James D. Thomson

Flower Constancy, Insect Psychology, and Plant Evolution

Abstractu2002Individuals of some species of pollinating insects tend to restrict their visits to only a few of the available plant species, in the process bypassing valuable food sources. The question of why this flower constancy exists is a rich and important one with implications for the organization of natural communities of plants, floral evolution, and our understanding of the learning processes involved in finding food. Some scientists have assumed that flower constancy is adaptive per se. Others argued that constancy occurs because memory capacity for floral features in insects is limited, but attempts to identify the limitations often remained rather simplistic. We elucidate now different sensory and motor memories from natural foraging tasks are stored and retrieved, using concepts from modern learning science and visual search, and conclude that flower constancy is likely to have multiple causes. Possible constraints favoring constancy are interference sensitivity of short-term memory, and temporal limitations on retrieving information from long-term memory as rapidly as from short-term memory, but further empirical evidence is needed to substantiate these possibilities. In addition, retrieving memories may be slower and more prone to errors when there are several options than when an insect copes with only a single task. In addition to memory limitations, we also point out alternative explanations for flower constancy. We then consider the way in which floral parameters, such as interplant distances, nectar rewards, flower morphology, and floral color (as seen through bees eyes) affect constancy. Finally, we discuss the implications of pollinator constancy for plant evolution. To date there is no evidence that flowers have diverged to favor constancy, although the appropriate tests may not have yet been conducted. However, there is good evidence against the notion that pollinator constancy is involved in speciation or maintenance of plant species integrity.

Hypotheses for the evolution of dioecy in seed plants

Over the last decade, new hypotheses have been proposed for the evolution of dioecy in plants. Most of the selective mechanisms invoked have been suggested and supported by phylogenetic correlations. Here we review (1) the validity of the correlations (especially in light of recent critiques of the comparative method), and (2) the conformity of the proposed mechanisms to empirical data. None of the hypotheses can be flatly rejected on existing evidence, but the strength of their support varies. Future correlational studies must explicitly consider phylogeny; more importantly, such broad studies should also be supplemented by detailed studies of particular transitions to dioecy (e.g. within genera) - studies of the sort that have clarified analogous issues such as heterostyly.

Sensori-motor learning and its relevance for task specialization in bumble bees

Abstract Individual bees often restrict their visits to only a few species out of the multitude of available plants. This flower constancy is likely caused by limitations of memory for motor patterns, sensory stimuli, or reward levels. Here we test the implications of sensori-motor learning and memory for flower constancy. Artificial “flowers” with two distinct “morphologies” were used, so that in each flower type, a different motor pattern was needed to reach the nectar. As in natural flowers, these morphological types were associated with sensory signals (blue and yellow color stimuli). Bees which learned only a single task were more efficient in several ways than those which had learned two: they made fewer errors, had shorter flower handling times, took shorter times to correct errors, and transitions between flowers were initially more rapid. For bees which had learned two tasks, performance depended strongly on the training schedule: if each task was learned with blocked trials, the memory for the second appeared to interfere with that for the first. Interference affected only the association between flower signal and motor pattern, not the motor pattern itself. This was not the case if bees were trained for both tasks with alternating trials. In that case, bees rapidly learned both tasks, albeit with worse saturation levels than bees which had learned only one. Bees transferred the experience gained on one task to a second task: their initial performance on the second task was better than their initial performance on the first. On the other hand, performance on the second task in the saturation level (in which bees no longer improve their efficiency) was worse than on the first task (negative transfer). In the saturation phase, performance did not directly depend on switch frequency, but on whether the bee had one or two options in memory. Thus, while bees would become proficient at two tasks more quickly if their acquisition phase included switches, such switches had no measurable effect in the saturation phase. The implications of these findings for foraging are discussed using modern learning theory.

Dynamic nectar replenishment in flowers of Penstemon (Scrophulariaceae)

Plants that experience variation in pollinator visitation rates or fluctuations in weather conditions may be expected to have evolved homeostatic mechanisms that regulate their nectar offerings, thereby providing a more constant reward to the pollinators. A limited degree of such nectar homeostasis is reported here for Penstemon. First, nectar removal stimulates replenishment: when nectar was removed hourly for 6 h from P. speciosus, twice as much nectar was secreted cumulatively as when nectar was removed only at the beginning and end of the same 6-h period. Second, replacing artificial nectar in the nectaries of P. speciosus prevents replenishment. Third, the hummingbird-adapted P. barbatus made more nectar before leveling off than the bee-adapted P. strictus. Our work and previous studies with other plants imply mechanisms for dynamic regulation of nectar offerings, at least within broad limits. We speculate about the proximate physiology underlying this behavior and its evolutionary significance.

Comparative studies of pollen and fluorescent dye transport by bumble bees visiting Erythronium grandiflorum

SummaryIn the Colorado Rocky Mountains the glacier lily Erythronium grandiflorum exhibits a striking dimorphism in pollen color and is commonly pollinated by the bumble bee Bombus occidentalis. We induced bees to visit sequences of flowers in a flight cage, and compared dispersal of distinctively-colored pollen and fluorescent pigment (“dye”) that the bee had picked up at a single donor flower. Nonparametric and parametric analyses showed that dispersal properties of pollen and dye differed; consistently less pollen was deposited and it was carried consistently shorter distances than dye. Dye thus does not provide an accurate means of assessing exacty where or how far pollen travels in this plant-pollinator system. On the other hand, both pollen and dye responded similarly to several experimental manipulations of donor and recipient flowers. Hence dye may well be of value for a qualitative investigation of how floral traits influence pollen dispersal.

How Do Flowers Diverge

Darwin’s orchid book (1862) has been cited as his first detailed example of how to study evolution (Ghiselin, 1969; Gould, 1986). The book starts as a presentation of observations showing that the morphology of orchids is, in most cases, wonderfully well suited to having insects remove and deposit pollinia. It ends by tracing how the enormous diversity of orchids can be seen as arising through modifications from ancestral forms. What Darwin did not do was to explain how orchid flowers come to be different. He probably thought that by showing how to study the origin of adaptation he had shown how to study the origin of diversity. Mayr has often pointed out that Darwin failed to see genetic isolation as a precondition for speciation, and thus for diversification (e.g., Mayr, 1959). Likewise, we contend that evolutionists have seldom clearly dissected the alternatives for how divergence occurs, given isolation. We shall concern ourselves here with how different environments—in our case, different pollinator regimes— do or do not provide heterogeneity in selection that might adaptively drive the divergence of flowers.

Sexual reproduction and variation in floral morphology in an ephemeral vernal lily, Eyythronium americanum

SummaryIn a riparian population of Erythronium americanum (Liliaceae) in central New Jersey, experimentally self-pollinated plant produced markedly fewer fruit and fewer seeds per fruit than hand-outcrossed and open pollinated plants, even though differences were not evident between pollen tubes that penetrated stigmas from self or foreign pollen. This weak self-compatibility and a positive relation between the percentage of seeds set by outcrossed plants and the distance between pollen donor and recipient plants indicate that this population could be susceptible to inbreeding depression.Limited resources for seed development apparently constrained maximal seed production, based on low seed set (40.6%) by hand-pollinated plants and positive correlations for these plants between plant size and the number and size of seeds set. In contrast, naturally-pollinated plants set a smaller proportion of their ovules, suggesting that limited pollinator service reduced the quantity of seeds produced in this population. Free-foraging bees usually removed more than half of the available pollen in a single visit, so that individual plants probably have few opportunities to disseminate their pollen.Even though sexually reproductive ramets produce only a single flower per year, less than a third of variation in floral morphology is associated with variation in plant size. Within the flower, the sizes of some closely associated structures, such as the style and ovary, and the anthers and filaments, vary essentially independently of one another. Production of nectar and pollen, the ultimate attractors of pollinating insects, was positively correlated with flower size.

Systematic Increase in Pollen Carryover and Its Consequences for Geitonogamy in Plant Populations

The fraction of pollen that is carried over from one flower to the next as a pollinator visits a sequence of flowers has a strong effect on patterns or mating in plant populations. Although most studies have used simple exponential or geometric functions to represent carryover, pollen deposition patterns often show longer-than-geometrics tails, suggesting a systematic increase in the carryover fraction. We introduce a changing carryover model that allows the carryover fraction to increase or decrease during a sequence of visits (...)

Genetic Mosaics in Strangler Fig Trees: Implications for Tropical Conservation

Single trees of six species of strangler figs (Ficus spp., Moraceae) in Panama were found to be made up of multiple genotypes, presumably formed by the fusion of different individuals. The phenomenon is frequent enough that strangler fig populations will contain considerably more genetic variation than would be expected from the number of trees. How this cryptic variation affects populations depends on the flowering phonology of composite trees. If the genetically different portions of trees flower asynchronously, populations of pollinating wasps may be more resistant to low host population sizes than previously thought. If different portions flower synchronously, attempts to infer mating-system parameters from the parentage of fruit crops will be misleading. The fruiting of figs, which are considered a keystone species in tropical forests, is important for maintaining biodiversity but is also particularly susceptible to failure at small population sizes. It is therefore important to know both the number of trees and the number of genotypes in a population.