Tobias Riede

Fossil evidence of the avian vocal organ from the Mesozoic

From complex songs to simple honks, birds produce sounds using a unique vocal organ called the syrinx. Located close to the heart at the tracheobronchial junction, vocal folds or membranes attached to modified mineralized rings vibrate to produce sound. Syringeal components were not thought to commonly enter the fossil record, and the few reported fossilized parts of the syrinx are geologically young (from the Pleistocene and Holocene (approximately 2.5 million years ago to the present)). The only known older syrinx is an Eocene specimen that was not described or illustrated. Data on the relationship between soft tissue structures and syringeal three-dimensional geometry are also exceptionally limited. Here we describe the first remains, to our knowledge, of a fossil syrinx from the Mesozoic Era, which are preserved in three dimensions in a specimen from the Late Cretaceous (approximately 66 to 69 million years ago) of Antarctica. With both cranial and postcranial remains, the new Vegavis iaai specimen is the most complete to be recovered from a part of the radiation of living birds (Aves). Enhanced-contrast X-ray computed tomography (CT) of syrinx structure in twelve extant non-passerine birds, as well as CT imaging of the Vegavis and Eocene syrinxes, informs both the reconstruction of ancestral states in birds and properties of the vocal organ in the extinct species. Fused rings in Vegavis form a well-mineralized pessulus, a derived neognath bird feature, proposed to anchor enlarged vocal folds or labia. Left-right bronchial asymmetry, as seen in Vegavis, is only known in extant birds with two sets of vocal fold sound sources. The new data show the fossilization potential of the avian vocal organ and beg the question why these remains have not been found in other dinosaurs. The lack of other Mesozoic tracheobronchial remains, and the poorly mineralized condition in archosaurian taxa without a syrinx, may indicate that a complex syrinx was a late arising feature in the evolution of birds, well after the origin of flight and respiratory innovations.

Functional morphology of the Alligator mississippiensis larynx with implications for vocal production

ABSTRACT Sauropsid vocalization is mediated by the syrinx in birds and the larynx in extant reptiles; but whereas avian vocal production has received much attention, the vocal mechanism of basal reptilians is poorly understood. The American alligator (Alligator mississippiensis) displays a large vocal repertoire during mating and in parent–offspring interactions. Although vocal outputs of these behaviors have received some attention, the underlying mechanism of sound production remains speculative. Here, we investigate the laryngeal anatomy of juvenile and adult animals by macroscopic and histological methods. Observations of the cartilaginous framework and associated muscles largely corroborate earlier findings, but one muscle, the cricoarytenoideus, exhibits a heretofore unknown extrinsic insertion that has important implications for effective regulation of vocal fold length and tension. Histological investigation of the larynx revealed a layered vocal fold morphology. The thick lamina propria consists of non-homogenous extracellular matrix containing collagen fibers that are tightly packed below the epithelium but loosely organized deep inside the vocal fold. We found few elastic fibers but comparatively high proportions of hyaluronan. Similar organizational complexity is also seen in mammalian vocal folds and the labia of the avian syrinx: convergent morphologies that suggest analogous mechanisms for sound production. In tensile tests, alligator vocal folds demonstrated a linear stress–strain behavior in the low strain region and nonlinear stress responses at strains larger than 15%, which is similar to mammalian vocal fold tissue. We have integrated morphological and physiological data in a two-mass vocal fold model, providing a systematic description of the possible acoustic space that could be available to an alligator larynx. Mapping actual call production onto possible acoustic space validates the models predictions. Summary: Morphology and laryngeal biomechanics are used to model the boundaries of the alligators available acoustic space.

Coos, booms, and hoots: The evolution of closed‐mouth vocal behavior in birds

Most birds vocalize with an open beak, but vocalization with a closed beak into an inflating cavity occurs in territorial or courtship displays in disparate species throughout birds. Closed‐mouth vocalizations generate resonance conditions that favor low‐frequency sounds. By contrast, open‐mouth vocalizations cover a wider frequency range. Here we describe closed‐mouth vocalizations of birds from functional and morphological perspectives and assess the distribution of closed‐mouth vocalizations in birds and related outgroups. Ancestral‐state optimizations of body size and vocal behavior indicate that closed‐mouth vocalizations are unlikely to be ancestral in birds and have evolved independently at least 16 times within Aves, predominantly in large‐bodied lineages. Closed‐mouth vocalizations are rare in the small‐bodied passerines. In light of these results and body size trends in nonavian dinosaurs, we suggest that the capacity for closed‐mouth vocalization was present in at least some extinct nonavian dinosaurs. As in birds, this behavior may have been limited to sexually selected vocal displays, and hence would have co‐occurred with open‐mouthed vocalizations.

Rats concatenate 22 kHz and 50 kHz calls into a single utterance.

ABSTRACT Traditionally, the ultrasonic vocal repertoire of rats is differentiated into 22u2005kHz and 50u2005kHz calls, two categories that contain multiple different call types. Although both categories have different functions, they are sometimes produced in the same behavioral context. Here, we investigated the peripheral mechanisms that generate sequences of calls from both categories. Male rats, either sexually experienced or naïve, were exposed to an estrous female. The majority of sexually naïve male rats produced 22u2005kHz and 50u2005kHz calls on their first encounter with a female. We recorded subglottal pressure and electromyographic activity of laryngeal muscles and found that male rats sometimes concatenate long 22u2005kHz calls and 50u2005kHz trill calls into an utterance produced during a single breath. The qualitatively different laryngeal motor patterns for both call types were produced serially during the same breathing cycle. The finding demonstrates flexibility in the laryngeal–respiratory coordination during ultrasonic vocal production, which has not been previously documented physiologically in non-human mammals. Since only naïve males produced the 22u2005kHz-trills, it is possible that the production is experience dependent. Highlighted Article: Rat ultrasonic vocalizations are composed of identifiable vocal motor gestures that are combined and re-combined within a single breath.

Laryngeal airway reconstruction indicates that rodent ultrasonic vocalizations are produced by an edge-tone mechanism

Some rodents produce ultrasonic vocalizations (USVs) for social communication using an aerodynamic whistle, a unique vocal production mechanism not found in other animals. The functional anatomy and evolution of this sound production mechanism remains unclear. Using laryngeal airway reconstruction, we identified anatomical specializations critical for USV production. A robust laryngeal cartilaginous framework supports a narrow supraglottal airway. An intralaryngeal airsac-like cavity termed the ventral pouch was present in three muroid rodents (suborder Myomorpha), but was absent in a heteromyid rodent (suborder Castorimorpha) that produces a limited vocal repertoire and no documented USVs. Small lesions to the ventral pouch in laboratory rats caused dramatic changes in USV production, supporting the hypothesis that an interaction between a glottal exit jet and the alar edge generates ultrasonic signals in rodents. The resulting undulating airflow around the alar edge interacts with the resonance of the ventral pouch, which may function as a Helmholtz resonator. The proposed edge-tone mechanism requires control of intrinsic laryngeal muscles and sets the foundation for acoustic variation and diversification among rodents. Our work highlights the importance of anatomical innovations in the evolution of animal sound production mechanisms.

Grasshopper mice employ distinct vocal production mechanisms in different social contexts

Functional changes in vocal organ morphology and motor control facilitate the evolution of acoustic signal diversity. Although many rodents produce vocalizations in a variety of social contexts, few studies have explored the underlying production mechanisms. Here, we describe mechanisms of audible and ultrasonic vocalizations (USVs) produced by grasshopper mice (genus Onychomys). Grasshopper mice are predatory rodents of the desert that produce both loud, long-distance advertisement calls and USVs in close-distance mating contexts. Using live-animal recording in normal air and heliox, laryngeal and vocal tract morphological investigations, and biomechanical modelling, we found that grasshopper mice employ two distinct vocal production mechanisms. In heliox, changes in higher-harmonic amplitudes of long-distance calls indicate an airflow-induced tissue vibration mechanism, whereas changes in fundamental frequency of USVs support a whistle mechanism. Vocal membranes and a thin lamina propria aid in the production of long-distance calls by increasing glottal efficiency and permitting high frequencies, respectively. In addition, tuning of fundamental frequency to the second resonance of a bell-shaped vocal tract increases call amplitude. Our findings indicate that grasshopper mice can dynamically adjust motor control to suit the social context and have novel morphological adaptations that facilitate long-distance communication.

The functional morphology of male courtship displays in the Pectoral Sandpiper (Calidris melanotos)

ABSTRACT 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.

Vocal development in dystonic rats

Vocal production, which requires the generation and integration of laryngeal and respiratory motor patterns, can be impaired in dystonia, a disorder believed due to dysfunction of sensorimotor pathways in the central nervous system. Herein, we analyze vocal and respiratory abnormalities in the dystonic (dt) rat, a well‐characterized model of generalized dystonia. The dt rat is a recessive mutant with haploinsufficiency of Atcay which encodes the neuronally restricted protein caytaxin. Olivocerebellar functional abnormalities are central to the dt rats truncal and appendicular dystonia and could also contribute to vocal and respiratory abnormalities in this model system. Differences in vocal repertoire composition were found between homozygote and wild‐type dt rat pups developing after 3 weeks of life. Those spectro‐temporal differences were not paralleled by differences in vocal activity or maximum lung pressures during quiet breathing and vocalization. However, breathing rhythm was slower in homozygote pups. This slower breathing rhythm persisted into adulthood. Given that cerebellectomy eliminates truncal and appendicular dystonia in the dt rat, we hypothesize that the altered breathing patterns stem either from a disturbance in the maturation of respiratory pattern generators or from deficient extracerebellar caytaxin expression affecting normal respiratory pattern generation. The altered breathing rhythm associated with vocal changes in the murine model resembles aspects of vocal dysfunction that are seen in humans with sporadic dystonia.

Identity and novelty in the avian syrinx

In its most basic conception, a novelty is simply something new. However, when many previously proposed evolutionary novelties have been illuminated by genetic, developmental, and fossil data, they have refined and narrowed our concept of biological “newness.” For example, they show that these novelties can occur at one or multiple levels of biological organization. Here, we review the identity of structures in the avian vocal organ, the syrinx, and bring together developmental data on airway patterning, structural data from across tetrapods, and mathematical modeling to assess what is novel. In contrast with laryngeal cartilages that support vocal folds in other vertebrates, we find no evidence that individual cartilage rings anchoring vocal folds in the syrinx have homology with any specific elements in outgroups. Further, unlike all other vertebrate vocal organs, the syrinx is not derived from a known valve precursor, and its origin involves a transition from an evolutionary “spandrel” in the respiratory tract, the site where the trachea meets the bronchi, to a target for novel selective regimes. We find that the syrinx falls into an unusual category of novel structures: those having significant functional overlap with the structures they replace. The syrinx, along with other evolutionary novelties in sensory and signaling modalities, may more commonly involve structural changes that contribute to or modify an existing function rather than those that enable new functions.

Peripheral Vocal Motor Dynamics and Combinatory Call Complexity of Ultrasonic Vocal Production in Rats

Abstract Peripheral vocal motor dynamics describes how complex interactions of laryngeal, respiratory and vocal tract movements generate and shape vocal sounds in rats. Glottal airflow provides the energy and laryngeal movements set important boundary conditions. The integration of laryngeal and breathing movements is investigated through simultaneous recordings of subglottal pressure and electromyographic (EMG) activity of intrinsic and extrinsic laryngeal muscles. Laryngeal muscle activity and subglottal pressure are in a close and complex relationship associated with specific call types. Rats use combinations and recombinations of different synergies of laryngeal and respiratory muscles to produce more complex composite call types; in other words, simple calls are concatenated to complex calls. The combination of a small set of synergies to create more complex acoustic behavior is consistent with the concept of a hierarchical modular organization of the motor control network. This modular organization simplifies the neural control of vocal movement and enhances vocal complexity.