Pollinator Preference Research Articles

Competition for bumblebee visitation between Melampyrum pratense and Viscaria vulgaris with healthy and Ustilago-infected flowers.

We studied bumblebee foraging on two sympatrically and simultaneously flowering species, Melampyrum pratense (Scrophulariaceae) and Viscaria vulgaris (Caryophyllaceae) during the flowering season of Viscaria in south-west Sweden. We distinguished between healthy and Ustilago-infected Viscaria plants. Both species shared the main insect visitor, queens of Bombus hortorum, which collected nectar from both species but pollen from Melampyrum only. The pattern of visitation changed over the season: bumblebees preferred Viscaria early on, but changed to Melampyrum later in the season, probably because of the higher sugar content of Melampyrum nectar and the possibility of collecting both nectar and pollen from the same flower. Pollen collecting is probably of increasing importance since the need of pollen for the developing larvae will increase with time. Flowers of Viscaria received fewer visits in plots with other species than in pure Viscaria plots during one year and received more visits early than late in the season during both years. Melampyrum flowers received similar amounts of visits in mixed and pure environments. They also received more visits early than late, although this was probably a result of pollinator satiation since Melampyrum became very abundant with time. Ustilago-infected plants received far fewer visits but because of its long flowering time the proportion of open flowers receiving visits was still high. Viscaria flowers received significantly more visits than flowers of other species when bumblebees made heterospecific flower visits from Ustilago-infected plants; thus Ustilago spores were probably effectively dispersed from infected to healthy plants by the pollinators. The mechanism behind competition for pollination in this system was competition through pollinator preference, since the visitation rate to Viscaria actually decreased, but also competition through improper pollen transfer (grains of both species were found on the bodies of bumblebees) since the incidence of switching between the two species increased, probably resulting in an increased misplacement of conspecific pollen grains with time.

Physiological Basis and Ecological Consequences of Sugar Preferences in Cedar Waxwings

-In paired preference tests Cedar Waxwings (Bombycilla cedrorum) preferred glucose, fructose, and a mixture of glucose and fructose over sucrose. Preferences for simple sugars were ranked as: glucose = glucose + fructose > fructose > sucrose. To be absorbed by the brush border membrane, sucrose is hydrolyzed into its monosaccharide components, glucose and fructose. Because Cedar Waxwings preferred glucose and fructose over sucrose, we predicted that they would be sucrase deficient. We tested this by measuring the efficiency with which Cedar Waxwings absorbed glucose, fructose, and sucrose in vivo, and by directly assaying for sucrase in preparations of intestinal mucosa. Absorption efficiencies measured using a double isotope method falsified our prediction. Cedar Waxwings were able to absorb sucrose (absorption efficiency = 61% ? 1.2), but absorbed glucose and fructose more efficiently (absorption efficiencies = 92%? 1.5 and 88%?3.5, respectively). The presence of sucrase activity in Cedar Waxwings was confirmed in preparations of intestinal mucosa. Using a radioactively labeled inert marker, we found very short mean residence times of food particles in the gut of Cedar Waxwings (ca. 41 min). Because sucrose has to be hydrolyzed before it can be absorbed, the efficiency with which it is utilized may be hindered by the extremely fast passage rates in Cedar Waxwings. We suggest that the preference of Cedar Waxwings for monosaccharides over sucrose is due to the relative inefficiency of sucrose absorption. However, absorption efficiencies cannot explain the strong preference of glucose over fructose. In consequence, neither the caloric value of the sugars nor the absorption efficiency was adequate to explain the sugar preferences exhibited by Cedar Waxwings. We conclude that the preferences for simple sugars appear to be determined by the complex interaction between digestive constraints, postingestional effects, and taste. Received 19 January 1988, accepted 10 August 1988. THE disaccharide sucrose and the monosaccharide hexoses, fructose and glucose, are the most common simple sugars in fruit pulp and nectar (Chan and Kwok 1975; Baker and Baker 1983, 1986; Reid and Freeman MS). Hummingbird-pollinated plants produce nectars with a high proportion of sucrose whereas passerinepollinated plants produce nectars with a low proportion of sucrose and high proportion of hexoses (Cruden and Toledo 1977; Baker and Baker 1982, 1983). Small bird-dispersed fruits, which are typically consumed by passerines, contain mainly hexoses, whereas cultivated fruits used for human consumption tend to have high sucrose contents (Baker and Baker 1986, pers. comm.). These differences in sugar composition remain largely unexplained. It has been postulated that chemical characteristics of nectar and fruit pulp evolved in response to the 3Present address: Department of Zoology, University of Florida, Gainesville, Florida 32611 USA. preferences of pollinators and seed dispersers (Baker and Hurd 1968, Howell 1979, Levey 1987). With few exceptions (Hainsworth and Wolf 1976, Stiles 1976), the sugar preferences of birds that feed on nectar and fruit are unknown. Glucose, fructose, and sucrose have different modes of intestinal transport, and produce different metabolic effects after ingestion and absorption (Sestoft 1983). Even though they are similar chemically and in caloric value, these sweet substances may not be biologically equivalent. The European Starling (Sturnus vulgaris) rejects sucrose solutions but readily accepts solutions of fructose and glucose (Schuler, 1983). Sucrose aversion in the Starling is associated with a deficiency of the intestinal enzyme sucrase which hydrolyzes sucrose into fructose and glucose (Martinez del Rio et al. 1988). Animals that lack sucrase cannot digest and absorb sucrose. Consequently, the presence of undigested sucrose in the intestine of these animals can cause severe osmotic diarrhea. In this way, 64 The Auk 106: 64-71. January 1989 This content downloaded from 207.46.13.20 on Tue, 27 Dec 2016 17:57:48 UTC All use subject to http://about.jstor.org/terms January 1989] Sugar Preferences in Cedar Waxwings 65 the absence of intestinal sucrase can be associated with aversion for sucrose (Sunshine and Kretchmer 1964). We studied the sugar preferences of the Cedar Waxwing (Bombycilla cedrorum), one of the most heavily frugivorous birds in temperate North America (Martin et al. 1951), and analyzed the influence of taste and postingestional factors on these preferences. Because most birddispersed fruits in temperate North America are hexose-dominated (I. Baker and H. G. Baker in litt.), we predicted that Cedar Waxwings would prefer glucose and fructose over sucrose. We also hypothesized that this preference would be a result of sucrase deficiency. We examined these hypotheses by simple choice tests; by estimating the efficiency with which the birds digested and absorbed sucrose, glucose, and fructose in vivo; and by assaying for sucrase in preparations of intestinal mucosa.

FLORAL NECTAR SUGAR COMPOSITION AND POLLINATOR TYPE AMONG NEW WORLD GENERA IN TRIBE ANTIRRHINEAE (SCROPHULARIACEAE)

The floral nectar sugar compositions of 20 New World species from 10 genera and of five interspecific hybrids in tribe Antirrhineae have been analyzed using high‐performance liquid chromatography. Species are pollinated by short‐tongued bees, long‐tongued bees, and hummingbirds. Ornithophily represents the derived condition in the tribe and has arisen independently in subtribes Maurandyinae and Gambeliinae. All nectars analyzed are sucrose‐dominant or ‐rich, except for the hexose‐rich nectar of Mohavea breviflora. Despite the predominance of sucrose, floral nectar sugars from species pollinated by different pollen vectors have characteristic constituents. Nectar sugars from flowers visited by hummingbirds average 76.2% sucrose and have compositions remarkably similar to hummingbird nectars analyzed in previous studies of unrelated species. Long‐tongued bee nectars average 87% sucrose and differ from shorttongued bee nectars which have the lowest mean sucrose percentage (40.2%). The association of sugar constituent types and principal pollinators is concordant with previous data and supports hypotheses concerning pollinator preferences and the adaptive significance of certain nectar sugar compositions. Within this adaptive framework, phylogenetic constraint is also operative and may explain the predominance of sucrose in nectar sugars, similarities in sugar composition among hummingbird nectars in subtribes Maurandyinae and Gambeliinae, and the similarity of nectar from Galvezia leucantha (long‐tongued bee‐pollinated) to hummingbird‐pollinated species also in subtribe Gambeliinae.

The effect of nectar guides on pollinator preference: experimental studies with a montane herb.

Rare "albino" morphs of the montane larkspur Delphinium nelsonii differ from common blue-flowered morphs in overall flower color, and in the strength of a contrasting color pattern at the center of the flower that presumably guides pollinators to concealed nectar. Previous studies showed that bumblebees and hummingbirds discriminate against albinos when presented with mixtures of the 2 morphs, and that it takes these pollinators longer to fly between successive flowers on albino than on blue-flowered inflorescences. To explore the link between these observations, we measured pollinator preferences and flower-to-flower flight times ("handling times") before and after painting flowers in 2 alternative ways that enhanced albino nectar guides. In all of 16 experimental replicates discrimination against albinos was reduced or eliminated after painting, and albino handling times declined toward values for blue-flowered inflorescences. This consistent result indicates that an inferior nectar guide increases the energetic cost of foraging at albinos. Increased cost in turn explains discrimination, under the reasonable assumption that hummingbirds and bumblebees are sensitive to foraging economics.

The Mechanism of Competition for Pollination between Two Forest Herbs

The primary mechanism of competition for pollination between the two forest herbs Stellaria pubera and Claytonia virginica in piedmont North Carolina is interspecific pollen movement. The most common visitor, the bee fly Bombylius major, forages indiscriminately among flowers of the two species. In only one of five experiments did the presence of C. virginica reduce the pollinator visit rate per S. pubera flower, and in other experiments addition of C. virginica enhanced visit rate. Thus these plant species exhibit little or no competition through pollinator preference. In some natural populations, however, visits to S. pubera are frequently immediately preceded by a visit to C. virginica, and a flower receives less conspecific pollen and produces fewer seeds following such an interspecific visit than if the visitor has arrived directly from a conspecific flower. Interspecific pollen movement is responsible for most, if not all, of the reductions in seed set of S. pubera due to pollinator sharing. Although insects deposit a substantial amount of S. pubera pollen on stigmas of C. virginica, little C. virginica pollen is found on S. pubera stigmas. Moreover, application of foreign pollen to the stigma does not influence seed production of S. pubera. The effect of interspecific pollen movement is due to loss of conspecific pollen, not stigmatic interference.

COMPARATIVE REPRODUCTIVE BIOLOGY OF HERMAPHRODITIC AND MALE‐STERILE IRIS DOUGLASIANA HERB. (IRIDACEAE)

A comparative study of the reproductive biology of male‐sterile and hermaphroditic plants in a gynodioecious population of Iris douglasiana Herb. (Iridaceae) was conducted at the University of California's Marine Laboratory at Bodega Bay, California, between 1976–1979. Each year of the study, there were 11.1% male‐sterile plants in the population, some of which began blooming at the same time as the earliest blooming hermaphrodites. Male‐sterile flowers made up between 7–21% of the flowers produced during the male‐sterile flowering period.Male‐sterile flowers had smaller sepals and petals than hermaphrodites, there were fewer of them per square meter, and they had fewer pollinated stigmas than did hermaphroditic flowers. In a test to determine pollinator preference, intact hermaphroditic flowers tended to have more pollinated stigmas than did hermaphrodites with their stamens removed or those flowers with shortened sepals made to resemble the smaller male‐sterile flowers. Floral phenology and nectar‐flow patterns were similar in both types of flowers as were the kinds of amino acids and sugar rewards in the nectar. Male‐sterile flowers, however, produced much less nectar per flower. There were no significant differences in the number of ovules per flower or the number of seeds produced per capsule between the two flower types, but the loss of seeds through larval predation was much greater in capsules from hermaphroditic flowers. Early flowering and setting of seed by plants with male‐sterile flowers could give them a reproductive advantage over plants with hermaphroditic flowers which experience higher levels of larval predation later in the growing season.

Pollination biology of heteromorphic populations of Oxalis alpina (Rose) (Oxalidaceae) in south-eastern Arizona

In south-eastern Arizona, heterostylous (often trimorphic) populations of Oxalis alpina (Rose) Knuth are visited most commonly by females of the solitary bee Heterosarus bakeri Cockerell. Bees collect pollen from flowers and are presumed to be the major pollinators of O. alpina in this region. Analysis of pollen loads from the corbiculae of H. bakeri suggests that individual bees may specialize temporally on different floral forms. However, the apparent preferential collection of pollen probably results from spatial segregation of morphs and the localized foraging behaviour of bees rather than preference on the part of individual bees for particular stylar forms. As a group, bees appear to visit floral morphs of O. alpina indiscriminately, even though individual bees may have a preponderance of pollen from one morph type. Despite spatial segregation leading to pollinator flights between members of the same incompatibility group, capsule and seed production in populations of O. alpina is high for all forms. Loss of the mid form in some populations cannot be attributed to pollinator preferences for individual style morphs.

Pollination biology of heteromorphic populations of Oxalis alpina (Rose) (Oxalidaceae) in south-eastern Arizona

In south-eastern Arizona, heterostylous (often trimorphic) populations of Oxalis alpina (Rose) Knuth are visited most commonly by females of the solitary bee Heterosarus bakeri Cockerell. Bees collect pollen from flowers and are presumed to be the major pollinators of O. alpina in this region. Analysis of pollen loads from the corbiculae of H. bakeri suggests that individual bees may specialize temporally on different floral forms. However, the apparent preferential collection of pollen probably results from spatial segregation of morphs and the localized foraging behaviour of bees rather than preference on the part of individual bees for particular stylar forms. As a group, bees appear to visit floral morphs of O. alpina indiscriminately, even though individual bees may have a preponderance of pollen from one morph type. Despite spatial segregation leading to pollinator flights between members of the same incompatibility group, capsule and seed production in populations of O. alpina is high for all forms. Loss of the mid form in some populations cannot be attributed to pollinator preferences for individual style morphs.

Competition for Pollinators between Simultaneously Flowering Species

Species with similar floral structures and with similar flowering periods and time of pollen and nectar presentation may compete for the service of the same pollinators. The outcome of interspecific competition was analyzed with a simple two-species model. The reproductive success of a species depends on its relative frequency. The minority species will be at a reproductive handicap because it suffers a larger percentage of heterospecific pollinations. The reproductive handicap of the minority species leads to a smaller standing crop in the next generation, which in turn enhances the minority disadvantage. This should lead to rapid exclusion of the minority species from the immediate flora. An increase in pollinator constancy to a given plant species retards the elimination of the rarer species. Pollinator preference for a given plant species may enhance or retard this progression depending on whether the minority species is preferred, since preference alters the effective frequencies of the two species. The minority disadvantage is reduced if the competing species have different habitat requirements or if they form large patches of regular size.

QUANTITATIVE STUDIES ON MATING SYSTEMS. III. METHODS FOR THE ESTIMATION OF MALE GAMETOPHYTIC SELECTIVE VALUES AND DIFFERENTIAL OUTCROSSING RATES.

Evidence was presented in the first paper of this series (Harding and Tucker, 19!64) that outcrossing rates of different genotypes are subject to genetic control. Significantly different outcrossing rates, were observed for genotypes from several populations of Phaseolus lunatus L. In Population 2 mean outcrossing rates for genotypes varied from as low as 3.2% to as high as 24.2%. In addition to the genotypic differences in propensity for cross-fertilization there was considerable environmental variation. In the estimation of outcrossing rates the assumption was made that different genotypes contributed equally to the male gametophytic population, i.e., there was no male gametophytic selection. Thus, male gametophytic selection is defined as the change in gene frequency which occurs between the parental sporophytic population and the population of gametes at fertilization. Any selective advantage indicated by the male gametophytic selective value may result from sporophytic pollen fecundity or pollinator attraction as well as from gametophytic fitness. One of the most common assumptions in population genetics is the equation q = R + 1/2 H where the gene frequency of reproduction is calculated from the frequencies of recessive (R) and heterozygous (H) diploid parents. But many studies indicate that gamete frequencies cannot be accurately estimated from sporophytic frequencies. Differences in pollen production have been reported in Vicia faba (Drayner, 1959) and Oenothera (Hoff, 1962). Pollinator preference has been reported in Medicago sativa where bumble bees were shown to prefer genotypes with higher sugar levels in the nectar (Pedersen and Bohart, 1953). Variation in fragrance (e.g. Jodon, 1944), as well as variation in flower color, can result in pollinator preference. Gametophytic competition has been reported in Zeac mays (Jones, 1920), Primula sinensis (Beale, 1939), Sorghum bicolor (Riccelli-Mattei, 1968), Gossypium hirsutum (Afzal and Khan, 1950) and Cheiranthus cheiri (Bateman, 1956). Vasek (1964) has presented a method which circumvents the assumption of equal gene frequency in the sporophytic and male gametophytic generations. By progeny testing heterozygotes as well as recessives, he estimated simultaneously the outcrossing rate and the gene frequency among male gametes of Clarkia exilis. However, the outcrossing rates of the recessive and the heterozygote were assumed to be equal. The analytical problem is that two progeny tests, yielding one degree of freedom each, provide only two degrees of freedom. Therefore, the choice is between assuming no male gametophytic selection and estimating an outcrossing rate for each genotype, or assuming no differential outcrossing and estimating one outcrossing parameter and the gene frequency among male gametes. The purpose of the present investigation is to develop statistical models and experimental methods which make possible the simultaneous estimation of differential outcrossing rates and male gametophytic selective values. These methods will be applied to data from three populations of Phaseolus lunatus and one population of Zea mays.