vocalisation in birds Coen Elemans Wageningen University , The Netherlands

Introduction Colors are a communication code for birds.

Fig1: Photographies of Hymalayan monal pheasant and Wilson bird of paradise

But birds also communicate with their song. Their song has different functions: species recognition, alarm calls, territorial dispute... The diversity and complexity of birdsong is no match for vocalisations of other vertebrates. The sounds can reach very high frequencies. When we want to study birds vocalization, we are confronted to several questions : how is sound produced and controlled? how is sound production learned? how is the information for vocal control stored in the brain? La diversité et la complexité des chants d’oiseaux est sans comparaison par rapport à d’autres vertebrés. Les sons peuvent notamment atteindre de très hautes fréquences.

Plusieurs questions se posent sur la production vocale chez les oiseaux : -Comment le son est il produit et contrôlé? -Comment se fait l’acquisition de la maîtrise de la production vocale? -Comment l’information du contrôle moteur du geste vocal est-il stocké dans leur cerveau? 1) The syrinx Les oiseaux possèdent également un larynx, appelé syrinx. La grosse différence par rapport à l’appareil vocal humain est que les oiseaux possèdent des « sacs d’air ». Le syrinx se trouve au milieu de cet ensemble de sacs d’air.

Fig2 : Localization of the syrinx and the air sacs in the bird’s body

Syrinx is considered as the principle sound generating organ. This term of ‘syrinx’ was introduced by Huxley in 1877 to avoid confusion, with the notions of upper and lower larynx. The syrinx is a modification of the airway at the bifurcation of the trachea in the two principle bronchii, comprising a cartilaginous (or bony) framework. There are also flexible membranes stretched between element of this framework, and muscles to vary tension of these membranes. Many times they are enclosed by airsacs. This production system is unique to birds. The vocal tract (inclusive larynx) modifies generated sound by syrinx. To understand sound production it is essential to understand the notions of modulation in amplitude and frequency.

Fig3 : Syrinx’s anatomy

The syrinx is onstituted by 2 pairs of vibrating labial masses also called “collide” (Goller & Larsen, PNAS 1999)

Fig4 : Localization of the labial masses (“collides”) in the syrinx

The songbirds have 2 independently controlled voices (Suthers, Nature 1999) 6 pairs of muscles are present in the syrinx and birds are able to control their position and tension in labia to vary the amplitude and the pitch of the produced sounds. We are also intersted in understanding how the labia behave during the vibration, and if there are some coupling effects between the left and the right systems?

Fig5 : Anatomic represntation of a syrinx

The syrinx of non-songbirds show a very large diversity between species.

Fig6 : Syrinx’s configuration for three different birds species.

Although variation is vast, we decided to build a one membrane system to start with. This can be found in many birds.

Position, size, etc of these membranes vary but we hope to get insight in the functioning of this system. 2) Modeling the syrinx as a mechanical model The adavantages of models compared to in vivo measurments ar multiple : - models do not fly, molest equipment and thy stay silent when you do not want them to. It even more difficult to work on birds than with humans because you ca’t even ask them to do or not to do something. - models allow detailed study / precise measurements - models allow change of important parameters To model mechanicaly the syrinx, we focused the “ring dove” and it muscular controls in vivo, although it is a non-songbird. Actually songbirds produce most intricate, learned songs, but teir morphology is very complex and above all they are very small birds, that leads to difficulties for surgery.

Fig7 : Acoustic analysis of the ring dove’s song

Fig8 : First tries of mechanical modeling of the syrinx

When we observ a real syrinx, it seems that a vortex generates sound or that the flow induces MTM vibrations . These vibrations are then modulated by LTM . From a modelling point of view, the flow induces LTM vibrations but the modulation mechanism is unknown For pervious works, let see Larsen & Goller, J. Exp. Biol. 200, 2165-2176 and Beckers et al, J. Exp. Biol. 206 1833 - 1843 Many morphological observation were done with either wrong model in mind or purely desciprions of structure without mechanics in mind. Therefore we went back to morphology

Fig9 : Anatomic cuts of TL and ST muscles

Fig10 : Mechanical model of a syrinx

To model the syrinx, we’ve based on the obersevation on a pigeon syrinx. It is basically a tube with membranes and an airsac around it.We constructed a metal tube with an oval hole, whereon we can mount a single latex membrane. This whole is enclosed by a chamber which we can pressurize, simulating the airsac.When we pressurize the airsac the membrane will bulge inward the metal tube and therefore form a constriction.

Fig11 : Conception of an artificial syrinx

Results Our model behaves like a clarinet. There is a strong coupling oscillations with resonance frequency of closed tube. Moreover, there is a slight effect of membrane properties on frequency. The coupling is different from what we observe in most birds with e.g. Heliox experiments (Nowicki, Nature 1998). The question is: are this difference explainable either by the tracheal dimensions, the used materials, the feedback mechanisms or else by the muscle activity? 3) In vivo experiments We simulatneously measured the TL and ST Muscles activity during spontaneous vocalizing , and the pressure pb in thoracic airsac

Fig12 : Representation of the experimental setup

Fig13 : Pression in the thoracic airsac during spontaneous vocalizing

Fig14 : EMG measurments during a spontaneous vocalization

Fig15 : Details of EMG measurments during a spontaneous vocalization

On a trill, we observ that the two antogonist muscles are both contracted . We can also notice that the contraction speed of TL et ST muscles is very high (about 9.2 ms and10.3 ms)

Fig16 : Contraction speeds of ST and TL at different temperatures

Concluding These important qualitative observations changed ideas that were around for centuries dramatically. Since we understand some mechanisms that underly vocalisation qualitatively, mathematical modeling becomes relevant to quantitative insights

Acknowledgements Experimental Zoology / Wageningen, The Netherlands Johan van Leeuwen Mees Muller Igor Spierts Centre of Sound Communication / Odense, Denmark Ole Larsen Goller lab / Salt Lake City, USA Franz Goller Anooskha Jansen