Skip to main content
Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Short- and mid-wavelength artificial light influences the flash signals of Aquatica ficta fireflies (Coleoptera: Lampyridae)

  • Avalon Celeste Stevahn Owens,

    Roles Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Department of Biology, Tufts University, Medford, Massachusetts, United States of America

  • Victor Benno Meyer-Rochow,

    Roles Conceptualization, Writing – review & editing

    Affiliations Department of Genetics and Physiology, Oulu University, Oulu, Finland, Research Institute of Luminous Organisms, Tokyo, Japan

  • En-Cheng Yang

    Roles Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – review & editing

    ecyang@ntu.edu.tw

    Affiliation Department of Entomology, National Taiwan University, Taipei, Taiwan

Abstract

Urbanization can radically disrupt natural ecosystems through alteration of the sensory environment. Habitat disturbances are predicted to favor behaviorally flexible species capable of adapting to altered environments. When artificial light at night (ALAN) is introduced into urban areas, it has the potential to impede reproduction of local firefly populations by obscuring their bioluminescent courtship signals. Whether individual fireflies can brighten their signals to maintain visibility against an illuminated background remains unknown. In this study, we exposed male Aquatica ficta fireflies to diffused light of varying wavelength and intensity, and recorded their alarm flash signals. When exposed to wavelengths at or below 533 nm, males emitted brighter signals with decreased frequency. This is the first evidence of individual-level light signal plasticity in fireflies. In contrast, long wavelength ambient light (≥ 597 nm) did not affect signal morphology, likely because A. ficta cannot perceive these wavelengths. These results suggest long wavelength lighting is less likely to impact firefly courtship, and its use in place of broad spectrum white lighting could augment firefly conservation efforts. More generally, this study demonstrates benefits of bioluminescent signal plasticity in a “noisy” signaling environment, and sheds light on an important yet understudied consequence of urbanization.

Introduction

As human populations grow, cities and suburbs expand into formerly natural lands [1]. Urbanization is a severe form of ecosystem disturbance, and one of the leading causes of species endangerment [2]. The impacts of deforestation, habitat fragmentation, and chemical pollution on species endemic to affected habitats have been widely recorded [36]. However, many species manage to survive and even thrive in urban centers, despite these myriad threats [710]. Opportunistic generalists such as cockroaches, rats, bats, and pigeons are inherently disposed to disturbed habitats [11], while other species persist through adaptation to their altered surroundings [12]. Population-level phenotypic change may occur over relatively long time scales, as has been observed in the case of industrial melanism in the peppered moth Biston betularia [13]. Concurrently, individual-level behavioral change can produce immediate fitness benefits. Urban populations of several bird species have been found to sing more loudly and at higher frequencies to compensate for increased ambient noise [14,15]. In these and other cases, signal plasticity promotes information transmission within noisy signaling environments [16].

In addition to noise, heat, and chemical pollution, urbanization commonly results in the introduction of artificial light at night (ALAN), the effects of which are infrequently studied in isolation [17]. ALAN transforms the nocturnal landscape: upward-directed “astronomical light pollution” obscures the night sky [18], while downward-directed “ecological light pollution” can affect species on the ground [17,19]. Among invertebrates, the attraction of moths and other flying insects to streetlamps is a particularly well studied phenomenon [20,21]. In contrast, the potential vulnerability of species with light-based communication systems to ALAN interference has only recently attracted the attention of researchers [2228].

Bioluminescence has evolved multiple times within a broad range of bacterial, protist, fungal, and animal lineages, and is used in diverse contexts [29]. On land, bioluminescence is most common among insects: “glowworm” larvae of some fungus gnats use bioluminescent lures to attract prey [30], while four families of beetles, including the firefly family Lampyridae, have separately evolved a diverse range of light signals and signaling behavior [31,32]. Many adult fireflies use bioluminescent signals as part of courtship, with one or both sexes emitting prolonged glows, discrete flashes, or timed flash patterns to attract conspecifics [3335]. During the mating season, adults begin flashing late in the day, when ambient light levels have declined to a species-specific threshold [36,37]. High levels of broad spectrum ALAN can delay or inhibit male signaling activity, and negatively affect female receptivity to bioluminescent signals [27,28].

How a particular light source impacts firefly activity depends in part on the intersection of its spectral emission with the spectral sensitivity of the species in question: if the firefly does not detect most wavelengths emitted by the source, courtship activity will likely be unaffected. Single copies of UV-sensitive (UVS) and long-wavelength-sensitive (LWS) opsin genes have been identified in multiple firefly species [38,39]. Peak sensitivity of the LWS visual pigment, after filtration by associated screening pigments, often corresponds to the peak wavelength of conspecific bioluminescence [4043]. Short-wavelength-sensitive (SWS) opsins have yet to be found, although blue sensitivity has been described from electroretinograms (ERGs) and behavioral studies of multiple species [4447]. The discrepancy may be due to opsin sensitization by as-yet-undescribed “antenna pigments” [48], or secondary interactions of screening pigments [42,45].

Recent studies have shown that broad spectrum white lighting negatively impacts firefly flash frequency (flashes/min) and/or the total number of flashing individuals present [27,28]. However, few studies have measured how specific wavelengths of ambient light interact with the firefly visual system and overlying neurobehavioral architecture to influence courtship behavior (but see [49,50] for studies of the spectral cues that initiate male flash activity). Different wavelengths are likely to have different effects. For example, receptive Photinus pyralis females emit response flashes exclusively to simulated male flashes of wavelengths longer than 480 nm, even though their eyes are sensitive to UV light [51]. To quantify the impact of different artificial light sources on firefly courtship behavior, we must compare the ways in which ambient light of different wavelengths affect firefly flash activity.

In this study we used monochromatic LEDs to test how specific wavelengths affect the signaling activity (intensity and frequency of flashes) of Aquatica ficta males. The resulting plot of activity vs. wavelength quantifies the effects of ambient light on two dimensions of A. ficta signal morphology, and positively identifies a range of wavelengths to which this species is visually sensitive. It is also the first controlled study of firefly signal plasticity, investigating the capacity for individual-level variation in flash intensity and frequency. Although likely too costly and inefficient under daytime illumination [52], some degree of signal plasticity may be used to promote signal visibility under twilight illumination, or in areas with low level ALAN. Thus we predict that A. ficta will flash more brightly under dim ambient light, but only of wavelengths to which they are visually responsive.

Materials and methods

Study organism

A. ficta is a common Taiwanese firefly notable both for its aquatic larvae and multivoltine life history [53]: most adults eclose in late April to May, but a second generation ecloses in mid-August [54]. A. ficta larvae require clean water and soft, mildly alkaline soil for development [54]. Conversion of streams into cemented irrigation ditches prevents these fireflies from using stream beds as oviposition or pupation sites, while water pollution and pesticide use may affect larvae and adults alike. The impacts of light pollution on A. ficta are unknown. Notably, small populations of A. ficta can still be found in a few areas within Taipei city center. Additionally, in 2016 the Taipei City Government Department of Public Works in collaboration with NGOs (re)introduced A. ficta to five prominent green spaces around Taipei: Da’an Forest Park, Muzha Cui Lake, Fuyang Eco Park, Zhongqiang Park, and Rongxing Garden [55].

Three male A. ficta fireflies were collected three times from Yongjian Eco Park (24.990195, 121.555824; May 4, May 7, and May 11, 2016), where they could be found approximately 20 min after sundown flying over a shaded stream emitting courtship flashes: periodic single yellow-green flashes (peak wavelength: 565 nm; bandwidth: 60 nm; n = 6) approximately 1 sec in duration. Specimens were transferred into transparent containers (250 ml volume) under natural conditions [54], and kept in an open-air courtyard by the National Taiwan University Insectarium. After a one day adjustment period, a single specimen was tested each evening over three consecutive evenings (no specimens were tested more than three days post-collection). Trials commenced 30 min after sunset and ran for 32 min, after which the specimen was released to prevent accidental retesting. The final sample size was limited by small local population numbers as well as the short adult lifespan and brief nightly activity period of this species.

Artificial light

ALAN was simulated with eight LED pucks (Oznium.com, Pagosa Springs), circuit boards (diameter: 5 cm) populated by 30 monochromatic LEDs of identical peak wavelength, placed in plastic housing (diameter: 7 cm) and covered with 50% opaque frosted epoxy diffusers. Puck wavelengths were semi-evenly distributed across a range from near-UV to red (444 nm to 663 nm) in increments of 20–30 nm. Puck illumination was attenuated by a 72 mm H&Y adjustable neutral density filter (diameter: 7.5 cm, range: ND 0.3 to ND 2.4) before penetrating an opaque light chamber (S1 Fig). Ambient illumination intensity could be adjusted and observed in real time using a model 1935-C series power meter sensor (Newport) placed inside the light chamber. Trials were conducted in near darkness to minimize interference from outside light.

Signal morphology

To obtain action spectra of firefly flash behavior, specimens were isolated within the light chamber, and the intensity over time of their light signals recorded and analyzed. Fireflies were secured to a piece of foam by a thin wire (22 ga) slid between their wings and dorsal abdomen. The act of restraint induced a series of fast (approx. 200 ms duration, 200–300 ms flash interval) alarm flashes in this species, which were produced with remarkable consistency throughout the entire experimental period. The foam was mounted to a slide cover, which was adjusted within a transparent acrylic slide cover box (2.5 cm3) to align the light organ of the specimen to the sensor of a USB4000 FLAME-S-XR1-ES spectrometer (Ocean Optics, Dunedin) connected to a Dell XPS 9343 laptop running SpectraSuite software (Windows Vista version 6.2). The “color chart” function of SpectraSuite was used to record average relative intensity (counts) of wavelengths from 565 nm to 569 nm over 32 min, capturing the peak wavelength of A. ficta bioluminescence. Averages were calculated and saved every 100 ms.

Experimental protocol

After a 5 min adaptation period, each specimen underwent one 32 min trial without interruption, during which it was exposed to each of the eight pucks in a randomized order determined by a random sequence generator (http://www.random.org, S1 Table). For each wavelength, specimens were exposed to both dim (1×) and bright (10×) intensities; the order of exposure (i.e. dim or bright first) was secondarily randomized within wavelengths. Here intensity refers to quantum flux (photons per unit area per second), converted from power meter measurements of μW/cm2 and equalized across wavelengths: ranging from 0.107 ± 0.02 μmol m-2 s-1 and from 1.075 ± 0.212 μmol m-2 s-1 for dim and bright exposures, respectively. For both intensities of all wavelengths, exposures lasted 1 min and were always preceded by 1 min dark recordings, a total recording time of 4 min per wavelength.

Data analysis

Eight sets of data were collected from eight A. ficta males on the evenings of May 5–9 and May 12–14, 2016 (S2 Fig; one male died before it could be tested). Of these, two recordings (May 5 and May 13) were disregarded due to measurement inconsistencies maintained over > 10 min of recording time. Flash intensity and frequency data from six individuals were separated into 1 min recordings (8×2×6 = 96 light recordings, and an equal number of dark recordings) and analyzed in R (version 3.2.3 [56]). The first 15 s of each recording was defined as the “adaptation period” (from light to dark or vice-versa) and omitted from subsequent analysis. Average intensity over time of light signals was zeroed within each recording to account for spectrometer noise, and average peak intensity calculated by isolating local maximums. Measurements ≤ 200 counts were excluded as noise, as peak intensity of A. ficta flashes consistently exceeded several thousand counts. The total number of peaks thus isolated was summed to obtain the average flash rate per individual for each exposure (peaks/min).

After removing the 15 s adaptation period, dark recordings still showed significant variation within and among individuals, suggesting high natural variation in A. ficta signal morphology as well as potential lingering effects of previous exposures (Fig 2A). Each set of light recordings was therefore compared to the initial set of dark recordings obtained previous to any ambient light exposure. Average flash intensity and frequency under each wavelength of exposure was compared using generalized linear mixed models (GLMM) from the R package ‘lme4’ [57]. Exposure wavelength was set as a fixed effect, and both specimen and exposure order (1 to 16; eight wavelengths × two intensities) initially included as random effects. Due to rank deficiency, both exposure intensities were analyzed separately, as were the effects on flash intensity and flash frequency (S1 Table). Exposure order explained a large amount of observed variation in flash frequency. However, it did not have an observable impact on flash intensity and was subsequently dropped from that set of models.

Results

A. ficta bioluminescent signaling behavior changed in response to environmental light (Fig 1A, Table 1). In comparison to base level data taken in complete darkness, average peak intensity of flash signals significantly increased, sometimes more than 100%, when individuals were exposed to dim intensities of short- and mid-wavelength light (Fig 2A, Table 1; 444 nm: p = 0.0021; 463 nm: p = 0.01; 488 nm: p = 0.017; 515 nm: p = 0.021; 533 nm: p = 0.066). Increases in flash intensity under dim short- and mid-wavelength illumination were accompanied by significant reductions in flash frequency (Fig 2B, Table 1; 444 nm: p = 0.0042, 463 nm: p = 0.049, 488 nm: p = p < 0.0001, 515 nm: p = 0.0098; 533 nm: p = 0.046). The decline is due to increases in interpulse interval [58] and, to a lesser extent, flash duration (S2 Table); in addition, sporadic periods without flashing were more common under illumination, sometimes continuing for 10 or more seconds. More extreme reductions in flash frequency were seen when males were exposed to bright intensities of the same wavelengths (Fig 2B, Table 1; 444 nm: p = 0.0019; 463 nm: p < 0.0001, 488 nm: p < 0.0001, 515 nm: p = 0.0018, 533 nm: p = 0.032). In fact, under bright short- and mid-wavelength illumination, three of six males ceased signaling entirely (Fig 1B). Due to the consequent lack of data, average peak intensity of flash signals became erratic under bright short- and mid-wavelength illumination (444 nm: p = 0.23; 463 nm: p = 0.19; 488 nm: p = 0.13; 515 nm: p = 0.59; 533 nm: p = 0.051). Notably, neither dim nor bright intensities of long wavelength (≥ 597 nm) illumination had a significant effect on flash intensity or frequency (p ≥ 0.3 in all instances; Fig 2).

thumbnail
Fig 1. Plastic effects of 533 nm ambient light exposure on firefly flash morphology.

(A) Example of change in intensity of flashes emitted by A. ficta male under different illumination conditions (indicated above each section), recorded in units of average counts per 100 ms over 4 min. (B) Changes in signal intensity over 4 min of separate A. ficta male under the same illumination conditions (indicated above each section).

https://doi.org/10.1371/journal.pone.0191576.g001

thumbnail
Fig 2. Effects of exposure wavelength and intensity on firefly flash morphology.

Change in average (± 1 SE) flash intensity (A) and frequency (B) of light signals emitted by A. ficta under illumination by eight wavelengths and two intensities of ambient light (N = 6). Base values for average flash intensity (5420 counts) and flash frequency (43.167 peaks/min) obtained from 1 min dark recordings have been subtracted out.

https://doi.org/10.1371/journal.pone.0191576.g002

thumbnail
Table 1. Average peak intensity and frequency of light signals produced by A. ficta under exposure to varying wavelengths and intensities of ambient light.

https://doi.org/10.1371/journal.pone.0191576.t001

Although some males underwent remarkably rapid changes in average flash intensity, individuals often appeared to remain at least partially affected by the previous series of exposures (Fig 1A and 1B). When analysis of variance (ANOVA) was used to compare models, results showed that number of previous exposures had a significant negative effect on flash frequency (1×: p < 0.0001, χ2 = 15.205; 10×: p = 0.0012, χ2 = 14.668), but not flash intensity (p = 1.0 and χ2 = 0 in both 1× and 10× models). Thus, the brightness of male flashes was apparently only influenced by the current level of ambient illumination, while the total number of flashes per minute was determined by both current and previous light exposures.

Discussion

Our results suggest that A. ficta is not visually responsive to red wavelengths. However, short wavelength ambient light (including blue) significantly affects their signaling behavior, inducing increased flash intensity as well as decreased flash frequency. Erratic measurements obtained during bright (10×) exposures across wavelengths may reflect the small sample size, necessitated by the limited population numbers and highly seasonal life history of A. ficta, or conflict between two opposing behaviors: 1.) increasing light signal intensity in response to low level environmental light and 2.) ending light signal production in response to high level environmental light. The latter behavior likely relates to entrainment of diurnal and nocturnal modes of activity: fireflies do not engage in courtship activity during their subjective daytime [36,37]. The former may be an adjustment to the nocturnal mode of activity, a plastic response to increases in environmental light levels within some “nighttime” range.

This is the first description of individual-level variation in the average peak intensity of firefly flash signals. Previous studies on the characteristic flash patterns of North American Photinus fireflies have described intraspecific variation in several other signal parameters. These include flash rate, flash duration, and interpulse interval [5962], in addition to flash frequency (total flashes/min) [27,28,36,59] and flash wavelength [63]. Individual- and/or population-level variation has been shown to be related to age [64], habitat type [63], temperature, humidity, time of day, and ambient light [27,28,36]. Our results open up another dimension of signal morphology for future behavioral studies. They also suggest that while fireflies can brighten their flashes in response to ambient light, this potentially beneficial behavior may require some decrease in average flash frequency [correlation coefficient: -0.9655009 (1×), -0.8027756 (10×)].

The plastic increases in alarm flash intensity we observed during dim (1×) exposures may be a product of natural or sexual selection. Alarm flashes, which serve as aposematic signals [65,66], will be more easily perceived by potential predators if they have greater contrast against the background. When given a choice among simulated courtship flashes of varying intensity, P. pyralis males and females [67,68] and L. noctiluca males [46] all prefer brighter signals, likely due to their greater visibility. Temporary increases in signal intensity could also help to maintain a base level of visibility against artificially illuminated backgrounds. Resilience of urban firefly populations to low level ALAN will depend on the success with which these signal modifications maintain inter- and intraspecific lines of communication, and the fitness costs of doing so. Flash signal production may have a relatively low metabolic cost [69]. If this is the case, increasing the average intensity of one’s light signals could help ensure continued predator deterrence and/or courtship success without any corresponding fitness cost, offering a fascinating case study of the benefits of behavioral plasticity in urbanized environments. However, other evidence suggests that flash production does require high levels of lipid metabolism [70], and therefore certain tradeoffs (such as decreased flash frequency) may be involved.

Regardless of metabolic cost, even extremely bright flashes should be impossible to perceive in sufficiently bright environments, which may be why half of the A. ficta specimens stopped flashing under bright (10×) exposures (1× and 10× exposures roughly correspond to 20 and 200 lux, respectively, although photometric units are not suited to the analysis of monochromatic light; see S1 Text). Fireflies do not flash under daytime levels of artificial or natural illumination [36,37]. Hagen et al. [27] observed significant decreases in the average number of flashing Photinus sp1 individuals encountered in brightly lit conditions (1.5–4.45 lux). Firebaugh and Haynes [28] also found decreases in flash frequency (flashes/min, a proxy for abundance) of Photuris versicolor in an experimental plot lit by LED floodlights to ~301 lux. However, flash frequency of Photinus pyralis males was unaffected. P. pyralis is a common crepuscular species, while P. versicolor is nocturnal and may be less resilient to changes in the light environment. Despite this, the receptivity of P. pyralis females to male signals decreased in experimental plots. Females may have been unable to see these signals, or less receptive to them due to their decreased contrast against the background; females are likely unable to distinguish decreases in contrast (perceived intensity) from decreases in emitted intensity. Plastic increases in male flash intensity are unlikely to greatly promote visibility in this context, due to the extreme brightness of the artificial light source.

Selecting artificial light sources that have the least chance of interfering with firefly communication can help to reduce disturbance of urban firefly populations. Blue light is often employed in firefly observations and experiments in the west, as it is thought to be minimally disruptive to local species. Although thus far genetic analysis has failed to uncover blue opsin genes in any firefly species [38,39], we found that blue wavelengths did significantly affect the flash signaling behavior of A. ficta. Our results suggest artificial light sources emitting the majority of their light in wavelengths ≥ 597 nm, including a range of yellow to red wavelengths visible to humans, would be most suitable for A. ficta habitats. These conclusions receive support from ERG spectral sensitivity studies of Luciola cruciata, a close relative of A. ficta, which have described sensitivity peaks in the green-yellow range of 555–565 nm wavelengths [71,43]. Low-pressure sodium vapor lamps emit light concentrated at 590 nm, well beyond this range [72]. However, in recent decades these lamps have been phased out in favor of brighter and more energy efficient alternatives such as LEDs, which often emit a large portion of their light in the blue region of the spectrum. We suggest spectral emission be given greater consideration when installing artificial lights around firefly habitats. The directionality of light sources (streetlamps vs. path lights) and distinction between point sources and larger sources of diffused light are also relevant to these discussions. Free-roaming A. ficta in the lab continue to emit courtship signals when exposed to small points of light, regardless of the intensity or distance of the point source from their eyes, although they appear to exhibit some degree of negative phototaxis (pers. obs.). However, A. ficta respond to high levels of short wavelength diffused light by decreasing the frequency of their flash signals, and eventually ceasing them altogether.

A. ficta do not exchange precisely timed flash patterns during courtship, so decreases in flash frequency like those we observed in dim light conditions may not cause a significant loss of signal information, and the commensurate increase in intensity may suffice to maintain signal visibility in natural settings. It remains to be seen how ambient light affects the courtship of Photinus fireflies, which use flash patterns to communicate information about species identity and individual fitness. Changes to flash rate, flash duration, or interpulse interval are highly likely to impact the reproductive success of these species; even slight differences in flash rate have been shown to affect male reproductive success [60,73].

Much remains to be done to quantify the total fitness impact of ALAN of varying spectral composition on firefly species of varying spectral sensitivity and courtship behavior. Observed decreases in A. ficta populations over the past few decades indicates that they have been negatively affected by habitat alterations occuring within this time (Wu Chiahsiung, personal communication). The impacts of habitat destruction, climate change, pesticides, and ALAN on fireflies are all relevant, and likely mutually reinforcing, but those of ALAN deserve equal consideration. This is especially the case because fireflies can serve as “flagship species”, charismatic mascots of public outreach efforts to reduce or eliminate ALAN in urban areas. Improving our understanding of the degree to which fireflies everywhere are able to respond and adapt to ALAN is crucial should we hope to protect these species going forward, both for the robustness of the ecosystem and the enjoyment of many generations to come.

Supporting information

S1 Fig. Simplified schematic of experimental setup.

LED pucks fitted into upper box (base: 14×8.5 cm; height: 3 cm) shine through a neutral density filter, the transparency of which is adjusted via rotation of this box. Walls of the light chamber (base: 9×6.5 cm; height: 5.5 cm) are covered in opaque dark room fabric. The USB4000 spectrometer is connected to a Dell laptop running SpectraSuite software. Walls of the light chamber (base: 9×6.5 cm; height: 5.5 cm) are covered in opaque dark room fabric.

https://doi.org/10.1371/journal.pone.0191576.s001

(TIF)

S2 Fig. Signal morphology of eight A. ficta males over eight separate 32 min trials.

During each trial, one unique individual was exposed to two intensities of eight wavelengths of LED for 1 min each. Trial date is given to the left of each recording. All light exposures were preceded by a 1 min dark exposure, summing to 32 exposures total (16 light and 16 dark). Exposure order (intensity and wavelength) was randomized; semi-transparent colored overlays indicate the series of exposure intensities and wavelengths for each recording, corresponding to the colors used in Fig 2 and S1 Table. Bioluminescence was recorded in units of average intensity (counts) per 100 ms.

https://doi.org/10.1371/journal.pone.0191576.s002

(TIF)

S1 Table. Sample experimental procedure, taken from trial on May 5, 2016.

Trial began 30 min post-sunset at 18:56. The order of LED wavelengths has been randomized, as has the order of exposure intensity (dim or bright first) within wavelengths. Relative quantum flux density (μmol m-2 s-1) is approximately equal across wavelengths; variation in energy measurements (μW/cm2) reflects inherent differences in the energy of photons of different wavelength.

https://doi.org/10.1371/journal.pone.0191576.s003

(DOCX)

S2 Table. Change in A. ficta flash duration and interpulse interval under short- and mid-wavelength illumination.

Data from four of eight experimental trials, organized by trial date, are given above. The first column contains average values of flash duration and interpulse interval (duration between flashes) from the initial 1 min dark recording of each insect. The following columns contain average values for all five short- to mid-wavelength exposures (444–533 nm), at 1× and 10× intensity, respectively.

https://doi.org/10.1371/journal.pone.0191576.s004

(DOCX)

S1 Text. Relevance of experimental design to urban and suburban light environments.

https://doi.org/10.1371/journal.pone.0191576.s005

(DOCX)

Acknowledgments

We thank Leo Jeng and Phil Suslow for technical support, Duncan Wright for assistance with data collection, and Dr. Sara Lewis (Tufts University), Dr. Christian Wegener, and one anonymous reviewer for valuable comments on the manuscript. This study was supported by a grant from the Friends of Da’an Forest Park Foundation to ACSO and ECY.

References

  1. 1. Gillham O. The Limitless City: A Primer on the Urban Sprawl Debate. Island Press; 2002.
  2. 2. Czech B, Krausman PR, Devers PK. Economic associations among causes of species endangerment in the United States. Bioscience; Oxford. United States; US, United Kingdom: Oxford University Press, UK; 2000;50: 593–601.
  3. 3. Fahrig L. Effects of Habitat Fragmentation on Biodiversity. Annu Rev Ecol Evol Syst. Annual Reviews; 2003;34: 487–515.
  4. 4. Zvereva EL, Kozlov MV. Responses of terrestrial arthropods to air pollution: a meta-analysis. Environ Sci Pollut Res Int. Springer-Verlag; 2010;17: 297–311.
  5. 5. Isaksson C. Pollution and its impact on wild animals: a meta-analysis on oxidative stress. Ecohealth. 2010;7: 342–350. pmid:20865439
  6. 6. Kupfer JA, Franklin SB. Linking Spatial Pattern and Ecological Responses in Human-Modified Landscapes: The Effects of Deforestation and Forest Fragmentation on Biodiversity. Geography Compass. Blackwell Publishing Ltd; 2009;3: 1331–1355.
  7. 7. McKinney ML. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosyst. Springer US; 2008;11: 161–176.
  8. 8. Adams CE, Lindsey KL. Urban Wildlife Management, Third Edition. 3 edition. CRC Press; 2016.
  9. 9. Niemelä J, Breuste JH, Elmqvist T, Guntenspergen G, James P, McIntyre NE, editors. Urban Ecology: Patterns, Processes, and Applications. Oxford: Oxford University Press; 2011.
  10. 10. Kegel B. Tiere in der Stadt: Eine Naturgeschichte. 1st ed. DuMont Buchverlag GmbH & Co. KG; 2013;21.
  11. 11. Douglas I, James P. Urban Ecology: An Introduction. 1 edition. Routledge; 2015.
  12. 12. Alberti M. Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol Evol. 2015;30: 114–126. pmid:25498964
  13. 13. Cook LM, Saccheri IJ. The peppered moth and industrial melanism: evolution of a natural selection case study. Heredity. 2013;110: 207–212. pmid:23211788
  14. 14. Hu Y, Cardoso GC. Which birds adjust the frequency of vocalizations in urban noise? Anim Behav. 2010/4;79: 863–867.
  15. 15. Schuster S, Zollinger SA, Lesku JA, Brumm H. On the evolution of noise-dependent vocal plasticity in birds. Biol Lett. 2012;8: 913–916. pmid:22977069
  16. 16. Endler JA. Some general comments on the evolution and design of animal communication systems. Philos Trans R Soc Lond B Biol Sci. 1993;340: 215–225. pmid:8101656
  17. 17. Rich C, Longcore T. Ecological Consequences of Artificial Night Lighting. Island Press; 2006.
  18. 18. Falchi F, Cinzano P, Duriscoe D, Kyba CCM, Elvidge CD, Baugh K, et al. The new world atlas of artificial night sky brightness. Sci Adv. 2016;2: e1600377. pmid:27386582
  19. 19. Navara KJ, Nelson RJ. The dark side of light at night: physiological, epidemiological, and ecological consequences. J Pineal Res. 2007;43: 215–224. pmid:17803517
  20. 20. MacGregor CJ, Pocock MJO, Fox R, Evans DM. Pollination by nocturnal Lepidoptera, and the effects of light pollution: a review. Ecol Entomol. 2015;40: 187–198. pmid:25914438
  21. 21. Longcore T, Aldern HL, Eggers JF, Flores S, Franco L, Hirshfield-Yamanishi E, et al. Tuning the white light spectrum of light emitting diode lamps to reduce attraction of nocturnal arthropods. Philos Trans R Soc Lond B Biol Sci. 2015;370. pmid:25780237
  22. 22. Viviani VR, Rocha MY, Hagen O. Fauna de besouros bioluminescentes (Coleoptera: Elateroidea: Lampyridae; Phengodidae, Elateridae) nos municípios de Campinas, Sorocaba-Votorantim e Rio Claro-Limeira (SP, Brasil): biodiversidade e influência da urbanização. Biota Neotrop. 2010;10: 103–116.
  23. 23. Ineichen S, Rüttimann B. Impact of artificial light on the distribution of the common European glow-worm, Lampyris noctiluca (Coleoptera: Lampyridae). Lampyrid. 2012.
  24. 24. Picchi MS, Avolio L, Azzani L, Brombin O, Camerini G. Fireflies and land use in an urban landscape: the case of Luciola italica L. (Coleoptera: Lampyridae) in the city of Turin. J Insect Conserv. Springer Netherlands; 2013;17: 797–805.
  25. 25. Merritt DJ, Clarke AK. The impact of cave lighting on the bioluminescent display of the Tasmanian glow-worm Arachnocampa tasmaniensis. J Insect Conserv. Springer Netherlands; 2013;17: 147–153.
  26. 26. Bird S, Parker J. Low levels of light pollution may block the ability of male glow-worms (Lampyris noctiluca L.) to locate females. J Insect Conserv. Springer International Publishing; 2014;18: 737–743.
  27. 27. Hagen O, Santos RM, Schlindwein MN, Viviani VR. Artificial night lighting reduces firefly (Coleoptera: Lampyridae) occurrence in Sorocaba, Brazil. AE. 2015;03: 24–32.
  28. 28. Firebaugh A, Haynes KJ. Experimental tests of light-pollution impacts on nocturnal insect courtship and dispersal. Oecologia. 2016; pmid:27646716
  29. 29. Oba Y, Schultz DT. Eco-evo bioluminescence on land and in the sea. Adv Biochem Eng Biotechnol. 2014;144: 3–36. pmid:25084993
  30. 30. Meyer-Rochow VB. Glowworms: a review of Arachnocampa spp. and kin. Luminescence. 2007;22: 251–265. pmid:17285566
  31. 31. Lloyd JE. Bioluminescent Communication in Insects. Annu Rev Entomol. Annual Reviews; 1971;16: 97–122.
  32. 32. Kundrata R, Bocakova M, Bocak L. The comprehensive phylogeny of the superfamily Elateroidea (Coleoptera: Elateriformia). Mol Phylogenet Evol. 2014;76: 162–171. pmid:24680915
  33. 33. Jeng ML. The firefly legacy. Science Development. 2013;18–27 (in Chinese).
  34. 34. Lewis SM, Cratsley CK. Flash signal evolution, mate choice, and predation in fireflies. Annu Rev Entomol. 2008;53: 293–321. pmid:17877452
  35. 35. Lewis SM. Bioluminescence and sexual signaling in fireflies. In: Meyer-Rochow VB, editor. Bioluminescence in focus: a collection of illuminating essays. Kerala, India: Research Signpost; 2009.
  36. 36. Buck JB. Studies on the Firefly. I. The Effects of Light and Other Agents on Flashing in Photinus pyralis, with Special Reference to Periodicity and Diurnal Rhythm. Physiol Zool.; 1937;10: 45–58.
  37. 37. Dreisig H. Environmental control of the daily onset of luminescent activity in glowworms and fireflies (Coleoptera: Lampyridae). Oecologia. Springer-Verlag; 1975;18: 85–99.
  38. 38. Martin GJ, Lord NP, Branham MA, Bybee SM. Review of the firefly visual system (Coleoptera: Lampyridae) and evolution of the opsin genes underlying color vision. Org Divers Evol. Springer Berlin Heidelberg; 2015;15: 513–526.
  39. 39. Sander SE, Hall DW. Variation in opsin genes correlates with signalling ecology in North American fireflies. Mol Ecol. 2015;24: 4679–4696. pmid:26289828
  40. 40. Lall AB, Chapman RM, Ovid Trouth C, Holloway JA. Spectral mechanisms of the compound eye in the firefly Photinus pyralis (Coleoptera: Lampyridae). J Comp Physiol. Springer-Verlag; 1980;135: 21–27.
  41. 41. Seliger HH, Lall AB, Lloyd JE, Biggley WH. The colors of firefly bioluminescence—I. Optimization model. Photochem Photobiol. Blackwell Publishing Ltd; 1982;36: 673–680.
  42. 42. Cronin TW, Järvilehto M, Weckström M, Lall AB. Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae). J Comp Physiol A. 2000;186: 1–12. pmid:10659037
  43. 43. Oba Y, Kainuma T. Diel changes in the expression of long wavelength-sensitive and ultraviolet-sensitive opsin genes in the Japanese firefly, Luciola cruciata. Gene. Elsevier B.V; 2009;436: 66–70.
  44. 44. Lall AB, Lord ET, Ovid Trouth C. Vision in the firefly Photuris lucicrescens (Coleoptera: Lampyridae): Spectral sensitivity and selective adaptation in the compound eye. J Comp Physiol. Springer-Verlag; 1982;147: 195–200.
  45. 45. Lall AB, Strother GK, Cronin TW, Seliger HH. Modification of spectral sensitivities by screening pigments in the compound eyes of twilight-active fireflies (Coleoptera: Lampyridae). J Comp Physiol A. 1988;162: 23–33. pmid:3351784
  46. 46. Booth D, Stewart AJA, Osorio D. Colour vision in the glow-worm Lampyris noctiluca (L.) (Coleoptera: Lampyridae): evidence for a green-blue chromatic mechanism. J Exp Biol. 2004;207: 2373–2378. pmid:15184509
  47. 47. Lau TFS, Ohba N, Arikawa K, Meyer-Rochow VB. Sexual dimorphism in the compound eye of Rhagophthalmus ohbai (Coleoptera: Rhagophthalmidae): II. Physiology and function of the eye of the male. J Asia-Pacific Entomol. 2007;10(1): 27–31.
  48. 48. Kirschfeld K, Feiler R, Franceschini N. A Photostable Pigment within the Rhabdomere of Fly Photoreceptors No. 7. J Comp Physiol. 1978;125: 275–284.
  49. 49. Lall AB. Action spectra for the initiation of bioluminescent flashing activity in males of twilight-active firefly Photinus scintillans (Coleoptera: Lampyridae). J Insect Physiol. Elsevier Ltd; 1993;39: 123–127.
  50. 50. Lall AB. Spectral cues for the regulation of bioluminescent flashing activity in the males of twilight-active firefly Photinus scintillans (Coleoptera: Lampyridae) in nature. J Insect Physiol. Elsevier Ltd; 1994;40: 359–363.
  51. 51. Lall AB, Worthy KM. Action spectra of the female’s response in the firefly Photinus pyralis (Coleoptera: Lampyridae): evidence for an achromatic detection of the bioluminescent optical signal. J Insect Physiol. 2000;46: 965–968. pmid:10802109
  52. 52. Mills R, Popple J-A, Veidt M, Merritt DJ. Detection of light and vibration modulates bioluminescence intensity in the glowworm, Arachnocampa flava. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2016;202: 313–327. pmid:26897608
  53. 53. Fu X, Ballantyne LA, Lambkin CL. Aquatica Gen. Nov. From Mainland China With A Description Of Aquatica Wuhana Sp. Nov. (Coleoptera: Lampyridae: Luciolinae). Zootaxa. 2010;2530(2530).
  54. 54. Ho J-Z, Chiang P-H, Wu C-H, Yang P-S. Life cycle of the aquatic firefly Luciola ficta (Coleoptera: Lampyridae). J Asia Pac Entomol. 2010/9;13: 189–196.
  55. 55. Wu C, Yang P, Jeng M, Ho J, Chen H, Tsai J. Habitat restoration of the Aquatic firefly, Aquatica ficta (Olivier, 1909) restoration in Taipei city, Taiwan [Internet]. The International Firefly Symposium 2014; 2014 Aug 14; Gainesville, FL.
  56. 56. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. 2014.
  57. 57. Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software 2015;67(1): 1–48.
  58. 58. Stanger-Hall KF, Lloyd JE. Flash signal evolution in Photinus fireflies: character displacement and signal exploitation in a visual communication system. Evolution. 2015;69: 666–682. pmid:25627920
  59. 59. Branham MA, Greenfield MD. Flashing males win mate success. Nature. Nature Publishing Group; 1996;381: 745–746.
  60. 60. Michaelidis CI, Demary KC, Lewis SM. Male courtship signals and female signal assessment in Photinus greeni fireflies. Behav Ecol. 2006;17: 329–335.
  61. 61. Cratsley CK. Sexual selection in Photinus fireflies. Lewis SM, editor. PhD, Tufts. 2000.
  62. 62. Cratsley CK, Lewis SM. Female preference for male courtship flashes in Photinus ignitus fireflies. Behav Ecol. 2003;14: 135–140.
  63. 63. Hall DW, Sander SE, Pallansch JC, Stanger-Hall KF. The evolution of adult light emission color in North American fireflies. Evolution. 2016;70: 2033–2048. pmid:27412777
  64. 64. Sharkey EK, South A, Moosman PR, Cratsley CK, Lewis SM. Assessing Condition-dependence of Male Flash Signals in Photinus Fireflies. J Insect Behav. Springer Science & Business Media; 2010;23: 215–225.
  65. 65. Moosman PR, Cratsley CK, Lehto SD, Thomas HH. Do courtship flashes of fireflies (Coleoptera: Lampyridae) serve as aposematic signals to insectivorous bats? Anim Behav. 2009;78: 1019–1025.
  66. 66. Long SM, Lewis S, Jean-Louis L, Ramos G, Richmond J, Jakob EM. Firefly flashing and jumping spider predation. Anim Behav. 2012;83: 81–86.
  67. 67. Vencl FV, Carlson AD. Proximate Mechanisms of Sexual Selection in the Firefly Photinus pyralis (Coleoptera: Lampyridae). J Insect Behav. Kluwer Academic Publishers-Plenum Publishers; 1998;11: 191–207.
  68. 68. Case JF. Flight Studies on Photic Communication by the Firefly Photinus pyralis. Integr Comp Biol. Society for Integrative and Comparative Biology; 2004;44: 250–258.
  69. 69. Woods WA Jr, Hendrickson H, Mason J, Lewis SM. Energy and Predation Costs of Firefly Courtship Signals. Am Nat. The University of Chicago Press; 2007; pmid:17926292
  70. 70. Goh K-S, Li C-W. A Photocytes-Associated Fatty Acid-Binding Protein from the Light Organ of Adult Taiwanese Firefly, Luciola cerata. PLoS One. Public Library of Science; 2011;6: e29576.
  71. 71. Eguchi E, Nemoto A, Meyer-Rochow VB, Ohba N. A comparative study of spectral sensitivity curves in three diurnal and eight nocturnal species of Japanese fireflies. J Insect Physiol. 1984;30: 607–612.
  72. 72. Elvidge CD, Keith DM, Tuttle BT, Baugh KE. Spectral identification of lighting type and character. Sensors. 2010;10: 3961–3988. pmid:22319336
  73. 73. Demary K, Michaelidis CI, Lewis SM. Firefly Courtship: Behavioral and Morphological Predictors of Male Mating Success in Photinus greeni. Ethology. Blackwell Verlag, GmbH; 2005;112: 485–492.