See and be seen: Understanding trade-offs in bioluminescent signalling and how it is affected by artificial lighting at night

Almost all animals are sensitive to their light environment. They use light for diverse functions including entraining their biological rhythms and vision. Consequently, any alteration to light levels within the environment has potentially enormous consequences for animals, shifting activity cycles and affecting vision. Even if animals can adapt rapidly to such profound changes to their environment, they may still incur severe costs because they cannot fully compensate. For instance, the presence of bright light in formerly dark environments may disrupt the activity and sleep patterns of animals.

Humans have dramatically altered the light regimes in the environment through the introduction of artificial lighting at night (ALAN), which is now present across vast areas of the planet. The most prevalent form of ALAN is road lighting, which proliferates as road networks expand. Satellite images of the Earth at night attest to the extent of road lighting across much of the planet. Indeed, the newest LED street lighting means that ALAN is cheaper and more energy efficient than ever before, promoting widespread adoption. These LED lights are brighter and whiter than ever before, quite different from the orange sodium lamps they replace. Yet the presence of ALAN disturbs nocturnal animals, potentially displacing them to darker 'refuge' habitats. Moreover, day-active animals may extend their activity into the night, creating additional pressures on nocturnal species. Although it is clear that ALAN affects the activity patterns of animals, there is little understanding of the mechanisms by which their behaviour and physiology is altered, or of larger scale effects upon populations.

Our aim is to understand how ALAN affects animals at the behavioural, physiological, and population levels. We will use glow worms as an indicator species, a proverbial 'canary in the mine'.

Our choice of indicator species is determined by their unique mating behaviour in which flightless female glow worms generate a bioluminescent glow in their abdomen that attracts males, which fly to them to mate. Our strategy will be to exploit this mating behaviour to quantify the effects of ALAN upon glow worms. Our data indicate that these effects are likely to be severe because female glowing consumes substantial amounts of energy that cannot be replenished because they do not feed as adults. Our preliminary data also show that far fewer males are attracted to females when they are illuminated by artificial lighting, so females glowing under ALAN use valuable energy for little benefit. Moreover, lighting along roads may act as a barrier by preventing males from dispersing through the environment to find females, affecting the structure and ultimately the survival of glow worm populations.

We will use a combination of laboratory and field experiments to directly test hypotheses about the effects of ALAN upon glow worm reproduction. We will couple this with assessing the genetic structure of glow worm populations to determine how fragmented they have become already. We will then use statistical and modelling techniques to map the distribution of populations, the gene flow among them, and the presence of ALAN at both the local and broader scales. By doing so, we will identify the mechanistic cause of the effect of ALAN upon glow worm biology, with potentially broad implications for other nocturnal animals. We will also explicitly test the hypothesis that ALAN has had, and continues to have, a severe impact upon glow worm populations, potentially isolating them and driving them to extinction. By maintaining close links with policy makers and nature conservation practitioners throughout (see Pathways to Impact), our project has the potential to inform policy around ALAN and the extent to which its effects on wildlife can be mitigated.

Artificial lighting at night (ALAN) is now present across large areas of the planet primarily because of the illumination of roads and buildings. Changes in the photic environment caused by ALAN are a form of environmental disturbance displacing nocturnal animals to darker 'refuge' habitats. Moreover, by allowing diurnal animals to extend activity into the night, they create additional pressures on nocturnal species. Although spatial and temporal displacement caused by ALAN has been documented, there is little understanding of its impacts upon the basic biology of most animals, or of the larger scale effects upon populations. Our aim is to understand how ALAN affects animals at the behavioural, physiological, population and ecological levels, using glow worms as an indicator species, a proverbial 'canary in the mine'. Our preliminary data suggest that the effects of ALAN upon glow worms may be severe because metabolic costs of glowing are high but females attract significantly fewer males when illuminated by artificial lighting. Yet females continue to invest in signalling even in brightly lit environments, potentially robbing them of valuable energy that must be diverted from reproduction. Moreover, national survey data suggest that glow worm populations are fragmentary, raising the prospect that roadside lighting may act as a barrier to dispersal affecting the structure of populations and their ultimate survival. We will use a unique combination of laboratory and field experiments coupled with establishing the genetic population structure and spatial modelling to quantify the impact of ALAN upon the fundamental biology of glow worms at the local and national scales. Using these techniques we will test the hypothesis that ALAN has a severe impact upon glow worm populations, potentially isolating them and driving them to extinction. By doing so, we will provide a unique data set that will have impacts for both academics and policy makers (see Pathways to Impact).

1. Academic Community: We envisage that our findings will have broad impact upon the academic community. Our experiments will yield data of significance for academics studying the impact of artificial lighting at night (ALAN) upon the behaviour of nocturnal species. By quantifying the energy consumption of physiological tissues and processes, including male photoreceptors, we will produce insights of value to physiologists and visual neuroscientists. Additionally, the data we obtain during the grant will provide new physiological insights into the trade-offs governing investment in mating and reproductive effort, expanding the influence of our project to behavioural ecologists. Our findings will also provide insights into the genetic structure of insect populations, and how gene flow is affected by differential movement of males and females, which will be of significance for population geneticists. Moreover, by assessing the impact of manmade barriers upon populations, we will provide data of relevance for conservation scientists. We will disseminate our findings in peer-reviewed journals and at scientific conferences to ensure we reach a broad audience (see Academic Beneficiaries). The project will contribute to capacity building by exposing the PDRA to multidisciplinary approaches and training in numerous techniques including in vivo intracellular electrophysiology, statistical modelling and GIS, histology, metabolic rate analysis.

2. Policy: A key part of the impact will be to engage with policy makers at both the local and national levels. At the local level, we will make use of the position of our sites within the South Downs National Park and the UNESCO Brighton & Lewes Downs Biosphere and through a local NGO, the Sussex Wildlife Trust, to link to local policy makers (see Letters of Support). We have already made links to the local council through these organisations. We will engage with these organisations throughout the duration of the grant and beyond. At the national level, we will work with Natural England, Buglife and a major land owner, the National Trust (see Letters of Support). Our links with these organisations will allow us to advertise the project, and to engage with policy makers and the public. Where possible, we will focus on the means of mitigating the impacts of ALAN on glow worms through relatively simple interventions, such as extinguishing unnecessary lighting that does not impact on public safety.

3. Public Outreach: There is broad public interest in glow worms with numerous amateur groups meeting across the country each summer to find glowing females. We will harness this interest by developing an app on which sightings of glowing females can be recorded and uploaded to a national database as part of a citizen science project (see Pathways to Impact), as well as through workshops/outreach events. We have already piloted an event during National Insect Week 2018 taking members of the public onto the South Downs to find glow worms. Using this as our template, we will repeat these outreach events in which we will instruct members of the public on monitoring populations by capturing males as well as finding glowing females. We have also requested funds to make artificial lures for males that we will supply to entomology groups across the country (see Pathways to Impact). We will use already established links to many such groups through the Amateur Entomological Society and Sussex Wildlife Trust to advertise these events. Locally, we will discuss our work and findings at Café Scientifique and the Brighton Science Festival. We will also make use of university contacts to visit local schools to talk about our research and findings. Finally, we will also make use of our contacts within the media to reach a wide audience. These links are very effective as demonstrated by the experiments we performed to obtain preliminary data for this application being televised on BBC Countryfile Diaries.