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Measurements on the Turtle’s Shell that Help Illuminate How the Fishes Lateral Line Function Was Replaced by the Reptilian Hearing Organ

The acoustic sense of fish, embodied in the lateral line, no longer worked when amphibians ventured onto the land. The new acoustic environment where sound traveled in the thin medium of air rather than the relatively dense medium of water presented a major chal-lenge. The multiple sensors of the lateral line were replaced by one gross sensor, the tym-panic membrane or eardrum. We show acoustical measurements on the turtle shell that can suggest a possible explanation of how the turtle dealt with the issue of sensing the directionality of incoming sounds.


INTRODUCTION
The transition from fish living in aquatic space to vertebrates living in air required several adjustments. Mobility, for example, involved the morphing of fins into limbs. Morphing, however, did not suffice when it came to converting the aquatic acoustic sense realized by the fishes lateral line [1], to a terrestrial hearing organ. A hearing organ that allowed the early reptile to sense the airborne acoustic space it now lived in was essential to its survival. Hearing in the air required the development of a new acoustic computation paradigm and a new hearing organ to carry out the task of sensing the spatial origin of incoming sounds. We will show that the reflectivity of textural singularities of the turtle shell can be considered part of the turtles hearing system [2]. The main novelty and new contribution of this work lies in considering acoustic reflections from turtle shell to be an important part of the turtles interaction with its environment.

BACKGROUND
Before considering how amphibians and reptilians may have evolved the equipment to sense and process airborne sounds, we must understand how fish detect and process aquatic acoustic sounds with the lateral line. A description of the fishes lateral line from reference [1] describes the starting point of the Open Access Natural Science evolution of reptilian hearing: In daylight the eye informs the fish about its surroundings. However, at night, the fish monitors its sound field just as humans listen in the dark to sense surrounding space acoustically. While humans use our ears to keep track of the sounds around us, the fish senses the surrounding acoustic space with its Lateral Line. The lateral line is a row of vibration sensors spaced along each side of the fish from the head to the tail. These sensors, each composed of groups of vibration sensing hair cells, monitor the vibrations in the water surrounding the fish. Each lateral line sensor, called a stitch, is represented by a dot in Figure 1.
If the direction of arrival of the vibration is at right angles to the body of the fish, all the individual lateral line sensors will be stimulated simultaneously. If the vibration comes from a position near the front of the fish the sensors at the front of the fish are stimulated first. The stimulation then sweeps from the front to the back. If the vibration comes from a position near the rear end of the fish the stimulation sweeps from the rear to the front of the fish. The lateral line, with its array of simultaneous detectors, provides a panoramic acoustic image of surrounding activity [1].
In the fish, each of the dots on the lateral line, called a "stitch", is an individual sensor that is picking up the aquatic sound wave, or waterborne vibration, as it sweeps along the lateral line. Each lateral line sensor sends a fiber to the fishes brain. In the brain, the relative arrival time of vibrations contains the information needed to solve for the direction of arrival.

The Medium
Amphibians and Reptiles lost the functions of the lateral line when they left the sea. The vibrations in the water were able to stimulate the individual sensors of the lateral line. However, the vibrations in air were not able to couple to the small surface of the individual lateral line sensors. Water is a dense medium when compared with air. Vibrations in water are able to move the small sensing surface of the individual sensors of the lateral line. In order for vibrations in air to couple to a sensor, the sensor surface exposed to the vibrations, the eardrum, must be much larger than the tiny surface of the individual lateral line sensors.

The Sensor
The need to couple the acoustic vibrations in air to an array of hair cell sensors in the inner ear of amphibians and reptiles led to the development of a relatively large surface exposed to the air-born acoustic vibrations. This surface, the tympanum, that we call an "eardrum", is then attached to a plunger in the fluid of the labyrinth. This produces a vibration in the fluid medium in which the vibration sensors, the hair cells, are designed to operate [3]. In the brain, the relative arrival time of vibrations contains the information needed to solve the direction of arrival, but so far, we don't know how the fish does this. Natural Science What is new in Reptiles and Amphibians is the development of a new group, or cluster, of Hair Cell sensors placed in a long row in the labyrinth adjacent to the Utricle (Figure 2). This row of sensors is arranged in the path of the fluid vibrations produced by the plunger driven by the eardrum. These vibrations, which produce a traveling wave, contain reflections originating at different parts of the body with different delays based on the distance of the reflecting surface to the eardrum. The particular sound that is received at the eardrum is the sum of the original wave and the reflections from prominent reflecting surfaces on the animal's body. We begin by exploring the relative timing of reflections from different parts of the body in the turtle.

MATERIALS AND METHODS
Measurements were made on a photographic image of a 200 m year fossilized turtle which carries the same shell structure as present day turtles. Distances from an incoming sound wavefront, through reflection shell singularities, to the tympanum were measured with a ruler calibrated in mm.
Subtracting the wavefront to tympanum distance from the reflective measurements exposes the echo timing as a function of the direction of sound arrival.

MEASUREMENT AND COMPUTATION
A sound source, as it travels away from the source, expands spherically on its way to its destination. For example, a sound source one meter away from a turtle will present an incoming wavefront that is part of the circumference of a two-meter diameter circle. Since the part of this spherical wave that interacts with the turtle is only about 10 cm in the present case, the incoming sound wavefront is approximated by a straight line in the example that follows. The sounds that are reflected from bumps on the turtle shell travel to the ear with a delay that depends on the distance traveled from the incoming wavefront to the ear. This travel distance was measured on the image of the turtle shell in mm, and then converted to a time delay using the speed of sound in air of 343 m/s. This computation was performed for two different angles of incidence. The 60 deg computation shows a sound coming from the left-front of the animal. The 120 deg computation is from a sound source at the right-rear of the animal (Figure 3). Natural Science  Figure 4 to illustrate how the timing of the echoes is directly related to the angle of the sound source relative to the central axis of the shell.
It would be easy to write a computer program to decode the data plotted in Figure 4. The periodicity seen in the echoes is a higher frequency than the kilocycle hearing of the turtle. This opens the question: does the turtle listen to each individual echo, or does she perceive the group, together, as a single reflection centered in the group of echoes? If the group of echoes is sensed as a single reflection the decoding problem remains the same. The delay between this single reflection and the direct signal needs to be transformed into a sensation of directionality. Natural Science

CONCLUSION
In order for a land-based fauna to flourish, it was necessary for early amphibians and reptilians to develop a new system of hearing to replace the lateral line which no longer was functional in the relatively thin air of the new environment. We have shown measurements that illustrate how the relative timing of an incoming acoustic signal and the reflections from prominent singularities on its shell contain the information needed for the turtle to locate a sound source. We have shown that both the lateral line and the new reptilian mode of hearing required that the delay between different components of the incoming signal be measured and converted to a sensation of directionality in the animal.