Thomas E. Hetherington

Timing of development of the middle ear of Anura (Amphibia)

SummaryThe opercularis system and tympanum-stapes complex of the anuran middle ear develop at different times relative to metamorphosis. In early larvae, the fenestra ovalis is represented by a large lateral opening in the otic capsule filled with connective tissue. At later larval stages, but well before metamorphosis, a cartilaginous operculum begins to form at the posterior margin of the fenestra ovalis, and proceeds to expand to fill all except the anterior part of the fenestra. The opercularis muscle forms along with the levator scapulae superior muscle at the anteromedial edge of the developing suprascapular cartilage of the shoulder girdle. The muscle fibers extend anteroventrally towards the operculum and otic capsule, and, just before emergence of the forelimbs, that portion that will form the opercularis muscle inserts on the lateral surface of the operculum. At this stage, when the metamorphosing frogs first show terrestrial habits, the opercularis system is complete and presumably functional. Timing of development of the tympanum-stapes complex is more variable. The stapes begins as a cartilaginous condensation in the anterior part of the fenestra ovalis, and develops laterally to eventually contact the epidermis and dermis that together will form the tympanum. Meanwhile a middle ear cavity and tympanic annulus form to complete the complex. In several species, especially those that metamorphose at a smaller body size, the tympanum-stapes complex is quite incomplete by the end of metamorphosis, and in Hyla crucifer it takes about 60 days to fully develop. The presence of a complete opercularis system by the start of terrestrial activity is consistent with an hypothesized seismic function of the system. The independent timing of development of the opercularis system and tympanum-stapes complex does not support functional hypotheses linking the opercularis system with modulation of responsiveness of the tympanum-stapes complex to aerial sound. Newly metamorphosed frogs with poorly developed tympanum-stapes complexes are presumably either insensitive to aerial sound or employ alternate mechanisms for transmission of sound energy to the inner ear, possibly involving the opercularis system.

Use of vibratory cues for detection of insect prey by the sandswimming lizard Scincus scincus

The sandfish lizard, Scincus scincus, inhabits the Sahara Desert and spends most of its time buried in the sand. Laboratory experiments were performed to determine if Scincus can respond and orient to insects on the sand surface by detecting vibrations produced by movements of the insects. When buried, Scincus can detect and respond to crickets and mealworms moving over the surface at distances up to about 15 cm. These responses were guided by vibratory cues, not olfactory cues, as the lizards responded much less frequently to dead insects placed on the surface at equal distances. The lizards obtain directional information from the vibrations, and can localize the insects, orient toward them, and emerge from the sand to capture them. When walking on the surface of the sand, Scincus often displays a peculiar behaviour of plunging its head into the sand. Experiments determined that this behaviour aids lizards in detecting vibrations produced by insects moving through the sand, and presumably facilitates transmission of sand-borne vibrations to the inner ear.

Thermoregulation in a nocturnal, tropical, arboreal snake

Abstract Few studies have focused on the thermal biology of tropical or nocturnal snakes. We recorded preferred body temperatures (Tb) of seven Brown Treesnakes (Boiga irregularis) in the laboratory and compared these to operative temperatures obtained with copper models and Tbs obtained by radiotelemetry from 11 free-ranging snakes on Guam. Operative temperatures on Guam did not vary across refuge types, unless the site received direct solar radiation. In a thermal gradient and on Guam, Brown Treesnakes thermoregulated around two distinct temperature ranges (21.3–24.9°C; 28.1–31.3°C). In the gradient, brown treesnakes exhibited elevated Tb into the higher range only in the evening. On Guam, snakes achieved Tbs in the high range only when direct solar radiation was available during the afternoon, a period when snakes were inactive. Higher mean Tbs on sunny days corresponded with observations of basking behavior.

The effects of body size on functional properties of middle ear systems of anuran amphibians.

Both tympanic and nontympanic pathways of sound reception are utilized by anuran amphibians. The relationship between body size and the acoustic responsiveness of various body surfaces that may serve as pathways for sound reception in anurans was analyzed. The motion of the different surfaces (tympanum, lateral body wall, lateral head surface, and dorsal shoulder surface) produced by sound was measured with a laser vibrometer in anuran species. The frequency response and amplitude levels of motion of these body surfaces clearly were linked with size. In all animals, nontympanic surfaces were most responsive to low frequencies, and the tympanum was most responsive to high frequencies. However, the responsiveness of nontympanic surfaces was greater, and extended to higher frequencies, in small anurans. In the smallest animals studied, nontympanic surfaces were often more responsive than the tympanum up to frequencies as high as 2500 Hz. In larger anurans, nontympanic responsiveness tended to decrease, and tympanic responsiveness tended to increase. In the largest animals studied, the tympanum was the most responsive surface at all except very low frequencies below about 200-300 Hz. These results suggest that small anurans can utilize nontympanic pathways for effective sound reception over a broad frequency range, whereas large anurans are more restricted to using a standard tympanic middle ear for hearing. This effect of body size on the utility of nontympanic sound reception may explain evolutionary patterns of tympanic ear reduction and loss observed in several small species of anurans.

Biomechanics of vibration reception in the bullfrog,Rana catesbeiana

SummaryThe opercularis system (OPS) of amphibians consists of an opercularis muscle that connects the shoulder girdle skeleton to the operculum, a movable element in the oval window of the otic capsule. The role of the OPS in reception of vibrations was examined in bullfrogs (Rana catesbeiana) tested in various postures that manipulated differential motion between the shoulder girdle (the origin of the opercularis muscle) and skull (including the inner ear). Amplitude and phase relationship of motions of the suprascapular cartilage of the shoulder girdle and the posterior skull were also measured during these tests.1.Microphonic responses to vertical vibrations from 25–200 Hz were typically highest when frogs were in a normal, sitting posture with the head held off the vibrating platform. Responses from animals in which the head directly contacted the platform were often less (by up to 10 dB at certain frequencies). Responses from all test positions were highest at lower frequencies, especially between 50–100 Hz.2.Suprascapular accelerations were typically highest in the normal, sitting posture, and at lower frequencies (50–75 Hz) were often greater than that of the vibrating platform by up to 8 dB. The shoulder girdle skeleton of the bullfrog is therefore readily affected by vertical substrate motion.3.The amplitude of microphonic responses in the different test postures did not correspond well with head acceleration. Rather, response amplitude corresponded best with the absolute difference between shoulder and head motion. For example, in the normal posture, suprascapular motion was much greater than head motion, and responses were relatively high. If only the head was vibrated, head motion was high and shoulder motion low, and responses also were relatively high. If the head and body were vibrated together, their motions were similar, and responses to the same platform accelerations were often reduced. Phase differences between shoulder and head motions were small at the frequencies examined and may be of little functional significance. The importance of differences in shoulder and head motion suggests that the resulting differential motion of the operculum and inner ear fluids can produce waves that stimulate appropriate end organs (such as the saccule).4.Removal of the opercularis muscle reduced responses up to 18 dB at certain frequencies in some of the test postures. The most significant reductions were observed in those postures with a significant difference between shoulder and head motion (such as the normal posture). The opercularis muscle is therefore effective in translating differential motion of the head and shoulder into motion of the operculum relative to the inner ear fluids.5.Vertical vibrations produced higher microphonic responses than longitudinal or transverse vibrations of the same acceleration. Also, removal of the opercularis muscle produced a greater decrease in responses to vertical vibrations than in responses to the other types of vibrations. This suggests that the OPS of the bullfrog is specialized for reception of vertical substrate motions, such as Rayleigh waves, natural surface waves with a largely vertical energy component.

Semaphoring in an earless frog: the origin of a novel visual signal

Abstract Social communication in anuran amphibians (frogs and toads) is mediated predominantly by acoustic signals. Unlike most anurans, the Panamanian golden frog, Atelopus zeteki, lacks a standard tympanic middle ear and appears to have augmented its communicatory repertoire to include rotational limb motions as visual signals, referred to here as semaphores. The communicatory nature of semaphoring was inferred from experimental manipulations using mirrored self-image presentations and nonresident introductions. Male frogs semaphored significantly more when presented with a mirrored self-image than with a nonreflective control. Novel encounters between resident males and nonresident frogs demonstrated that semaphores were used directionally and were displayed toward target individuals. Females semaphored frequently and this observation represents a rare case of signaling by females in a typically male-biased communicatory regime. Semaphore actions were clearly linked to a locomotory gait pattern and appear to have originated as an elaboration of a standard stepping motion.

Sexual differences in the tympanic frequency responses of the American bullfrog (Rana catesbeiana)

Adult male and female American bullfrogs (Rana catesbeiana) have sexually dimorphic middle ears. The most conspicuous feature is the relatively large tympanum of adult males. The acoustic responsiveness of the tympana of adult male and female bullfrogs was studied with a laser vibrometer. Clear sex‐related differences in middle ear frequency responses were observed between the sexes. The middle ear of adult males was generally more sensitive, but, more significantly, it showed a distinct peak in sensitivity at very low frequencies around 200 Hz that was entirely lacking in the female middle ear. The male middle ear therefore is especially responsive to the distinct low‐frequency peak in the male mating call centered around 200–300 Hz. The enlarged middle ear of male bullfrogs therefore may have evolved as a result of selective pressure to improve detection of the mating vocalizations of other males. Female bullfrogs lack tympanic sensitivity to the low‐frequency peak in the male mating call, and presumabl...

THE MIDDLE EAR MUSCLE OF FROGS DOES NOT MODULATE TYMPANIC RESPONSES TO SOUND

The effect of the opercularis (= middle ear) muscle on the acoustic responsiveness of the tympanic middle ear of anuran amphibians was studied using laser vibrometric measurements of tympanic responses to sound. Removal of the muscle or direct stimulation of denervated muscles had no measurable effects on tympanic responses to sound in either American bullfrogs (Rana catesbeiana) or green treefrogs (Hyla cinerea) at any frequency or at any sound-pressure level studied. These results suggest that, contrary to proposed hypotheses, the opercularis muscle of the anuran middle ear is not capable of modulating the responsiveness of the tympanic middle ear. Instead, the opercularis system most likely functions as an independent system involved in acoustic reception.

Behavioural use of seismic cues by the sandswimming lizard Scincus scincus

The sandfish lizard, Scincus scincus (Linnaeus) inhabits the deserts of Africa and the Middle East and spends most of its time buried in the sand. Laboratory experiments have determined that Scincus can respond and orient to insects on the sand surface by detecting vibrations produced by movements of the insects. When buried, Scincus can detect and respond to crickets and mealworms moving over the surface at distances up to about 15 cm. These responses are guided by vibratory cues, not olfactory cues, as the lizards respond much less frequently to dead insects placed on the surface at equal distances. The lizard obtain directional information from the vibrations, and can localize the insects, orient toward them, and emerge from the sand to capture them. Scincus buried in the sand also respond differently to crickets and mealworms; the faster moving crickets elicit appropriately quicker emergences. Tests with artificial signals have demonstrated that the lizard respond differently to different temporal pat...

Histochemical studies on the amphibian opercularis muscle (Amphibia)

SummaryHistochemical studies of the opercularis muscle of the bullfrog (Rana catesbeiana) and the tiger salamander (Ambystoma tigrinum) provide evidence that the opercularis muscle of anurans is a specialized, tonic portion of the levator scapulae superior muscle. Staining results for myosin adenosine triphosphatase (ATPase) and succinate dehydrogenase (SDH), combined with measurements of muscle fiber diameters, demonstrate that the opercularis/levator scapulae superior muscle mass of both the tiger salamander and bullfrog consists of an anterior tonic portion, a middle fast oxidative-glycolytic (FOG) twitch portion, and a posterior fast-glycolytic (FG) twitch portion. In R. catesbeiana the tonic fibers represent 57.3% of the fiber total and (because they have relatively narrow diameters) about 29% of the cross-sectional area of the muscle mass, and form that part of the muscle (=opercularis muscle) that inserts on the operculum. In Ambystoma the tonic fibers represent only 8.8% of the fiber total and represent about 4% of the cross-sectional area. In the tiger salamander, the entire levator scapulae superior muscle inserts on the operculum and therefore represents the opercularis muscle. The bullfrog differs from the tiger salamander, therefore, in that the anterior tonic part of the opercularis/levator scapulae superior complex is greatly enlarged and the insertion on the operculum is limited to these tonic fibers. No evidence of a columellar muscle was found in R. catesbeiana. Previous reports of one in this species and in other anurans may be based on the tripartite nature of the opercularis/levator scapulae superior muscle mass. The middle FOG portion of the muscle may have been considered a muscle distinct from the anterior tonic portion (=opercularis muscle) and the posterior FG portion.