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- Materials and methods
- Supporting Information
Coastal areas are under increasing pressure from human activity and development worldwide. The demand for the construction of industrial complexes, hotels and residential properties throughout the coastal zone is driven primarily by access to the sea. The rate and magnitude of coastal development is increasing on a global scale, often elevating the nocturnal illumination of biologically productive areas. The negative effects of artificial lighting on orientation amongst animals as they move between the sea and the land have been well documented (le Corre et al. 2002; Longcore & Rich 2004; Tuxbury & Salmon 2005). Its effects, however, upon ecological processes, such as predator–prey interactions, are less well understood.
The intertidal zone along exposed coastlines and estuaries provides essential habitat for migrating shorebirds. Many shorebirds also spend the winter on the intertidal, duly establishing body reserves before making the return migration to summer breeding grounds at high latitudes. For those shorebirds overwintering in temperate regions, diurnal feeding alone has been reported to be insufficient to balance energy budgets (Goss-Custard 1969; Turpie & Hockey 1993; Zwarts et al. 1996). This is not only due to increased metabolic demands during adverse weather but also because foraging time is restricted by short day length and fluctuating tides (Goss-Custard et al. 1977; Mouritsen 1994). To feed efficiently throughout the diel cycle, some species of shorebirds switch their foraging behaviour between high and low ambient light levels (Robert, McNeil & Leduc 1989; McNeil, Drapeau & Goss-Custard 1992). During the day, these birds employ visual information to guide bill position when detecting prey (i.e. visual foraging). At night, however, birds switch to using tactile information on prey, obtained by probing or sweeping the bill in soft substrates (Piersma et al. 1998; Martin & Piersma 2010). As sight-based foraging behaviour allows birds to search and select for the most profitable prey items (Goss-Custard 1969; Robert & McNeil 1989), it is generally preferred when natural light levels are adequate (Pienkowski 1983; Robert, McNeil & Leduc 1989).
In this study, the influence of nocturnal light levels on night foraging in shorebirds was examined using an individual-based approach. Posture-sensitive VHF radio transmitters were used to collect quantitative measurements of behaviour and habitat use of free-ranging common redshank Tringa totanus. This provided a non-disruptive method to study animal behaviour and habitat use over extensive and inaccessible tidal flats, even under poor visibility, darkness and inclement weather which would be highly challenging under a conventional visual-based approach. Measuring light levels using hand-held photo-detectors at each shorebird location would have been unreliable as human presence would likely have disturbed the foraging birds. We utilised geo-referenced night-time satellite imagery data obtained from the U.S. Air Force Defence Meteorological Satellite Program (DMSP), with the Operational Linescan System (OLS) to quantify artificial illumination under the night sky (Elvidge et al. 1997; Imhoff et al. 1997; Sutton et al. 1997; Cinzano, Falchi & Elvidge 2001). Night-time satellite data provided by DMSP/OLS were captured on cloudless nights under very low or no lunar illuminance and transformed into values of night brightness (Elvidge et al. 1999; Letu et al. 2010); an archive of global data sets is available online. Although this is the first use of these data known to us for an animal behavioural study, DMSP/OLS maps have been applied to investigate electrical power consumption (Elvidge et al. 1999; Letu et al. 2010), predict offshore fishing vessel density (Waluda et al. 2002; Kiyofuji & Saitoh 2004) and to monitor biomass burning and gas flares (Elvidge et al. 1997).
Using these tools, the relative contribution of ambient light to foraging persistence and behaviour in redshank was examined throughout the middle reaches of the industrialised Forth estuary in Eastern Scotland, U.K. The method allowed us to test whether individuals took advantage of artificial light, in a similar manner to moonlight, whilst determining whether night foraging was contingent on moonlight levels rather than on the influence of the lunar cycle on prey behaviour (Milsom, Rochard & Poole 1990). We hypothesised that the positive effects of light may not simply open up opportunities with respect to extending the daily foraging period, but it may also allow individuals to switch foraging modalities (e.g. from touch to sight) and thus make nocturnal foraging relatively more efficient.
- Top of page
- Materials and methods
- Supporting Information
Studies into the effects of artificial light pollution on animal behaviour are uncommon and generally document negative effects (le Corre et al. 2002; Longcore & Rich 2004; Tuxbury & Salmon 2005). Here, we show that artificial light generated from a large industrial site situated upon an estuary in Eastern Scotland, significantly altered the foraging strategy of common redshank. The 24 h light emitted from lamps and flares created, in effect, a perpetual full moon across the local inter-tidal area. Consistent with the study hypothesis, greater nocturnal illumination increased the potential for birds to forage for longer periods at night and to use a potentially more effective foraging behaviour to locate prey. Our findings parallel observational studies on wetland birds under wholly natural light, including many wildfowl, which similarly take advantage of moonlight to increase foraging opportunities (e.g. Pienkowski 1983; Robert, McNeil & Leduc 1989; Sitters 2000; Tinkler, Montgomery & Elwood 2009). Empirical studies have shown that foraging periods utilising a visual over a touch-based behaviour provides a higher net food intake for inter-tidal feeding birds (Lourenço et al.2008; Santos et al. 2010), and we argue that the effects of artificial lighting upon the Forth estuary enhanced feeding opportunities for redshank.
The tagged redshank did not select illuminated areas for feeding. Rather, they maintained a high degree of site-fidelity to the area where they were captured and tagged (Fig. 3c). Redshanks are known to live within a small home range on their winter feeding grounds (Furness & Galbraith 1980; Burton 2000; Rehfisch, Insley & Swann 2003), where individuals are known to redistribute according to social status and habitat quality (Cresswell 1994). If feeding opportunities were enhanced under artificial lighting, then relatively higher densities of redshank might occur within localities of artificially elevated ambient light levels (Sutherland 1983). Similarly, the usage of these favoured areas may be age-dependent; whereby juveniles are excluded by the more experienced adults (Cresswell 1994). It was not possible to record bird density during the night, because at low tide, the birds would forage up to 2 km from the shore and were mixed with other species of shorebird. Furthermore, poor visibility made it impossible to distinguish between adult and juvenile birds out on the mudflats. The logistical constraints on visual observations coupled with the sensitivity of redshank to human presence made behavioural observation through VHF telemetry the only reliable method by which nocturnal activities could be monitored throughout the home range of known-age birds. Future studies should seek to use these techniques to investigate intraspecific responses of individual birds to ambient light levels according to social status.
Studies into the effect of light levels on wildlife behaviour have hitherto measured ambient light directly using a hand-held photo-detecting diode (e.g. Gorenzel & Salmon 1995; Tuxbury & Salmon 2005). These measurements would not have been possible in the present study because the birds regularly occupied inaccessible mudflats, moreover, behaviour would have been altered by any human approach. Consequently, direct measurements of light would be biased towards localities close to the shoreline and would have resulted in an erroneous association between measured ambient light levels and the behaviour exhibited by the bird. Our approach, which utilised remotely sensed DMPS/OLS light radiance values gathered by satellite, provided a novel measure of ambient light levels throughout the entire estuary at a broad-scale resolution. We found that birds inhabiting areas with higher light radiance values foraged for significantly longer periods than birds inhabiting areas with lower radiance values. Similarly, the proportion of birds foraging on cloudy nights was elevated regardless of lunar illuminance (Fig. 2), presumably due to the reflection of artificial light sources with increased cloud cover (Kyba et al. 2011). While there was evidence of a relationship between foraging behaviour and DMSP/OLS light radiance values, this was not statistically significant. This may be attributed to low-intensity fine-scale point sources of light undetected by the satellites, the absence of truly dark areas in an urbanised estuary as well as undetected factors inherent to such a complex ecological system.
Observational studies have shown that nocturnal foraging may be less efficient than daytime foraging. This is because shorebirds are unable to detect the presence of the most profitable prey visually, making them less selective in prey choice under darkness (Goss-Custard 1969; Sutherland 1982). Foraging visually also allows shorebirds to scan for prey and handle prey at the same time, also increasing foraging efficiency (Evans 1976). Those shorebirds foraging by touch, however, are unlikely to locate more than one prey at a time. In this study, our tagged redshank exhibited a transmitter-pulse rate which implied visual foraging under a full moon, but this was not apparent when the full moon was obstructed by cloud cover. Similarly, tagged redshank inhabiting artificially illuminated areas exhibited a pulse rate indicative of visual foraging and operated independently of lunar phase. We argue that this allowed redshank to detect and select the most profitable prey.
When considering the trophic chain on a larger scale, redshank are predated by raptors by day (Whitfield 2003; Cresswell & Whitfield 2008), while owls and mammalian carnivores (including foxes Vulpes vulpes) can pose a serious threat at night (Page & Whitacre 1975; Sitters et al. 2001; Piersma et al. 2006). Tawny owls Strix aluco, short-eared owls Asio flammeus and red foxes were all observed hunting in areas frequented by the tagged redshank (R.G. Dwyer personal observation). While ambient light levels were found to improve visibility for sight-based foraging, increased night-time lighting could also affect predator and prey relationships. We suggest that higher light levels would not provide a significant advantage for nocturnal ambush predators with excellent night vision, perhaps even imposing a penalty, but could provide improved predator detection by their shorebird quarry. For example, some birds will choose to roost in areas of high night-time illumination in response to predation risk from owls (Gorenzel & Salmon 1995). The location of the eyes in many species of shorebird results in a blind area to the rear of the birds' head, rendering the bird vulnerable to predation when employing tactile foraging (Martin & Piersma 2010), and as a consequence, there will be a trade-off between being vigilant for predators or searching for prey items (Cresswell & Whitfield 2008). Shorebirds will often increase levels of vigilance in areas of poor visibility (Metcalfe 1984; Burger & Gochfeld 1991), and redshank may therefore be able to reduce vigilance time and also increase nocturnal feeding potential when foraging under elevated ambient light levels. Furthermore, tagged redshank in our study spent a similar amount of time foraging during the day regardless of the degree of nocturnal illumination in their foraging area. This provides further evidence that rather than a trade-off against predator disturbance, increased foraging under nocturnal illumination reflected improved foraging opportunities through enhanced visibility.
Estuarine and coastal areas throughout the world are being developed for industry, agriculture, mariculture, leisure and housing. These are critical habitat for shorebirds, yet the extent to which light pollution may impact upon their ecology has received little attention. Our study has shown that localised artificial illumination affects foraging behaviour in redshank in a manner similar to elevated natural light. We suggest that in estuaries close to major urban and industrialised regions, artificial illumination should be considered as an important environmental factor driving nocturnal habitat selection, foraging behaviour and potentially the structuring of animal communities. The integration of VHF radio transmitters with inbuilt posture sensors and illumination data from DMSP/OLS satellites provided an insight into the relationship between behaviour and ambient light levels which would have been otherwise logistically challenging. The study provides a framework for future investigators to assess the impact of artificial light upon animal behaviour and predator–prey relationships.