Elsevier

Environmental Pollution

Volume 274, 1 April 2021, 116585
Environmental Pollution

Artificial light at night (ALAN) affects the downstream movement behaviour of the critically endangered European eel, Anguilla anguilla

https://doi.org/10.1016/j.envpol.2021.116585Get rights and content

Highlights

  • An experiment assessed the impact of ALAN on a critically endangered fish.

  • Fish behaviour was affected by ALAN.

  • Individuals were less likely to select to pass an illuminated route when given the choice.

  • Individuals passed downstream faster when the illuminated route was selected.

Abstract

Artificial light at night (ALAN) is considered one of the most pervasive forms of environmental pollution. It is an emerging threat to freshwater biodiversity and can influence ecologically important behaviours of fish. The European eel (Anguilla anguilla) is a critically endangered catadromous species that migrates downstream to the ocean to spawn in the Sargasso Sea. Given the pervasive nature of ALAN, many eel will navigate through artificially lit routes during their seaward migration, and although considered negatively phototactic, their response has yet to be quantified. We investigated the response of downstream moving European eel to simulated ALAN using a Light Emitting Diode unit in an experimental flume. We presented two routes of passage under: (1) a dark control (both channels unlit), (2) low ALAN (treatment channel lit to ca. 5 lx), or (3) high ALAN (treatment channel lit to ca. 20 lx). Eel were: (i) more likely to reject an illuminated route when exposed to high levels of ALAN; (ii) less likely to select the illuminated channel when given a choice; and (iii) passed downstream more rapidly when the illuminated route was selected. This study quantified the response of the critically endangered European eel to ALAN under an experimental setting, providing the foundations for future field based research to validate these findings, and offering insight on the ecological impacts of this major environmental pollutant and driver of global change.

Introduction

The world has experienced rapid and wide-scale urbanisation in recent decades, with the percentage of the global population inhabiting urban areas predicted to grow from 30% in 1950 to 68% by 2050 (United Nations, 2018). This has resulted in dramatic modification of the natural environment, including increased artificial light at night (ALAN; e.g. from street lighting, vehicles, industry, and domestic sources), a factor that is now considered one of the most pervasive forms of environmental pollution (Falchi et al., 2016). More than 80% of the world’s population live under artificially illuminated skies (Falchi et al., 2016), and both the extent and brightness of the earth’s artificially lit surface continue to increase by more than 2% per year (Kyba et al., 2017). While this major driver of global environmental change (Davies and Smyth, 2017) may be convenient to modern society, allowing humans to remain safe and active at night, it also has wide-ranging unintended ecological consequences (summarised in recent reviews, e.g. Davies and Smyth, 2017; Gaston et al., 2015; Hopkins et al., 2018; Owens and Lewis, 2018). These include impacts to circadian rhythms (Kupprat et al., 2020), community composition (Garratt et al., 2019), foraging (Russ et al., 2015), predator avoidance (Wakefield et al., 2015), energy expenditure (Pulgar et al., 2019) and reproductive behaviour (Botha et al., 2017), development (Dominoni et al., 2018) and success (Fobert et al., 2019).

Humans have traditionally settled close to fresh water, driven by the provision of food and water supply and opportunities for transport of goods. More than 50% of the world’s population live within 3 km of a freshwater body (Kummu et al., 2011), and rivers in particular are focal points for major urbanisation (Ceola et al., 2015), especially in the lower reaches and estuaries, where they are heavily influenced by artificial light. Impacts may be direct, through emissions to the water surface from lighting along banks, at ports and harbours, bridges and other infrastructure, and vessels; and indirect, through scattering and reflection, resulting in skyglow (Jechow and Hölker, 2019). Although research is currently biased towards the ecological influences of ALAN in terrestrial environments, a small but growing body of evidence highlights negative impacts on freshwater taxa (Perkin et al., 2011), and light pollution is increasingly considered a major emerging threat to freshwater biodiversity (Reid et al., 2019).

Current evidence, for coastal and freshwater fishes at least, suggests ALAN may have several negative ecological consequences acting through modification of behaviour. For example, the nest-guarding activity of lake-dwelling smallmouth bass (Micropterus dolomieu) was elevated when exposed to both continuous low (1.8–3.4 lx) and intermittent high (10.2–58.2 lx) illumination, generated to simulate shoreline and automobile lighting, respectively (Foster et al., 2016). Such alterations to behaviour may increase the energetic cost associated with parental care and ultimately reduce reproductive success (Foster et al., 2016). In a laboratory tank-based study, the exposure of the Trinidadian guppy (Poecilia reticulata) to low levels of ALAN (ca. 0.5 lx), reflecting conditions more akin to skyglow, reduced their emergence time from cover (Kurvers et al., 2018). Faster emergence from cover and more time spent in open areas will likely increase individual risk (Kurvers et al., 2018), potentially compromising fitness. In another example, the abundance of small shoaling and large predatory fishes increased during nights when lights from a floating pontoon located in the lower (estuarine) reaches of a river were switched on (Becker et al., 2013). Attraction to light was presumed to be the result of enhanced foraging capabilities of both groups, highlighting the potential for ALAN to create unnatural top-down regulation of fish populations (Becker et al., 2013). These examples document alterations to the behaviour of fish while resident in freshwater and coastal environments. However, migratory (diadromous) species may be particularly exposed to light pollution as they must navigate between fresh and marine waters to complete their life-cycle.

The pervasive nature of ALAN in urbanised reaches of river through which diadromous fishes migrate means that individuals from most populations will encounter artificially illuminated conditions, possibly multiple times. Modified fish behaviour during migratory life-phases is therefore likely as they must react and/or adjust to spatial variations in light intensity. Indeed, illumination from street lights (14 lx) impacted the migratory behaviour of Atlantic salmon (Salmo salar), with juveniles (smolts) tending to be reluctant to move downstream during nights when lights were switched on during experimental manipulation, instead preferring to migrate the next morning (Riley et al., 2012). Avoiding passage through areas of ALAN may be logical as night-time migration of smolts is often considered a predator avoidance tactic. Indeed, in support of this there is evidence of elevated feeding on Pacific salmon smolts (Oncorhynchus spp.) by harbour seals (Phoca vitulina) at illuminated bridges at night (Yurk and Trites, 2000). Ultimately, however, the propensity for smolts to migrate the morning after exposure to ALAN may still result in elevated risk of predation from visual piscivores, negatively impacting overall survival (Riley et al., 2012). Despite some research on the impacts of ALAN on migratory salmonids, the effect of ALAN on the behaviour of other diadromous species is lacking.

The critically endangered European eel (Anguilla anguilla) is a diadromous fish of high conservation concern due to dramatic declines in recruitment (>98% in some parts of its range) over recent decades (ICES, 2019). Sexual maturation during the development to the silver phase occurs as eel migrate downstream, typically at night (between August and December), with peak numbers often reported under darker moonless conditions (Lowe, 1952; Vøllestad et al., 1986). During maturation, eel undergo morphological and physiological changes that include an increase in eye size (Pankhurst, 1982) and a shift in visual spectral sensitivity towards shorter wavelengths (Bowmaker et al., 2008). Furthermore, they become increasingly negatively phototactic (Lowe 1952), and as such their sensitivity to artificial light may be highest as the maturing fish approach the sea where the potential impacts of ALAN associated with urbanisation of coastal areas (e.g. cities, towns and ports) may be most severe. However, the nature and magnitude of the impact of artificial light pollution on the downstream movement of eel remains poorly understood.

This study investigated the influence of simulated ALAN on the response of downstream moving European eel when presented with a choice of two routes through an experimental flume under either (a) a dark control (both routes unlit), (b) low ALAN treatment (one route lit to ca. 5 lx) or (c) high ALAN treatment (one route lit to ca. 20 lx). We recorded (1) the initial response (reaction, route switch, rejection, no observable response) during the first approach to the entrance of the selected route, (2) the nature (treatment or control) of the route selected, and (3) the time taken to pass through the selected channel. If eel exhibited no observable preference for either route (H0) we would expect the selection of the test channel not to differ from 0.5. Likewise, if illumination had no effect on downstream passage, the time taken to pass either channel should not differ. We also investigated whether degree of sexual maturation influenced response to illumination (H0: nature of response is independent of degree of maturation).

Section snippets

Study fish and husbandry

Eel (n = 120, mean ± SD length and mass: 545 ± 88 mm, 319 ± 135 g) were captured in fyke nets installed in a drainage channel in the Lincolnshire Fens (UK) by a licenced fisherman and transported to the International Centre for Ecohydraulics Research (ICER) at the University of Southampton in aerated water on November 7, 2019. They were held in large tanks (ca. 1000 L) containing aerated and filtered water under ambient temperature (10.7 ± 0.5 °C) and photoperiod (9:15 h light:dark) and

Initial response

Eel typically exhibited no observable response (90.0%) when approaching the control channel, independent of treatment (Wald’s χ2 = 0.31, d.f. = 2, p = 0.855; Fig. 3) and degree of silvering (Wald’s χ2 = 1.73, d.f. = 1, p = 0.188). When approaching the treatment channel, initial response was influenced by light treatment (Wald’s χ2 = 7.43, d.f. = 2, p < 0.05), with a greater probability to react, switch route or reject during low (61.5%; p < 0.05) and high (52.9%; p < 0.05) ALAN compared to the

Discussion

When exposed to realistic levels of direct artificial light at night (ALAN) simulated by a broad-spectrum LED unit under an experimental setting, downstream moving European eel (Anguilla anguilla) tended to exhibit clear behavioural responses when approaching an illuminated route. Although the overall proportion of fish responding was greater under low ALAN, route switch and rejection (higher magnitude behaviours) were more prevalent under higher intensity conditions. Eel were more likely to

Conclusions

Our results demonstrate that realistic levels of direct ALAN, simulated using a LED unit under experimental settings, can influence the downstream movement behaviour of the critically endangered European eel. Given the consistent and pervasive nature of light pollution compared to natural variations in illumination, which are influenced by periodic lunar phases and stochastic weather (such as cloud cover), the unintended impacts on eel movement and migration may be large. We therefore recommend

Author contributions

ASV conceived the study and designed and performed the experiment. ASV conducted formal analysis of the data and drafted the original paper. PSK contributed to the writing, editing and critical review of the paper. Both authors agreed on the final version to be submitted.

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.

Acknowledgements

This work was funded by a Fisheries Society of the British Isles Research Grant awarded to ASV. The study was sanctioned by the University of Southampton Ethical Review Board. Thanks go to the ICER Team for assistance during the experimental period, and to Terry Smith for capture of the eels. Data published in this article are available from the University of Southampton repository at https://doi.org/10.5258/SOTON/D1724.

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