The Pectoral Sandpiper (Calidris melanotos) is one of a few highly polygynous shorebirds with strong sexual size dimorphism. The vocal part of the male courtship display has received some attention, but how the sound is generated is largely unknown. To fill this gap, we analyzed video and sound recordings collected on the breeding grounds at Barrow, Alaska, USA. The anatomy of 2 males was investigated by macroscopic and histological dissection. Synchronized wing movements and a closed beak accompany hooting calls during flight displays. Courtship vocalizations on the ground include stereotypic beak and hyoid movements. We found a symmetric bipartite syrinx with songbird-like adduction and abduction mechanisms. Lateral and medial labia consisted of homogeneous extracellular matrix containing collagen fibers, which were only loosely organized, few elastin fibers, and a high proportion of hyaluronan. The upper vocal tract includes the trachea and an inflatable esophagus supported by thick and heavy skin over the ventral neck region. A highly organized network of fat and collagen makes this skin region relatively thick but also stretchable and robust. The hyoid skeleton was not distinctly different from that of pigeons, a group that also uses esophagus inflation to produce their characteristic sounds. These data lay a foundation for understanding the acoustic properties of the vocal signals used in territorial and courtship contexts.
The combination of visual and acoustic courtship signals is a hallmark of many complex mating displays and is particularly spectacular in promiscuous species (e.g., Darwin 1871). A vivid example is the elaborate courtship display of the male Pectoral Sandpiper (Scolopacidae: Calidris melanotos; Pitelka 1959, Pitelka et al. 1974, Myers 1982, Nelson 1884). Males produce “hooting” calls while performing a ritualized flight pattern, either along the border of their territory (Myers 1982) or low, over a female hidden in the tundra vegetation (Figure 1A–1C). Males also produce a different acoustic signal together with a visual display while on the ground near a female (Figure 1D, 1E; Myers 1982, Lesku et al. 2012). Here, we report on the anatomical basis of 2 striking features of this multimodal display: the extension of the neck region (“throat sac”) and the vocal “hooting” signal.
The Pectoral Sandpiper's mating system is unusual among the subfamily Calidridinae. Shorebirds (Charadriiformes: ∼350 species—sandpipers, plovers, gulls, and allies) demonstrate a large diversity of mating systems (Székely and Reynolds 1995, Reynolds and Székely 1997, Bokony et al. 2003, Thomas et al. 2007). The Pectoral Sandpiper breeds in the Arctic and can be categorized as highly polygynous (Farmer et al. 2013) and as displaying on an exploded lek (Emlen and Oring 1977). The Pectoral Sandpiper shows strong sexual dimorphism, as is typical for species in which strong sexual selection on elaborate male displays occurs through male–male competition or female choice. Males defend territories and actively pursue and court females 24 h a day, but females do not necessarily forage or nest on the territory (Lesku et al. 2012, Farmer et al. 2013). Females build the nest, incubate the eggs, and brood and guard the hatchlings without any male assistance. No persistent bond is formed between the male and female.
The vocal part of the male courtship display has received some attention, but how it is generated remains largely unknown (Farmer et al. 2013). The courtship call in flight is a low-pitched hooting call, and the calls are uttered in long bouts (Miller et al. 1988) with an extended neck region (“throat sac”) (Figure 1A–1C). The “throat sac” is also extended during parts of the courtship on the ground (Figure 1D, 1E), but the vocalizations are very different (Lesku et al. 2012). The anatomical basis of the temporal neck extension has been debated (Nelson 1884, Sutton 1932, Pitelka 1959, Portenko 1968), but it resembles what has been described as esophagus inflation in pigeons (Columbidae; Riede et al. 2004). The gas volume inside the esophagus increases when air flows through the syrinx in the expiratory direction. To sustain this inflation, the beak and nares must be closed to provide a tight seal (cf. Riede et al. 2004). Although the syrinx anatomy of some Charadriiformes has been studied (King 1989, Brown and Ward 1990), the syrinx of the Pectoral Sandpiper has not been investigated, and it is unclear how much it contributes to the characteristic low-pitched aerial vocalization.
Vocalizations were recorded with a Sennheiser ME67 directional microphone and a Microtrack II, M-Audio solid-state recorder near Barrow, Alaska, USA (71°18′N, 156°44′W). Using an acoustic analysis of hoot and courtship vocalizations, we determined fundamental frequency range and spectral emphasis using PRAAT version 5.2.12 (see Acknowledgments).
Video recordings became available through cameraman Ralf Schiecke (Doclights, Hamburg, Germany). Two sequences of hoot vocalization during flight and 2 sequences during ground displays were recorded at 240 frames s−1, with a playing speed of 25 frames s−1. One video of a phase 1 courtship display was recorded at 33 frames s−1. Video analysis was performed with MaxTraq version 2.12b (Innovision Systems, Columbiaville, Michigan, USA). Distances were computed from the coordinates of 4 manually placed points (tips of upper and lower beak, distal tip of left wing, and shoulder joint) in each video frame. Wing movement was estimated as the distance between the wingtip and a horizontal line through the shoulder joint (Figure 2; Supplemental Material Video 1). Beak gape was estimated as the distance between the 2 beak markers. Videos also revealed movements of the hyoid skeleton. When the lateral elements of the hyoid skeleton (“cornua”) moved laterally, they generated a bulging of the neck area ( Supplemental Material Video 2). The presence or absence of this lateral bulging was marked in each video frame.
Two male specimens of Pectoral Sandpipers were collected during the peak period of male display in June 2011, at the breeding site in Barrow (Lesku et al. 2012). The 2 specimens were subjected to macroscopic dissection and photographic documentation while being submersed in water. This technique facilitates the discerning of structural details. Photographic documentation was done with a Canon XTi digital camera. Dissections focused on the proportions of the oral, pharyngeal, and esophageal cavity and surrounding tissues, the hyoid skeleton, the beak, and the histological structure of the syrinx.
Labia in the syrinx contain cellular components (fibroblasts) and extracellular matrix (elastin, collagen, and hyaluronan). All 3 matrix components determine viscoelastic properties, or how the respective tissue responds to deformation (oscillations of labia or stretching of the skin). Syrinx and ventral neck-skin specimens were fixed in 10% buffered formalin phosphate (SF100-4; Fisher Scientific) for 1 wk. Serial coronal sections of the syrinx and skin cross sections (5 μm thick) were stained with haematoxylin–eosin for a general overview, Masson's Trichrome (TRI) for collagen fiber stain, Elastica-Van Gieson (EVG) for elastic fiber stain, or alcian blue (AB) stain (pH 2.5) for mucopolysaccharides and glycosaminoglycans. We also performed a digestion procedure with bovine testicular hyaluronidase (2 hr at 37°C) in combination with a subsequent AB stain. Incubation with bovine testicular hyaluronidase increases specificity for various acid mucosubstances in the AB stain. If hyaluronan is a major component of the mucosubstances, the AB stain is destroyed. All stains were performed in conjunction with control stains on human tissue in order to confirm positive stains for the respective material (liver for TRI, artery for EVG, and umbilical cord for AB). Staining was conducted at the HSC Cores Research Facility at the University of Utah (Salt Lake City, Utah, USA). Stained sections were digitized with a ScanScope CS2 slide scanner (Aperio, Vista, California, USA).
Sound and Video Analysis
Acoustic analysis of the vocalizations used in courtship showed a fundamental frequency range from 170 to 600 Hz. In hoot calls given during flight, the fundamental frequency (F0) appears to be between 170 and 220 Hz (Figure 3), and the second harmonic (2F0) is emphasized. An alternative interpretation that there are sidebands at exactly half of the fundamental frequency cannot be ruled out, but it seems unlikely without an apparent modulation at this frequency.
Video analysis suggests that multiple wing movements are associated with each hoot vocalization. Two large and one smaller wing movement occur with every beak opening (Figure 4). At the end of the second large wing movement, the beak was opened for 62 and 91 ms, respectively, which is similar to the duration of the pauses between 2 hoot calls (76 ± 2.6 ms; averaged means measured in 4 hooting sequences from 4 different birds). We assume that the beak opening coincides with an inspiration. The function of the half wingbeat is not clear. It could be part of a visual signal or simply a stabilizing movement before the next hoot call. Every inhalation is accompanied by a rapid upward movement of the head and downward movement of the throat. This, in combination with the bouncing throat sac, could disturb the bird's balance, requiring adjustment with an additional, smaller wingbeat.
Hoot calls are typically given at a rate of 2–4 s−1, in series of 10–20 calls (Figure 3; also see Pitelka 1959). Call rates are fastest in the center or toward the end of the hooting series, reaching an average rate of 3.9 hoots s−1 (n = 576 recordings from 79 color-banded males). A hoot series contains, on average, 16 hoot calls but can contain ≤50 calls.
Courtship vocalization sequences given on the ground consist of 3 phases that transition into each other. One such transition between 2 phases is shown in Figure 5. F0 in such courtship vocalizations ranges between 400 and 600 Hz. Different phases are characterized by an emphasis on different harmonics (Figure 5C). Video analysis of a phase 1 sequence shows that sounds are produced with open beak and slightly extended throat sac (Figure 6). Before and after this calling sequence, the throat sac was more inflated, which suggests that the partly inflated throat sac during phase 1 functions as a visual signal rather than serving an acoustic filter function. Interestingly, beak and hyoid skeleton are moved synchronously. As x-ray studies in doves have shown, the esophagus is actively inflated prior to vocalization (Riede et al. 2004). It remains partially extended even when the beak opens and internal pressure equalizes with ambient pressure. A full deflation requires contraction of skin musculature.
The emphasis in the frequency range between 2,000 and 3,000 Hz (Figure 5E) is probably also produced with open beak, whereas the singular emphasis on the range around F0 (500 Hz) is probably produced with closed beak and inflated esophagus (Figures 1E and 5F). In summary, throat inflation associated with a closed beak is required during phase 2 and serves an acoustic filter function (such as during hoot calling). During phases 1 and 3, the throat sac remains partially inflated and may serve mostly a visual function.
The dissection revealed that the esophagus is the only inflatable structure in the head and neck area (Figure 7). No pouches or other extensions could be identified in the oropharyngeal area, the esophagus, or the trachea. The esophagus of both specimens could be injected with dental cast to a volume of 50 mL (Figure 7). However, it is unlikely that sandpipers inflate their esophagus much beyond 30 mL, because the trachea became compressed at volumes greater than that, which would prevent airflow and, thus, further inflation and syringeal sound production.
The skin overlying this area of the esophagus was thicker than in dorsal areas and below the neck because of large amounts of fat embedded into connective tissue. Strands of striated muscle were embedded in the composure of fat and connective tissue. A thick subepithelial layer of collagen fibers was also present, probably providing tensile stability (Figure 8). Fat cells were encased in pockets made of collagen fibers.
The hyoid skeleton, which helps to facilitate tongue movement, is composed of the basihyale, urohyale, pairwise ceratobrachiale, and epibrachiale (Figure 9). The most prominent difference from a columbiform hyoid is the longer paraglossale.
The tracheae of the 2 birds measured 82 and 88 mm, respectively, between larynx and tracheal bifurcation (similar to previous measurements by Audubon 1842). The bronchial syrinx of the sandpiper is a bipartite vocal organ with a high degree of symmetry between both sides (Figure 10). A pessulus-like structure is formed by 2 thin parallel beams that bridge the tracheal lumen between the ventral and dorsal wall. A medial membrane (composed of a medial labium and medial tympaniform membrane in songbirds) is 70–200 μm thick. It spans from the pessulus cranially to the 5th bronchial ring rostrally. It consists of collagen, elastin, hyaluronan, some fibroblasts sandwiched between epithelia facing the interclavicular air sac medially and the bronchial lumen laterally. The lateral labia are very large on both sides. Their tissue appears to be homogeneous and is composed of collagen, elastin, and hyaluronan. No interbronchial ligament was found.
The tracheolateral muscle (TLM) runs laterally on the trachea and attaches via a narrow tendon to the third bronchial half ring (A3) (Figure 11). The attachment to the tympanum or the first bronchial half ring is described as the ancestral condition (King 1989:123), indicating a somewhat derived condition in the Pectoral Sandpiper. King (1989) suggests that this condition in which the TLM moves its insertion caudally—as in the Pied Plover (Vanellus cayanus), another species within Charadriiformes—could represent an intermediate stage in the evolution or differentiation of an extrinsic to an intrinsic syringeal muscle from a caudal portion of the TLM. The TLM attachment in Pectoral Sandpipers resembles the pattern found in songbirds, in which the dorsal and ventral tracheobronchial muscles attach to and cause a rotation of A3 either to adduct or abduct the lateral labia (e.g., Larsen and Goller 2002). The exact function in Pectoral Sandpipers remains to be investigated, but it is most likely that TLM contraction abducts the lateral labium.
The morphological findings are summarized in Figure 12. Esophagus inflation is the most likely mechanism that causes the neck extension (“throat sac”) during the hoot calls in Pectoral Sandpipers. The highly flexible tissue characteristics of the esophagus wall and overlying skin facilitate the extension. Similar morphology has been described in Columbidae, which use esophagus inflation to produce their calls (Riede et al. 2004). The sandpiper syrinx is a bipartite symmetric sound source. Lateral labia are large homogeneous tissue masses consisting of extracellular matrix that contains fibrillar proteins such as elastin and collagen as well as amorphic substances such as hyaluronan. The labia composition is not different from that in songbirds (Riede and Goller 2010a). The homogeneous one-layered morphology of the labial extracellular matrix, associated with a fundamental frequency range of <1 kHz, corresponds well with the predictive relationship between labial morphology and a species' fundamental frequency range found across songbirds (Riede and Goller 2014). Labia are probably set into vibration by a passing airstream. Muscle activity adducts the labia into prephonatory position, and their viscoelastic properties and the driving aerodynamic forces determine their oscillation rate and thereby the acoustic output (Riede and Goller 2010b). It is likely that the large homogeneous labia support the production of the low-fundamental-frequency sounds. Related species of similar size are reported to produce mostly higher-pitched sounds (Miller 1992, Miller and Baker 2009), and we would expect different labial morphology.
The adaptation of the geometry of the upper vocal tract is well-known in birds (Riede and Goller 2010b) and is achieved either by movements of the hyoid skeleton (Riede et al. 2006, 2013, Riede and Suthers 2009) or by esophagus inflation (Riede et al. 2004, Dantzker and Bradbury 2006), or, in the case of the Pectoral Sandpiper, by a combination of both. Initially, the esophagus is most likely inflated prior to vocalization by 1 to 3 expiratory movements and closed beak and nares, as has been found in doves. The anatomical challenge to inflate the esophagus is twofold. First, a tight seal rostral to the glottis must ensure that expired air is collected in the esophagus and not leaking through the beak. The larynx can engage with the palate to form a tight seal (Zweers et al. 1981, Zweers 1982, Zweers and Berkhoudt 1986). Second, the pharynx, the esophagus, and the overlying skin must be sufficiently elastic and flexible to allow expansion.
Dynamics of Vocal Production and Inflation Behavior
Inflatable upper-vocal-tract structures associated with vocal production exist in many vertebrate taxa, not just in birds (e.g., frogs: Ryan 2001, Gridi-Papp 2008; mammals: Frey et al. 2007, Riede et al. 2008). Esophagus inflation in birds is used during vocal behavior by species from different families (e.g., Neunzig 1921, Chapin 1922, Niethammer 1961, Dantzker et al. 1999, Riede et al. 2004), which may indicate independent evolution of this feature. The inflated esophagus and sound radiation through the skin of the neck generate a strong filter effect (Fletcher et al. 2004, Riede et al. 2004). The stretched skin acts as a band-pass filter eliminating higher and lower spectral energy, thereby limiting energy to one harmonic (Fletcher et al. 2004). The tracheal tube is an initial resonant structure, and a subsequent filter effect is facilitated through the action of the extended hyoid and the inflated esophageal sac. The filter effect of this sac is only moderately affected by the degree of inflation.
In order to be engaged to act as a filter and acoustic coupling device, the esophagus must be inflated prior to vocalization; considering the large volume, this inflation must take several respiratory cycles. Once inflated, escape of air must be prevented by keeping the beak closed. Behavioral observations suggest that during a display flight, the esophagus is cyclically inflated and deflated (Pitelka 1959, Farmer et al. 2013). Presumably, opening the beak and/or disengaging the larynx from the palate for breathing causes a passive deflation through recoil of the esophagus wall and overlying skin, though not completely. At this point, in order to maintain an inflated esophagus for the next cycle, active deflation through muscles is unlikely. Ring Doves, for example, require 3 to 5 respiratory cycles to inflate the esophagus, and the inflated esophagus deflates by ∼30% within 1 s if the seal is opened (T. Riede personal observation).
If the esophageal pouch were filled with fully oxygenated air, and this air could be moved to the lung, 30 mL would sustain flight for ∼8.4 s, assuming a flight metabolic rate of 8 mL O2 s−1·kg−1 and a body mass of 94 g (e.g., Torre-Bueno and Larochelle 1978, Bundle et al. 2007). Therefore, it is not surprising that repeated inflation and deflation occur during a display flight, in which the hooting phase lasts, on average, 4 to 5 s. The throat is slowly inflated once before the hooting starts, then the throat sac swings forth and back with each hoot, and finally the throat is deflated again after the end of the hooting. Hoot calls are synchronously produced with wing beats (Pitelka et al. 1974, Miller et al. 1988, and video analysis in present study). The beak is rhythmically opened during the hooting as well as during the courtship vocalization (Figures 4 and 6). We assume that in hooting, the opening coincides with the short period of inhalation between hoots.
In doves, F0 and vocal-sac resonance match (Riede et al. 2004), whereas the sandpiper vocal tract (trachea, larynx, and vocal sac) emphasizes higher harmonics (i.e. frequencies of 350–2,500 Hz, but rarely F0; exception in Figure 5C). Sound is radiated from the inflated esophagus and overlying skin. Free skin—either on the entire neck, as in the Ostrich (Struthio camelus) and frigatebirds (Fregata spp.), or as smaller sacs, as in the Greater Sage-Grouse (Centrocercus urophasianus)—can generate specific radiation patterns around the vocalizing male. The specific radiation patterns can perhaps be advantageous in “targeting/addressing” a female in the vicinity (Dantzker et al. 1999). The inflation is often associated with an important and obvious visual signal, colorful skin or feathers in the throat area (frigatebirds and Greater Sage-Grouse), elaborate body movement (head bobbing in pigeons and doves), or a highly stereotyped flight pattern (sandpipers; Miller 1983a, 1983b). The rhythmic increase in neck size in less colorful species (e.g., Pectoral Sandpiper, pigeons, and doves) may serve to potentiate the advertisement signal and is evaluated by females or by other males.
Sexual selection acts through male–male competition and female choice (Darwin 1871), and sometimes these mechanisms favor different traits. Hoots are given in male–male competition: Males may hoot while flying in parallel next to each other or, more often, while flying alone along territory boundaries. Hoots are also produced in a context that suggests advertisement to females (W. Forstmeier and B. Kempenaers personal obervation). A male's long hooting flights appear to be specifically targeted to females sitting on the ground. The male performs 2 or 3 hooting flights, during which it passes just a few centimeters over the female's head before landing and approaching the female. During courtship (Figure 1), males perform multiple “phases” during which higher-pitched vocalizations (phases 1 and 3) as well as deep gurgling sounds (phase 2) are produced. Calls of phase 1 and phase 2 are illustrated in Figure 8. The use of low-pitched sounds in both male–male competition and advertisement to females strongly suggests that both components (intrasexual and intersexual selection) contribute to the evolution of this extreme signal.
We thank M. Valcu for help in designing the Barrow field study, for database management, and for discussion; A. Jacot for help with the sound recordings; a large number of assistants for help in the field; and R. Lanctot from the U.S. Fish and Wildlife Service (Anchorage) and G. Sheehan from the Barrow Arctic Science Consortium for logistical support. We thank L. Schlicht for the artwork in Figure 12. Birds were collected under U.S. Fish and Wildlife Service permit MB-210494-0 (principal investigators B.K. and Niels Rattenborg). PRAAT software is available at http://www.fon.hum.uva.nl/praat/. This work was supported in part by NIH grant DC06876 and by the Max Planck Society.
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A male Pectoral Sandpiper produces hoot calls during flight (high-speed video recording at 240 frames s−1, with a playing speed of 25 frames s−1). The tip of the left wing was marked with a white dot. The wing-movement analysis is presented in Figure 4. Video credit: Ralf Schiecke/Doclights
A male Pectoral Sandpiper produces a phase 1 courtship display (video recorded at 33 frames s−1). The beak-movement analysis is presented in Figure 6. Note how the hyoid movement caused a lateral bulging of the neck area. Video credit: Ralf Schiecke/Doclights