Paul A. De Luca

What's the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination

Many plant species have evolved floral characteristics that restrict pollen access. Some of these species are visited by insects, principally bees, which make use of vibrations to extract pollen from anthers. Buzz-pollination, as this phenomenon is generally known, is a widespread method of fertilization for thousands of species in both natural and agricultural systems. Despite its prevalence in pollination systems, the ecological and evolutionary conditions that favour the evolution of buzz-pollination are poorly known. We briefly summarize the biology of buzz-pollination and review recent studies on plant and pollinator characteristics that affect pollen removal. We suggest that buzz-pollination evolves as the result of an escalation in the competition between plants and pollen-consuming floral visitors (including pollen thieves and true pollinators) to control the rate of pollen removal from flowers.

Courtship Communication in Meadow Katydids: Female Preference for Large Male Vibrations

Males of the katydid Conocephalus nigropleurum (Orthoptera: Tettigoniidae) shake their body to produce a substrate-borne vibratory signal in the context of courtship and mate attraction. We measured the physical parameters of this tremulation signal and then tested its effectiveness in eliciting taxis by virgin females. We also investigated the role of these vibrations in the choices made by females of larger males as mates. A search for correlations between male weight and vibratory signal parameters revealed a strong negative relationship to inter-pulse interval (ipi). In two-choice playback experiments females oriented towards tremulation vibration when it was the only vibration stimulus provided. In further playback experiments females also distinguished conspecific tremulation from a control vibration. When offered simultaneous presentations of tremulation signals that differed in ipi, females moved toward the stimulus with the shorter ipi indicative of a larger male. This is the first study to demonstrate that tremulation signalling by male katydids encodes critical information on body size, and that females discriminate among different vibratory signals in favour of those indicating a larger male.

Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers

Buzz-pollination is a plant strategy that promotes gamete transfer by requiring a pollinator, typically bees (Hymenoptera: Apoidea), to vibrate a flower’s anthers in order to extract pollen. Although buzz-pollination is widespread in angiosperms with over 20,000 species using it, little is known about the functional connection between natural variation in buzzing vibrations and the amount of pollen that can be extracted from anthers. We characterized variability in the vibrations produced by Bombus terrestris bumblebees while collecting pollen from Solanum rostratum (Solanaceae), a buzz-pollinated plant. We found substantial variation in several buzzing properties both within and among workers from a single colony. As expected, some of this variation was predicted by the physical attributes of individual bumblebees: heavier workers produced buzzes of greater amplitude. We then constructed artificial “pollination buzzes” that varied in three parameters (peak frequency, peak amplitude, and duration), and stimulated S. rostratum flowers with these synthetic buzzes to quantify the relationship between buzz properties and pollen removal. We found that greater amplitude and longer duration buzzes ejected substantially more pollen, while frequency had no directional effect and only a weak quadratic effect on the amount of pollen removed. These findings suggest that foraging bumblebees may improve pollen collection by increasing the duration or amplitude of their buzzes. Moreover, given that amplitude is positively correlated with mass, preferential foraging by heavier workers is likely to result in the largest pollen yields per bee, and this could have significant consequences for the success of a colony foraging on buzz-pollinated flowers.

The effects of age and relatedness on mating patterns in thornbug treehoppers: inbreeding avoidance or inbreeding tolerance?

The social environment of many species includes synchronous maturation of siblings in family groups, followed by limited dispersal of adults from their natal site. Under these conditions, females may experience high encounter rates with same-age siblings during mate searching, increasing their risk of inbreeding. If inbreeding depression occurs, mating with a sibling is often considered maladaptive; however, in some contexts, the inclusive fitness benefits of inbreeding may outweigh the costs, favoring females that tolerate some level of inbreeding depression. We evaluated mating patterns in the treehopper Umbonia crassicornis, a semelparous species in which females encounter same-age siblings during mate searching. A female U. crassicornis that mates with a brother suffers from inbreeding depression. We used a free-choice mating design that offered females simultaneous mating opportunities with three groups of males: siblings, same-age nonsiblings, and older nonsiblings. These groups represent the types of males typically encountered by females during mate searching. Our goal was to assess whether mating patterns were influenced by inbreeding avoidance by evaluating two hypotheses: kin discrimination and age-based mating (older males cannot be siblings in this species). There was no difference in the proportions of females mating with siblings vs nonsiblings, suggesting an absence of kin discrimination. However, females mated with a greater proportion of older vs younger males. Given that females do not avoid siblings as mates despite a cost to inbreeding, our results provide a possible example of inbreeding tolerance. We also discuss some factors that may have contributed to the mating advantage of older males.

Comparison of pollination and defensive buzzes in bumblebees indicates species-specific and context-dependent vibrations

Bees produce vibrations in many contexts, including for defense and while foraging. Buzz pollination is a unique foraging behavior in which bees vibrate the anthers of flowers to eject pollen which is then collected and used as food. The relationships between buzzing properties and pollen release are well understood, but it is less clear to what extent buzzing vibrations vary among species, even though such information is crucial to understanding the functional relationships between bees and buzz-pollinated plants. Our goals in this study were (1) to examine whether pollination buzzes differ from those produced during defense, (2) to evaluate the similarity of buzzes between different species of bumblebees (Bombus spp.), and (3) to determine if body size affects the expression of buzzing properties. We found that relative peak amplitude, peak frequency, and duration were significantly different between species, but only relative peak amplitude differed between pollination and defensive buzzes. There were significant interactions between species and buzz type for peak frequency and duration, revealing that species differed in their patterns of expression in these buzz properties depending on the context. The only parameter affected by body size was duration, with larger bees producing shorter buzzes. Our findings suggest that although pollination and defensive buzzes differ in some properties, variability in buzz structure also exhibits a marked species-specific component. Species differences in pollination buzzes may have important implications for foraging preferences in bumblebees, especially if bees select flowers best matched to release pollen for their specific buzzing characteristics.

Age-related changes in an insect mating signal have no effect on female choice

The structure of male mating signals is often influenced by age. The causes and consequences of age-based signal variation have been much studied in visual, acoustic, and chemical signaling modalities, but are less explored in species that use vibrational signals for mate attraction. However, the complex structure of many vibrational signals makes them ideal for investigating the relationships between age, signal variation, and patterns of female choice. In the thornbug treehopper, Umbonia crassicornis, females mate more often with older males, but the mechanism underlying older male mating success is unknown. Our goals in this study were to determine whether male vibrational mate advertisement signals vary with age, and, if so, whether females prefer the signals of older males. We recorded male signals over four consecutive weeks beginning at the onset of signaling (a period spanning most of the male reproductive lifespan), and measured ten temporal, spectral, and energy-related parameters from each signal. Several features of male signals changed markedly with age. However, females responded similarly to signals representing males of different ages, indicating that they do not favor older males on the basis of long distance mate advertisement signals. Nonetheless, the results reveal that even in short-lived, determinate growth species age can have surprisingly large effects on mating signals, and we discuss some factors that may contribute to age-related signal variability in U. crassicornis.

Mass Correlates with Increased Mating Success for Older but Not Younger Males in Thornbug Treehoppers

ABSTRACT In many species, male mating success is often influenced by both age and mass. Because mass often increases with age, it can be difficult to disentangle their separate contributions to older male mating success. In species in which age and mass vary independently, it may be possible to determine the influence of mass on male reproductive success. For example, declines in residual reproductive value with age often result in older males increasing their reproductive effort. Mass may have an important influence on this relationship, if having greater mass provides an older male with a larger resource pool to invest in reproductive effort. Here, I evaluated the effect of mass on the reproductive success of males in an insect species in which age and mass are uncorrelated, but mass is highly variable within age classes. Female thornbug treehoppers [Umbonia crassicornis (Amyot and Serville) (Hemiptera: Membracidae)] were given simultaneous choices of younger (22 d) and older (30 d) males under free-choice conditions. Both age and mass contributed to male mating success, but their effects were not additive. Older males had higher mating success than younger males, and among older males, heavier individuals obtained more matings. In contrast, mass did not influence younger male mating success. These findings suggest age and mass interact in their effects, and together provide heavier, older males with a significant mating advantage. Large mass may, therefore, represent an indicator of male courtship performance that is reliably revealed at older ages, which in turn may allow thornbug females to make more effective mating decisions.

Metabolic efficiency in courtship favors males with intermediate mass in the Australian redback spider, Latrodectus hasselti.

Recent studies have suggested that metabolic efficiency may be an important factor in male mating success when females require vigorous and/or prolonged courtship. In capital breeding animals in which a males resource pool is fixed at adulthood the relationship between energy expenditure and courtship performance may be especially important, as males are expected to utilize their finite resources efficiently when soliciting mates. Males may benefit from being efficient, i.e., achieving a sufficiently high level of courtship signaling at low energetic cost, if it enables them to acquire mates before their limited energy reserves are depleted. We investigated the relationship between metabolic efficiency and courtship vibrational signaling in the Australian redback spider, Latrodectus hasselti, a semelparous capital breeder where males invest heavily in courtship to secure a mating. We assessed metabolic rate in a sample of males and measured two courtship components (duty cycle and amplitude) that reflected the energy content of web-borne vibrations. We then calculated two indices of metabolic efficiency for these courtship properties. There was a quadratic relationship between mass and duty cycle such that the highest duty cycle signals were performed by males having intermediate mass. Furthermore, intermediate-mass males were also the most metabolically efficient. Prolonged courtship is necessary in L. hasselti for successful mating, and the results of this study suggest that intermediate-mass males are superior courters because they utilize their finite resource pool most efficiently to produce high energy vibrational signals.

How well do acoustic recordings characterize properties of bee (Anthophila) floral sonication vibrations

ABSTRACT Floral sonication is a behaviour in which certain bees generate substrate-borne vibrations by contracting their flight muscles in order to extract pollen from poricidal anthers. Sonication vibrations, or ‘buzzes’, also contain a corresponding audible sound that results from vibrations radiating from the exoskeleton into the surrounding air. Acoustic recordings are often used as a proxy for analysis of floral sonication vibrations because they are more accessible to recording with conventional equipment such as microphones. However, the extent to which salient parameters of buzzes are reflected in the airborne components has not been experimentally verified. We examined correspondence in three properties (duration, frequency and amplitude) simultaneously recorded with acoustic and vibrational methods from freely foraging bumblebees. Duration and frequency are faithfully quantified from airborne recordings; however, two measures of acoustic amplitude (relative peak amplitude and sound pressure level) are not correlated with vibrational amplitude. Our findings validate acoustic recordings as a method to describe temporal and spectral components of floral sonication vibrations, but we caution against using acoustic measures of amplitude as proxies for the true vibrational power.