Spotlight on fish: Light pollution affects circadian rhythms of European perch but does not cause stress
Introduction
Recent decades have seen a profound transformation of nightscapes, with an increasing proportion of the Earth's surface being illuminated at night. Global light emissions increased at a rate of around 3–6% per year in recent decades (Hölker et al., 2010a). This substantial transformation demonstrates a pressing need to understand the effects of artificial light at night on biological processes. In particular, information regarding the ecological impact of light pollution on animal populations and whole ecosystems is crucial. Possible consequences of artificial light at night on many behavioural and physiological processes in various classes of animals have been reviewed recently (Gaston et al., 2013, Hölker et al., 2010b, Navara and Nelson, 2007). Most of these processes are coupled to circadian or seasonal rhythms (Falcón et al., 2003) which may be disrupted by light pollution.
In fish, seasonal rhythms include reproduction, growth and development, and migration, while patterns like locomotor activity, food intake, shoaling or diel vertical migration are mainly driven by circadian rhythms (Boeuf and Le Bail, 1999, Downing and Litvak, 2002, Duston and Bromage, 1986, Lowe, 1952, Mehner, 2012, Ryer and Olla, 1998, Vowles et al., 2014). The most important mechanism of the circadian system in vertebrates is the light-dependent production of melatonin (production at night, suppression during the day) by the pineal organ. The pineal organ of fish is light-sensitive and directly processes photoperiodic information, resulting in a circadian melatonin rhythm that provides periodic information for cells and organs, such as time of the day and season (Ekstrzm and Meissl, 1997, Falcón and Collin, 1989, Kulczykowska et al., 2010, Underwood and Goldman, 1987).
The influence of artificial light at night on fish has been an area of interest for researchers with respect to aquaculture, e.g., how to control growth (Biswas et al., 2005, Boeuf and Le Bail, 1999, Kissil et al., 2001), development (Porter et al., 1998, Thrush et al., 1994) and reproduction (Kissil et al., 2001). However, while photoperiod manipulation has proven beneficial for aquaculture, artificial light can have detrimental effects in nature.
Most studies that investigated the influence of artificial light at night on the melatonin rhythm used high light intensities above 100 lx and only a few studies using low light intensities (Bayarri et al., 2002, Migaud et al., 2006a, Takemura et al., 2006), which may occur in light polluted urban areas. However, none of these studies addressed the possible effect of artificial light at night on the physiology of fish and very little is known about dose–response relationships for a range of biological impacts (Gaston et al., in press).
Cortisol is the most measured indicator for stress in fish. Moreover, two of the major actions of cortisol in fish are hydromineral balance (e.g., seawater adaption in migratory fish) and energy metabolism (carbohydrate, protein, lipid metabolism).
In most fish species, blood levels of cortisol also exhibit a circadian rhythm. However this rhythm is species specific, subjected to seasonal influences and affected by other environmental cues (Wendelaar Bonga, 1997). In goldfish (Carassius auratus) for instance, the schedule is linked to the photoperiod and peak titres occur around light onset, minimum titres at light offset (Noeske and Spieler, 1983). In humans this pattern is called the cortisol awakening response (Kirschbaum et al., 2000) and was also found in Nile tilapia (Oreochromis mossambicus) (Binuramesh and Michael, 2011). However, in goldfish the feeding schedule can override photoperiod to trigger circadian serum-cortisol variations (Spieler and Noeske, 1984). In some salmonids, cortisol peaks were found during the dark phase of the photoperiod but also connected to feeding time (Laidley and Leatherland, 1988, Pickering and Pottinger, 1983), whereas in sticklebacks (Gasterosteus aculeatus) no circadian rhythm could be identified (Audet et al., 1986).
Previous studies regarding the effect of light at night on cortisol levels revealed no obvious impact. But most studies were working with prolonged or continuous photoperiods and relatively high light intensities. Biswas et al., 2006, Biswas et al., 2008 for example tested a constant illumination of 1500 lx on red sea bream (Pagrus major) and striped knifejaw (Oplegnathus fasciatus), but cortisol concentrations showed no significant differences to normal photoperiods. Bluefin tuna (Thunnus orientalis) showed no changes of circadian cortisol levels when subjected to 5, 15 or 150 lx compared to a 0 lx control (Honryo et al., 2013). However, the invasive sampling procedures (blood or whole body sampling) in the abovementioned examples may have introduced a sampling artefact that obscured potential differences in the stress response between treatments. The dynamics of the stress response to handling stress associated with surgical sampling methods cannot be generalized and seems to be highly species specific ranging from a few minutes (Ramsay et al., 2009) to one or several hours (Wendelaar Bonga, 1997). However, with a non-invasive sampling method, existing differences in cortisol rhythms in response to artificial light at night might be uncovered.
Our study presents data on the influence of artificial light at night on circadian rhythm and stress response of European perch (Perca fluviatilis). Perch belong to the most dominant fish species in Central European aquatic systems and inhabit a wide range of habitats, including all types of lakes and most streams (Kottelat and Freyhof, 2007). Perch are diurnal feeders and become inactive during the night, especially in the presence of nocturnal predators (Hölker et al., 2007).
We measured melatonin concentrations to assess the influence of light on the biological rhythms of perch. Cortisol was measured to evaluate the stress response to light pollution. In contrast to earlier studies, we based our results exclusively on non-invasive measurements, by extracting the hormones from water samples taken without disturbing the experimental animals and determined their concentrations. Ellis et al. (2004) proved a correlation between concentrations of cortisol in water and serum in rainbow trout (Oncorhynchus mykiss) with a phase delay of about 2 h due to excretion route and accumulation in the water. The work of Ellis et al. (2005) indicated a similar correlation for melatonin.
We hypothesised that artificial light at night has a clear effect on the natural circadian rhythm of melatonin production. We expected that with increasing light intensity, the nocturnal melatonin production is suppressed. Furthermore, we hypothesised a stress response caused by the presence of artificial light at night. Using non-invasive methods we expected to identify an increase in cortisol concentrations corresponding to increasing light intensity, especially during the dark phase of the photoperiod.
Section snippets
Experimental fish
European perch were taken from an existing population at the Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB) in Berlin, Germany. They were originally obtained from the nearby Lake Müggelsee that has a periurban surrounding including forests and housing. Prior to the experiment they were held in 600 L indoor tanks in a flow-through system with ground water, aeration and natural photoperiod and fed daily with frozen red bloodworms. Body mass of the fish at the time of the
Results
There were significant differences in melatonin tank water concentrations between the control (0 lx treatment) and all treatments (LMM treatment effect: F3 = 339.9; p = 0.000, Posthoc test Sidak: df 216; p ≤ 0.05) with melatonin concentration being up to three times higher in controls compared to light treatments (Fig. 1). 1 lx illumination was likewise significantly different to all other treatments and the control (LMM, Sidak). Control fish produced more melatonin over the 24 h sampling period and
Discussion
This study demonstrated that artificial light illuminating the water at night had a strong effect on the rhythm of melatonin production in European perch. Even at low light intensities of 1 lx, which is slightly brighter than the light produced by a full moon, there was already a substantial decrease of melatonin secretion. Fish in treatments with higher light intensities seemed to completely lack any circadian melatonin rhythm. Moreover, melatonin concentration in the water of the control tank
Conclusion
We found a strong effect of artificial light at night on the melatonin rhythm which leads us to conclude that light pollution in urban waters at realistic light levels has significant potential to inhibit circadian melatonin patterns. Considering the main task of melatonin-mediating between the current photoperiod and the different circadian and seasonal rhythms in a fish's life — it is likely that these rhythms will be altered too. Although light pollution is not yet measured consistently in
Acknowledgements
The authors thank T. Mehner, Alex Lumsdon and D. Murray for the helpful comments on the manuscript and M. Kunow and the students at the Leibniz-Institute of Freshwater Ecology and Inland Fisheries for the technical support. Funding was provided by the Verlust der Nacht project (Federal Ministry of Education and Research, Germany, BMBF-033L038A).
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