The evolution of stem-bird vocalization

I wrote this essay for a course on evolution last year. I’ve made a few edits and reproduced it here.

Most tetrapods capable of vocalization, such as mammals, utilize vocal cords located within the larynx for this purpose (Senter, 2008). Birds, however, utilize an organ located at the base of the trachea: the syrinx. Unlike the larynx, which produces sound through the vibration of vocal folds, the syrinx produces sound by vibrating the walls of the trachea. The syrinx is capable of more complex vocalization than the larynx, including being able to function asymmetrically and produce two sounds at once (Naish, 2009, Clarke et al., 2016). Only found in modern birds, the syrinx is an unusual example of a novel organ in that it has completely functionally replaced the larynx as the primary vocal organ (Kingsley et al., 2018). The syrinx presumably evolved somewhere on the stem-bird lineage, which contains non-avian dinosaurs and pterosaurs. Understanding the origin of the avian syrinx can therefore have implications regarding the potential vocalization of stem-birds.
Anatomy of the avian syrinx. Courtesy of All About Birds.

As birds use the syrinx for vocal communication, did stem-birds ever use laryngeal vocal cords? Senter (2008) suggested that, due to lack of fossil evidence of the syrinx or laryngeal vocal cords, stem-birds were likely mute. Modern tetrapods that lack both, such as New World vultures and many squamates, are limited to simple hissing and drumming sounds (Senter, 2008; pers. obs.). However, the potential presence of laryngeal vocal cords ancestrally in Ornithodira (the clade containing birds, non-avian dinosaurs, and pterosaurs) was not considered. The larynx leaves no osteological trace, making the presence or absence of vocal cords impossible to discern in the fossil record. Laryngeal vocal cords are present in the two extant outgroup taxa to the Aves total group, crocodylians and turtles, and laryngeal vocal cords have evolved many times independently in modern tetrapods (Senter, 2008; Chen and Weins, 2020). The presence of laryngeal involvement in vocalization has also been recorded in modern birds, albeit not through vibration of vocal folds (Naish, 2009). More modern hypotheses on syrinx evolution (e.g. Riede et al., 2019) assume the ancestral presence of vocal cords before the syrinx. If laryngeal vocal cords are an efficient enough sound production mechanism to evolve at least six times independently in tetrapods, it is not implausible that they may have also evolved in stem-birds.

The internal nasal passageways of Corythosaurus, Lambeosaurus, and Parasaurolophus (Weishampel, 1981)

The resonating chambers of lambeosaurine hadrosaurs may have implications regarding the presence of a vocal organ. These dinosaurs have prominent bony head crests, through which the nasal passages arc and loop through. It is likely that these nasal passages were used in sound production (Weishampel, 1981). The dinosaur most famous for this is probably Parasaurolophus, and the potential sound produced by the crest of P. tubicen has been reconstructed using a computer simulation, resonating virtual air waves through the nasal passages to produce a deep trumpeting sound (Diegert and Williamson, 1998). Among other tetrapods, ruminant ungulates perhaps bear the most functionally similar structures. Rutting male saiga (Saiga tatarica) inflate their nasal passages to produce a loud nasal roar, amplifying sound made by the larynx (Frey et al., 2007). The extinct bovid Rusingoyrx atopocranion had expanded bony nasal passages looping through a cranial dome, convergently evolved with those of lambeosaurines. The nasal passages of Rusingoryx were likely used similarly to those of saiga, amplifying sound made by the larynx (O’Brien et al., 2016). By analogy with these ungulates, it is possible that the nasal passages of lambeosaurines also have evolved to amplify and resonate sound produced by a vocal organ. Thus, these nasal passages may serve as indirect evidence for the presence of a vocal organ in non-avian dinosaurs.

Extension of the nose in a roaring male saiga (Frey et al., 2007). The crests of hadrosaurs (and if I may speculate, the expanded nasal regions of several other ornithischian dinosaurs) may have provided a similar function.

If non-avian dinosaurs and pterosaurs had vocal organs, what did they sound like? This is impossible to answer, as vocal organs never completely fossilize, but we can make a few inferences. By comparing the shape of the inner ear with those of birds and crocodilians, Gleich et al. (2005) inferred that many non-avian dinosaurs likely had a similarly well-developed sense of hearing. Although a few clades of ornithischian dinosaur may have secondarily lost external ear openings (Nassif et al., 2018), this does not necessarily preclude vocal ability, as certain living lepidosaurs that lack external ears produce sound anyways (Senter, 2008). Larger Mesozoic dinosaurs were more attuned to low-frequency sounds (e.g. Evans et al., 2009; Brusatte et al., 2016). Living large-bodied archosaurs, such as crocodylians and ratites, commonly utilize closed-mouth vocalization, in which sound is directed into an inflating resonating cavity, producing a lower-frequency sound than if the mouth was open. Examples include alligator bellows, ostrich booms, and owl hoots. These closed-mouth vocalizations may have also been prevalent in large stem-birds (Riede et al., 2016). This being said, open-mouth vocalizations were likely not absent in stem-birds; crocodylians and birds that frequently use closed-mouth vocalization also utilize open-mouth vocalization in different contexts (pers. obs.). Closed-mouth vocalizations are usually implemented in territorial or courtship displays (Riede et al., 2016), and are also present in a few mammal species, e.g. the nasal roar of the saiga and the inflatable throat sac of the siamang Symphalangus syndactylus (pers. obs.). However, most mammals adopt a different solution to produce loud, low-frequency sound; they evolve modifications of the vocal cords and vocal tract to produce deep “roaring” vocalizations (Frey and Gebler, 2010). It has been commonly reported in popular news media that non-avian dinosaurs did not roar (e.g. Orf, 2016). While it is unlikely that non-avian dinosaurs roared using the same mechanism as mammals, they may have produced functionally similar sounds regardless.

The exact timing of syrinx origin remains mysterious. Until recently it was thought that the syrinx could not fossilize, due to the lack of fossilized syrinxes older than the Pleistocene epoch. However, a good portion of the syrinx is biomineralized, similar to bone or shell, and this incorporation of hard minerals into tissue can increase fossilization potential. The mineralized portion of the syrinx has been identified in three genera of fossil anseriform birds: the Eocene Presbyornis, the Maastrichtian Vegavis (Clarke et al., 2016), and the Paleocene Conflicto (Tambussi et al., 2019). The fossilization potential of the syrinx raises the question of why no stem-birds have been found with fossilized syrinxes, even those close to crown-Aves. This may be due to the preservational bias in the fossil record, or it could indicate that the full syrinx was a late-arising feature in bird evolution (Clarke et al., 2017). In living birds, the syrinx remains unmineralized until after three months post-hatching, but can still produce sound before mineralization (Hogg, 1982). This raises the possibility that a sound-producing syrinx may have first appeared as an unmineralized structure, and thus would be difficult to fossilize.

Morphology of the syrinx in several birds, including Vegavis and Presbyornis (Clarke et al., 2016)

A proxy for timing of syrinx evolution has been proposed in the ornithodiran skeleton. The syrinx is entirely surrounded by the clavicular air sac, one component of the ornithodiran air sac system (Wedel, 2009). Embryological observations indicate that the clavicular air sac forms relatively late in ontogeny, as an outgrowth of the lungs and two other air sacs (Locy and Larsell, 1916). This suggests that the clavicular air sac is a later development than the rest of the ornithodiran air sac system (Senter, 2008). The presence of an air sac can be inferred osteologically, as air sacs often invade the surrounding bone, leaving pits or depressions. This phenomenon is called skeletal pneumaticity. The clavicular air sac pneumatizes the humerus, furcula, sternum, and pectoral girdle (Wedel, 2009). Pneumatization by the clavicular air sac is present in Ornithothoraces, a clade including modern birds, but not in avialans basal to this clade (Senter, 2008). However, pneumatization consistent with the clavicular air sac is also present in pterosaurs, the theropod genera Aerosteon and Buitreraptor (Wedel, 2009) and the sauropod clade Saltasaurini (Cerda et al., 2012). This suggests that either the clavicular air sac evolved multiple times, or the clavicular air sac may have been present deeper in the bird stem lineage than Ornithothoraces.

Embryology demonstrates that the ornithodiran air sac system develops before pneumatization of bones (Locy and Larsell, 1916), and two clades of modern birds, loons and penguins, lack postcranial pneumaticity entirely but still bear a full air sac system. Postcranial pneumaticity is entirely absent in ornithischians and non-dinosaurian dinosauromorphs, and it is unlikely the entire air sac system evolved multiple times. Therefore, the air sac system may have evolved once, at the base of Ornithodira, and only grew to pneumatize the surrounding bones in certain taxa (Wedel, 2009).  The same could also apply to the clavicular air sac; it may have evolved before the origin of Ornithothoraces, extending the potential origin of the syrinx even earlier. However, it cannot be ruled out that the clavicular air sac indeed evolved multiple times; after all, it does appear to be a later development than the rest of the air sac system, and two of the clades that bear it, pterosaurs and Ornithothoraces, may have needed it for flight.  As well, vocalization with the syrinx is possible without the clavicular air sac necessarily being involved (e.g. Brackenbury, 1980), but it is unclear whether this reflects a possible ancestral condition or is a novel occurrence in some bird species. Ultimately, the exact timing of syrinx evolution remains unclear, and more data is needed to pinpoint its exact origin.

The evolutionary reason for the appearance of the syrinx is also a question worth looking into. Riede et al. (2019) carried out models and experiments to test efficiency of the syrinx relative to laryngeal vocal cords. Their results found that a sound source at the base of the neck is more acoustically efficient than one at the top of the throat, supporting the idea that the syrinx is a more efficient vocal organ than the larynx. One reason for this is that, with a sound source at the base of the throat, the vocal tract can be longer, producing a more resonant sound. Therefore, the syrinx may have evolved initially as a complement to the larynx, in response to selective pressure for efficient vocalization. The syrinx is most efficient relative to the larynx if the tracheal length is between 50 and 100 cm (Riede et al., 2019). The lineage of theropods that led to birds underwent sustained miniaturization over time (Lee et al., 2014), so the syrinx may have begun to take over the larynx’s duties at a certain body size due to its increased efficiency. The larynx may have then simply become obsolete as a vocal organ, and use of vocal cords was lost before the avian MRCA.

Summarizing all these pieces of evidence, we may speculate a tentative picture of vocal evolution in stem-birds. Ancestrally, stem-birds may have produced sound using laryngeal vocal cords, perhaps sharing an evolutionary origin with those present in crocodylians. Larger-bodied stem-birds may have produced closed-mouth booming or bellowing sounds, while some clades, notably lambeosaurine hadrosaurs, expanded on this setup to produce more complex sound. Selective pressure for efficient vocalization in theropods may have led to the evolution of a new organ, the syrinx, as a complement at the base of the throat. As the bird lineage continued to shrink in body size, the syrinx took over as the primary vocal organ, leaving birds with a truly unique method of vocalization.


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