Elsevier

Science of The Total Environment

Volume 661, 15 April 2019, Pages 543-552
Science of The Total Environment

Artificial light pollution influences behavioral and physiological traits in a keystone predator species, Concholepas concholepas

https://doi.org/10.1016/j.scitotenv.2019.01.157Get rights and content

Highlights

  • Juveniles of C. concholepas seek out and choose their prey in dark conditions.

  • Light pollution increases righting times of juvenile C. concholepas.

  • Light pollution increases metabolism of juvenile C. concholepas

  • In nature small C. concholepas are more abundant in darkened habitats.

  • Influence of light pollution at night may have implications on community structure.

Abstract

Artificial Light At Night (ALAN) is an increasing global problem that, despite being widely recognized in terrestrial systems, has been studied much less in marine habitats. In this study we investigated the effect of ALAN on behavioral and physiological traits of Concholepas concholepas, an important keystone species of the south-eastern Pacific coast. We used juveniles collected in intertidal habitats that had not previously been exposed to ALAN. In the laboratory we exposed them to two treatments: darkness and white LED (Lighting Emitting Diodes) to test for the impacts of ALAN on prey-searching behavior, self-righting time and metabolism. In the field, the distribution of juveniles was observed during daylight-hours to determine whether C. concholepas preferred shaded or illuminated microhabitats. Moreover, we compared the abundance of juveniles collected during day- and night-time hours. The laboratory experiments demonstrated that juveniles of C. concholepas seek out and choose their prey more efficiently in darkened areas. White LED illuminated conditions increased righting times and metabolism. Field surveys indicated that, during daylight hours, juveniles were more abundant in shaded micro-habitats than in illuminated ones. However, during darkness hours, individuals were not seen to aggregate in any particular microhabitats. We conclude that the exposure to ALAN might disrupt important behavioral and physiological traits of small juveniles in this species which, as a mechanism to avoid visual predators, are mainly active at night. It follows that ALAN in coastal areas might modify the entire community structure of intertidal habitats by altering the behavior of this keystone species.

Introduction

Marine environments are facing a growing number of stressors associated with global climate change, local human activities and the urbanization of coastal areas. In the face of this proliferation of human impacts, artificial light pollution has often been overlooked despite growing evidence that ALAN could pose a threat to the diversity and functioning of biological communities in terrestrial (Gaston et al., 2014; Davies et al., 2016; Davies et al., 2017; Davies and Smyth, 2017) and marine communities (Becker et al., 2013; Gaston et al., 2014; Davies et al., 2015; Bolton et al., 2017; Davies and Smyth, 2017). For example, exposure to ALAN increased the total abundance, and modified the community composition, of spiders and beetles in a grassland ecosystem (Davies et al., 2017). In marine ecosystems, Lorne and Salmon (2007) showed that sea turtle orientation was negatively affected by ALAN, impairing the ability of hatchlings to respond to natural orientation cues. Similarly, in nocturnally migrant birds ALAN altered multiple behaviors (Van Doren et al., 2017) and even human health traits such as sleep, circadian timing, next-morning alertness and increased risk of breast cancer has been shown to be affected by ALAN (e.g. Chang et al., 2015; Keshet-Sitton et al., 2015; Zielinska-Dabkowska, 2018).

Shifts in spectral signatures associated with ALAN might affect visually guided behaviors across a broad taxonomic group of animals (Davies et al., 2013). It has been estimated that ~19% of the global land area of the world it is now affected, to some extent, by ALAN (Cinzano et al., 2001, Kyba et al., 2017, Kyba, 2018). Moreover, it is estimated that the total area affected by this anthropogenic change in lighting technology is increasing by 6% per year (Hölker et al., 2010), which suggest that this stressor might have far reaching consequences. Light-emitting diodes (LEDs) are cheap, bright, highly efficient and reduce energy consumption. All of which means that LEDs are rapidly becoming one of the world's most important light sources (Zissis and Bertoldi, 2014) and are increasingly being used for lighting in both residential and commercial areas as well as the transport routes between them. In the marine environment this will specifically include beachfront developments, ports, marinas and shipping. Therefore, the potential impact of this change to LED illumination on marine communities needs to be considered (Gaston et al., 2015).

In the marine realm, many species have evolved behavioral and morphological responses to minimize visual predation (Troscianko et al., 2009; Manríquez et al., 2009). For instance, some intertidal species are most active during the night as a mechanism to avoid visual predators (Wells, 1980). In addition, being active at night minimizes thermal abiotic stress and desiccation at low tide. This is particularly advantageous for organisms performing energy-demanding activities (e.g. Kennedy et al., 2000). Recently, ALAN has also been shown to affect the locomotor activity, circadian rhythm and growth rate of intertidal amphipods (Luarte et al., 2016) as well as the small-scale diel vertical migrations of zooplankton species (Ludvigsen et al., 2018). Therefore, the modification of the natural light-dark regime by ALAN in coastal environments could have important consequences for the species inhabiting these areas.

The “Loco” or “Chilean abalone”, Concholepas concholepas (Bruguière, 1789), is a keystone species (i.e. its presence maintains the structure and integrity of the community) in rocky shores of the south-eastern Pacific Ocean coast (Castilla and Paine, 1987, Power et al., 1996, Castilla, 1999). This species is an economically and ecologically important component of the rocky intertidal and subtidal communities along the Chilean coast (Castilla, 1999). According to observations conducted under laboratory conditions with intertidal individuals, C. concholepas prey mainly at night (Castilla et al., 1979, Castilla & Guisado, 1979, Castilla and Cancino, 1979, Guisado and Castilla, 1983). Meanwhile, studies conducted using subtidal individuals indicated that C. concholepas prey over the entire 24-h cycle (Stotz et al., 2003) suggesting that, in this species, intertidal and subtidal populations display different activity patterns. Competent larvae of C. concholepas show a marked circadian rhythm in their swimming behavior, displaying most of their activity at night (Manríquez & Castilla, 2001). However, it is not yet known if the behavior of benthic stages of this species is also timed over the lunar or tidal cycle. Among the most important prey items of C. concholepas are barnacles, mussels and ascidians (Stotz et al., 2003; Manríquez and Castilla, 2018), all of which are sessile or have limited mobility. Therefore, it is highly unlikely that preying at night in this species is a mechanism that evolved to avoid being perceived while approaching prey. Instead, it can be argued that preying at night might be a potential mechanism evolved by C. concholepas to avoid its own visual predators: the crab Acanthocyclus hassleri (Manríquez et al., 2013a, Manríquez et al., 2013b), the birds Larus dominicanus and Haematopus ater (Castilla and Cancino, 1979), the sea otter Lontra felina (Castilla and Bahamondes, 1979), and the fish Pimelometopon maculatus and Syciasis sanguineous (Viviani, 1975).

Similar to most mollusks, C. concholepas can use chemical and visual stimuli during sensory perception (Manríquez et al., 2014; Domenici et al., 2017). In this species, the detection of chemical cues associated with prey and predators play an important role in feeding and predation avoidance (Manríquez et al., 2013a; Manríquez et al., 2014). Moreover, as in other marine gastropods, chemoreception of odor cues emanating from food items, conspecifics or predators, involves the osphradium, an external sensory organ, which monitors the physiochemical properties of the surrounding seawater (Huaquín and Garrido, 2000). The structurally simple eyes of these gastropods are situated in each tentacle, and provide information on gross differences in light intensity (distinguishing light and dark), regulate daily and seasonal activities, egg laying behavior, mediate phototaxic behavior and locomotion, and in some species, provide also visual detection of forms (Serb, 2008; Ter Maat et al., 2012). Tentacles withdraw in response to sudden decreases in light intensity, exhibiting a shadow response consisting of partial or total retraction of the body into the shell and downward movement of one or both tentacles (Stoll, 1972; 1976). In C. concholepas specifically, shadow response is observed under field and laboratory conditions once light intensity is suddenly interrupted near the cephalic region of the individuals with an opaque object (Manríquez PH. pers. obs). This suggests that the cephalic eyes, or other sensitive areas in the cephalic region, might play an important role in detecting habitats with appropriate light illumination. Hence, ALAN is likely to have a significant effect on the activity of this species.

Coastal urbanization and tourism development is followed by coastal land reclamation, creation of artificial beaches (Chee et al., 2017) and beachfront lighting (Hölker et al., 2010). This is particularly important in Antofagasta, northern Chile, where the urban fringe is narrow and urbanization takes place near the coast (Corsin, 2001). As previously mentioned, the intertidal habitat is subject to a wide range of stressors including ALAN (Underwood et al., 2017), so the rocky intertidal zone and the organisms inhabiting there are good models to investigate the eco-physiological consequences of ALAN. In this study, we conducted laboratory experiments using juveniles of C. concholepas to investigate the potential effects of ALAN (using LED lighting) on prey searching, self-righting speed and metabolism. In this particular environment, prey searching and self-righting success are important traits in mediating both predator-prey interactions and the ability to return to a normal posture after dislodgement, respectively. Moreover, we conducted a field survey to determine whether the distribution of juveniles in shallow subtidal rocky habitats was influenced by the ambient light conditions. Our hypothesis was that exposure to ALAN has significant effects on behavioral and physiological traits of juveniles of this keystone species. We expected that ALAN exposure would inhibit the activity of small juveniles of C. concholepas and prompt them to incur increased metabolic costs in searching for food in darkened areas. Given that overturned individuals are more vulnerable to visual predators, we also expected that ALAN would speed up self-righting.

Section snippets

Influence of natural lighting conditions on the abundances of loco in the field

This field sampling was conducted to explore the link between the response of small juveniles of C. concholepas to ALAN in the laboratory and their natural abundances during night hours. Daytime natural abundances on shaded or illuminated shallow subtidal microhabitats might give cues about where the small juvenile of this species prefer to be more active (e.g. searching for prey). Similarly, night-time abundances might help to know if this pattern changes in absence of light. The location and

Influence of natural lighting conditions on the abundances of loco in the field

The abundance of small juveniles of C. concholepas was significantly different between microhabitats (F1,28: 0.9307; p < 0.00001). Approximately 4 and 5 times more individuals were found in the shaded than in the illuminated microhabitats at El Lenguado and Trocadero, respectively (Fig. 2a). The same analysis found that sampling site (F1,28: 0.05; p 0.3429) and the interaction with microhabitats type (F1,28: 0.05; p = 0.8261) were not significant. At Calfuco during day-time hours, almost 4

Discussion

Field surveys of rock boulders in shallow tide pools indicated that, during the day, juvenile Concholepas concholepas congregate on the underside of rock boulders. However at night, these juveniles were present both on top of and on the underside of the boulders. Since these individuals were below the water level, they were not exposed to desiccation or thermal stress. Hence, those results suggest that they were actually avoiding light. Previous studies have indicated that large subtidal

Conclusions

Combined, our results indicate that when exposed to ALAN, small juveniles of C. concholepas showed significantly longer self-righting times, higher metabolic rates, and were less frequently found near the food items available. Moreover, in shallow subtidal habitats, small juveniles of this species preferred shaded areas during the day, but had no preference during night-time hours. Such evidence suggests that, due to ALAN, these juveniles become less efficient at finding food and more

Acknowledgments

The field part of this study was supported by the Fondo Nacional de Desarrollo Científico y Tecnológico, FONDECYT grant No 1050841 (2005–2007) to Patricio H. Manríquez (PHM). The experimental work of this study was supported by the FONDECYT grant No 1171056, to Cristian Duarte (CD). During this study PHM was under the tenure of the grant “Climate driven Changes in the Habitat Suitability of Marine Organisms” (CLIMAR, ELAC2015/T01-0495) funded by the Network of the European Union, Latin America

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