Coral reefs, which are highly sensitive and complex ecosystems, are continuously exposed to a variety of both direct anthropogenic disturbances: e.g., sewage, nutrient enrichment, and diving activities [1
]; and indirect ones: e.g., water thermal stress and acidification [2
]. In many cases, such disturbances have been found to be a key factor in contributing to changes in coral-reef community structure [1
]. From an ecological perspective, the light-quality regime (intensity and spectrum composition) is a crucial factor in affecting coral settlement [4
] and survivorship [6
], and hence strongly determines recruitment success [7
]. Different responses of coral planulae to light quality and quantity have led to a species-specific spatial settlement in the reef [8
]. Consequently, due to the corals’ light reaction mechanism, even the slightest change in light intensity and composition, as a result of artificial changes (i.e., light pollution), may alter the settlement pattern of different species, and directly affect the local and spatial community structure [4
Previous studies have indicated that even low levels of light pollution may have an impact on the daily changes in moonlight that occur during the lunar cycle, and which are essential for maintaining the normal lunar periodicity; and, as a result, affect the coral’s biological clock (e.g., gene transcription) [9
]. Using LED lighting as the light source, Boch et al. [11
] demonstrated that the major driver of spawning on a given night of the lunar cycle appears to be that of a critical threshold, determined by lunar photoperiod cues and possibly also wavelength-dependent. Those mechanisms were found to be synchronized in accordance with the detection of moonlight by blue-light-sensing photoreceptor cryptochromes, which absorb mainly blue light [12
]. Tamir et al. [13
] demonstrated that in light-polluted areas, artificial light intensity at night can be higher than that of full moonlight. Thus, the combined accumulation of natural and anthropogenic stressors can result in adverse effects on coral reproduction [9
], and may lead to a diminished or unsynchronized supply of coral planulae [15
]. This may in turn cause a negative cascading effect on larval dispersal and recruitment in coral reefs [14
Symbiotic dinoflagellates of the family Symbiodiniaceae are known to have a fundamental mutualism with many reef invertebrates, notably, stony corals [16
]. This relationship was found to be influenced by differential adaptation to light conditions [17
]. Frade et al. [18
] found a strong functional within-colony uniformity in symbiont diversity due to variability in physical factors (e.g., irradiance, light spectral distribution, temperature) even among closely-related coral species. Byler et al. [19
] presented evidence that juvenile colonies of Stylophora pistillata
may utilize both vertical and horizontal symbiont acquisition strategies. Hence, changes in light conditions due to artificial sources may alter this natural pattern and affect the composition of the symbionts acquired at a coral’s early life stages (i.e., as larvae or juvenile colonies). However, this hypothesis has not yet been validated. Recently, Rosenberg et al. [20
] demonstrated variability in chlorophyll (Chl-a
) concentration in LED-illuminated Acropora eurystoma
corals, which exhibited higher values than the control ambient samples.
However, little is currently known about coral recruitment dynamics (e.g., settlement and post-settlement survivorship and growth) under a continuous change in the natural light regime at night, due to artificial lighting. Moreover, compared to daylight [8
], the potential for habitat selection by larvae in the presence of artificial light at night is largely unknown.
Following the increase in the human population along coastal areas in recent decades, the natural nocturnal physical conditions have been altered by means of artificial lighting [21
]. This spread of electric lighting has been shown to be a major perturbation to the natural nocturnal light regime [22
]. The potential impact of such nocturnal light is indicated in the term “ecological light pollution” [23
]. For a variety of reasons, this phenomenon is rapidly increasing in coastal areas [21
The potential of artificial light at night-time to disrupt coastal and marine environments [22
] has only recently become widely recognized as an environmental issue [24
]. Moreover, insufficient attention has been given to date to its potential impact on coral reefs in general and on coral initial life stages in particular.
The different lighting methods that characterize a city’s illumination result in variability in the spectrum and intensity of the artificial light sources [25
]. Tamir et al. [13
] showed that as a result of water clarity and the proximity of artificial light sources to the coastline, light pollution could be detected down to 30 m depth in the northern Red Sea. The significant change in the night-time light regime in the shallow depth zone is therefore expected to have a crucial effect on the northern Gulf of Eilat/Aqaba (GoE/A) coral-reef ecosystem. Nevertheless, despite the potential significant impact of light on coral settlement, survival, and distribution, insufficient attention has been paid to date both to the role of light pollution in dictating the settlement and zonation assemblages of corals, and to light pollution effects on such crucial mechanisms to corals as photosynthetic efficiency and calcification rates.
Considering the limited studies engaging with these issues to date, our current data on this phenomenon’s potential impact provide a novel and better understanding of these issues. Here, for the first time, we present a long-term experiment examining the effects of two artificial light sources on a coral’s initial life stages, as well as the potential effects of artificial light on a coral’s basic physiological systems and processes (e.g., photosynthesis and calcification).
Finding a suitable settlement site is a crucial process for the recruitment and survivorship of marine sessile invertebrate larvae [4
], and thus may directly determine the distribution of different species at specific locations [14
]. The findings from the present work have enabled us to elucidate the physiological and ecological effects of two different types of common urban artificial lighting on crucial life stages and physiology (i.e., settlement, survivorship, growth rates, calcification rates, and photosynthetic efficiency) of the coral Stylophora pistillata
. Over the past few decades, light source diversity has increased [34
]. This trend, together with the adoption of lighting technologies presenting a broader spectrum, i.e., featuring ‘white’ light (e.g., LED lighting methods) specifically, is becoming more common [25
]. As a result of the LED short wavelengths combined with the water’s physical characteristics [13
], an ever-increasing area of the reef and of its specific coral community that thrives at shallow depths (0–30 m), is expected to experience greater disturbance from such artificial illumination at night.
The results of our settlement experiments indicate that light pollution is likely to reduce the percentage of S. pistillata
planulae settling on the substrate (Figure 1
). S. pistillata
is currently the most common recruited species among the stony corals in the shallow depths in the GoE/A [27
]. Since the shallows are in close proximity to the shore, these corals are more exposed to such artificial illumination [13
], in addition to other anthropogenic disturbances. This, in the long term, may be potentially harmful to certain coral species.
Bolton et al. [35
] demonstrated a dramatically direct effect of artificial lighting on the predatory behavior of fish, which increased their pace of predation at night; as well as the indirect effects of this lighting on sessile assemblage structures (e.g., barnacles, ascidians, and polychaetes). This change in substrate may have an indirect but crucial effect on coral recruitment and resilience (e.g., new settlers). Such changes in benthic community composition can play an important role in coral recruitment dynamics [36
]. Hence, in the long term, along with the increasing use of artificial light, and specifically LED lights, S. pistillata
settlement patterns may be interrupted.
The “recruitment-limited” theory for open-water marine populations was first postulated for coral-reef fishes [37
], and later accepted as applying to many marine sessile organisms possessing a dispersive larval stage [38
]. This theory predicts that population dynamics will be primarily driven by the magnitude and variation in the supply of larvae to the population, rather than by processes acting post settlement; as well as driven by ecological phenomena such as fish predation during coral spawning. This may be an important source of coral larvae mortality [40
], which has the potential to increase under light pollution. Hence, changes in the coral larvae natural light regime may result in the degradation of a coral community as a consequence of the reduced supply of larvae. Given that coral larvae frequently travel between reefs [41
], a large spatial variation is expected in coral larvae availability due to the light pollution regime, on the scale of both entire reefs and within-reef habitats. Moreover, globally, asynchronous planulae release by different coral species [9
], due to slight changes in the light regime, may lead to reproductive isolation and prevent gene flow between shallow coral reefs communities that are exposed to light pollution globally [42
]. Although it has not yet been proven, such asynchronization may be affected by light pollution, leading to changes in the proportion of recruited brooding versus broadcast-spawning species [45
Our findings for the survivorship stage revealed an opposite trend, in which the artificially-illuminated corals demonstrated higher percentages of survivorship (Figure 2
). Similarly, under illuminated conditions, they demonstrated significantly higher growth rates than their counterparts in the control (Figure 3
). These survivorship and growth rate results indicate the potential advantage of possessing an additional photosynthetic energy flux, which in this case is acquired at night [46
]. Previous studies have engaged with the question of increasing plant production capacity through the use of controlled artificial lighting systems [46
]. Their findings revealed how LED can mimic natural light to conduce to the growth and development of photosynthetic organisms. Nonetheless, the survivorship percentages between the light treatments and the control in the present study were not significant.
Despite the higher survivorship, there was a lower photosynthetic efficiency pattern in both light-polluted coral treatments than in the control. The lower photosynthetic efficiency (i.e., lower slope—α) of the symbionts in the corals exposed to artificial lighting (Figure 4
, Table 1
) could be due to the photosynthetic apparatus being either not fully activated normally, or inactivated. These differences in photosynthetic efficiency (α) between the two treatments and the control could be due to the higher respiration rate of the latter. In addition, the lower slope (α) resulting from the light treatment may indicate possible damage to RuBisCO efficiency and CO2
assimilation ability [48
], despite the increase in light intensity; or could be due to the low amount of RuBisCO present [49
]. RuBisCO is known to be a limiting factor mainly at high light intensity, i.e., mostly limiting the maximum potential photosynthetic rate (Pmax
There was a difference between the control and light-polluted treatments in PE curves and long dark-incubation respiration (Figure 4
a and Figure 5
a). The PE curves, measured during daytime, lasted 20 min at each light intensity (or dark); while the long dark-incubation period was during the night, reflecting the corals’ normal daily cycle. It is possible that the faster respiration of the control corals was measured in the pre-PE dark period, because their photosynthesis during the day was higher compared with the ‘LED’ corals. This difference between night and day respiration in the control corals was not evident in the ‘LED’ corals, possibly implying a disruption of their natural cycle. Recently, Ayalon et al. [50
] reported a significantly lower photosynthesis performance (decreasing levels of PSII electron transport rate—ETR) of Acropora eurystoma
and Pocillopora damicornis
when exposed to LED lights. Moreover, they demonstrated that the blue and the white LED spectra demonstrated a more negative impact on coral physiology compared to the Yellow LED. Thus, similar to previous studies, the differences found between our control and light treatment photosynthesis performances may reflect the variability that exists between the effects of the different artificial lighting methods on a coral’s basic physiology parameters.
Interestingly, despite the lower photosynthetic efficiency and rates of the ‘LED’ corals throughout the entire 24-h incubation period, calcification was higher than in the control corals (Figure 5
). This might be explained by the light-enhanced calcification (LEC) process, which leads to variation in growth rates. Even though the interrelationship of hermatypic coral-calcification and photosynthesis has been determined as a general concept [51
], previous studies have shown the potential of LEC to be directly affected by light without the mediation of photosynthesis [52
]. Furthermore, Cohen et al. [52
] suggested that a blue light signal and its receptors in animals may be involved in the enhancement of calcification by hermatypic corals. The faster growth of the corals under the LED treatment supports the assumption that this trend may be due to the presence of LED at night. Thus, the observed increase in growth rates of corals illuminated by LED light may be explained by the absorption of blue light by several blue light photoreceptors found in the coral host [54
]. Such photoreceptors have been discovered in several Acropora
spp. corals and identified as cryptochromes and opsins, which absorb mainly blue light [12
]. However, we do not know how a longer light exposure of the corals to LED might affect their physiology. This question, in addition to estimating the time it takes for light to stimulate calcification at night, should be addressed in future studies.
Rocha et al. [55
] examined the effect of the artificial light spectrum on growth performance of cultured scleractinian corals following exposure to identical photosynthetically-active radiation (PAR) intensities. They tested this by calculating the effect of different light spectra delivering identical PAR by means of fluorescent lamps (used as a control treatment), Light Emitting Plasma (LEP), and Light Emitting Diode (LED) on the photobiology of two scleractinian corals: Acropora formosa
and S. pistillata
. The particular light spectrum significantly affected coral growth of both species. A. formosa
cultured under LED presented a specific growth rate 99% higher than conspecifics grown under fluorescent illumination (control). Wijgerde et al. [56
] exposed Galaxea fascicularis
to similar LEP and LED light intensities. Interestingly, under relatively low irradiance (40–60 μmol m−2
), the growth rate of these corals was higher under the LED treatment. This trend was reversed when light intensity was increased. Such a trend may be a result of the LED higher blue peak. These findings may explain the higher growth rate under the light treatments, even though the artificial night-time light levels were very low (i.e., below the compensation point; Figure 5
a). In addition to the effect of blue light on coral physiology, it was found that red light also has a considerable potential negative effect on S. pistillata
health and survivorship, even under the combination of blue and red wavelength peaks (452 and 665 nm; [57
]). The two light treatments in the current experiment also yielded a portion of red light. An additional potential negative trend has recently been found by using transcriptome analysis under LED treatment to compare corals growing under natural light cycles and under light pollution conditions [20
]. Disorders expressed as alterations in gene expression pathways (cell proliferation, organismal injury and abnormalities, and reproductive system disease genes) were demonstrated to be a direct result of the exposure to light pollution [20
]. That study revealed many altered pathways that had resulted in cell-cycle progression, cell proliferation, survival, and growth in the long term.
The various city light sources i.e., roadside lights, car headlights, street lighting, and other city lights, especially those located next to roads and other marine structures such as ports and oil jetties [13
], may interrupt natural processes (e.g., photosynthesis and calcification). Bennie et al. [58
] contended that in practice, the measurable effects of light on carbon fixation in terrestrial vegetation are likely to be limited to situations in which the leaves are in very close proximity to a light source, or when artificial lighting is introduced into naturally dark situations such as cave systems. A similar situation can be found at those reef sites where a naturally dark regime becomes illuminated by permanent artificial lights. However, no evidence of a photosynthesis process taking place under low artificial lighting was found in our study. Thus, although the artificial lighting effect is seemingly advantageous, i.e., higher survivorship and rapid growth rate, it will not necessarily contribute to the thriving of a particular species, especially if such lighting is detrimental to that species’ ability to recruit, mainly due to a reduced supply of larvae and lower settlement success. The question, however, is how does the added survivorship relate to the reduced settlement—do they balance each other out? Based on the “recruitment-limited” theory [37
] and the fact that during the settlement stage the planulae had remained in closed vessels, thus preventing any possibility of settling elsewhere, we conclude that in a natural reef under a light pollution regime, the ‘recruitment equilibrium’ will become unbalanced. We should therefore consider the overall consequences of light pollution on coral-reef physiology and ecology, and avoid drawing unequivocal conclusions regarding each of the coral life phases separately.
Understanding the impacts of light pollution at night on coral species requires knowledge of the intensity, spatial pattern, spectral distribution, duration, and timing of the artificial lighting to which corals are exposed. Hence, specific crucial aspects pertaining to coral life-traits (e.g., recruitment, settlement, and survivorship) should also be examined in a variety of coral species. In addition, it is necessary to determine the importance of recruitment relative to post-settlement survivorship related to processes such as predation [35
], competition, and disturbance [59
] under a light pollution regime. Moreover, in addition to methods such as determining gene expression in relation to advanced life stages, the effect of artificial lights on zooxanthellae acquired at early life stages of larvae or juvenile coral colonies, as well as skeleton structure, ecological studies (e.g., reproductive fecundity) are also needed in order to address the effects of light pollution on coral physiology and ecology.