L. VAN DER. 1961. Ecological aspects of flower evolution. II Zoophilous flower classes. Evolution 15: 44-59.

PIJL, L. VAN DER, AND C. H. DODSON. 1966. Or- chid flowers, their pollination and evolution. Univ. of Miami Press.

POPHAM, E. J. 1941. The variation in the color of certain species of Arctocorisa (Hemiptera: Corixidae) and its significance. Zool. Soc. Lond. Proc. (A) III:135-172.

RO3ERTSON, C. 1895. The philosophy of flower seasons, and the phaenological relations of the entomophilous flora and the anthopilous insect fauna. Amer. Natur. 29:97-117. . 1924. Phenology of entomophilous flow-

ers. Ecology 5:393-407. STILES, F. G. 1974. Ecology, flowering phenol-

ogy, and hummingbird pollination of some Costa Rican Heliconia. (in press).

TINBERGEN, L. 1960. The natural control of insects in pinewood. I. Factors influencing the intensity of predation by songbirds. Arch. Neerl. Zool. 13:265-336.

WERTH, E. 1949. Zum Begriff der Hummel- blumen. Ber. Naturf. Ges. Augsburg. 2:11-127.

ZERRHAHN, A. 1933. Formdressur und Form- unterscheidung bei der Honigbiene. Z. Vergl. Physiol. 20:117-150.



Documents

Bee Flowers: A Hypothesis on Flower Variety and Blooming Times