Floral Form Research Articles

Flowers and Enemies: Predation by Nectar-Thieving Ants in Relation to Variation in Floral Form of an Alpine Wildflower, Polemonium viscosum

Flowers of the alpine skypilot, Polemonium viscosum, are attacked by nectar-thieving ants of Formica neorufibarbus gelida. Plants in this species display continuous variation in floral form from long, broadly-flared flowers to short, narrow flowers. This study addresses three aspects of the potential for ants to exert selection on floral traits in P. viscosum: the effect of ant visitation on seed production, the relationship between ant visitation patterns and variation in floral form among co-occurring between ant visitation patterns and variation in floral form among co-occurring individuals, and the behavioral mechanisms underlying nonrandom flower choice by ants. Ants visiting flowers of P. viscosum interfere with seed production by dislodging the style from the ovary. In 1982 and 1997 plants protected from ant visits set significantly more seeds per flower than open controls. Plants with broadly-flated flowers incurred significantly higher rates of ant damage than individuals with narrower flowers in 1995. Similarly, in 1997, damage increased significantly with plant score on a principal component positively correlated to corolla flare and length. Ant abundance declines with elevation above timberline, and, in 1997, damage associated with corolla flare and length was significantly greater for plants in the timberline (krummholz) habitat than for plants higher on the alpine tundra. Laboratory choice trials showed that ants prefer flowers with long broadly-flared corollas over flowers with short narrow corollas. Ant preference may reflect differences in floral reward: broadly-flared flowers contain more nectar sugar than narrow ones in P. viscosum. Additionally energetic costs associated with nectar collection depend in part on flower form. In choice experiments, handling time, or the time required for an ant to move from the corolla opening to the nectary decreased significantly with corolla flare and was also less variable for ants choosing broadly-flared flowers than those choosing narrow ones. Ants have the potential to exert selection on flower form in P. viscosum, as their activity negatively affects the female component of reproductive fitness and is nonrandomly associated with different floral phenotypes. In this system, enemies show similar flower choice patterns to bumblebee pollinators, and their behavior may help maintain heritable variation in flower form within populations of P. viscosum.

Breeding system in the cleistogamous species <i>Centaurea melitensis</i> (Asteraceae)

Cleistogamy involves structural, developmental, and functional differences between the open (chasmogamous) and closed (cleistogamous) floral forms produced by a species. Functional differences relate to the breeding system: progeny is obtained partly by obligate selfing, cleistogamous flowers and, at least potentially, by outcrossing, chasmogamous flowers. This study addresses theoretical predictions about the breeding system in Centaurea melitensis L. Comparative analysis of cleistogamous and chasmogamous flower heads produced by this species was based on studies of the morphological features of floral capitula, fruit production, pollen/ovule ratio, pollinators, stigma receptivity, and pollen-tube growth in the absence of pollinators. As expected, cleistogamous heads displayed characteristics typical of an obligate selfing flower. However, two apparently contradictory trends were discerned in chasmogamous heads: (i) a very high selfing rate and own-pollen germination at a very early stage in floral ontog...

FLORAL SYMMETRY AND ITS ROLE IN PLANT-POLLINATOR SYSTEMS: Terminology, Distribution, and Hypotheses

▪ Abstract Floral symmetry has figured prominently in the study of both pollination biology and animal behavior. However, a confusion of terminology and the diffuse nature of the literature has limited our understanding of the role that this basic characteristic of flower form has played in plant-pollinator interactions. Here, we first contribute a classification scheme for floral symmetry that we hope will resolve some of the confusion resulting from the inconsistent application of terms. Next, we present a short review of the distribution of floral forms in angiosperm families. Finally, we provide a list of hypotheses and, when available, supporting evidence for the causes of the evolution of floral symmetry.

The relationship between floral nectar composition and visitors in Lycium (Solanaceae) from Argentina and Chile: what does it reflect?

We evaluated the relationship between floral nectar composition, flower visitors, and floral form for Lycium species from Argentina and Chile. Our goal was to determine whether nectar chemical composition is correlated with floral form and pollinators or whether it is a conservative character. We analysed 54 populations from 14 species and six varieties. This sample is representative of the floral variation in the genus, and the taxa come from its main area of diversification. The nectar of all the taxa contains both amino acids and sugars. The mean nectar sugar concentration is high: 48.4% ± 19.8. There is a remarkable constancy in the nectar sugar ratio among the taxa: 90% of them present a hexose dominant one, i.e. nectar has <10% sucrose and >90% fructose and glucose. Visitors include Hymenoptera, Diptera, and Lepidoptera; the most common family of each order is Anthophoridae, Syrphidae, and Nymphalidae, respectively. Only one species is visited by hummingbirds. Most of the plant taxa (68.4%) are visited by members of two or three insect orders. No patterns have been detected between the kinds of visitors and the flower morphology. The homogeneity of nectar sugar composition in contrast to the variety of visitors and flower forms indicates that there is no correlation between the nectar sugar ratio and floral form or pollinators. This suggests that nectar ratio is a conservative character in Lycium .

Phylogeny of Cobaea (Polemoniaceae) Based on Sequence Data from the ITS Region of Nuclear Ribosomal DNA

The phylogenetic relationships of 16 of the 18 species of the neotropical genus Cobaea (Pole- moniaceae) were investigated using sequences of the ITS1 and ITS2 regions of nuclear ribosomal DNA. Can- tua and Bonplandia were used as outgroups. Six most-parsimonious trees (length = 558 steps, CI excluding uninformative characters = 0.688, RI = 0.875) were produced, and support for most branches, based on boot- strap and decay analyses, was quite strong. Insertion/deletion events provide further support for some clades. There are two unresolved nodes in the strict consensus tree, and one of the unresolved nodes is among samples of one species. The ITS phylogeny suggests that two of the three sections of Cobaea are not mono- phyletic; the third is monotypic. The three characters used to distinguish the sections, corolla lobe shape, inflo- rescence position, and stamen length, were of questionable utility in sectional circumscription. The genus Cobaea consists of 18 species occurring mainly in montane cloud forests from central Peru to northern Mexico, and is one of the few tropical genera of the Polemoniaceae. The genus is well- defined and easily distinguished from other genera in the Polemoniaceae by a number of synapomor- phies: a scandent habit; pinnately compound leaves with the terminal leaflet modified into a tendril; nearly free calyx segments; septicidally dehiscent capsules; and very large (102-223 ,um), pantopo- rate, reticulate pollen (Prather, in press). Cobaea is especially notable because of the remarkable diver- sity in floral form among its species (Fig. 1), even when compared with similar sized or larger genera

Ontogenetic Contingency and Floral Morphology: The Effects of Architecture and Resource Limitation

Floral form and function commonly vary quantitatively and qualitatively within inflorescences. Overall floral size, the sizes of individual floral organs, and the frequency of successful fruit and/or seed maturation may decline distally within inflorescences. These frequently observed patterns of variation have been attributed to competition for limited resources among developing flowers and fruits. The variation, however, can also be due to architecture, that is, to sources of variation inherent in plant axes. Floral morphology may change with position on an inflorescence axis, even in the absence of resource competition. Experimental analyses of Solanum hirtum and Arabidopsis thaliana identify the separate effects of architectural and resource limitation on floral development and morphology. The effects of architecture may mimic, mask, or lead to misinterpretation of the effects of resource competition on floral form. Floral morphology and function may be characterized as ontogenetically contingent: the morphology and fate of a developing flower depend on the events that have preceded it during the ontogeny of the organism and on where it occurs within the architecture of the individual. Careful consideration of the role of ontogenetic contingency in diverse taxa will be required to fully understand patterns of variation in floral morphology and function within individuals and may ultimately enhance our understanding of morphological diversification among taxa.

Developmental Homeostasis and Floral Form: Evolutionary Consequences and Genetic Basis

Plant biologists have largely ignored the role of developmental homeostasis in the evolution of floral traits. In this brief review, we discuss the relationship between floral form and developmental homeostasis, emphasizing that developmental homeostasis, as any other character, may respond to natural selection. We discuss the implications of developmental homeostasis being a selectively labile trait for the evolution of floral characters. A trait's ability to respond to selection is in part determined by its genetic basis. Therefore, we also discuss evidence for the genetic basis of developmental homeostasis and how it influences the evolution of developmental homeostasis and ultimately floral diversity. We conclude with a series of suggestions for future research, calling for a synthetic approach utilizing ecological, morphological, quantitative genetic, and molecular methodologies.

RECONSTRUCTION OF THE EVOLUTION OF REPRODUCTIVE CHARACTERS IN PONTEDERIACEAE USING PHYLOGENETIC EVIDENCE FROM CHLOROPLAST DNA RESTRICTION-SITE VARIATION.

We reconstructed the phylogenetic history of Pontederiaceae using chloroplast DNA restriction-site variation from approximately two-thirds of the species in this family of aquatic monocotyledons. The molecular phylogeny was used to evaluate hypotheses concerning the evolution of reproductive characters associated with the breeding system. The family has four main genera, two of which (Eichhornia and Pontederia) have tristylous, predominantly outcrossing species, while two (Monochoria and Heteranthera) have enantiostylous taxa. Self-incompatibility is restricted to some but not all tristylous species. In Eichhornia and Pontederia, predominantly selfing species with small monomorphic flowers (homostyly) have been hypothesized to result from the multiple breakdown of tristyly. Restriction-site variation provided a well supported phylogeny of ingroup taxa, enabling the mapping of reproductive characters onto trees. Two contrasting optimization schemes were assessed, differing in the relative weights assigned to shifts in character states. The reconstructed sequence of floral character-state change was used to assess competing hypotheses concerning the origin and breakdown of tristyly, and the relationships between tristylous and enantiostylous syndromes. Our results indicate that the class of optimization scheme used was the most critical factor in reconstructing character evolution. Despite some topological uncertainties and difficulty in reconstructing the primitive floral form in the family, several broad conclusions were possible when an unordered, unequally-weighted optimization scheme was used: (1) tristyly originated either once or twice, while the occurrence of enantiostyly in Monochoria and Heteranthera was always found to have independent origins; (2) tristyly has repeatedly broken down leading to selfing, homostylous taxa; and (3) self-incompatibility probably arose after the origin of floral trimorphism, a sequence of events that conflicts with some evolutionary models.

Mechanisms of Hummingbird‐Mediated Selection for Flower width in Ipomopsis Aggregata

The form of angiosperm flowers is thought to have evolved in part via selection that excludes ineffective pollinators and increases the efficiency of pollen transfer by effective ones. In previous studies with the montane plant Ipomopsis aggregata, we documented pollinator—mediated selection on several aspects of floral form, including flower width. This character varies continuously within natural populations of I. aggregata, and individuals with wider flowers export more pollen per flower to surrounding plants. We previously showed that this component of phenotypic selection is due primarily to the pervisit effectiveness of hummingbirds, the most important pollinator in our study populations. Here we investigate mechanisms of differential visit effectiveness in greater detail. First, counts of pollen in unvisited flowers showed that pollen production itself increases with width. In aviary experiments, hummingbirds also removed a greater proportion of available pollen as width increased. We next videotaped visits to flowers that varied in width either naturally, or by experimental treatment, and found that hummingbirds inserted their bills more deeply into wider flowers. Finally, we directly manipulated how deeply birds could insert their bills, and found that more pollen was removed after deep insertion. Thus, several mechanisms appear to underlie selection on corolla width via visit effectiveness in pollen export. One involves a phenotypic correlation with pollen production; this underscores the value of experiments for untangling indirect from direct selection. Another mechanism involves direct selection due to the depth of insertion of a hummingbird's bill; this is rare evidence for one form of selection involving the “fit” between pollinator and flower.

Self-compatibility in distylousHedyotis salzmannii (Rubiaceae)

Hedyotis salzmannii (Rubiaceae) is distylous. Experimental pollination revealed that both morphs are self-compatible. However, the thrum morph proved to be more self-compatible. Hand cross-pollination between different plants of the same floral form produced less seed-sets per pollination than hand cross-pollination between pin and thrum or thrum and pin pollination. Two species ofHymenoptera, oneApidae and oneHalictidae, and two species ofDiptera (Syrphidae) were observed as pollinators.

Pollen‐Foraging Dynamics of Subalpine Bumblebees (Bombus Latr.)

Abstract A 23‐year study on Mount Rainier of nectar‐foraging hummingbirds and pollen‐foraging bumblebees (Bom‐bus Latr.) indicated a constant relative frequency of Bombus species in the area and a wide occurrence of insect species on flowers plus a wide range of flower species pollinated by a single insect. Early‐blooming plants had a high queen/worker pollinator ratio, while workers predominated on later‐blooming plants. No altitudinal difference in distribution of Bombus species occurred. Analysis of 955 corbicular pollen loads from 1158 bumblebees collected yielded 49.5% monolecty for queens and 34.5% for workers with a wider range for queens than for workers. Colors of corollas photographed in visible and ultraviolet light corresponded to the visual spectra of animal pollinators. In the stable plant‐pollinator community investigated, pollinating insect activity appears phenologically controlled by floral anthesis and behaviorally related to floral form and function. Bumblebee tongue length, however. Is not a valid determinant for foraging niche separation except in Castilleja with a deep corolla tube accommodating long tongues of hummingbirds and bumblebees. It is concluded that in a biotic community well‐coordinated with the physical environment, limited flower constancy of pollen‐foraging pollinators appears to contribute a necessary degree of adaptive versatility through sharing of insect and floral resources. Flower constancy is primarily a function of the circumstance in which a pollinator operates and not simply a characteristic of the pollinator itself.

Morphological and growth rate differences among outcrossing and self‐pollinating races of Arenaria uniflora (Caryophyllaceae)

AbstractPopulations of Arenaria uniflora exhibit intraspecific variation in floral size and degree of protandry in association with the evolution of self‐pollination. Heterochrony, or a simple change in the absolute timing or rate of developmental events, is proposed as the evolutionary mechanism underlying the origin of the small, self‐pollinating flowers from their large, outcrossing progenitors. Inflorescence growth in two autogamous populations and their related outcrossing progenitors was studied to provide the temporal data necessary for testing the hypothesis of heterochrony. All four races showed significant variation in the growth and mature length of inflorescence organs. Inflorescences of selfing races were smaller, and had slower relative growth rates and a two‐fold increase in the plastochron relative to outcrossing populations. The large‐flowered races were both significantly protandrous. A more detailed growth analysis of flower development in two races indicated that the selfing flowers develop at a slower rate and for a longer duration relative to outcrossing flowers. The implications of these temporal changes in floral ontogeny for the heterochronic origin of self‐pollinating floral forms are considered.

Pollination in an understorey vine, Smilax rotundifolia, a threatened plant of the Carolinian forests in Canada

Round-leaved greenbrier, Smilax rotundifolia L. (Liliaceae), is an insect-pollinated, dioecious, understorey vine. Its pollen is linked by viscin threads, effectively preventing wind dispersal. In most sites populations are not sexually reproductive, being unisexual, but do not spread vegetatively. Where both sexes occur, fruits and seeds are produced naturally. Artificial cross-pollinations can enhance the level of fruit and seed set. Understanding the biology of this threatened species is important for habitat management and conservation. Key words: dioecy, greenbrier, viscin, floral form, conservation, pollination.

Floral development in Arabidopsis thaliana: a comparison of the wild type and the homeotic pistillata mutant

Homeosis is sometimes defined as the replacement of one member of a meristic series by another member normally formed in a different position. The pistillata floral mutant of Arabidopsis thaliana (Brassicaceae) has petals replaced by sepal-like organs ("petals"), is male sterile, and has abnormal gynoecial development. We compared the ontogeny of wild type and pistillata flowers to determine the developmental basis for their divergent final forms. Normal sepal development in wild type pistillata flowers is indistinguishable in terms of initiation events, anatomical and morphological development, and allometric growth. Wild type petals and pistillata "petals" are initially ontogenetically similar in these same respects. The first observable difference between the two floral forms is abnormal patterns of cell division in pistillata at stamen inception. Tissues in the normal position of the androecium appear congenitally fused to the gynoecium to various extents and differentiate gynoecial cell fates. Form divergence between wild type petals and pistillata "petals" becomes evident when these organs reach 90 μm in length, after androecial developmental divergence has occurred. Pistillata does not have petals replaced by sepals; pistillata "petals" are intermediate in form between wild type sepals and petals because of the developmental switching of petal primordia into the ontogenetic pattern characteristic of wild type sepals after petal primordia are initiated.

MEASURING POLLINATOR-MEDIATED SELECTION ON MORPHOMETRIC FLORAL TRAITS: BUMBLEBEES AND THE ALPINE SKY PILOT, POLEMONIUM VISCOSUM.

Sweet-flowered plants of Polemonium viscosum in Colorado are visited by a fly-dominated pollinator fauna at timberline (krummholz), but almost exclusively by bumblebees in higher-elevation tundra habitats. Significant increases in flower size and height are associated with increasing elevation along this habitat gradient. This paper presents the results of an experiment designed to test whether bumblebees exert sufficient selection on morphometric floral phenotypes to account for the clinal shifts seen in natural populations. Two populations of sweet-flowered plants of krummholz origin were established: one randomly pollinated, the other solely bumblebee-pollinated. I tested the effects of two independent axes of floral variation, obtained by principal-components analysis, on mean seed set per flower of plants in each population. PC1, with strong correlations to corolla diameter, corolla length, and stem height, explained a significant amount of variance in seed set for bumblebee-pollinated plants but had no bearing on that of randomly pollinated plants. PC2, with strong correlation to flower number, did not influence seed set in either population. Bumblebee behavior was correlated with variation in PC1 scores of the selected population, yielding positive directional selection on morphometric floral traits associated with PC1. Selection coefficients for PC1, corolla length, corolla diameter, and inflorescence height were estimated, respectively, as 0.11, 0.09, 0.07, and 0.06 (P < 0.025 in all cases). These results support the hypothesis that pollinator-mediated selection can bring about changes in floral form, and can explain shifts in floral morphology of P. viscosum along natural habitat gradients.

Breeding System in Ficus carica, the Common Fig. I. Floral Diversity

Coevolution in Ficus carica (Moraceae) and the fig wasp (Blastophaga psenes, Agaonidae, Chalcidoidea) has resulted in a complex breeding system involving two tree morphs (Caprifig and Edible fig), three floral forms (long-styled female, short-styled female, and male flowers) and the insect pollinator. The two female floral forms have been reported to differ only in style length and stigma shape. In the present study, we demonstrate that the two female flowers differ from inception—short-styled flower primordia are smaller and exhibit significantly greater individual variation than do those of the long-styled flower, and the relative growth rate of each flower type differs. Mature forms exhibit disparity in style length, in stigma characteristics, and in degree of fusion of stylar lobes. Female flowers of both tree morphs are unisexual from inception. Male flowers of the Caprifig tree morph are initiated as hermaphrodites and gynoecium abortion occurs before megaspore mother cell stage. A single inflorescence therefore expresses two pathways to unisexuality. Hermaphrodite flower primordia were repeatedly found in the supposedly unisexual female syconium of the Edible fig tree morph. Based on its developmental morphology, Ficus carica appears to be of gynomonoecious ancestry.

BREEDING SYSTEM IN FICUS CARICA, THE COMMON FIG. I. FLORAL DIVERSITY

Coevolution in Ficus carica (Moraceae) and the fig wasp (Blastophaga psenes, Agaonidae, Chalcidoidea) has resulted in a complex breeding system involving two tree morphs (Caprifig and Edible fig), three floral forms (long‐styled female, short‐styled female, and male flowers) and the insect pollinator. The two female floral forms have been reported to differ only in style length and stigma shape. In the present study, we demonstrate that the two female flowers differ from inception—short‐styled flower primordia are smaller and exhibit significantly greater individual variation than do those of the long‐styled flower, and the relative growth rate of each flower type differs. Mature forms exhibit disparity in style length, in stigma characteristics, and in degree of fusion of stylar lobes. Female flowers of both tree morphs are unisexual from inception. Male flowers of the Caprifig tree morph are initiated as hermaphrodites and gynoecium abortion occurs before megaspore mother cell stage. A single inflorescence therefore expresses two pathways to unisexuality. Hermaphrodite flower primordia were repeatedly found in the supposedly unisexual female syconium of the Edible fig tree morph. Based on its developmental morphology, Ficus carica appears to be of gynomonoecious ancestry.

A Preliminary Study of the Pollination Ecology of Pedicularis (Scrophulariaceae) in Japan

Abstract An introductory study of the pollination ecology of six Japanese species of Pedicularis conducted in 1982 and 1983 indicated a close parallel between characteristics of floral mechanisms in Japan and those previously investigated in North America. Floral color, floral form, total dissolved solids in floral nectar, and polinator behavior on flowers of Japanese species are similar to those of North American species. Blooming phenology of Japanese species also corresponds to the North American sequence of long‐tongued, nectar‐foraging queen bumblebees (Bombus Latr.) pollinating nectariferous, earlier‐blooming species nototribically and short‐tongued, pollen‐foraging workers pollinating nectarless, rostrate flowers of later‐blooming ones sternotribically. Electrofocus analysis of peroxidase systems in two Japanese species indicated considerable intrapopulational heterozygosity. Nectar component analysis of two transboreal species indicated intraspecific differences in kinds of sugars between widely disjunct Japanese and North American populations. A tentative conclusion is that the Japanese and North American Pedicularis floras have evolved in a parallel manner from Himalayan migrants, while their transboreal elements are in process of vicariant diversification.

Potential roles of scaling and post‐anthesis developmental changes in the evolution of floral forms of Eucnide (Loasaceae)

Six of the fourteen species of Eucnide (Loasaceae) are investigated to understand the potential roles of size scaling and post‐anthesis ontogenetic changes in the evolution of the floral diversity that characterizes the genus. Principal components analysis of quantitative aspects of mature flowers showed that most of the measured floral features strongly covary and that size was responsible for most of the quantitative variation among the investigated species. Size scaling trends were further investigated by using bivariate comparisons. Scaling trends are strongest among species of sect. Eucnide. Stamen and style length, the most strongly scaled features, have a nearly isometric relationship (slope = 1) in the evolution of the genus. Given this strict scaling which would probably promote self‐pollination, it appears that cross‐pollination in the genus is most likely to be associated with the evolution of large flowers, compounded by protogyny and differential elongation of stamens and style during post‐anthesis ontogeny. Common changes during post‐anthesis development include failure of the corolla to spread and variations in the relative elongation patterns of the corolla, stamens, and style.

Caste‐specific patterns of flower visitation in bumble bees (Bombus kirbyellus) collecting nectar from Polemonium viscosum

ABSTRACT. Foraging routes of worker and queen bumble bees (Bombus kirbyellus Curtis) collecting nectar from flowers of the alpine sky pilot, Polemonium viscosum Nutt., were followed and the corolla tube length, corolla diameter, floral scent, and number of flowers on plants visited or bypassed by bees were monitored. Additionally, the number and proportion of flowers visited per inflorescence and distance flown from each to the next were recorded. Queens and workers differed significantly in choice of flowers. However, intra‐inflorescence visitation rates and departure distances were similar between castes. Castes differed in the extent to which visitation reflected patch quality versus individual floral traits. Both queens and workers failed to visit skunky‐flowered plants more often than they failed to visit sweet‐flowered ones, and preferred large over small inflorescences. However, queens visited large‐flowered plants more often than small‐flowered ones, while workers preferred flowers with shorter corolla tubes, regardless of their diameter. Although a number of studies have documented caste specialization on alternate species of host plants, ours is one of the first to show that morphological preferences promote comparable foraging differences between castes on monospecific plant resources. Queens, once on a plant, responded to floral traits by probing more flowers on large inflorescences, as well as on those with broader floral form. Workers did not alter intra‐inflorescence visitation rate in response to floral traits. For workers, no significant relationship was demonstrated between the likelihood of passing by a plant and the number of flowers probed on the previous inflorescence visited. Thus, workers appeared to accept or reject each plant of P. viscosum independently. However, queens passed by fewer plants when leaving rich inflorescences than poor ones. These results suggest that workers use only individual plant acceptability in choosing which plants to visit, whereas queens base plant choice on patch and individual attributes. Such differences between castes in foraging rules when exploiting the same floral resource have received little attention, and provide insights into the heterogeneity of harvestable reward distributions from the perspective of the forager population.