Sleep is a vital component of self-maintenance and plays an important role in energy conservation, cellular repair, and learning (Siegel 2005; Stuber et al. 2015). Severe sleep deprivation can reduce cognitive and physical performance (Huber et al. 2004), or may require compensatory adjustments at the expense of other activities (Fuchs et al. 2006). Sleep behavior varies considerably among bird species (Amlaner and Ball 1983; Campbell and Tobler 1984; Lesku et al. 2006). Amlaner and Ball (1983) describe sleep and rest postures for a range of species, including many waterbirds (predominantly gulls and ducks), finding similarities among closely-related species. In addition to evolutionary history, environmental factors such as light levels (Amlaner and Ball 1983), tidal state (Galusha and Amlaner 1978), predation risk (Lima et al. 2005), and social factors (e.g. Beauchamp 2011) can also strongly influence sleep.

Although sleep, rest and vigilance have been studied for several waterbird orders (Dewasmes and Telliez 2000; Gauthier-Clerc and Tamisier 2012; Handel and Gill 2012; Hayward et al. 2014), we are aware of only a single published study involving diurnal sleep in terns (Skipnes 1983) and none for nocturnal sleep (although see Weseloh & Shutt [2008] for roosting behavior prior to sleep). Across the day, Skipnes (1983) recorded an average of 13.9-35.6% of birds in a sleeping posture equivalent to Back Sleep as reported in other species (Amlaner and Ball 1983), with fewer birds sleeping late in the day. Contrastingly, large gulls (genus Larus) have been the focus of many studies (Galusha and Amlaner 1978; Bartholomew and Dawson 1979; Amlaner and McFarland 1981; Amlaner and Ball 1983), but these species may differ from terns in their sleep behavior because of disparities in exposure to interspecific predators at breeding colonies (Beauchamp 2011), preferences for nesting vegetation (Fasola and Canova 2006), or diet and daily activity cycles (Pearson 1968; Fasola and Bogliani 1990). The absence of information on nocturnal sleep represents an important knowledge gap, particularly for Common Terns (Sterna hirundo), because nocturnal predation is a major cause of breeding failure (Cuthbert et al. 2003; Nisbet et al. 2017). Thus, understanding sleep behavior and vigilance may have significant conservation value.

Many studies have reported effects of predators on sleep behavior. Under immediate (or perceived) predation threat, birds alter sleeping postures, becoming more vigilant (changing from deep-sleep to rest-sleep postures, opening eyes) and reducing rates of eyelid closure (Amlaner and McFarland 1981; Lendrem 1983, 1984). Other factors that may affect sleep include nesting habitat, colony or group size, and the presence of other nesting waterbirds. Vegetation cover at nest sites has been found to interact with predation risk, increasing vigilance of incubating Mallards (Anas platyrhynchos) when line-of-sight is blocked (Javůrková et al. 2011). Increased group size also affects vigilance as lower levels are required of an individual, per capita predation threat may be reduced (“dilution effect”), and many potential prey may create confusion for hunting predators (Foster and Treherne 1981; Beauchamp and Ruxton 2008, 2012). Reduced necessity for watchfulness may lead to increased sleep or different sleep behaviors (Gauthier-Clerc et al. 1998, 2002; Dominguez and Dominguez 2003; Lima et al. 2005). Advantages of group size might also be derived from nesting in mixed-species colonies, assuming that information about predation risk can be interpreted from other species (Beauchamp 2011).

We studied nocturnal sleeping postures of incubating Common Terns and explored variation in sleep and vigilance for six breeding seasons at Gull Island, Ontario, a small mixed-species colony in Lake Ontario. To examine whether sleep behaviors and vigilance varied between colonies, in 2018, we also collected the same data at a larger, single-species breeding colony at Oneida Lake, New York State, USA. At both colony sites, we used data concerning eye closure and posture to provide a first description of nocturnal sleep behavior of incubating Common Terns and its variability.

Methods

Data Processing

Over 1.3 million images were captured, and all nocturnal images were visually checked for presence of nest predators, periods when active nests were unattended, adverse weather (rain and wind), and flooding from high water events. Prior to extraction of data on nocturnal posture and vigilance, we excluded any camera-nights without a complete sequence of nocturnal images: uninterrupted images at 1-min intervals throughout the nocturnal period. This period was defined as from 30 min after infra-red flash activation to 30 min prior to flash deactivation. We also excluded any camera-nights when no visible terns were actively nesting or visible terns were within management grids of the Gull Island colony, since grids on this island were designed to protect terns from predators and may potentially influence vigilance and sleep behavior.

Figure 1.

Possible sleep postures used by waterbirds, illustrated for gulls (in which all behaviors except HG have been recorded [Amlaner and McFarland 1981; Amlaner and Ball 1983; Henson et al. 2007]): HG = Head on Ground; BH = Bill Horizontal (bill in line with or above body axis); BS = Back Sleep (head turned back, bill on back and/or tucked under scapulars); and FS = Front Sleep (head drawn slightly in, bill below horizontal body axis). Illustration by Zoe Korpi.

Study nests were then determined prior to data extraction for each sequence of images taken within the same field of view, often over multiple nights. Two criteria determined study nests: birds at study nests were consistently visible (i.e., not obscured by vegetation or other birds) over a series of images taken throughout the sequence, and they were close enough for eye closure to be detectable on images (≤ 7 m from the camera). Any nests that became permanently abandoned before or during observation periods were excluded from the study. Nocturnal posture and vigilance (see Analyses) were recorded for birds incubating at study nests (“study birds”) between the onset of darkness and dawn, defined as 30 min after infrared flash activation and 30 min prior to infrared flash deactivation. Number of study birds during each sequence ranged from 1-4 at Gull Island and 1-3 at Little Island over the nights that fulfilled all the above criteria (83 at Gull Island, 40 at Little Island).

In each image, the behavioral posture of each study bird was assigned to one of the categories described by Amlaner and Ball (1983) for sleep postures across the class Aves (illustrated in Fig. 1), and we also recorded whether at least one of each study bird's visible eyes was open or closed. If neither of the bird's eyes were visible temporarily, e.g., bird with back to camera, we excluded this record. Electroencephalographic measurements have shown that eye closure and sleep are closely related (Rattenborg et al. 1999), making eye closure a reliable indicator of sleep in birds (Amlaner and Ball 1983; Campbell and Tobler 1984; Wellmann and Downs 2009). Finally, we recorded the number of study birds that were visible but standing away from their nests (“off the nest”) and images in which all study birds were absent (as a proxy for nocturnal desertion).

Results

Only two (Back Sleep, BS and Front Sleep, FS) of the four potential sleep postures (Fig. 1) were used for nocturnal sleep by incubating Common Terns in our study. There were large differences between our two study colonies in the proportion of time spent by Common Terns in different sleep behaviors (Fig. 2), with much less sleep at Gull Island (22% of nocturnal hours vs 65% at Little Island), of which only 7% were deep sleep (Fig. 2). Common Terns at Gull Island were far more vigilant than those at Little Island (64% vs. 17%) and spent less time with eyes closed in Back Sleep (the deepest sleep posture) (7% vs. 42%, Fig. 2). Proportion of time spent in Back Sleep was 75% lower at Gull Island than at Little Island. Terns at both colonies spent a similar proportion of time in Front Sleep, but at Gull Island they were twice as likely to have open eyes in this posture (Fig. 2). Overall, Common Terns incubating at Gull Island were vigilant for 63.7% of the night versus only 17.2% at Little Island (Fig. 2).

Figure 2.

Relative proportions of time spent by incubating Common Terns in three categories of behavioral posture at (a) Gull Island and (b) Little Island during nocturnal hours. These categories are further subdivided according to whether at least one eye was open (-O, strippled fill) or not (-C, solid fill). Time spent off the nest is excluded from these graphs but accounted for <1%. NS represents non-sleep behaviors, predominantly BH with eyes open, but a small proportion of other behaviors, e.g. calling. HG postures were never observed. Illustration by Zoe Korpi.

Nightly Proportional Vigilance varied between predation risk categories (F_{2, 58} = 94.5, P < 0.001), although the only statistically significant differences were those between “No Predation Risk” (Little Island) and the other two categories (Gull Island). Much overlap existed in Proportional Vigilance between nights classified as “No Immediate Predation Risk” and “Immediate Predation Risk” (Fig. 3), both categories comprising data from Gull Island only. Periods of nocturnal desertion by birds at all visible study nests were highly variable across nights, and the mean proportion of a night deserted (mean ± SD) was 0.21 ± 0.18 for “No Predation Risk”, 0.21 ± 0.28 for “No Immediate Predation Risk”, and 0.32 ± 0.29 for “Immediate Predation Risk”.

Figure 3.

Boxplot of proportion of incubating Common Terns recorded with eye(s) open (“Proportional Vigilance”) during nocturnal hours at Gull Island when a predator was likely present (“Immediate Predation Risk”, n = 8 nights), at Gull Island when no predator was present (“No Immediate Predation Risk”, n = 13 nights) and at Little Island when no predator was present (“No Predation Risk”, n = 40 nights). Circles indicate outliers: 1.5 × interquartile range above the upper quartile.

Discussion

To date, no quantitative data have been published on nocturnal sleep posture in terns. Our results indicate that Common Terns utilize Back Sleep and Front Sleep, which are sleep/rest postures reported for many bird species (Amlaner and Ball 1983). In Back Sleep, Common Terns turned their head backwards and tucked their bill under their scapulars to differing degrees. In Front Sleep, the head was forward, but drawn in slightly, and the bill hung below the horizontal body axis. These two postures are nearly identical to those recorded for sleep/rest in closely-related species, such as gulls (Bartholomew and Dawson 1979; Amlaner and McFarland 1981; Amlaner and Ball 1983; Shaffery et al. 1985) and shorebirds (Dominguez and Dominguez 2003; Handel and Gill 2012). In Herring Gulls, for example, the deepest sleep posture is Back Sleep, where the bill is tucked under the scapulars, while Front Sleep, with the head drawn into the breast and head and bill slightly lowered, is a rest-sleep posture (Amlaner and Ball 1983, Amlaner and McFarland 1981). Slight variations of these two postures are also common among less closely-related waterbirds, such as ducks and penguins (Amlaner and Ball 1983; Stahel et al. 1984; Dewasmes and Telliez 2000), as well as distantly-related species, such as raptors and passerines (Amlaner and Ball 1983). Thus, these sleep postures are likely to be derived largely from shared evolutionary history and/or morphological constraints of body design.

Common Terns at Gull Island were far more vigilant than those at Little Island and spent less time with eyes closed in Back Sleep (the deepest sleep posture). These differences were surprisingly large, and because Common Terns at Gull Island slept barely one-third as much as terns at Little Island this could possibly lead to long-term physiological impacts (Huber et al. 2004) or necessitate compensatory mechanisms (e.g., increased diurnal sleep, Fuchs et al. 2006). Such differences between sites also indicate that in terns, as in other species (Rattenborg et al. 2017), prevailing environmental factors may play an important role in determining nocturnal sleep.

Because predation risk is one of the best studied and most commonly reported factors influencing sleep (Lima et al. 2005), we attempted to examine the effect of predation risk separate from the other factors that varied between our two colonies. However, because our two colonies differed in other factors that may have affected sleep behavior (colony size, vegetation, other nesting waterbirds), we could not fully dissociate the effects of predation from other site differences. By categorizing Gull Island observations as either “Immediate Predation Risk” or “No Immediate Predation Risk”, we expected vigilance to decline following this order (as in other studies, Lima et al. 2005; Stuber et al. 2014) and be lowest at Little Island, where nocturnal predation was not recorded in the year of study (“No Predation Risk”). Even though vigilance was lower at Little Island, lack of a significant difference between “Immediate Predation Risk” and “No Immediate Predation Risk” categories (both from Gull Island, Fig. 3) does not strongly implicate predation as driving vigilance differences between our two sites. It is possible that this result may be confounded if nightly sleep is already constrained to its required minimum levels at Gull Island (preventing elevated response under immediate predation threat), or if terns respond to nocturnal predation up to a week after a predator's final visit (e.g., Hunter and Morris 1976; Nisbet and Welton 1984; Wendeln and Becker 1999; Arnold et al. 2006), thus obscuring vigilance differences on nights categorized as “No Immediate Predation Risk”. Periods of nocturnal desertion showed a different trend, being only longer on nights of “Immediate Predation Risk” but were too variable to permit a statistical comparison of appropriate power.

Aside from predation risk, possible explanations for disparity in sleep between our two study colonies are differences in colony size (Beauchamp and Ruxton 2012), vegetation cover (Javůrková et al. 2011), and proximity to other species (Roberts 1996). Our data were insufficient to examine colony size effects distinct from predator effects, because nights with substantially different colony sizes were rare. Vegetation close to nests has been reported to increase vigilance behavior in nesting Mallards, whose nest predators primarily use olfactory cues (Javůrková et al. 2011). Night-herons and owls hunt by auditory or visual detection (Hunter and Morris 1976; Nisbet and Welton 1984) and terns, like gulls (Ball et al. 1984), probably also use auditory and visual cues to detect predators. Thus, although extensive and tall (>1 m) vegetation decreases the chance of being seen by a predator, it also requires that terns rely more on auditory predator detection, which may increase vigilance (Ball et al. 1984). Increased vigilance at Gull Island supports this idea, but vegetation effects are largely confounded with predation risk because of the absence of predation at Little Island in our study. Alternatively, it is possible that the presence of 20,000-30,000 nesting Ring-billed Gulls at Gull Island may be responsible for increased vigilance. Ring-billed Gulls compete with Common Terns for nest sites (Cuthbert et al. 2003; Morris et al. 2010), can eat tern eggs (Nisbet et al. 2017), and also provide constant noise (ranging from 77.4 - 102.5 dB, Blokpoel and Neuman 1997) that may hamper auditory surveillance against predators.

In addition to providing the first detailed description of nocturnal sleep behavior in terns, we found that the extent of nocturnal sleep achieved by incubating Common Terns varied greatly between colonies; it was notably very low at Gull Island (deepest sleep during <7% of nocturnal hours). Because sleep deprivation can lead to physical and cognitive impairment (Huber et al. 2004), and may require compensatory diurnal sleep that reduces provisioning rates and vigilance (Fuchs et al. 2006), our results call for a deeper exploration of these potential consequences as well as the possible factors influencing sleep in terns.