Lawrence D. Harder

The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination

The prospect that a global pollination crisis currently threatens agricultural productivity has drawn intense recent interest among scientists, politicians, and the general public. To date, evidence for a global crisis has been drawn from regional or local declines in pollinators themselves or insufficient pollination for particular crops. In contrast, our analysis of Food and Agriculture Organization (FAO) data reveals that the global population of managed honey-bee hives has increased approximately 45% during the last half century and suggests that economic globalization, rather than biological factors, drives both the dynamics of the global managed honey-bee population and increasing demands for agricultural pollination services. Nevertheless, available data also reveal a much more rapid (>300%) increase in the fraction of agriculture that depends on animal pollination during the last half century, which may be stressing global pollination capacity. Although the primary cause of the accelerating increase of the pollinator dependence of commercial agriculture seems to be economic and political and not biological, the rapid expansion of cultivation of many pollinator-dependent crops has the potential to trigger future pollination problems for both these crops and native species in neighboring areas. Such environmental costs merit consideration during the development of agriculture and conservation policies.

EVOLUTIONARY OPTIONS FOR MAXIMIZING POLLEN DISPERSAL OF ANIMAL-POLLINATED PLANTS

On the average, nectar-collecting bumble bees deposited 0.6% of the pollen removed from the flowers of Erythronium grandiflorum (Liliaceae) onto the stigmas of subsequently visited flowers. Because the proportion deposited declined as the amount removed increased, an individual plant would maximize its total pollen dispersal by relying on many pollen-removing visits while limiting the pollen removed by each pollinator. This restriction of pollen removal could be achieved by a plant presenting only a small portion of its pollen at one time (packaging) and/or by limiting the amount of presented pollen that a pollinator removes during a single visit (dispensing). The restriction of pollen removal required to maximize the expected total deposition on stigmas depends on the number of pollinator visits a plant receives, variation in the frequency of visits, and the pattern of pollen removal during a series of visits. Many aspects of floral biology contribute to a plants ability to restrict pollen removal, including inflorescence size, flower morphology, anthesis patterns, nectar production, and dichogamy. Selection increasing paternal fitness of animal-pollinated plants could therefore elicit one of a variety of evolutionary responses; the specific response will depend on characteristics of both the plant and the pollinator.

Pollen Dispersal and Mating Patterns in Animal-Pollinated Plants

Immobility complicates mating by angiosperms because the transfer of male gametes between individuals requires pollen vectors. Although abiotic and biotic vectors can transport pollen considerable distances (Bateman, 1941a; Squillace, 1967; Kohn and Casper, 1992; Godt and Hamrick, 1993), the resulting pattern of pollen dispersal does not intrinsically maximize the number and quality of matings. Consequently, floral evolution generally involves two classes of adaptations that promote mating success. The morphological traits that characterize floral design and display modify the actions of pollen vectors so as to enhance fertility (see below). In contrast, physiological traits mitigate unsatisfactory pollen dispersal by rejecting unsuitable male gametophytes (Jones, 1928; de Nettancourt, 1977; Marshall and Ellstrand, 1986; Seavey and Bawa, 1986; Barrett, 1988; Snow and Spira, 1991; Walsh and Charlesworth, 1992) or zygotes (Stephenson, 1981; Casper, 1988; Becerra and Lloyd, 1992; Montalvo, 1992). As a result of postpollination processes, the realized mating pattern does not simply mirror the pattern of pollination (e.g., Campbell, 1991; also see Waser and Price, 1993). However, these processes can only filter the incipient mating pattern established during pollination, so that pollination fundamentally determines the maximum frequency and diversity of mating opportunities. Consequently, the role of pollination in governing the scope for mating inextricably links the evolution of pollination and mating systems.

Ecology and evolution of plant mating

Plants exhibit complex mating patterns because of their immobility, hermaphroditism and reliance on vectors for pollen transfer. Research on plant mating attempts to determine who mates with whom in plant populations and how and why mating patterns become evolutionarily modified. Most theoretical models of mating-system evolution have focused on the fitness consequences of selling and outcrossing, stimulating considerable empirical work on the ecology and genetics of inbreeding depression. Less attention has been given to how the mechanics of pollen dispersal influence the transmission of self and outcross gametes. Recent work on the relation between pollen dispersal and mating suggests that many features of floral design traditionally interpreted as anti-selling mechanisms may function to reduce the mating costs associated with large floral displays.

Evolution and Development of Inflorescence Architectures

To understand the constraints on biological diversity, we analyzed how selection and development interact to control the evolution of inflorescences, the branching structures that bear flowers. We show that a single developmental model accounts for the restricted range of inflorescence types observed in nature and that this model is supported by molecular genetic studies. The model predicts associations between inflorescence architecture, climate, and life history, which we validated empirically. Paths, or evolutionary wormholes, link different architectures in a multidimensional fitness space, but the rate of evolution along these paths is constrained by genetic and environmental factors, which explains why some evolutionary transitions are rare between closely related plant taxa.

Global growth and stability of agricultural yield decrease with pollinator dependence

Human welfare depends on the amount and stability of agricultural production, as determined by crop yield and cultivated area. Yield increases asymptotically with the resources provided by farmers’ inputs and environmentally sensitive ecosystem services. Declining yield growth with increased inputs prompts conversion of more land to cultivation, but at the risk of eroding ecosystem services. To explore the interdependence of agricultural production and its stability on ecosystem services, we present and test a general graphical model, based on Jensens inequality, of yield–resource relations and consider implications for land conversion. For the case of animal pollination as a resource influencing crop yield, this model predicts that incomplete and variable pollen delivery reduces yield mean and stability (inverse of variability) more for crops with greater dependence on pollinators. Data collected by the Food and Agriculture Organization of the United Nations during 1961–2008 support these predictions. Specifically, crops with greater pollinator dependence had lower mean and stability in relative yield and yield growth, despite global yield increases for most crops. Lower yield growth was compensated by increased land cultivation to enhance production of pollinator-dependent crops. Area stability also decreased with pollinator dependence, as it correlated positively with yield stability among crops. These results reveal that pollen limitation hinders yield growth of pollinator-dependent crops, decreasing temporal stability of global agricultural production, while promoting compensatory land conversion to agriculture. Although we examined crop pollination, our model applies to other ecosystem services for which the benefits to human welfare decelerate as the maximum is approached.

Pollen Removal by Bumble Bees and Its Implications for Pollen Dispersal

Realized paternity should decelerate with increased allocation of resources to male function for hermaphroditic plants. If these diminishing returns result from the pollination process, total pollen dispersal would be maximized by restricting removal by individual pollinators and using the services of all available pollinators. The optimal restriction of removal by individual pollinators should depend on pollinator availability, the deceleration in dispersal, and the pattern of pollen removal during succeeding visits to a flower. In this study I measured pollen removal from six species (Aconitum delphinifolium, Aralia hispida, Lupinus sericeus, Mertensia paniculata, Pedicularis bracteosa, and P. con- torta) to determine the extent to which removal is restricted and to quantify the removal pattern during repeated visits. For all species except Lupinus, I collected the pollen left in a flower after 1-4 visits by freely foraging bumble bees (Bombus). Pollen removal was estimated by subtracting the pollen remaining in a visited flower from total pollen pro- duction by an adjacent unvisited anther or flower on the same plant. The pollen-dispensing mechanism of Lupinus allowed me to measure pollen removal directly. Much interspecific variation in pollen removal depends on the likelihood of contact between pollinator and anthers. Bumble bees removed a median of 50-80% of the available pollen during first visits to species with exposed anthers. In contrast, only 19% was removed during the initial manipulation of lupine flowers, which present pollen indirectly. Within species, removal increased with visit duration; it did not additionally depend on the number of visits involved. Removal typically changed in direct proportion to differences in pollen availability. Pollen size also affected removal, but it is unclear that this effect is direct. In most cases, removal was unaffected by the species or caste of bee involved. Succeeding visits to a flower removed either a fixed or, more commonly, a declining proportion of the pollen remaining in a flower. A model of pollen dispersal indicates that a constant removal proportion would maximize dispersal when the number of visits a flower receives varies little. In contrast, diminishing proportional removal would allow plants to maintain pollen dispersal when the frequency of pollinator visits is uncertain.

Morphology as a Predictor of Flower Choice by Bumble Bees

This paper examines whether the use of 14 plant species as nectar sources by eight species of bumble bees relates systematically to differences in bee morphology. I predicted that a particular bee should have fed from a given plant species if the bee was physically more similar to the other bees visiting that plant species than to bees on any other species. Glossa (=tongue) length, body mass, and wing length all influence a bumble bees foraging ability and its choice of flowers and were therefore included in the analysis. Morphological differences between bees were associated with use of different plant species; however, the role of bee morphology in flower choice was most evident when preferred plant species bloomed abundantly. The interaction between morphology and flower choice was also influenced by plant species richness, season, the plant species visited, and the species of bee; but was not affected by the time of day that the bee was foraging, overall bee density, or the bees caste. Bee species with long glossae had access to nectar in a greater variety of flowers than those with short glossae, and they tended to feed from a larger number of plant species. Also, their use of a particular species was less predictable. Discrimination between bees using different plant species depended on joint consideration of several morphological characters: no character alone accurately separated the bees.

A Clarification of Pollen Discounting and Its Joint Effects with Inbreeding Depression on Mating System Evolution

Given the predominance of outcrossing by angiosperms, large costs must often overwhelm the genetic benefit of selfing derived from contributing two haploid genomes to each off‐spring rather than one. In addition to the well‐studied genetic cost of inbreeding depression, selfing imposes a mating cost whenever self‐pollination reduces opportunities for pollen export. Because self‐pollination is a heterogeneous process, pollen discounting and its evolutionary consequences vary with pollination conditions. In this article we model self‐pollination as comprising discounting and nondiscounting components, and we consider the consequences of this heterogeneity for outcross siring success. Aided by this depiction of pollination, we then compare previous theoretical representations of pollen discounting and consider their relative virtues. Finally, we consider conditions that would allow a population to be invaded by a variant with different pollination characteristics. This analysis exposes the pollination conditions implicit in standard results of mating system theory. It also identifies associations between four possible changes in pollination expected in different reproductive environments, including the incidence of positive or negative correlations between self‐pollination and pollen export. These results emphasize the benefits of expanding the theory of plant reproduction to recognize explicitly when and how pollination mechanisms affect mating outcomes.

Behavioral responses by bumble bees to variation in pollen availability

SummaryPollen-collecting bumble bees (Bombus spp.) detect differences between individual flowers in pollen availability and alter their behavior to capitalize on rewarding flowers. Specific responses by bees to increased pollen availability included: longer visits to flowers; visits to more flowers within an inflorescence, including an increased frequency of revisits; an increased likelihood of grooming while the bee flow between flowers within the inflorescence; and more protracted inter-flower flights, probably because of longer grooming bouts. The particular suite of responses that a bee adopted depended on the pollen-dispensing mechanism of the plant species involved. Bees buzzed previously-unvisited Dode-catheon flowers longer than empty flowers. In contrast, pollen availability did not significantly affect the duration of visits to Lupinus flowers, which control the amount of pollen that can be removed during a single visit. Simulation results indicate that the observed movement patterns of bumble bees on Lupinus inflorescences would return the most pollen per unit of expended energy. The increased foraging efficiency resulting from facultative responses by bees to variation in pollen availability, especially changes in the frequency and intensity of grooming, could correspondingly decrease pollen dispersal between plants.