Effects of artificial light on growth, development, and dispersal of two North American fireflies (Coleoptera: Lampyridae)
Graphical abstract
Introduction
Artificial light at night (ALAN), often referred to as light pollution, is an increasingly prominent disruption to both urban and rural ecosystems (Falchi et al., 2016, Gaston et al., 2015, Guetté et al., 2018/7., Kyba, 2018) recently recognized as an emerging threat to global biodiversity (Davies and Smyth, 2017, Hölker et al., 2010, Koen et al., 2018, Rich and Longcore, 2006). ALAN can impact insects in myriad ways (Desouhant et al., 2019, Grubisic et al., 2018, Owens et al., 2019, Owens and Lewis, 2018), most dramatically by accelerating, decelerating, or otherwise altering the course of their development, and by influencing their movements throughout a landscape.
ALAN can interfere with insect development in two ways: either by directly inhibiting or promoting certain nocturnal or diurnal activities, primarily foraging and feeding (Farnworth et al., 2018), or by interfering with circadian, circamensual, and circannual rhythms of activity and maturation. Most insects use changes in the intensity and spectra of ambient light at dawn and dusk as cues to entrain their biological rhythms to the outside world (Lall, 1994, Saunders, 2012). Previous research into the developmental importance of these rhythms has uncovered numerous fitness impacts of asynchrony (Kouser et al., 2014, Saunders and Cymborowski, 2008, Xu et al., 2011), often induced via laboratory exposure to constant light.
More recently, researchers interested in the developmental consequences of artificial light per se have begun explore the impacts of dim artificial light at night (dLAN) layered on top of a standard day-night cycle. dLAN more closely imitates skyglow, a pervasive disturbance to both urban and suburban habitats (Jechow and Hölker, 2019, Kyba and Hölker, 2013), and appears to be perceived by insects as a lengthened twilight (Kim et al., 2017). Over time, it can interfere with detection of seasonal changes in daylength, disrupting photoperiodic as well as circadian processes (Meuti and Denlinger, 2013, Sanders et al., 2015, Saunders, 2013, Schroer et al., 2019). Recent studies on a range of rapidly developing animals have found accelerated development under dLAN to be associated with alternately smaller (Dananay and Benard, 2018, van Geffen et al., 2014, Willmott et al., 2018) or larger (O’Connor et al., 2019) adults, and delayed development under dLAN associated with smaller (Luarte et al., 2016) or larger (Durrant et al., 2018) adults as well.
Point sources of ALAN have been repeatedly demonstrated to alter the distribution of insects in a landscape (e.g. Šustek, 1999, Perkin et al., 2014, Davies et al., 2015, Degen et al., 2016, Macgregor et al., 2017, Manfrin et al., 2017, Manríquez et al., 2019). If the fitness of larval and/or adult insects is negatively affected by ALAN, they might be predicted to disperse away from lit areas toward more suitable habitat. However, while some insect taxa do avoid lit areas (e.g. Wertman et al., 2018, Farnworth et al., 2018, Thomas et al., 2016, van Geffen et al., 2015), for reasons unknown a significant proportion instead direct their movements toward artificial light sources (Donners et al., 2018). While we currently lack a conceptual framework for understanding the remarkably diverse impacts of ALAN on both the development and movement of insects, studies on a broader range of taxa and developmental stages can help to bridge this gap.
Bioluminescent firefly beetles have a complex relationship to light. Like many other nocturnal insects, adult fireflies use circadian changes in the intensity and spectra of ambient light to time their nightly courtship activities (Dreisig, 1975, Lall, 1994). But unlike the vast majority of terrestrial organisms (Oba and Schultz, 2014), fireflies communicate using light of their own making, the product of an enzymatic oxidation reaction that is housed in their abdominal lanterns. Firefly bioluminescence can serve both as an aposematic warning signal and as a courtship advertisement (Branham and Wenzel, 2003, Leavell et al., 2018, Lloyd, 2008), and may be inhibited or obscured by ALAN. Previous research has shown that ALAN impacts the behavior, movement, and reproductive fitness of firefly adults (Firebaugh and Haynes, 2018, Owens and Lewis, 2018). Yet the impact of ALAN on other firefly life stages, all of which bioluminesce, remains almost entirely unexplored (but see Wanjiru Mbugua et al., 2019, Murphy and Moiseff, 2020).
Among North American fireflies the adult stage lasts only two to six weeks (Lloyd, 2008), during which time females are thought to be mostly stationary (Lewis and Wang, 1991). In many species most dispersal may take place during the larval stage, which can last up to two years. However, we know of no studies assessing the impact of any environmental threat on either the development or movement of larvae of any North American firefly species (but see Lee et al., 2008, Kakehashi et al., 2014, Wanjiru Mbugua et al., 2019), despite the indisputable importance of this information in determining whether a population is likely to persist (Crouse et al., 1987, Schultz et al., 2019).
In this study, we conducted a series of laboratory experiments on larvae of two North American fireflies to explore the impact of long-term exposure to dLAN on the fitness of juvenile fireflies, measuring their survivorship, the durations of egg, larval, and pupal stages, and larval growth. We also tested whether larvae moved toward or away from point sources of artificial light, as this behavior could determine the fate of firefly populations in light polluted habitats.
Section snippets
Study organisms
Female fireflies in the genus Photuris oviposit in soil or leaf litter (McLean et al., 1972); newly hatched Photuris larvae burrow into the soil, where they develop over the next few months to several years (Faust, 2017, Lewis, 2016, Lloyd, 2018). On suitably warm and wet evenings, however, Photuris larvae are often found scavenging on the soil surface (Keiper and Solomon, 1972, McLean et al., 1972, Williams, 1917). Fully grown larvae typically pupate in early summer, and eclose within
Effects of dLAN on egg development time and hatching success
On average, Photuris eggs hatched after a minimum of 12.0 ± 1.9 days (n = 123); as the exact oviposition date is unknown, this figure is likely an underestimate. P. obscurellus eggs hatched after 18.8 ± 3.2 days (n = 546) across light treatments. Duration of the egg stage did not differ significantly among the dark control, the 12/12 control, or the dLAN treatment in either Photuris (Table 1; one-way ANOVA, Poisson distribution; light treatment: LR χ2 = 0.92, df = 2, P = 0.6326) or P.
Discussion
Artificial light at night threatens nocturnal insects (Owens et al., 2019, Owens and Lewis, 2018), and species with bioluminescent signals may be especially at risk (Lewis et al., 2020, Owens and Lewis, 2018, Reed et al., 2019). The impact of ALAN on adult insects is often markedly different than that on their larval forms (e.g. increased predation rates on adult moths but not moth caterpillars: Bailey et al., 2019, Cravens et al., 2017, Grenis et al., 2015). However, despite pronounced
CRediT authorship contribution statement
Avalon C.S. Owens: Conceptualization, Methodology, Investigation, Data curation, Formal analysis, Visualization, Writing - original draft, Writing - review & editing. Sara M. Lewis: Conceptualization, Methodology, Supervision, Resources, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We are grateful to many Tufts undergraduates for their help in larval rearing and data collection, including Annie Nguyen, Vaidehi Chotai, Rhémi Toth, Francisca Donkor, Brian Felter, Gabriel Yerdon, Alexandra Arsenault, and Caroline Dressler. Special thanks to Atticus Murphy for designing and executing the T-maze experiment. We also thank the Starks and Lewis joint lab meeting group for feedback on experimental design and data visualization.
References (86)
- et al.
The origin of photic behavior and the evolution of sexual communication in fireflies (Coleoptera: Lampyridae)
Cladistics
(2003) - et al.
Photons and foraging: artificial light at night generates avoidance behaviour in male, but not female, New Zealand weta
Environ. Pollut.
(2018) - et al.
Worldwide increase in Artificial Light At Night around protected areas and within biodiversity hotspots
Biol. Conserv.
(2018/7) Spectral cues for the regulation of bioluminescent flashing activity in the males of twilight-active firefly Photinus scintillans in nature
J. Insect Physiol.
(1994)- et al.
Light pollution reduces activity, food consumption and growth rates in a sandy beach invertebrate
Environ. Pollut.
(2016) - et al.
Live fast, die young: Behavioural and physiological impacts of light pollution on a marine fish during larval recruitment
Mar. Pollut. Bull.
(2019) Insect photoperiodism: measuring the night
J. Insect Physiol.
(2013)- et al.
The impact of streetlights on an aquatic invasive species: artificial light at night alters signal crayfish behaviour
Appl. Anim. Behav. Sci.
(2016) - et al.
The circadian clock interacts with metabolic physiology to influence reproductive fitness
Cell Metab.
(2011) - et al.
An experimental test of the allotonic frequency hypothesis to isolate the effects of light pollution on bat prey selection
Oecologia
(2019)