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

RESEARCH ARTICLE Short- and mid-wavelength artificial light influences the flash signals of Aquatica ficta fireflies (Coleoptera: Lampyridae) Avalon Celeste Stevahn Owens1, Victor Benno Meyer-Rochow2,3, En-Cheng Yang4* 1 Department of Biology, Tufts University, Medford, Massachusetts, United States of America, 2 Department of Genetics and Physiology, Oulu University, Oulu, Finland, 3 Research Institute of Luminous Organisms, Tokyo, Japan, 4 Department of Entomology, National Taiwan University, Taipei, Taiwan a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Owens ACS, Meyer-Rochow VB, Yang EC (2018) Short- and mid-wavelength artificial light influences the flash signals of Aquatica ficta fireflies (Coleoptera: Lampyridae). PLoS ONE 13(2): e0191576. https://doi.org/10.1371/journal. pone.0191576 Editor: Christian Wegener, Biocenter, Universität Würzburg, GERMANY Received: May 19, 2017 Accepted: January 8, 2018 Published: February 7, 2018 * 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. Copyright: © 2018 Owens et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Dryad DOI: 10.5061/ dryad.73qg8. Funding: Funding for firefly research provided to National Taiwan University by the Friends of Da’an Forest Park Foundation (http://www. daanforestpark.org.tw/ - grant number: FD97011). Some funding was allocated to ECY’s laboratory, and used by ECY and ACSO to purchase experimental equipment. The funders had no role in study design, data collection and analysis, 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 [3–6]. However, many species manage to survive and even thrive in urban centers, despite these myriad threats [7–10]. 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 PLOS ONE | https://doi.org/10.1371/journal.pone.0191576 February 7, 2018 1 / 14 Fireflies flash more brightly in illuminated environs decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. 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 [22– 28]. 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 [33–35]. 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 [40–43]. Short-wavelength-sensitive (SWS) opsins have yet to be found, although blue sensitivit (...truncated)