Every year, billions of seasonal migrants connect continents by transporting nutrients, energy, and pathogens between distant communities and ecosystems. For animals that power their movements by endogenous energy stores, the daily energy intake rates strongly influence the speed of migration. If access to food resources varies cyclically over the season, migrants sensitive to changes in daily energy intake rates may adjust timing of migration accordingly. As an effect, individuals adjusting to a common temporal cycle are expected to approach synchrony in foraging and movement. A large-scale periodic pattern, such as the dark–light cycle of the moon, could thus synchronize migrations across animal populations. However, such cyclic effects on the temporal regulation of migration has not been considered. Here, we show the temporal influence of the lunar cycle on the movement activity and migration tactics in a visual hunting nocturnal insectivore and long-distance migrant, the European nightjar, Caprimulgus europeaus. We found that the daily foraging activity more than doubled during moonlit nights, likely driven by an increase in light-dependent fuelling opportunities. This resulted in a clear cyclicity also in the intensity of migratory movements, with occasionally up to 100% of the birds migrating simultaneously following periods of full moon. We conclude that cyclic influences on migrants can act as an important regulator of the progression of individuals and synchronize pulses of migratory populations, with possible downstream effects on associated communities and ecosystems.

(A) Locations of breeding (square), wintering (triangles), and stopover (circles) sites. Colors correspond to panels B and C. (B) Individual stopover durations in the Temperate and Sahel zones, respectively. Vertical bars indicate medians, boxes indicate 25th to 75th percentiles, whiskers indicate ranges, and black dots indicate outliers. (C) Pooled distribution of stationary durations showing a peak at 22 days. The map was plotted using the R package rworldmap [ 20 ]. Underlying data are found in S1 Data .

We studied how the lunar cycle affects the migration tactic of European nightjars migrating between north European breeding areas and wintering grounds in southern Africa [ 18 ] using archival data loggers (global positioning system [GPS; n = 17], geolocation system [GLS; n = 12], and multisensor data loggers [MDLs; n = 10]) to record the movements of 39 individuals ( S1 Table ). The GPS and GLS position data documented the location and duration of stationary periods within the Temperate and Sahel zones, respectively ( Fig 1 ). We used wingbeat-induced acceleration data sampled by the MDL-tags to record daily flight activity patterns and evaluated the birds’ flight activity relative to the lunar cycle using periodic regression [ 19 ].

The approximate 30-day lunar cycle is a powerful periodicity globally affecting physiological and behavioral rhythms in a range of organisms [ 1 ], with documented effects on activity pattern and space use [ 2 – 5 ], predator–prey interactions [ 6 – 9 ], and reproduction [ 9 – 13 ]. By affecting foraging conditions in a predictable manner, the lunar cycle could potentially act as an important driver for the temporal progress of many animal migrants through its impact on daily energy intake rates during fuelling periods at stopovers [ 14 ]. However, studies on migration strategies generally assume static intake rates, while the temporal influence of periodically fluctuating fuelling conditions on migration speed has not been considered [ 14 – 16 ]. Within the nocturnal avian family of Caprimulgidae, several species are visual predators, whose activity patterns during breeding are influenced by the lunar cycle [ 9 – 11 ]. Dark nights restrict foraging activity to periods of twilight around dusk and dawn, while moonlit nights appear to relax this temporal constraint [ 9 ]. As migration speed is closely related to the time spent on fuelling at stopover and thereby the rate of fuelling [ 15 ], migratory Caprimulgids could minimize the overall time and energy spent on migration if their foraging effort results in high daily energy intake rates [ 17 ]. Hence, we expect that European nightjars adjust fuelling episodes during migration according to the lunar cycle in order to maximize daily foraging duration, and thereby reach maximum daily energy intake rates [ 14 , 17 ].

Results and discussion

The flight activity data revealed a predominantly sedentary lifestyle outside shorter episodes of migratory flights, with incidents of intermittent activity records around dusk and dawn, confirming the primarily crepuscular lifestyle of nightjars (Fig 2A, S1 Fig and S2 Data) [9–11]. We also found a periodic activity pattern during nighttime throughout the nonbreeding season, measured both as the daily number of activity registrations and daily number of hours with activity registrations, which were positively correlated with periodicity of the lunar cycle (linear mixed model: β = 2.09, SE = 0.230, P < 0.001, R2 = 0.285, var (Intercept) = 0.078, SD (Intercept) = 0.280, var (slope) = 0.327, SD (slope) = 0.572, S3 Data). The longest daily activity episodes of the nightjars thus matched the most moonlit nights in the lunar cycle (Fig 2B), during which the daily duration of intermittent activity was almost 2.5 times longer than during dark nights without moonlight. The individual heterogeneity in the relationship between the lunar cycle and presumed daily foraging duration may be a result of individual variation in seasonal phenology of the tracked birds [18]. Because of the latitudinal effect on night length (Fig 2A), the full moon will have a weaker effect on daily foraging duration at higher latitudes than within Africa. As the birds’ activity is recorded by the MDL-tag through its vertical axis, individual differences in tag orientation may also influence activity detection. Together these factors could contribute to individual heterogeneity in flight activity, as indicated by the variation in individual intercept.

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larger image TIFF original image Download: Fig 2. Individual activity pattern and presumed daily foraging time during the nonbreeding season of European nightjars. (A) Actogram showing the hourly activity index of an individual with no (white) to continuous (black) flight activity throughout the nonbreeding season. Gray corresponds to intermittent flight activity representing foraging flights. The bird’s activity is confined to the night and only exceptionally is activity recorded during daylight hours, which demonstrates the species’ crepuscular and nocturnal lifestyle. Black vertical lines represent periods of high activity spanning over several hours (indicative of migratory flights), and aggregations of black lines represent consecutive nights of migratory flights. Intermittent flight activity, presumably related to foraging, is concentrated towards dusk and dawn (horizontal arrows to the right). Following the daily cycle of the moon, intermittent flight activity is also registered during nighttime, resulting in diagonal bands throughout the nonbreeding season (vertical arrows). Notice the shorter activity periods from mid-April to May and in August, which reflect the shorter nights at northern latitudes. (B) The number of hours with registrations of presumed foraging activity per day and individual of nightjars in 2016–2017 (small dots) and daily means (large dots). Superimposed is a sine curve with a 29.54-day period, approximating the lunar cycle. Underlying data are found in S2 Data and S3 Data. GMT, Greenwich Mean Time. https://doi.org/10.1371/journal.pbio.3000456.g002

Daily increase in foraging activity may be due to (i) an increase in time available for foraging [9] or (ii) reduced foraging efficiency if lunar-phobic prey becomes less active and therefore less available during moonlit nights [6]. To distinguish between these two hypotheses, we tested how the daily travel intensity among the tracked nightjars correlated with the lunar cycle. Under the prediction that migrants will commence movement as they reach their preferred departure fuel loads [15], we expect elevated daily travel intensities (i.e., a larger fraction of the population to undertake migratory flights) after periods of moonlit nights if moonlight promotes fuel accumulation. To quantify daily travel intensity, we extracted migratory nights (defined by ≥3 hours of continuous flight, as registered by the MDL-tags, or >100 km covered by the GPS-tracked birds, respectively) and calculated the daily fraction of tagged individuals performing migratory flights. Like the daily foraging activity, the seasonal distribution of migratory flight nights showed a clear periodic pattern, with reoccurring episodes when the majority (occasionally 100%) of the tracked birds undertook migratory flights simultaneously (Fig 3A). When pooling the data relative to lunar cycle, the periodic pattern remained, with a peak in travel intensity 11 days following full moon (Fig 3B). This was also indicated by the significant relationship between lunar cycle and the tracked nightjar’s flight nights (generalized linear mixed model: β = 0.618, SE = 0.086, P < 0.001, var (Intercept) = 0.021, SD (Intercept) = 0.145, var (slope) = 0.123, SD (slope) = 0.351, S5 Data), which is expected if moonlit nights enhance daily fuelling rates according to hypothesis (i) above. Although the overall pattern shows lunar cycle–associated cyclicity in migratory flights, there is a great deal of individual variation (Fig 3). Migratory flights do occur also around new moon, but they are more frequent after full moon (Fig 3B). Such variation may arise if arrival to a new stopover is mistimed in relation to the full moon in order to enjoy optimal foraging conditions. In turn, optimal departure on migratory flights may be affected by winds because a wind may change the utility of the current fuel load [21, 22], leading to knock-on effects at subsequent stopover and timing of departures.

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larger image TIFF original image Download: Fig 3. Daily travel intensity of European nightjars. (A) Daily fraction of individuals tracked during 2015–2018 undertaking a migratory flight, ranging from none (0) to all (1). Filled and open circles represent the timing of new and full moon, respectively. (B) Travel intensity data from the migration periods pooled relative to the lunar cycle. The daily fraction of traveling nightjars increases during the waning moon and peaks 11 days after the full moon. Underlying data are found in S4 Data. https://doi.org/10.1371/journal.pbio.3000456.g003

The fuelling period is a time-consuming part of the migration, and variations in daily fuelling rates may have profound effects on the overall speed of migration [15]. Migrants whose objective is to minimize the overall time of migration are expected to depart from a stopover when their marginal rate of gain in flight distance, i.e., the instantaneous speed of migration, drops to the expected migration speed [15,17]. Individuals that have reached the minimum fuel load required for the next flight step could thus depart as a response to reduced daily foraging duration (and associated fuelling rates) [14]. The most rapid decline in foraging duration occurs one week after full moon and provides a potential fixed proximate departure trigger that could result in the synchronous migration pattern of the birds (Fig 4, dashed line). Alternatively, if the migrant could time fuelling periods relative to the lunar cycle, it should strive to allocate stopovers to the most moonlit nights, i.e., by centering stopovers around full moon. By doing so, it would maximize the ratio of foraging time for a certain fuel load and total time spent at the stopover. This would result in a positive relation between stopover duration and departure timing, relative to the lunar cycle (Fig 4, solid line). However, when evaluating the stopovers in the annual cycle of the European nightjars (Fig 1B), we did not find any relationship between stopover duration and the lunar-related departure timing (S2 Table). This may be due to individuality in timing of the initiation of migration (onset of first fuelling period) not influenced by the lunar cycle and/or external factors such as knock-on effects from earlier annual events. For example, a tail wind may trigger departure from a stopover before the optimal fuel load has been reached, which leads to suboptimal arrival with respect to the lunar cycle at the next stopover. Furthermore, the departure timings were consistently earlier than expected if the nightjars were striving to maximize the ratio between cumulative foraging time and total stopover duration (paired t test: t 37 = −9.11, P < 0.001, S3 Fig), suggesting that the birds respond to a fixed trigger relative to the lunar cycle when timing their departures. Our approach to use individual-based data loggers enabled us to record the nonbreeding movement of European nightjars and document the activity pattern related to the lunar cycle. However, we still lack information about feeding success and daily fuelling rates in relation to moon phases. It is therefore critical in future studies to focus on stopover ecology under the influence of the lunar cycle, preferably by studying individual departure decisions in relation to fuelling rates and fuel loads.

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larger image TIFF original image Download: Fig 4. Realized departure events and relative benefit of optimal departure timing under a range of stopover durations. Box plots at median stopover durations corresponding to the four annual stopovers (see Fig 1). Bars indicate median departures, boxes indicate 25th to 75th percentiles, whiskers indicate ranges, and black dots show outliers. Departures could be triggered by dwindling fuelling rates as a fixed proximate factor regardless of stopover duration (horizontal dashed line). Alternatively, the nightjars may strive to maximize the ratio between cumulative foraging time and total stopover duration by centering the stopover around full moon. This would lead to a positive correlation between stopover duration and departure timing relative to the lunar cycle, increasing from full moon to new moon as stopover duration increases towards one lunar month (solid line). Underlying data are found in S1 Data. https://doi.org/10.1371/journal.pbio.3000456.g004

European nightjars clearly exhibit periodically fluctuating activity patterns on both daily and seasonal scales that are strongly associated with the lunar cycle and likely driven by light-dependent foraging opportunities [9]. This temporal arrangement of the annual schedule allows for substantially increased migration speeds through increased daily fuelling rates [5]. However, it is not clear how the timing of migration translates into other annual events and how nightjars are able to keep their circannual schedule while tracking the shifting cycles of the moon [23]. As an example, under climate change, mistiming of arrival to the breeding area may have long-lasting negative population and fitness consequences [24–25]. In particular, the influence of periodically varying foraging conditions on the progression of migration could aggravate cross-seasonal effects such as substantially delayed arrival to breeding grounds if the migrants need to adjust departure timing to a new cycle of peak conditions [26]. Interestingly, a few of the tracked nightjars spent surprisingly long stationary periods prior to crossing the Sahara Desert (Fig 1B), suggesting that they may have awaited a second lunar cycle before commencing the barrier crossing. The link between arrival to the breeding ground and breeding success in nightjars is little known, although a temporal association between breeding events and the lunar cycle has been suggested for several species of Caprimulgids, including the European nightjar [10–11].

The lunar cycle is likely an important driver of the migration tactic of European nightjars, and this discovery may extend to other animal migrants whose foraging is affected by a periodically varying environment [1]. The lunar cycle has, for example, been directly linked to foraging behavior in nocturnal species of several groups that depend on vision for detecting and catching prey, such as seabirds [2,4,8], nightjars [10–11], and shorebirds, foraging in intertidal zones [27–28]. These groups comprise several species well known for their continent-wide migrations, whose timing of migration in relation to the lunar cycle remains unknown (except for the European nightjar as described here). Periodic fuelling conditions may affect both the timing of migration and its progression over large spatial scales, with potential downstream impact on both the migrants themselves and associated communities and ecosystems [29–31]. The degree to which large-scale movements of migratory populations are synchronized and temporally influenced could, for example, have potentially profound effects on local ecosystem functioning and pathogen dynamics [31–32]. Incorporating temporal dynamics of relevant environmental factors, such as celestial bodies, could thus be a promising inroad to further our understanding of the seasonal pulses of animal migrations and their trophic effects.