Effects of artificial light on growth, development, and dispersal of two North American fireflies (Coleoptera: Lampyridae)

https://doi.org/10.1016/j.jinsphys.2021.104200Get rights and content

Highlights

  • We studied how artificial light affects immature firefly development and dispersal.

  • In general, firefly eggs, larvae and pupae were not affected by dim light at night.

  • However, early-instar Photuris larvae gained body mass more quickly when lit.

  • Late-instar Photuris larvae burrow down to escape light instead of dispersing away.

  • This escape behavior may have downstream consequences for the fitness of adults.

Abstract

Holometabolous insects exhibit complex life cycles in which both morphology and ecological niche change dramatically during development. In the larval stage, many insects have soft, slow-moving bodies and poor vision, limiting their ability to respond to environmental threats. Artificial light at night (ALAN) is an environmental perturbation known to severely impact the fitness of adult insects by disrupting both temporal and spatial orientation. The impact of ALAN on earlier life stages, however, is largely unknown. We conducted a series of laboratory experiments to investigate how two distinct forms of ALAN affect the development and movement of immature Photuris sp. and Photinus obscurellus fireflies. Although long-term exposure to dim light at night (dLAN), akin to urban skyglow, did not impact overall survivorship or duration of egg, larval, and pupal stages in either species, it did accelerate weight gain in early-instar Photuris larvae. Late-instar Photuris exposed to point sources of ALAN at the start of their nightly foraging period were also significantly more likely to burrow beneath the soil surface, rather than disperse across it. ALAN may therefore impede dispersal of firefly larvae away from illuminated areas, which could have downstream consequences for the reproductive fitness of adults.

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.

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