Firefly Courtship: Behavioral and Morphological Predictors of Male Mating Success in Photinus greeni

Differences in male mating success can generate selection on male morphological traits and courtship behaviors involved in male–male competition or female mate choice. In Photinus fireflies (Coleoptera: Lampyridae), courtship is based on bioluminescent flash signals produced by both sexes. We conducted field observations of Photinus greeni fireflies engaged in competitive courtships, in which females are able to simultaneously assess several males, to identify male morphological traits and courtship behaviors that might predict male mating success. Male morphological traits did not differ between males that successfully mated compared with unsuccessful males (dialoging males that did not mate). However, courtship behavioral interactions differed: successful males tended to have higher flash pattern rates (number of flash patterns per minute), and their courtship flashes were more likely to be answered by females. We also examined how the risk of predation by Photuris fireflies altered courtship behavior of their Photinus prey. When predatory Photuris fireflies were present, P. greeni females were less likely to mate, and showed decreased flash responses to most males. However, P. greeni males that did successfully mate in spite of Photuris presence were males that maintained high flash pattern rates that elicited female responses. These results suggest that both female mate choice and Photuris predation exert strong selective pressures on the evolution of courtship signals in Photinus fireflies.     

Assessing Condition-dependence of Male Flash Signals in <Emphasis Type="Italic">Photinus</Emphasis> Fireflies

Females often show a preference for exaggerated male sexual traits or courtship behaviors. Such preferences can benefit females if trait expression is correlated with male genetic quality or phenotypic condition. Previous studies of several Photinus fireflies have revealed considerable intraspecific variation in the bioluminescent courtship signals emitted by males, and have also demonstrated that females prefer more conspicuous male signals. Thus, females might gain information about male phenotypic quality if courtship signals reflect male condition. We examined possible condition-dependence of Photinus male courtship signals using two complementary approaches. First we experimentally manipulated male mating status, which is expected to affect male condition by depleting resources required for nuptial gift formation, and looked at how individual male flash signals changed with mating status and over time. We used an additional approach to assess condition-dependence by examining whether a relationship exists between flash signal parameters and measures of male condition and body shape. We found that the pulse rate of P. greeni courtship signals was not altered by male mating status or age, and that the pulse duration of P. ignitus signals was also not affected by male mating status. In P. pyralis fireflies, males showed a non-significant trend toward reduced signal pulse duration with age. When we examined the relationship between male flash signals and condition measures, we found no effect of male condition or body shape on courtship signals in P. greeni or P. ignitus; in P. pyralis, males with wider body shapes produced longer duration flash signals. On the other hand, we found no evidence in P. pyralis that condition predicted flash duration. Taken together, these results indicate that Photinus males’ flash signals do not reflect adult male condition, and suggest that females are unlikely to use courtship signals as an indicator of male phenotypic quality.     

Flash signals, nuptial gifts and female preference in photinus fireflies

The evolution of male courtship signals such as the bioluminescentflashes of fireflies may be shaped, at least in part, by femalepreference for particular characteristics of the male signal.These female preferences for male courtship signals may ariseas a result of the benefits of choosing males with particulartraits. One possible benefit of mate choice occurs if femalescan use male courtship signals as an honest indicator of malenutritional contributions at mating, nuptial gifts. This paperreviews female preference for male flash characteristics inPhotinus fireflies (Coleoptera: Lampyridae), and the potentialfor females to use male flash characteristics to predict nuptialgift quality. In Photinus firefly species with single pulseflashes females preferentially respond to flashes of greaterintensity and duration. Male Photinus provide a nuptial giftto females at mating in the form of a spermatophore and flashduration serves as a good predictor of spermatophore mass formales collected early in the season. However, Photinus firefliesdo not feed as adults, so spermatophore mass decreases withsubsequent matings. In response, nutrient-limited females maystop preferentially responding to longer duration flashes, increasingtheir overall responsiveness later in the mating season as theyforage for spermatophores. Therefore, the evolution of malecourtship signals in Photinus fireflies is the product not onlyof female preference for male flash characteristics, but alsothe costs and benefits of female choice that shape these preferences.     

Flash signal evolution in Photinus fireflies: Character displacement and signal exploitation in a visual communication system

Animal communication is an intriguing topic in evolutionary biology. In this comprehensive study of visual signal evolution, we used a phylogenetic approach to study the evolution of the flash communication system of North American fireflies. The North American firefly genus Photinus contains 35 described species with simple ON–OFF visual signals, and information on habitat types, sympatric congeners, and predators. This makes them an ideal study system to test hypotheses on the evolution of male and female visual signal traits. Our analysis of 34 Photinus species suggests two temporal pattern generators: one for flash duration and one for flash intervals. Reproductive character displacement was a main factor for signal divergence in male flash duration among sympatric Photinus species. Male flash pattern intervals (i.e., the duration of the dark periods between signals) were positively correlated with the number of sympatric Photuris fireflies, which include predators of Photinus. Females of different Photinus species differ in their response preferences to male traits. As in other communication systems, firefly male sexual signals seem to be a compromise between optimizing mating success (sexual selection) and minimizing predation risk (natural selection). An integrative model for Photinus signal evolution is proposed.     

Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae)

Sexual communication between male and female fireflies involves the visual detection of species-specific bioluminescent signals. Firefly species vary spectrally in both their emitted light and in the sensitivity of the eye, depending on the time when each is active. Tuning of spectral sensitivity in three firefly species that occupy different photic niches was investigated using light and electron microscopy, microspectrophotometry, and intracellular recording to characterize the location and spectral absorption of the screening pigments that filter incoming light, the visual pigments that receive this filtered light, and the visual spectral sensitivity. Twilight-active species had similar pink screening pigments, but the visual pigment of Photinus pyralis peaked near 545 nm, while that of P. scintillans had a λ_max near 557 nm. The night-active Photuris versicolor had a yellow screening pigment that was uniquely localized, while its visual pigment was similar to that of P. pyralis. These results show that both screening and visual pigments vary among species. Modeling of spectral tuning indicates that the combination of screening and visual pigments found in the retina of each species provides the best possible match of sensitivity to bioluminescent emission. This combination also produced model sensitivity spectra that closely resemble sensitivities measured either with electroretinographic or intracellular techniques. Vision in both species of Photinus appears to be evolutionarily tuned for maximum discrimination of conspecific signals from spectrally broader backgrounds. Ph. versicolor, on the other hand, appears to have a visual system that offers a compromise between maximum sensitivity to, and maximum discrimination of, their signals. Accepted: 29 September 1999     

Abdomen Posture and Flash Gesture Direction in a Female Synchronic Firefly <Emphasis Type="Italic">Photinus carolinus</Emphasis> (Green) (Coleoptera: Lampyridae)

North American Photinus fireflies use bioluminescent flashes to communicate an individual’s species and sex, and to attract potential mates. A female firefly responds to a male firefly’s courtship flash with her own species-specific flash. We used a photic stimulator to produce male-like species-specific P. carolinus LED courtship flashes. These evoked species-specific response flashes from a female. The female’s flashes were preceded by a flash gesture comprising a sequence of abdominal postural adjustments (pitch, roll, and yaw). These gestures changed her lantern’s orientation which, at rest, was downward towards the substrate. Our results demonstrate that these gestures mediate a lateralization of the female’s response flashes towards the direction of the stimulating LED. That is, she directs her response to the left of midline when stimuli are presented from her left, and similarly, she directs her response to the right of midline when stimuli are presented from her right. The directional aspect of the flash gesture adds a new perspective to the complexity of the behaviors associated with flash communication in fireflies. Lateralization of the flash gesture suggests that the female’s visual system processes information about the location of male’s flashes as well as their temporal pattern.     

Allometry and proximate mechanisms of sexual selection in photinus fireflies, and some other beetles

Ever since Darwin identified it as the force responsible forthe evolution of exaggerated male characters, sexual selectionhas been the focus of research aimed at understanding the mostbizarre and intriguing morphologies and behaviors in Nature.Two congeneric species in the firefly genus Photinus, P. pyralisand P. macdermotti, afford a unique opportunity to examine theinteraction between sexual and countervailing natural selectionthat act to shape the evolution of mating behavior and bodysize in closely related species with very different courtshipstrategies. Photinus pyralis males emit very bright flashesduring their extended patrolling flights and form ‘loveknots’ of competing suitors, while P. macdermotti males,whose courtships seldom exceed two competing males, produceweaker flashes during a shorter patrolling period. Possibly as a consequence of their scramble competition andlong flights, not only is there an extremely wide range of bodysizes in P. pyralis males, but they also exhibit wing allometricslopes greater than one, and lantern allometries less than one.In contrast, P. macdermotti males do not have allometric slopessignificantly different from one. Small males, when tested inan artificial scramble situation move faster than large males,an advantage in the intense competition that ensues once a femaleis located. Females answer several males in alternation andfail to respond to all male flashes, with the evident consequencethat love knots frequently develop around such fickle females.Allometric relationships in two non-luminescent beetle specieswith non-visual courtship protocols are compared. Visual, sexuallyselected characters showed positive allometric slopes, whilenon-visual characters showed isometry or negative slopes. Datapresented here support the existence of distinct patterns inmodality-specific sexual selection.     

Effects of traffic-regulated street lighting on nocturnal insect abundance and bat activity

New technological developments modulate the light levels of LED street luminaires according to traffic volumes: light levels are increased given traffic and reduced in its absence. Such dimming of street lights reduces the level of artificial light at night (ALAN) and may thus contribute to mitigate light pollution. To quantify the impact of traffic-driven dimming of street lights on nocturnal insect abundance and bat activity in comparison to full light (i.e., dimming functions of luminaires switched off), we mounted 20 insect flight-interception traps and ten batloggers on street light poles along two dimmable street light sections. Insect abundance and bat activity were measured alternately with one week of full street lighting followed by a week with light levels modulated by traffic volumes. In total, 16 dimmed and 16 full-light days were investigated. Overall, traffic-driven dimming reduced light levels by 35%. Weather conditions (warm, dry nights) were the main drivers of insect abundance and bat activity, but traffic-driven dimming resulted in lower numbers of insects caught and reduced bat activity. Among insect groups, Heteroptera benefited most from dimming. For bats, urban exploiters (Pipistrellus spp.) benefited from increased availability of prey at brightly lit street lights, while less frequent species (Myotis spp.) did not benefit from street lighting. We conclude that street light dimming technology may contribute to mitigate negative effects of ALAN on nocturnal organisms, although the measure may not be efficient enough to support light-sensitive and threatened species.     

Nuptial gifts and sexual selection in photinus fireflies

The phenomenon of nuptial gift transfer during mating occursacross a remarkably wide range of taxa, and such male donationsare likely to influence both pre-copulatory and post-copulatorysexual selection. This paper reviews what is known about nuptialgifts in Photinus fireflies (Coleoptera: Lampyridae), and discussesthe adaptive significance of spermatophores in firefly matingsystems. During copulation Photinus males transfer a spiral,gelatinous spermatophore to the female: sperm are released intothe female's spermatheca for storage, while the remainder ofthe spermatophore disintegrates within a specialized gland.Radiolabelling studies indicate that male-derived protein isused to help provision the female's developing oocytes, andmultiply-mated females show increased fecundity. As most Photinusadults do not feed, these studies suggest that females shouldcontinue to forage for matings to supplement their diminishinglarval reserves, even after they have gained sufficient spermto fertilize their eggs. Male spermatophore mass declines acrosssequential matings, and smaller spermatophores are associatedwith lower paternity success in situations where males competefor fertilizations. Declining spermatophore size across sequentialmatings may thus lead to diminishing reproductive returns forfirefly males. Taken together, these results suggest that seasonalchanges in nuptial gift availability may contribute to reversalsof traditional courtship roles, with male choice and female-femalecompetition occurring as spermatophore availability declines.     

萤火虫的研究、保护及开发利用进展

萤火虫是萤科和凹眼萤科昆虫的统称,既是科学研究的良好材料,也具有巨大的产业潜力。本文从分类学(包括分类现状和分子系统学研究进展)、生物学(包括生活史、分布、天敌、视蛋白、人工光照的影响、生物指示作用、体内共生菌等)、行为学(包括发光、求偶、交配、取食、防御、报警、拟态、叠背、成虫后多次蜕皮等)等方面全面梳理了国内外萤火虫基础研究的进展,分析了萤火虫的消亡原因(环境污染、旅游影响、科普欠缺、生物入侵及其它等)、保护情况并提出了保护萤火虫的若干措施建议,系统地阐述了当前国内外萤火虫开发利用的现状,最后从萤火虫的科学研究、资源保护、人工养殖、产业发展等方面提出了建议,以期推动萤火虫的研究和资源开发工作。     

Flash Precision at the Start of Synchrony in Photuris frontalis

Synchronous flashing occurs in certain species of SoutheastAsian and North American fireflies. Most Southeast Asian synchronyinvolves stationary congregating fireflies, but North Americansynchrony occurs in flying fireflies that do not congregate.Southeast Asian synchrony is usually continuous, but North Americansynchrony is interrupted. Photuris frontalis, the only memberof the North American genus Photuris to synchronize, shows anintermittent synchrony. This involves synchronization and repeatedre-synchronizations while in flight. The precision that occursat the start of synchrony was studied in Ph. frontalis usingcaged fireflies and photometry. Barrier experiments (using twofireflies) or flash entrainment experiments (using one LED andone firefly) were performed to measure the temporal precisionof the first entrained flash. In both cases, the first entrainedflash was close to unison synchrony (phase = 1.0) and showedlittle variability. The behavioral implications of the abilityto synchronize with the first entrained flash are not known,but it might facilitate male-male interactions during brief,transient encounters such as maintaining distance between closelyflying males in search of females.     

Pyrazine emission by a tropical firefly: An example of chemical aposematism?

Although famous for photic courtship displays, fireflies (Coleoptera: Lampyridae) are also notable for emitting strong odors when molested. The identity of volatile emissions and their possible role, along with photic signals, as aposematic warnings of unpalatability have been little explored, especially in tropical species. Pursuant to the observation that the widespread Neotropical fireflies, Photuris trivittata and Bicellonycha amoena, emit pungent odors, glows, and flashes when handled, we investigated their cuticular and headspace chemistry. Gas chromatography–mass spectrometry analyses revealed that both fireflies have species‐specific cuticular hydrocarbon profiles. Photuris trivittata headspace was dominated by 2‐methoxy‐3‐(1‐methylpropyl) pyrazine (hereafter, pyrazine), on the order of 1.59 ng/individual and a suite of sesquiterpenes, while B. amoena emitted 3‐methoxy‐2‐butenoic acid methyl ester and a few ketones. This is the first report of such compounds in fireflies. We investigated the role of pyrazine in P. trivittata's interactions with potential predators: sympatric ants, toads, and bats. Solvent‐washed P. trivittata painted with pyrazine incurred lower ant predation than did their solvent‐washed counterparts. Pyrazine significantly repelled ants at baits in concentrations as low as 9.8 × 10^?4 ng/μl. The toad, Rhinella marina, readily accepted intact fireflies, pyrazine‐coated and uncoated mealworms. Both Myotis nigricans and Molossus molossus bats rejected fireflies, but accepted both pyrazine‐coated and uncoated mealworms. While pyrazine repels ants, its role as an aposematic signal warning other potential predators of firefly distastefulness requires further investigation. Our results underscore the idea that multiple enemies exert conflicting selection on firefly defenses.     

Flight Studies on Photic Communication by the Firefly Photinus pyralis

Flash communication by the firefly Photinus pyralis was studiedin a stationary, simulated flight apparatus in which an individualof either sex could be "flown" and its flashing behavior andflight orientation recorded in response to photic stimulation.Males made long "flights" showing many of the characteristicsof their natural, female-seeking patrol flights. Males orientedtheir flight vectors towards light emitting diode (LED) flashesthat mimicked the responses of females to their patrol flashes.Females flew and responded to male-emulating LED flashes, makinga previously unknown early response followed by the typical2 sec delayed response characteristic of the dialoging perchedfemale, including abdominal aiming of the flash. Pairs consistingof males, in tethered flight, and females, perched, were runin an integrating sphere photometer, permitting the first determinationsof flash intensities of both sexes during courtship dialog.The implications of this work on thought about evolution ofphotic behavior in fireflies are considered.     

Limits to Nuptial Gift Production by Male Fireflies, Photinus ignitus

Males of diverse insect species provide females with nuptial gifts, and limits on males' ability to produce these gifts may influence courtship behavior and mating systems. In the firefly Photinus ignitus, males transfer a complex spermatophore to females during mating. We provided firefly males unlimited access to responsive females to examine whether spermatophore production limits male mating success. Male spermatophore mass decreased significantly across sequential matings, and the percentage of successful matings declined during the second half of each male's life span. Male body mass explained a significant proportion of variation in size of the first spermatophore produced by P. ignitus males, but this relationship disappeared with second spermatophores. This study indicates that males' ability to produce spermatophores declines over their lifetime and that limits on nuptial giftproduction can constrain male mating success in Photinus fireflies.     

TiLIA: a software package for image analysis of firefly flash patterns

As flash signaling patterns of fireflies are species specific, signal‐pattern analysis is important for understanding this system of communication. Here, we present time‐lapse image analysis (TiLIA), a free open‐source software package for signal and flight pattern analyses of fireflies that uses video‐recorded image data. TiLIA enables flight path tracing of individual fireflies and provides frame‐by‐frame coordinates and light intensity data. As an example of TiLIA capabilities, we demonstrate flash pattern analysis of the fireflies Luciola cruciata and L. lateralis during courtship behavior.     

Changes in volatile production during interspecific interactions between four wood rotting fungi growing in artificial media

Effects of volatile organic compounds (VOCs) produced during interspecific mycelial interactions were examined by measuring extension rate of ‘target’ fungi growing in agar plates taped above two interacting mycelia – Bjerkandera adusta, Hypholoma fasciculare, Stereum gausapatum and Trametes versicolor in all combinations. Extension rates of T. versicolor, S. gausapatum and H. fasciculare above self-pairings were not significantly different (P > 0.05) to growth above agar controls, but the extension rate of B. adusta was significantly (P ≤ 0.05) greater. Extension rates of T. versicolor and B. adusta were often significantly greater above inter-specific interactions and above other species compared with growth above self or agar controls. VOC production was quantified and qualified, by gas chromatography–mass spectrometry (GC/MS), over the course of interactions with T. versicolor replacing S. gausapatum, deadlocking with B. adusta and replaced by H. fasciculare. VOC production was species- and interaction-specific. It varied over the time course of interactions, and changes in production were correlated with production of pigments in interactions involving S. gausapatum. VOCs included 3 monoterpenes, benzoic acid, alkenols of different chain lengths, two long-chain hydrocarbons and a quinolinium-like compound. Their possible roles are discussed.     

Temporal Dynamics of Top Predators Interactions in the Barents Sea

The Barents Sea system is often depicted as a simple food web in terms of number of dominant feeding links. The most conspicuous feeding link is between the Northeast Arctic cod Gadus morhua, the world''s largest cod stock which is presently at a historical high level, and capelin Mallotus villosus. The system also holds diverse seabird and marine mammal communities. Previous diet studies may suggest that these top predators (cod, bird and sea mammals) compete for food particularly with respect to pelagic fish such as capelin and juvenile herring (Clupea harengus), and krill. In this paper we explored the diet of some Barents Sea top predators (cod, Black-legged kittiwake Rissa tridactyla, Common guillemot Uria aalge, and Minke whale Balaenoptera acutorostrata). We developed a GAM modelling approach to analyse the temporal variation diet composition within and between predators, to explore intra- and inter-specific interactions. The GAM models demonstrated that the seabird diet is temperature dependent while the diet of Minke whale and cod is prey dependent; Minke whale and cod diets depend on the abundance of herring and capelin, respectively. There was significant diet overlap between cod and Minke whale, and between kittiwake and guillemot. In general, the diet overlap between predators increased with changes in herring and krill abundances. The diet overlap models developed in this study may help to identify inter-specific interactions and their dynamics that potentially affect the stocks targeted by fisheries.     

Spatial variability in prey phenology determines predator movement patterns and prey survival

Species have phenological variation among local habitats that are located at relatively small spatial scales. However, less studies have tested how this spatial variability in phenology can mediate intra-/inter-specific interactions. When predators track phenological variation of prey among local habitats, survival of prey within a local habitat strongly influenced by phenological synchrony with their conspecifics in adjacent habitats. Theory predicts that phenological synchrony among local habitats increases prey survival in local habitat within spatially structured environments because the predators have to make a habitat choice for foraging. Consequently, total survival of prey at regional scale should be higher. By using a spatially explicit field experiment, we tested above hypothesis using a prey–predator interaction between tadpole (Rhacophorus arboreus) and newt (Cynops pyrrhogaster). We established enclosures (≈regional scale) consisting of two tanks (≈local habitat scale) with different degree of prey phenological synchrony. We found that phenological synchrony of prey between tanks within each enclosure decreased the mean residence time of the predator in each tank, which resulted in higher survival of prey at a local habitat scale, supporting the theoretical prediction. Furthermore, individual-level variation in predator residence time explained the between-tank variation in prey survival in enclosures with phenological synchrony, implying that movement patterns of the predator can mediate variation in local population dynamics of their prey. However, total survival at each enclosure was not higher under phenological synchrony. These results suggest the importance of relative timing of prey phenology, not absolute timing, among local habitats in determining prey–predator interactions.     

Inter- and Intra-Specific Density-Dependent Effects on Life History and Development Strategies of Larval Mosquitoes

We explored how inter- and intra-specific competition among larvae of two temporary-pool mosquito species, Culiseta longiareolata and Ochlerotatus caspius, affect larval developmental strategy and life history traits. Given that their larvae have similar feeding habits, we expected negative reciprocal inter-specific interactions. In a microcosm experiment, we found sex-specific responses of larval survival and development to both intra- and inter-specific larval competition. C. longiareolata was the superior competitor, reducing adult size and modifying larval developmental time of O. caspius. We observed two distinct waves of adult emergence in O. caspius, with clear sex-specific responses to its inter-specific competitor. In males, this pattern was not affected by C. longiareolata, but in females, the timing and average body size of the second wave strongly varied with C. longiareolata density. Specifically, in the absence of C. longiareolata, the second wave immediately followed the first wave. However, as C. longiareolata abundance increased, the second wave was progressively delayed and the resulting females tended to be larger. This study improves our understanding of the way intra- and inter-specific competition combine to influence the life histories of species making up temporary pond communities. It also provides strong evidence that not all individuals of a cohort employ the same strategies in response to competition.     

Fatal Attraction of Short-Tailed Shearwaters to Artificial Lights

Light pollution is increasing around the world and altering natural nightscapes with potential ecological and evolutionary consequences. A severe ecological perturbation caused by artificial lights is mass mortalities of organisms, including seabird fledglings that are attracted to lights at night on their first flights to the sea. Here, we report on the number of fledging short-tailed shearwaters Ardenna tenuirostris found grounded in evening and morning rescue patrols conducted at Phillip Island, Australia, during a 15-year period (1999–2013). We assessed factors affecting numbers of grounded birds and mortality including date, moon phase, wind direction and speed, number of visitors and holiday periods. We also tested experimentally if birds were attracted to lights by turning the lights off on a section of the road. Of 8871 fledglings found, 39% were dead or dying. This mortality rate was 4–8 times higher than reported elsewhere for other shearwater species, probably because searching for fledglings was part of our systematic rescue effort rather than the opportunistic rescue used elsewhere. Thus, it suggests that light-induced mortality of seabirds is usually underestimated. We rescued more birds (dead and alive) in peak fledging, moonless and windy nights. Mortality increased through the fledging period, in the mornings and with increased traffic on holiday periods. Turning the road lights off decreased the number of grounded birds (dead and alive). While moon, wind and time are uncontrolled natural constraints, we demonstrated that reduction of light pollution and better traffic management can mitigate artificial light-induced mortality.