Introduction

One of the most investigated topics in behavioral ecology is that of birds and their vocal behavior in general, and songbirds and their songs in particular. Numerous studies have sought to explain the amazingly widespread phenomenon of the so-called dawn and dusk chorus [1], [2], i.e. the sunrise and sunset peaks in bird song output. As many as twelve non-exclusive hypotheses have been proposed to explain why twilight peaks in vocal display might be advantageous [1], [2], [3]. However, even after more than two decades of study, the basis underlying the dusk and dawn chorus is still unclear, in part because the complexity of this behavioral pattern seems to reflect different but non-conflicting needs within the same species [2], [4]. To date, the majority of studies on this topic have focused on songbirds, which might contribute to a biased view of bird vocal communication. It seems likely that if multiple hypotheses are necessary to explain songbird dawn and dusk choruses, many others could be necessary to explain the functions of vocal signaling at sunrise and twilight in other bird families. Until we gain a better understanding of daily patterns in signaling by as many as possible bird families, we will not completely understand why birds sing. In addition, we need to examine nonvocal means of communication and how they might be associated with vocalization. It is well-known that diurnal birds use an astonishing variety of color signals to visually communicate: did crepuscular and nocturnal species find a way to communicate by visual signals? Our present study shows that crepuscular and nocturnal species appear to have evolved white patches that, shown in association with vocal displays, allow them to communicate in dark surroundings.

Previous empirical studies have shown that ambient light plays a role in the evolution of color patterns and signals [5], [6], [7]. Therefore, any visual signal used around dawn and dusk should optimize the use of the available light. In this context, achromatic plumage patches are the best candidates for crepuscular signaling, as contrast is more important than color. In fact, the setting or rising sun forms the best light angle for using a white patch as a high-contrast signal against a dark background [5], [8], [9]. Not surprisingly, brightness contrast is a very common animal strategy for enhancing conspicuousness [9].

By studying the nocturnal eagle owl Bubo bubo that has been shown to perform dawn and dusk chorusing behavior [10], [11], [12], we herein investigate a novel hypothesis on why nocturnal birds with patches of white feathers call at twilight. We propose that white plumage patches and the timing of visual signaling have co-evolved to maximize the effectiveness of social communication such as the dusk chorus. This hypothesis centers on the recent discovery that eagle owls can adopt specific forms of visual signaling [13], [14], [15], and is supported by the observation that adult eagle owls possess a white throat badge that is only visible during vocal displays, when the throat is repeatedly inflated and deflated (e.g. coverable badges [16]; Video S1).

Results

The white throat badge contrasted most with the surrounding background and body during the owls' twilight chorusing (Figure S1). The levels of brightness contrast of white badge vs. background averaged 117.1±3.0, 138.8±3.0 and 37.7±4.4 during the pre-calling, calling and post-calling periods, respectively (F_2,482 = 276.7, P<0.0001; Table 1). Similarly, the contrast between the badge and the body was significant between the calling and post-calling periods, but not between the pre-calling and calling periods (F_2,482 = 291.7, P<0.0001;Table 1): the levels of brightness contrast of white badge vs. body averaged 139.6±6.0, 128.8±2.5 and 36.7±4.3 during the pre-calling, calling and post-calling periods, respectively. These two models explained 74.1% and 73.4% of the original deviance, respectively.

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Table 1. The main features of the two GLIMMIXs testing for the differences of the white badge versus background and white badge versus owl body during the pre-calling period, when owls were calling and during the post-calling period (see text for additional information).

https://doi.org/10.1371/journal.pone.0004960.t001

Discussion

As predicted, eagle owls perform their dusk vocal displays under the light conditions that best allow them to visually communicate with conspecifics through their badges. Due to incomplete knowledge of the physiological functioning of eagle owls, there are several different proximate mechanisms that can also contribute to the time of calling (e.g. peaks in testosterone before sunrise), but most of the main hypotheses previously used to explain the dawn and dusk chorus in birds [1] do not seem sufficient to fully explain the twilight behavior of eagle owls, at least when employed without the support of a visual signaling hypothesis. In fact, because this owl performs dawn and dusk choruses throughout the entire year, it seems difficult to believe that such calling solely represents a method of regulating daily hormone levels depending on the immediate social situation (i.e. self-stimulation hypothesis), attracting females (i.e. mate-attraction hypothesis), stimulating reproductive development (i.e. mate-stimulation hypothesis), or guarding mates (i.e. mate-guarding hypothesis). These hypotheses would seem unlikely because the mate fidelity of territory owners is generally expected to be stronger in eagle owls than in songbirds, and mate attraction, stimulation or guarding during or after the dawn chorus is nonsensical because after sunrise individuals retreat to their diurnal roosts to rest. Finally, since the eagle owl is a top nocturnal predator, it does not have to call under low light conditions to better avoid predation or because foraging is limited and low light levels could interfere with the ability to search for prey (as appears to be the case for Passerines; low predation and inefficient foraging hypotheses, respectively). We could further discard the inefficient foraging hypothesis because the activity peaks of the rabbit Oryctolagus cuniculus [17], the main prey of the eagle owl in Mediterranean regions [18], [19], partially overlaps with the eagle owls' dawn and dusk choruses.

Therefore, our findings concerning the patterns of vocal signaling allows us to hypothesize that eagle owls may principally vocalize at twilight because this timing of signaling maximizes the visual contrast of the white feathers associated with their vocal displays. Consequently, visual signaling may represent an important aspect of conspecifics communication. Under such a viewpoint, the evolution of a white badge that operates jointly with call displays at dawn and dusk may be relevant to the eagle owls' social dynamics. The need for visual signaling and social interactions under the best conditions of the eagle owl daily cycle could represent an alternative, or at least not mutually exclusive, to the proposed [20], [21] but controversial [22] acoustic transmission hypothesis, which predicts that birds are merely taking advantage of better sound propagation close to sunrise and sunset.

In their review of dawn chorusing, Staicer et al. [1] suggested that: “Many of the hypotheses are weak on explaining timing. A useful hypothesis must show that its proposed function depends on singing before sunrise…This problem can be addressed by collecting data for other species…Light level is obviously an important proximal cue for the time of acoustic signaling in birds, but, surprisingly, no one seems to have addressed why different species are cued by different light intensities.”

Finally, our explanation for the dawn and dusk chorus of eagle owls may possibly represent an overlooked but common pattern of signaling among crepuscular and nocturnal birds that combine patches of white feathers with twilight displays, such as other owls (e.g. great horned owl Bubo virginianus, great grey owl Strix nebulosa, little owl Athene noctua), great snipes (Gallinago media [23], bustards (Otis tarda), little bustards (Tetrax tetrax [24]) and nightjars [25]. Furthermore, our findings could be relevant to songbirds that breed in dark forest habitats and have contrasting white badges, as well as birds living in open habitats and showing contrasting bars (e.g. Charadrius plovers, many larks).

Materials and Methods

Supporting Information

Acknowledgments

The first draft of the manuscript was deeply improved based on the criticisms and suggestions of G.J.L. Beckers, G. Bortolotti, H. Pietiäinen, G.A. Sonerud, and D. Spector. Prof. L. Monje helped us with the Photoshop analyses of brightness contrast.