3.3.1. Prohibition to Kill Specimen of Protected Species
The prohibitory effect applies if light-sensitive specimen of protected species can be injured or killed. The application of ALAN situations to the prohibition is limited in scope due to three reasons. First, the prohibition to kill specimen of protected species covers only specific species (see Annex IV (a) Habitats Directive and § 7 para. 2 no. 13 BNatSchG). These include all bat species, European wild bird species and 41 butterfly species, but not nocturnal light-sensitive organisms per se. Among light-sensitive and threatened taxa are especially amphibians, bats, birds and nocturnal Lepidoptera [12
]. In our literature research we found only one paper that explores the effects on a specially protected species as listed in Annex IV (a) Habitats Directive (92/43/EEC) except for the studies on bats and wild birds. This study addresses the effects of illumination on an amphibian, the brown frog tadpoles (Rana temporaria
]. Two thirds of all the studies (202 articles) indicate severe impacts of ALAN on a very broad range of taxa, but these impacts are difficult to apply to the prohibition to kill or disturb specimen, because the tested organisms do not belong to the list of specially protected species.
Secondly, the killing risks need to be determined as significant. Significance is given if specimens are affected, which, because of their behavior, may be exposed to uncommon increased risks through the effects of the lighting system and if these risks cannot be prevented by mitigation measures [20
] (pp. 91 et seq.). The significant killing risks criterion requires knowledge of the community composition and the light-sensitivity of the species concerned; both can be hard to obtain [20
] (p. 98). The difficulty that arises under the Habitat Directive is similar. The act to be prohibited (e.g., the installation and the operation of a lighting system) has to be deliberate. This also requires knowledge of potentially affected protected species in the vicinity of the lighting system as well as knowledge of their sensitivity to ALAN.
The insect order of Lepidoptera, for example, is declining in rapid numbers [44
] and from this group especially those seem to be threatened that are providing greater eye size for capturing low intense night time lighting [46
]. In the UK and Ireland light pollution accounted for 20% of the variation in long-term changes in moth abundance [45
]. In addition, ALAN is still successfully used in pest management of insects [47
]. Further indications of the significance of ALAN on the decline are still lacking. However, there is strong evidence that flight-to-light behavior of nocturnal insects can directly or indirectly increase mortality. Lepidoptera attracted to street lamps have been shown to be less able to execute their normal evasive flight behavior [49
] and often stay trapped flying around the lamps until they die of exhaustion or as prey.
The third difficult criterion for the application of the prohibition is that the injury or death of the specimen must be a direct consequence of the lighting system’s light emission (BVerwG, NVwZ 2009, p. 302 mno. 91). A deterioration of a habitat, for example, due to a decline in available food sources or other ecological functions (as described above) on the specimen is not sufficient to prohibit the light emission under this provision.
3.3.2. Prohibition to Disturb Specimen of Protected Species
ALAN affects animals during the period of breeding, rearing, hibernation, and migration. Bats are a positive example where the prohibition to disturb could be applied. Their responses to ALAN can be divided into three groups: opportunistic, neutral and avoiding. The latter is mostly observed within almost all species at roosts (day and winter) and when drinking [51
]. The behavior of light-sensitive bats can be impaired within the radius of up to 50 m distance to the light source, even if the luminance level is as low as 1 lux [52
]. High intensity lighting can create a barrier to movements at foraging transfer flights across illuminated streets to even relatively common and opportunistic or neutrally behaving bats, such as the common pipistrelle (Pipistrellus pipistrellus
]. The avoidance of lit passages can lead especially to disturbed drinking behavior for many bat species [51
]. While slow flying species such as Myotis
spp. avoid ALAN, fast flying species, e.g., Pipistrellus
spp. can be attracted especially to white and green lights [56
] and become distracted by phototaxis from their migration routes [57
]. Thus, both groups experience negative impacts of ALAN. Azam et al. (2016) judge the effects of ALAN on bat populations as being more impacting on the occurrence and the activity of bats than the factor land surface sealing [58
]. These behaviors exist during periods in which specimens are typically vulnerable. It is likely that bats due to their avoiding behavior abandon habitats, which causes a decline in the local population. If such development is likely, the prohibition applies.
However, only one third of the studies were conducted on listed protected species like bats. Effects of disturbances caused by ALAN are manifold and affect a broad spectrum of species (Table 2
). An omnipresent disturbance of various taxa is the suppression of circadian or seasonal rhythms when the natural signal of light is disguised by ALAN and hormone performance is affected [7
Field monitoring for the shift in the reproduction period of a strictly seasonal wild mammal due to ALAN is yet not well documented. A leading example is an outdoor study in Australia. The study was conducted on a kangaroo species, the Tammar wallaby (Macropus eugenii
), observing a temporal shift in the reproductive cycle between animals living in unlit bushland and animals living on an illuminated and fenced naval base. The animals were tagged with light sensors, which recorded a 20-fold higher light exposure of the animals on the naval base [59
]. The animals in the bushland experienced less light and a moonlight dependent cyclical change in light levels during the night. The natural illumination of the nocturnal environment is ten times less intense than the constant nocturnal ALAN exposure at the naval base. While over 70% of the female kangaroos gave birth in December and January in the bushland, the period for births at the naval base was delayed until late April. This study is only one example of how ALAN can impact the reproduction cycle of seasonal species. Similar shifts in the seasonality of reproduction have been documented, e.g., the gray mouse lemur (Microcebus murinus
), which is affected by ALAN causing earlier readiness for mating [60
]. For goats (Capra hircus
), which mate in autumn, the signal for reproductive organ development was disguised and the organs remained smaller [62
]. It has been further observed that lighting in winter caused stagnant reproductive development and caused early growth and hair change toward the summer type in dwarf hamsters (Phodopus sungorus
Street lighting next to a water body suppressed in fish (perch and roach) the gene expression of gonadotropins (follicle-stimulating and luteinizing hormones) and the content of sex steroids (17β-estradiol, 11-ketotestosterone) [65
] at 13 to 16 lux at the water surface and 6.5 to 8.5 lux at a depth of 50 cm [66
]. This could hamper the reproduction success of these common fish species.
Also, artificial lighting can change the seasonal behavior of birds. Molting and sexual maturity, for example, occurred in laboratory tests using low light levels (0.3 lux, comparable to a bright full moon) during night time up to three weeks earlier than in birds examined in absolute darkness during the night [67
]. The fitness-relevant effects of extended daily and seasonal activity of birds have not been sufficiently studied. Likewise, to extended day use, the extended seasonal activity can potentially be beneficial to birds as more time can be spent on foraging per day and the season can be elongated. However, the advantages can be reversed if the supply of food is low due to frost in the spring [67
] and if the daily extended foraging time is at the expense of the immune response [68
The same applies to plants. Premature bud formations are mainly observed in illuminated areas [69
]. It seems that rather light signals trigger this phenomenon than temperature conditions. Accordingly, early bud formation rather occurs in illuminated than non-illuminated, warm urban areas. The changes in flowering times cause adverse effects if they take place outside the flying times of pollinators and only a few or no insects are available for the propagation of these affected wild plants. Since plants react with different sensitivities to light and differences in day length [70
], artificial lighting can lead to the loss of sensitive species and consequently to a reduced supply of flower forms, which in turn can affect the occurrence and diversity of pollinating insects [13
lists the results of the literature research for disturbed seasonality and reproduction performance by ALAN. Suppressed seasonality can worsen the conditions for reproduction and affect the response on environmental stressors such as chemical pollutants and climate change.
Yet, it remains unclear whether a shift in seasonality in reproduction causes a negative effect on population dynamics. The effects of ALAN indicate a disturbance of the organisms and thus presumably a relevant stressor to these species. However, the prohibition to disturb specially protected species only applies in very specific cases: disturbances of hormones are often neither expressed in anxiety, flight, nor in fright reactions nor hormonal stress responses, such as increased cortisol. Hence, the impact of outdoor lighting often cannot be recognized as a stressor to light exposed organisms (e.g., in perch [72
]). Only if light is applied at very high intensities, evidence for stress symptoms such as anxiety can be observed, e.g., salmon exposed to 160 lux [73
]. In a diurnal toad (Melanophryniscus rubriventris
), stress symptoms were observed when exposed to ALAN throughout the whole night analyzing the leukocyte composition in blood samples [74
] and the stress hormone corticosterone of nesting great tits (Parus major
) was increased [75
]. The proof of the stress level in the wild bird required blood samples, which makes it difficult to provide evidence to determine stress levels and, subsequently, to apply the prohibition to disturb protected specimen. Except for the wild bird (Parus major
) neither the toad nor the fish species discussed above are listed as protected species in Annex IV (a) Habitats Directive.
In conclusion, the prohibition can be used for the protection of species that show evident avoidance behavior and belong to the strictly protected species of the Annex IV list. However, the lack of anxiety, flight or fright reaction against ALAN makes the provision hardly applicable, thus, creating a protection gap. The same applies as far as disturbances are concerned on a broad range of taxa, which are not listed in Annex IV (Table 2
and Table 3
3.3.3. Protection of Natura 2000 Areas and Protected Breeding Sites and Resting Places
Light has been introduced in places, times and at intensities at which it does not naturally occur [278
]. Thus reproductive and resting places and other light-sensitive habitats, including Natura 2000 areas, experience increasing disturbances due to (a) direct artificial light irradiation [279
], (b) scattered light from illuminated spaces outside the habitats [280
], and (c) skyglow from distant urban areas, caused by reflection of ALAN at atmosphere molecules, aerosols, and especially clouds [282
]. Nightscapes can be affected by skyglow from urban settlements in the far distance [283
]. The impact is highly dependent on light intensity and shielding of luminaires [283
]. Guette et al. discussed that despite the establishment of buffer zones around nature reserves, core areas of the protected sites are increasingly affected by ALAN [285
]. In Europe, special protected natural habitats are increasingly threatened by skyglow and the sources for the disturbance are often unknown [16
ALAN can significantly change nightscapes and have detrimental effects on the ecological functions of the affected site. It can increase the spatial resistance, cause habitat fragmentation for various organisms (Table 3
) and deteriorate the suitability of habitat for migrating species (Table 4
). While there is empirical evidence from laboratory and experimental studies that light level comparable to urban skyglow has adverse effects on organisms (e.g., references [86
]), there is as of yet only limited evidence from field monitoring (e.g., references [253
The responses to ALAN depend on the species and their developmental stage. For example, amphibians can perceive light intensities as low as 10−5
]. Due to their high adaptation capability to low light conditions, amphibians can easily be blinded and stay immobile against threats such as predators or cars when suddenly exposed to light [76
]. A study by Grunsven et al. indicated that migrating toads stopped to migrate when exposed to ALAN [173
]. This behavior is light color–dependent: red lighting did not prevent toads from migration, while green and white light emissions interrupted migration until dawn, when the lights were switched off.
Birds have an extraordinarily good visual performance and many species are highly attracted to light sources and are therefore threatened to fatal collisions by ALAN. Migrating birds as well as many sea birds and petrels have been observed to collide with buildings or coastal formations when strongly illuminated [208
]. Cabrera-Cruz et al. argue that the global migratory behavior of birds could be adversely affected by illuminated landscapes and that the birds can be at risk of approaching non suitable habitats in urban settings instead of wetlands for their resting on migratory routes [291
Migrating fish can also be disturbed by ALAN. Mature silver stage European eel (Anguilla anguilla
) are highly light-sensitive. For example, flume experiments demonstrate a strong avoidance reaction of silver eels to ALAN [292
]. This can result in a reversed, upward migration against the current when lights are directed upstream [293
]. Although salmon (Salmon salar
) is more apt to adjust to ALAN, hatchery studies reveal that juvenile specimens are attracted to ALAN and stay in lit areas for a long period while delaying their dispersal [220
]. Thus, the spatial resistance of a landscape increases with ALAN and the migration becomes more time and energy consuming, which can jeopardize the natural synchronized reproduction especially for long distances migratory species such as eel or salmon [294
Nocturnal Lepidoptera (moths) may substantially suffer from landscape deterioration and fragmentation by nightlights. Degen et al. calculated that the attraction radius for moths to streetlights is 23 m or more [258
]. When street lighting is installed with lighting points of for example 40 m distance to each other, the illumination can become a barrier to the insect dispersal. However, other flying organisms are also affected. The giant water bug (Lethocerus deyrollei
), for example, lost the habitat when illuminated. In a field study in Korea, Choi et al. found that the giant bugs could no longer be detected in a radius of 700 m around artificial light sources and anthropogenic influences and their occurrence was considerably limited within a radius of 3 km around the light sources [260
]. Perkin et al. described altered flight behavior in up to 40 m distance to a light source for other aquatic insects [251
Studies indicate that biodiversity seems to be reduced in close vicinity of streetlights. Although 70% more moths were found at streetlights than at unlit sites, the diversity of moth species decreased by more than 25% [247
]. Moreover, the moths carried plant pollen from a smaller number of different plants than in natural darkness. In addition, moths were found to produce fewer pheromones under illumination, possibly decreasing their reproductive performance [128
]. Thus, the attraction and altered behavior of insects in lit areas can hamper the provision of food sources for many animals, such as bats, birds and fish, including threatened species.
Illumination can further impair the ecological function of nighttime pollinators with severe consequences on the vegetation as a food source for daytime pollinators [237
]. The seed dispersal from fruit-eating bats was also observed to be reduced [198
]; this study does not affect European landscapes, because it examines tropic species, but is a vivid example of how an ecological function (here seed dispersal) could be disturbed with unknown consequences for the surrounding vegetation and landscapes.
Ecological functions in riparian areas can be similarly affected. Grubisic et al. found that direct LED lighting on aquatic freshwater bodies can interfere with the communities of periphyton, the primary growth of plants, presumably due to the high emission of blue light [157
Furthermore, skyglow can reduce the vertical migration of algae consuming zooplankton in freshwater lakes [287
]. If Daphnia no longer migrate to the upper layer of the water column at night due to ALAN, algae will be released from Daphnia consumption. As a result, algae biomass and cloudiness of the lake may increase, although the nutrient load is unchanged [294
]. Aquatic insects can be attracted to the light sources in high numbers after emerging the water body [294
]. Reproduction is further reduced by the strong signal of lighting amplified by artificial, reflective surfaces near water, which can disguise the natural signal, and prevent aquatic insect ovipositioning in suitable habitat [295
]. Outside of suitable aquatic habitats, the offspring can be threatened to drought.
Flying insects are attracted to streetlights in high numbers, ALAN captivate insects from their natural habitats and deprive their ecological function, an impact which can be described as a vacuum cleaner effect [297
]. Both, exhausted and dead insects that accumulate on the ground are a food source for insectivorous predators or scavengers [250
]. Naturally nocturnal spiders, carrion beetles and slugs have been observed to extend their foraging until late in the day—presumably to benefit from higher abundance of exhausted or dead insects in the area of the lamps [249
Other distortions in ecosystems appear because some diurnal species such as fish or birds can use lit areas to extend their daily activity into the night: Some predatory fish species have higher foraging success [218
]. Feeding places for songbirds are being visited longer [217
] and in higher numbers [300
]. Prolongation of the daily activity of songbirds was observed [67
], and the extended activity phase correlated with the level of luminance in many birds such as robins, chaffinches, blackbirds, great and blue tits [286
]. At lit beaches, waders have been observed hunting for sandworms even after dark [95
]. A prolonged activity phase can be beneficial to the foraging success, but it can be detrimental to the immune system of higher vertebrates in the long term [68
], altering predator–prey relationships and distorting whole food webs [249
In conclusion, the impact of lighting systems can be calculated by the detrimental impact on landscapes (Table 4
), the disturbance of species in their circadian and seasonal performance (Table 2
) and changed behavior due to avoidance and phototaxis (Table 3
). The deterioration of conditions for protected and other species are in most cases due to natural landscape deteriorations produced by lighting systems outside of Natura 2000 and resting- and breeding sites [285
]. However, the distance up to which skyglow effects have an impact on light-sensitive species remains unclear. Therefore, evidence for a significant impairment of the conservation objectives of the respective protected area is lacking. Hence, the aim of European law to ensure a strict protection regime for special areas of conservation under the Habitat Directive falls often short in ALAN-related situations. The same applies to the general protection regime of nature and landscape under German law. Although it does not distinguish between protected and unprotected species and has in general a broad spatial scope of application, it requires a substantial impact from a single lighting source.
In order to minimize the direct light immission in sensitive habitat, two regulations have been recently enforced. In France, any direct light emission towards water bodies is prohibited [301
], while Bavaria require to avoid light emission on insect habitat [42
] (art. 11a Bavarian Nature Conservation Law).