How Flies Are Flirting on the Fly

Background  Flies have some of the most elaborate visual systems in the Insecta, often featuring large, sexually dimorphic eyes with specialized “bright zones” that may have a functional role during mate-seeking behavior. The fast visual system of flies is considered to be an adaptation in support of their advanced flight abilities. Here, we show that the immense processing speed of the flies’ photoreceptors plays a crucial role in mate recognition. Results  Video-recording wing movements of abdomen-mounted common green bottle flies, Lucilia sericata, under direct light at 15,000 frames per second revealed that wing movements produce a single, reflected light flash per wing beat. Such light flashes were not evident when we video-recorded wing movements under diffuse light. Males of L. sericata are strongly attracted to wing flash frequencies of 178 Hz, which are characteristic of free-flying young females (prospective mates), significantly more than to 212, 235, or 266 Hz, characteristic of young males, old females, and old males, respectively. In the absence of phenotypic traits of female flies, and when given a choice between light emitting diodes that emitted either constant light or light pulsed at a frequency of 110, 178, 250, or 290 Hz, males show a strong preference for the 178-Hz pulsed light, which most closely approximates the wing beat frequency of prospective mates. Conclusions  We describe a previously unrecognized visual mate recognition system in L. sericata. The system depends upon the sex- and age-specific frequencies of light flashes reflecting off moving wings, and the ability of male flies to distinguish between the frequency of light flashes produced by rival males and prospective mates. Our findings imply that insect photoreceptors with fast processing speed may not only support agile flight with advanced maneuverability but may also play a supreme role in mate recognition. The low mating propensity of L. sericata males on cloudy days, when light flashes from the wings of flying females are absent, seems to indicate that these flies synchronize sexual communication with environmental conditions that optimize the conspicuousness of their communication signals, as predicted by sensory drive theory

Foraging and Communication Ecology of the Common Green Bottle Fly, Lucilia sericata (Meigen) (Diptera: Calliphoridae)

In accordance with their physiological state, adults of Lucilia sericata must locate mates, food and oviposition resources. I investigated the cues they exploit to obtain these resources. As females require a protein-rich diet and frequently visit pollen/protein-rich flowers, I studied the effects of generic floral scent and colour cues, and of Oxeye daisy-specific cues, on foraging decisions by flies. I show that (1) flies in the presence of generic floral scent respond more strongly to a uniformly yellow cue than to most other uniform colour cues (green, white, black, blue, red); (2) daisy scent enhances the attractiveness of a yellow cue; and (3) pollen with adequate moisture content facilitates oocyte maturation of flies. Males respond to long-range mate recognition cues. I show that (1) wing movement of females is a visual mate recognition cue, (2) wings are thin-film reflectors that produce light flashes during movement, and (3) light flashes are absent under diffuse light. Wings also produce stable structural colours, UV- and polarized-light reflections, but these optic effects per se are insufficiently gender-specific and thus do not appear to serve as mate recognition cues. Instead, the frequency of light flashes reflected off moving female wings may allow males to recognize prospective mates.Foraging decisions by females change in accordance with their physiological state. Protein-hungry females respond to feces and carrion, whereas protein-fed gravid females with mature oocytes respond only to fresh carrion. Gravid females discriminate against aging carrion (which is detrimental to their offspring) as soon as it produces appreciable amounts of indole, which is an abundant feces semiochemical and apparently serves as an indicator of a food rather than an oviposition resource. Gravid females locate recently deceased vertebrates as oviposition sites in response to dimethyl trisulfide and carrion-type colour cues (dark red, black), indicating that a bimodal cue complex signifies suitable oviposition sites.Oviposition site-seeking females do not respond to an oviposition pheromone. Instead, they coopt semiochemicals associated with feeding flies as resource indicators. This conclusion is based on data that gravid or non-gravid females ovipositing and/or feeding on oviposition resources enhance their attractiveness to gravid and non-gravid females

Nature versus nurture: Structural equation modeling indicates that parental care does not mitigate consequences of poor environmental conditions in Eastern Bluebirds (Sialia sialis)

How organisms respond to variation in environmental conditions and whether behavioral responses can mitigate negative consequences on growth, condition, and other fitness measures are critical to our ability to conserve populations in changing environments. Offspring development is affected by environmental conditions and parental care behavior. When adverse environmental conditions are present, parents may alter behaviors to mitigate the impacts of poor environmental conditions on offspring. We determined whether parental behavior (provisioning rates, attentiveness, and nest temperature) varied in relation to environmental conditions (e.g., food availability and ectoparasites) and whether parental behavior mitigated negative consequences of the environment on their offspring in Eastern Bluebirds (Sialia sialis). We found that offspring on territories with lower food availability had higher hematocrit, and when bird blow flies (Protocalliphora spp.) were present, growth rates were reduced. Parents increased provisioning and nest attendance in response to increased food availability but did not alter behavior in response to parasitism by blow flies. While parents altered behavior in response to resource availability, parents were unable to override the direct effects of negative environmental conditions on offspring growth and hematocrit. Our work highlights the importance of the environment on offspring development and suggests that parents may not be able to sufficiently alter behavior to ameliorate challenging environmental conditions

Effects of Floral Scent, Color and Pollen on Foraging Decisions and Oocyte Development of Common Green Bottle Flies

<div><p>The common green bottle fly <i>Lucilia sericata</i> (Meigen) and other filth flies frequently visit pollen-rich composite flowers such as the Oxeye daisy, <i>Leucanthemum vulgare</i> Lam. In laboratory experiments with <i>L</i>. <i>sericata</i>, we investigated the effect of generic floral scent and color cues, and of Oxeye daisy-specific cues, on foraging decisions by recently eclosed flies. We also tested the effect of a floral pollen diet with 0–35% moisture content on the ability of females to mature their oocytes. Our data indicate that (1) young flies in the presence of generic floral scent respond more strongly to a uniformly yellow cue than to any other uniform color cue (green, white, black, blue, red) except for ultraviolet (UV); (2) the floral scent of Oxeye daisies enhances the attractiveness of a yellow cue; and (3) moisture-rich pollen provides nutrients that facilitate ovary maturation of flies. With evidence that <i>L</i>. <i>sericata</i> exploits floral cues during foraging, and that pollen can be an alternate protein source to animal feces and carrion, Pollen apparently plays a major role in the foraging ecology of <i>L</i>. <i>sericata</i> and possibly other filth flies. These flies, in turn, may play a significant role as pollinators, as supported by a recently published study.</p></div

Graphical illustrations of experimental designs.

<p>(A, B) Design of two-choice laboratory experiments (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g001" target="_blank">Fig 1</a>) with inverted bottle traps (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#sec002" target="_blank">methods</a> for detail), consisting of a green trap base and a funnel-like trap top covered with paper of a particular test color, and baited with honey (A), or with three freshly-cut Oxeye daisy inflorescences on 1-cm long stems or three corresponding stems (C) as the olfactory cues; (D) representative (<i>n</i> = 5 each) spectral reflectance profiles from (<b>I</b>) Oxeye daisy inflorescences [floral disc (yellow), petal tip (grey), petal base (black)], (<b>II</b>) yellow, white, red, blue, green, or black construction papers tested in color choice experiments, and (<b>III</b>) UV-reflective paper; the color of each reflectance curve in <b>I-III</b> corresponds to the color of the material measured; in <b>I</b> and <b>III</b>, black curves represent UV reflections.</p

Details on the diet of experimental flies, olfactory and visual cues tested, numbers of flies tested per replicate, the duration of replicates, and numbers of replicates per experiment.

<p>¹Oxeye daisy inflorescence on 1-cm long stem; ²1-cm long stem without inflorescence; ³honey bee-collected pollen; ⁴% moisture content.</p

Effect of diet on the ability of <i>Lucilia sericata</i> females to mature their oocytes.

<p>To assess the effect of diet [sugar (negative control; Exp.12), Oxeye daisy pollen from fresh inflorescences (Exp. 13), honey bee-collected pollen with 0%, ≤20% or ≤35% moisture content (Exps. 14–16), and milk powder (positive control, Exp. 17) (<i>n</i> = 9 each; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g001" target="_blank">Fig 1</a>) on the ability of <i>L</i>. <i>sericata</i> females to mature their oocytes, we scored 10 phases of ovary development according to Adams & Reinecke (47) and grouped phases into three main stages: (I) phases 0–3: oocytes with dividing cells; (II) phases 4–9: oocytes with yolk sac, and (III) phase 10: mature and chorionated eggs. Diet had a significant effect on ovarian maturation (<i>F</i>_{2, 147} = 153.62, <i>p</i> < 0.0001). Within each of stage I, II and III, bars with different letters indicate significant differences in the mean proportions of fly oocytes at that stage based on diet (Tukey’s HSD: <i>p</i> <0.05).</p

Interactions between visual and olfactory cues on attraction of <i>Lucilia sericata</i>.

<p>Mean number of females and males captured in experiments 8–11 (<i>n</i> = 10 each; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g001" target="_blank">Fig 1</a>) in paired bottle traps (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g002" target="_blank">Fig 2A and 2B</a>) baited with the following cue combinations: Exp. 8: Yellow with Oxeye daisy inflorescence (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g002" target="_blank">Fig 2C</a>) <i>versus</i> Black with Oxeye daisy inflorescence; Exp. 9: Yellow alone <i>versus</i> Black alone; Exp. 10): Yellow alone <i>versus</i> Black with Oxeye daisy inflorescence; and (Exp. 13): Yellow with Oxeye daisy inflorescence <i>versus</i> Black alone. Replicates of all experiments were run in parallel but those for experiment 9 (which tested the effect of color only) were run in a separate room. Flies significantly preferred traps with yellow funnel tops (<i>χ</i>^<i>2</i>_<i>1</i> (1, <i>N</i> = 40) <i>= 22</i>.<i>83</i>, <i>p</i> < 0.001) and traps baited with Oxeye daisy inflorescence odor (<i>χ</i>^<i>2</i>_<i>1</i> (1, <i>N</i> = 40) = 22.8, <i>p</i> = 0.003) but there was no interaction between color and odor (<i>χ</i>^<i>2</i>_<i>1</i> (1, <i>N</i> = 40) = 0.018, <i>p =</i> 0.894).</p

Effect of floral odor on attraction of <i>Lucilia sericata</i>.

<p>Mean proportion of 36-h-old, females and males captured in experiment 7 (<i>n</i> = 15; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g001" target="_blank">Fig 1</a>) in two inverted bottle traps (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g002" target="_blank">Fig 2A and 2B</a>) with yellow trap funnels that were baited with either three freshly-cut Oxeye daisy inflorescences on 1-cm long stems or three corresponding stems (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145055#pone.0145055.g002" target="_blank">Fig 2C</a>). The number in parenthesis indicates the total number of flies captured, and the asterisk (*) indicates a significant preference for the test stimulus (Z = -2.95, df = 1, <i>p</i> = 0.0028).</p