BIOLOGY 457/657 PHYSIOLOGY OF MARINE & ESTUARINE ANIMALS April 5, 2004 HEARING & MECHANORECEPTION
HEARING: SOUND UNDERWATER
Sources of Sound –
Passive: Waves, swimming, walking, muscle activity, splashing Active: Sound production – swimbladders, appendages, special organs (e.g. marine mammals). Stridulation in crustaceans. Frequency ranges: 1 – 35 Hz Changes in pressure, swimming 50 – 400 Hz Sounds > 1000 Hz (> 1 KHz) Echolocation
Sound in Water –
High speed (1500 m/s; about 4 to 5 times speed in air) Two distinct oscillatory mechanical effects: (1) Pressure change (2) Particle displacement
Nearfield vs. Farfield Effects
Far from source (Farfield): Both pressure change and particle
displacement are proportional to 1/r (r = radius from source)
Near to source (Nearfield): Pressure change continues to be proportional to
1/r, but particle motion is proportional to between 1/r2 to 1/r3. The region where particle movement (“flow”) dominates is called the nearfield, and the region dominated by pressure change is called the farfield. The border between the two lies at ~λ/6 (λ is wavelength, so for a 50 Hz sound, λ = 1500 m s-1 / 50 s-1 = 30 m; the nearfield extends to 30 m/6 or 5 m from the source). Obviously, the lower the frequency, the larger the nearfield.
The Receptors: Neuromast Organs in Vertebrates
Two sets of receptors exist in fishes, the labyrinth (ear) and the lateral line (body). Together, these constitute the acousticolateralis system. The actual receptors are neuromast cells, often grouped into neuromast organs. Each neuromast cell contains a kinocilium, together with a group of stereocilia. Bending of the kinocilium causes the cell to depolarize or hyperpolarize.
Electrophysiology of Neuromast Cells
The Labyrinth
In the labyrinth, the neuromast cells are located in 3 major regions – the utricle, the saccule, and the lagena. Each region also contains a solid otolith overyling the sensory epithelium (macula). As the otolith moves, the neuromast cells are stimulated. Thus, the labyrinth is sensitive to motion, not pressure.
Organization of the Macula
Changing Motion Sensitivity to Pressure Sensitivity
While the fish ear fundamentally responds to motion stimuli, pressure sensitivity can be conferred if pressure-caused vibrations are led to the inner ear. This can occur, for instance, if there are connections to the swimbladder. Such coupling can occur via: (1) Weberian ossicles (2) Gas-filled bulbs (the bulla; in clupeoids) This coupling can greatly decrease the threshold in the farfield.
Weberian Ossicles
Weberian ossicles form a direct mechanical link between the swimbladder and the inner ear. They are found in some cyprinid fishes (carps), including the humble goldfish.
The Bulla System: Clupeoids
In clupeoids (herrings), there is an actual gasfilled duct leading from the swimbladder to the bulla, a gas-filled bulb adjacent to the utricular macula.
Audiograms of Pressure-Sensitive Fishes
Invertebrate “Lateral Lines”
Some invertebrates (e.g. pelagic shrimps) have extended antenna “arrays” that act much like the lateral line systems of fishes, detecting mechanical stimuli (particle motion) directly. By having these “towed arrays”, spatial localization of stimuli is possible. Obviously, the receptors of such a system are not neuromasts, but instead are crustacean types of mechanoreceptors.
Localization of Sound Stimuli
The relatively great velocity of sound in water makes it impossible to use the types of directional discrimination systems that are generally used in air: comparison of time-of-arrival or of phase differences between 2 separated detectors. Particle motion is a vector stimulus – it has both amplitude and direction. The fish’s body moves back and forth in response to such particle motion, and because the otoliths are much denser than the rest of the fish, their relative inertia causes them to lag behind the rest of the fish and cause directional motion on the surfaces of the maculae. Neuromast cells on these maculae are most responsive to stimulation along particular axes (as illustrated previously). Pressure change is scalar - it has only amplitude. If pressure changes are conveyed to the labyrinth from the swimbladder, they have no directionality. By comparing the direct stimulation and the indirect stimulation (i.e. by comparing motion and pressure), both the direction and range to a vibrating source (source of sound) can be determined! This is possible because of differences between the rates of attenuation in the nearfield and farfield.
Localization of Sound Stimuli (2)
MECHANORECEPTION IN COPEPODS
Copepods cruise in search of prey or mates, and undergo diel vertical migrations. They also produce feeding currents to bring phytoplankton or small zooplankton within grasp of the feeding appendates. These locomotory currents create a region of flow around each individual which is much large than the actual animal (in Pleuromamma xiphias, it is 175 times the body volume). This extended flow field has 2 primary disadvantages: (1) It can alert and orient potential predators. (1) It can warn prey (if the species is a predator)
Escape Responses of Prey
Copepod nauplii escaping from Temora longicornis
As T. longicornis cruises in search of prey, it produces an area of flow in front. Potential prey (e.g. nauplii larvae of other copepods) can be alerted by the field and make appropriate escape responses (Yen & Fields, 1992).
Escape Responses of Prey
Copepod nauplii escaping from Temora longicornis (2)
The possible means by which a small zooplanktonic animal like a copepod nauplius could sense the oncoming predator by its flow field signature are: (1) Sensing of water acceleration by setae (the body lags behind). (2) Sensing of asymmetrical water flow by setal receptors.
Escape Responses of Prey
Copepod nauplii escaping from Temora longicornis (3)
Predator Detection: The Role of Distal Tip Setae
Simultaneous activity of many mechanoreceptors and chemoreceptors in copepod antennae can be recorded. A variety of receptor types can be identified by their response patterns and spike size. Mechanoreceptors can respond to very small stimuli (~10 µm displacements), and can encode stimuli at frequencies up to 500 Hz.
Large setae on the distal tip, which have unusually large sensory axons, are located in regions where the own animal’s flow field tends to be relatively weak. These may be particularly useful in the detection of nearby large predators.
Predator Detection: The Role of Distal Tip Setae