Flower Constancy Research Articles

A Model to Predict the Influence of Insect Flower Constancy on Interspecific Competition between Insect Pollinated Plants

Honeybees and bumblebees, among the most important pollinators in many plant communities, are known to exhibit flower constancy. When foraging, bees do not sample flowers randomly as they encounter them, but rather they exhibit a strong preference for one species of flower, and will ignore other species that they encounter. The species favoured depends on previous foraging success: ifa species of flower has previously provided a high reward, it will be favoured to the exclusion of others. Various models have been developed to describe the optimal foraging pattern of flower feeding insects, which explain, at least in part, observed behaviour. However, they do not consider the importance consequences of flower constancy for competition between plants dependant upon insects for pollination. Bees are most likely to favour a common species which they encounter frequently, and will fly directly between individuals of the favoured species, and thus provide efficient pollination. Conversely, they are unlikely to develop a preference for a scarce flower which necessarily is rarely encountered.A simple two-flower species model is developed which predicts the proportion of insects which will favour each of the two species for particular flower densities, assuming that individual insects favour the species which provides them with the greatest reward per time.The model predicts that scarce plant species will receive no pollinators below a threshold density of reward, and that scarce plants must provide a relatively huge reward per flower to achieve pollination. The threshold is lowered at high insect densities when the reward offered by the more common species becomes depleted. The implications of flower constancy to plant communities are discussed.

Modes and origins of mechanical and ethological isolation in angiosperms.

Mechanical and ethological isolation between species is widespread in angiosperms with specialized animal-pollinated flowers, being recorded in 29 species groups belonging to 27 genera and 16 families. Mechanical isolation occurs in two forms. (i) The common type, designated the Salvia type, operates when two or more species of flowers are adapted for different groups of pollinators with different body sizes and shapes. (ii) In the Pedicularis type two flower species have the same species of pollinator but pick up pollen from different parts of the pollinator's body. Four forms of ethological isolation are recognized. (i) In the Aquilegia type, which is widespread, ethological isolation is a side effect of mechanical isolation. (ii) The flower-constancy type, as the name suggests, is based on flower-constant foraging behavior. (iii) In the Ophrys type, floral scents attract male bees or wasps and play a role in their mating behavior; different species of flowers, often orchids, have different scents and attract different sets of hymenopteran species. (iv) The monotropy type occurs in plants pollinated by hymenopterans with species-specific or group-specific flower preferences for nutritive purposes (monotropic and oligotropic bees and fig wasps). Three modes of origin of floral isolation are confirmed by evidence: (i) mechanical and ethological isolation arising as a by-product of allopatric speciation, (ii) ethological isolation developing by selection for reproductive isolation per se, and (iii) mechanical isolation arising as a by-product of character displacement. Mode of origin i accounts for the Salvia and Aquilegia types of isolation in nine known species groups and for the Ophrys type in one group. Mode of origin ii accounts for the flower-constancy type of ethological isolation in two species groups. Mode of origin iii explains mechanical isolation in two groups. Sympatric origin of floral isolation by hybrid speciation and by flower constancy has been proposed, but these modes are undocumented and improbable.

Costs to foraging bumble bees of switching plant species

Many pollinators tend to move between flowers of the same species of plant even when flowers of other species are available. Reasons for this behaviour (known as flower constancy) are unclear. One possible explanation (proposed by Darwin) is that flower handling methods learned on one plant species interfere with previously learned handling methods of other plant species. Darwin's hypothesis was tested by measuring the constancy of bumble bees (Bombus fervidus) foraging in the field and looking for evidence of interference (increased handling times and flower handling errors) when bees switched among four species with relatively simple flowers (Prunella vulgaris, Trifolium pratense, T. hybridum, and Vicia cracca) and two species with more complex flowers (Aconitum napellus and Impatiens capensis). Bees foraging on simple flowers showed no tendency towards flower constancy, and switching between species did not increase handling times or handling errors. Foragers displayed strong constancy when visiting the species with more complex flowers and there was also some evidence of increased handling times and error frequencies following switches. However, the time costs of switching were small (about 1 s over the first flower visit after a switch) and are unlikely to account for flower constancy by bumble bees foraging under natural conditions.

Lack of Evidence for the Toxic Nectar Hypothesis: A Plant Alkaloid Did Not Deter Nectar Feeding by Lepidoptera

Floral nectars of many plant species contain alkaloids and other allelochemics that might deter butterfly visitors and promote flower constancy by specialized pollinators. The pyrrolizidine alkaloid, monocrotaline, has been implicated as such a feeding inhibitor in nectar, in support of this toxic nectar hypothesis. We tested this hypothesis by evaluating monocrotaline for deterrence of nectar feeding in the tobacco budworm moth, Heliothis virescens (Fab.), the cabbage looper moth, Trichoplusia ni (Hubner), and the gulf fritillary butterfly, Agraulis vanillae (L.). Concentrations of monocrotaline added to aqueous sucrose solutions did not reduce consumption in these three species, even with near saturation concentrations of monocrotaline. Also, gulf fritillary butterflies did not alter their preference for visiting orange artificial flowers when given the choice between yellow flowers with a sugar solution and orange flowers with a monocrotaline and sugar solution. Patterns of flower visitation by Lepidoptera are likely due to a combination of factors, such as attractants, feeding stimulants and deterrents, visual stimuli, flower morphology, and ecological factors that control nectar availability.

Flower constancy and learning in foraging preferences of the green‐veined white butterfly Pleris napi

Abstract. Evolutionary pressure should select for efficient foraging strategies, within the constraints of other selective forces. We assess the mechanisms underlying flower choice in the butterfly, Pieris napi (L.), which as an adult forages for nectar. Experiments were carried out on a laboratory colony, using artificial flowers of two colours, and replicated on two successive generations. When nectar was freely available from all flowers, equal numbers of butterflies visited each colour, but individual butterflies exhibited flower constancy, showing a strong preference for one colour or the other. Following 3 day conditioning periods in which nectar was available from flowers of one colour only, butterflies responded by developing a preference for this colour, which persisted when both flower colours were refilled. This preference could subsequently be switched to the other flower colour following a further 3 days of conditioning. These are interpreted as adaptive (learned) responses, which would have obvious selective benefits in the field, enabling butterflies to avoid flower species which experience has shown are poor sources of nectar, and to adapt to temporal and spatial changes in nectar availability.

Recall of flower handling skills by bumble bees: a test of Darwin's interference hypothesis

Pollinators tend to visit flowers of one plant species repeatedly even when flowers of other rewarding plant species are available. Darwin proposed that such flower constancy occurs because flower handling methods learned on one plant species interfere with previously learned flower handling methods of other plant species. Darwin's interference hypothesis was tested by first allowing bumble bees, Bombus bimaculatus, to learn flower handling methods on one plant species (comfrey, Symphytum officinale), and then retesting the bees on comfrey after they had learned to handle flowers of a second species (vetch, Vicia cracca). The same experiment was repeated with different bees and with the order of the plant species reversed. Interference effects were detected by comparing flower access times (time to insert tongue into the flower) during the retesting period with the initial flower access times. Bees relearning handling methods for comfrey returned to their initial access times after one flower visit; bees relearning handling methods for vetch took two flower visits. The interference effects detected were 0·8 s for comfrey (a 47% increase over initial access times) and 2·0 s for vetch (a 120% increase). These results indicate that learning to handle flowers of one plant species does interfere with remembering previously learned flower handling methods. However, interference effects resulting from switches between comfrey and vetch under biologically realistic conditions appear to be relatively small, and are unlikely to account fully for flower constancy by bumble bees.

Memory Constraints and Flower Choice in Pieris rapae

Darwin hypothesized that flower constancy in insects that feed on nectar results from the need to learn how to extract nectar from a flower of a given species. In laboratory tests, Pieris rapae, the cabbage butterfly, showed flower constancy by continuing to visit flower species with which it had experience. The time required by individuals to find the source of nectar in flowers decreased with successive attempts, the performance following a learning curve. Learning to extract nectar from a second species interfered with the ability to extract nectar from the first. Insects that switch species thus experience a cost in time to learn. These results support recent suggestions on the importance of learning in animal foraging.

Flower Constancy: Definition, Cause, and Measurement

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.

Image analysis in the orchidaceae

In orchids a number of variants of specific parameters of the floral image appear to have arisen from a common ancestral type and to have become established as genetically constant ones in the determination of sub-generic taxa. At the present time little is known of the genetic basis for their origin or establishment. Though it is not known at present whether perception and storage of a complex floral pattern play a role in the determination of flower constancy in pollinators (and thus in the genetic isolation of variants), we hypothesize that they do. As a step toward gaining the ability to test this hypothesis, we present a method for the comparative quantification of specific characteristics of floral images, which must bear some relation to the level of sophistication necessary in a processor if visual recognition is to be effected. A number of parameters in the images of orchid flowers have been so analyzed. The relation of these results to the possibility that the evolution of these images has been effected by visually mediated natural selection is discussed.

Orchids, bilateral symmetry and insect perception

The basic characteristics of orchids, possessing the greatest number of complex floral images of any Angiosperm family, are reviewed. Bilateral symmetry (zygomorphy) is shown by use of information theory techniques to give much greater possibilities for the transmission of visually mediated information than radial symmetry. The difference in information content is further enhanced by motion. The analysis is offered as evidence that the evolution of diversity in complex images, if effected by the unique behavioral specificity of pollinators known as “flower constancy”, is most economically explained by hypothesizing recognition and storage of the total image (“gestalt”) in the agents of natural selection.

Field Measures of Flower Constancy in Bumblebees

Field Measures of Flower Constancy in Bumblebees

The Energetics of Pollination

Many animals derive their food energy from the nectar of flowers, and the flowers may also provide them with the materials for growth and reproduction. To the plants, in turn, the animals are the vehicle for the transport of male gametes for fertilization. As a consequence, there is a mutual interdependence involving a set of evolved games where the pollinators try to get the most for their foraging effort, while flowers provide the least reward possible. The flowers must provide enough reward to attract the pollinators and keep them from visiting competitor species, but the rewards must be sufficiently small to keep them moving from one plant to another (Heinrich & Raven, 1972). Interesting complications arise in this simple scheme in male vs. female functions of flowers, when manyflowered vs. fewor single-flowered plants are considered, and when any one plant's most potent competitors are other individuals of the same rather than other species. The latter aspects have been little explored. In order for the pollination system to work requires several conditions. First, there must be advertisement of the rewards. Secondly, flower morphology must be appropriate for the pollinator to become dusted with pollen without dusting the pistil, and to transfer this pollen to a receptive pistil of another flower. The morphological features of the flower act to manipulate the close-in behavior of the pollinator to increase the percentage of cross-pollination events per given food reward provided, or per given forager-flower encounter (Macior, 1974). It is probably a safe working hypothesis that the foragers have selected, by those visits that have resulted in fertilization, most of the flowers that we know today. They have been the agents of flower horticulture in nature, and if we want to observe the selective pressures that have shaped or are shaping flower evolution, we must look to the foraging behavior of the flower visitors. The third major consideration is that the foragers must not only be appropriately manipulated at the flowers, they must also be caused to move between them (Heinrich & Raven, 1972). This involves energetics. And when one looks from the standpoint of energetics, it becomes necessary to consider the environment and the other plants relative to whom the pollinator's choices are made. Most pollinators are inherently promiscuous; they visit flowers for the rewards they contain, regardless of the shape or color of the flower's exterior. But to the plant, to whom flower constancy is important for cross-pollination, fidelity can be bought by providing large food rewards. But this purchase may be at a high price. In the immediate, ecological, sense, too strict a fidelity will hinder the contribution of male gametes to other flowers. A bee, for example, will return repeatedly to a single blossom, visiting no others, provided this blossom is sufficiently rewarding, conspicuous and isolated (McGregor et al., 1959). A second cost, one that may not be apparent unless measured against an evolutionary time

Food Niche Analyses of Bumblebees: A Comparison of Three Data Collecting Methods

We compared three methods for field data collecting in the niche analyses of nine subarctic bumblebee species. The basic information consisted of (a) direct observations of flower visits, (b) analyses of pollen contents in pollen loads and (c) in nectar loads of bumblebees. The number of flower species utilized by each bumblebee species turned out to be the same by all the three methods. The methods also agreed with the obtained niche width results (after square root transformation for the data on (b) and (c)). However, the method (c) scored the lowest niche evenness figures. Niche overlap values of the methods (b) and (c) were the same, while the smallest overlap values were obtained by the method (a). Reasons for the differences are discussed. Method (a) is considered to be the easiest to conduct, but methods (b) and (c) are required for certain types of studies (e.g., flower constancy). In studies where the interest is focussed on the number of flower species in the diet of bumblebee species, the result is independent of the method used, while the outcome of frequency dependent niche analyses is, to some extent, affected by the chosen method.

On the advantage of the specialization of flowers on particular pollinator species

A probability model is constructed to describe the competition of simultaneously flowering plant species for pollinators. The flowers are described by different states for which rate equations are set up. The visits of the pollinators are characterized by degrees of preference for the various flower species. One flower species which has a small amount of pollen and which is visited by a pollinator species with extreme flower constancy is singled out. The advantage of the attraction to other pollinator species without flower constancy is investigated. In particular, the number of pollinated flowers is calculated as a function of the degree of attraction. A minimum is found for different cases, such as when there are many or only two competing flower species, and for the case of the tropics. The possible implications for evolution are discussed.

Laboratory analysis of flower constancy in foraging bumblebees: Bombus ternarius and B. terricola

1. We established apparently normal foraging behavior in captive bumblebees utilizing artificial flowers. Syrup rewards of flowers visited were experimentally manipulated to correspond to nectar volumes found in flowers utilized in the field. 2. Bees became >90% flower-constant to either of two flower types (distinguished by color) when rewarded with 1.0 μl 50% sucrose at each visit to flowers of one color, while the others remained unrewarded. 3. Flower-constancy to ‘blue’ was achieved within 50 flower visits, but equal flower constancy to ‘white’ was achieved only after 250 flower visits. 4. While being trained to white flowers the bees increased their percent correct (rewarding) flower choice over consecutive foraging trips during the day, but decreased their performance overnight. 5. Bees trained to blue did not switch to white flowers even when the white were subsequently rewarded with more food than the blue. However, bees trained to white utilized blue flowers. 6. Most bees simultaneously presented with white flowers having six times greater syrup rewards than blue visited both in approximately equal proportions independent of flower density, while some individuals visited primarily blue flowers. 7. The laboratory experiments suggest that bumblebees, once conditioned, are relatively ‘constant’ foragers despite changes in resource availability.

The Use of Neutron Activation Analysis in Pollination Ecology

Neutron activation analysis in pollination ecology was examined with particular regard to external application of indicator elements. Movement of elements between flowers can be detected after external application either to the anthers or, in members of the Asteraceae, to the entire head. This technique is potentially useful in studying pollen flow within and between populations and in detecting flower constancy of pollinators. This technique is advantageous when compared with the use of radioactive tracers because potential health and environmental hazards inherent in the field use of unstable isotopes are eliminated.

POLLEN EXCHANGE AS A FUNCTION OF SPECIES PROXIMITY IN PHLOX.

The isolation of plant species has beei and remains a subject of active interes and research. There have been numerous studies of reproductive and environmenta factors which limit or preclude hybridi zation, and sufficient evidence is at hanc to warrant some generalizations about th4 isolating mechanisms of taxa sharing cer tain habits or habitats (cf. Grant, 1971) One factor which has a profound effect or the isolation of species, but which has re ceived little attention, is the proximity o heterospecific populations. Although refer ence is made to the fact that isolation iL less when populations are confluent rathei than discontinuous, or closely adjacenl rather than far apart, the writer knows oi no analysis relating, in quantitative terms the isolation of species in nature to the spatial association of their populations. The degree to which entomophilous spe cies are isolated by a given distance is E function of the pollen dispersal agent. Some groups of pollinators routinely fly long dis tances between consecutively visited plant. (Janzen, 1971), whereas others typicall3 traverse short distances on single flights (Levin and Kerster, 1968; Free, 1970) Accordingly, the degree of isolation experi enced by two species separated by a giver distance may be quite different from thal achieved by two other species separated b3 the same distance. Like flower constancy foraging flight distance is a behavioral at tribute of pollinators, and should be in cluded with flower constancy as an effector of ethological isolation. The present investigation was undertaker to determine the relationship between th( proximity of Phlox divaricata L. and P bifida L. and the level of pollen exchange These species are especially common in Brown County, Indiana, which was chosen as the study area. Phlox bifida generally is restricted to sites with open canopies prevailing in forest borders, and the more open oak-hickory forests of upper slopes and ridges. On the other hand, P. divaricata occurs under a spectrum of forest canopy conditions and in moister habitats, including wooded depressions, moist slopes, stream flats, and water drainage courses. In spite of these differences, the phloxes often grow within a few meters of each other, and occasionally form contiguous or confluent populations especially where the canopy has been thinned. The species flower for about six weeks and have overlapping flowering periods, P. bifida reaching its flowering peak in late April and P. divaricata in early May. Both have lavender corollas and are suited for lepidopteran pollination. The nectaries are located at the base of a salverform corolla whose tube varies from 9 to 14 mm in length in P. bifida and 11 to 16 mm in P. divaricata. Pollination of both species is accomplished by species of Papilio, Danaus, Colias, Polites, and other lepidopterans (Grant and Grant, 1965; Levin, unpubl.). Although there are no mechanical barriers to interspecific pollination, the flowers of the species are distinctive in two respects which relate to this discussion. First, the corolla lobes of P. bifida are strongly bifid, whereas those of P. divaricata are notched (Fig. 1). This feature may be an important recognition signal for pollinators. The ability of the aforementioned lepidopterans to discriminate between different corolla outlines in Phlox has been established (Levin, 1969). The species also differ in

THE EXPLOITATION OF POLLINATORS BY SPECIES AND HYBRIDS OF PHLOX.

Interspecific hybridization is perpetrated by animal pollen vectors in a multitude of plant genera where the floral mechanisms of the participating species can accommodate the same vector. The frequency and implications of hybridization has stimulated investigations on pollinator flower constancy, the basis of ethological and mechanical isolation, and the role of floral isolation in speciation. Many of the problems and contributions of pollination ecology as related to the evolutionary process have been elaborated upon by Grant (1949, 1963), Grant and Grant (1965), Baker (1963), Baker and Hurd (1968), and Faegri and van der Pijl (1966). In spite of the interest in pollination ecology during the past several years, certain aspects of the field remain unattended. When comparing species, or species and their hybrids in terms of their fitness components, little consideration has been given to the mating success of these entities except in relation to the breeding system. Mating success in animal-pollinated outbreeding plants is a function of pollinator service. Foremost among the questions to be answered are the following: Are related species and their hybrids equally efficient in exploiting the pollinator fauna? If there are differences among species and hybrids, to what factors can they be attributed? Answers to these questions were sought from Phlox drummondii Hook. var. drummondii and P. cuspidata Scheele. These annuals are indigenous to central Texas where they are abundant and occasionally in contact. Contact affords an opportunity for hybridization as the species have synchronous flowering periods, similar floral mechanisms, and weak genetic barriers to crossing (Erbe and Turner, 1962). Hybridization has been reported at several localities (Erbe and Turner, 1962; Levin, 1967). Correlative analysis of pollen fertility, chromosome pairing, and flavonoid profiles suggested that the hybrid swarms contaihed little other than the parental species and F1 hybrids (Levin, 1967). The two species are distinctive in reproductive and vegetative morphology, the former offering the most definitive taxonomic characters (Table 1). Their corollas are salverform, similar in conformation and adapted for lepidopteran pollination. They differ in size and pigmentation. Phlox drummondii displays relatively large red corollas; it is the only red-flowered Phlox. In contrast, the coroilas of P. cuspidata are diminutive, being the smallest in the genus, and are pink. Hybrids have corollas which are magenta in color and intermediate to their parents in dimensions. Phlox drummondii is an obligate outbreeder and P. cuspidata a facultative inbreeder (Erbe and Turner, 1962; Levin, unpubl.). The floral morphology of the species and hybrids shows that there are no mechanical barriers to pollen exchange between the entities. The presence of hybrids, and the presence of parental pollen on hybrid stigmas (as will be shown below) attests to the ability of pollinators to effectively transport pollen among the phloxes. It is likely that the phloxes are drawing upon the same pollinator pool. This is not to imply that a pollinator might not prefer one Phlox to another. Unfortunately, observations within hybridizing populations served only to reinforce the observation that P. drummondii is frequently pollinated by Papilio sp. (Whitehouse, 1939). Grant and Grant (1965) have observed the hawk

The Flower Constancy of Bumblebees

The Flower Constancy of Bumblebees

HYBRIDIZATION, HOMOGAMY, AND SYMPATRIC SPECIATION

Mayr (1947) has presented a strong case against the hypothesis of sympatric speciation in the course of supporting the universal hypothesis of geographic (or at least microgeographic) speciation. In the summary (p. 286) of that paper he made the following statement: is unproven and unlikely that reproductive isolation can develop between contiguous populations. Later, Grant (1949), in a discussion of pollination systems as isolating mechanisms, presented a model for sympatric speciation in angiosperms dependent on the known flower constancy of bees. This model indicated the means by which an important mutation in flower color or form might become established within a population, thus resulting in time in a new and well isolated species to which internal isolating mechanisms are unnecessary. In passing, the latter author suggested that hybridization might also provide an example of sympatric speciation. It is the purpose of the present paper to further develop this last hypothesis on the basis of a realistic model suggested by recent studies of hybridization and floral isolation in a group of Penstemon species. It is not the purpose of this paper to refute the general conclusions reached by Mayr (I.c.) on the importance of geographic speciation, but merely to indicate that sympatric speciation may be less unlikely than previously considered. The word, species, is here used in its biological sense.