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Allometry in vestibular responses of anurans
Pergamon www.elsevier.nl/locate/asr
A& Space Res. Vol. 23, No. 12, pp. 2083-2086,1999 0 1999 COSPAR. Published bv Elsevier Science Ltd. AI1 rights reserved Printed in &eat Britain 0273-I 177/99 $20.00 + 0.00 PII: SO273-1177(99)00166-O
ALLOMETRY IN VESTIBULAR RESPONSES OF ANURANS M. Yamashital, T. Naitohz, A. Kashiwag? 1Institute of 2Department 3Laborator-y 4Department
, Y. Kondo3 and R.J. Wassersugd
Space and Astronautical Science, Sagamihara, Kanagawa 229-8510, Japan of Biological Science, Shimane University, Matsue, Shimane 690-8504, Japan for Amphibian Biology, Hiroshima University, Higashihiroshima, 739, Japan of Anatomy & Neurobiology, Dalhousie University, Halifax, NS B3H 4H7, Canada
ABSTRACT Frogs and toads turn either their heads or bodies opposite to angular accelerations applied around the yaw axis. Thresholds exist for the minimum angular acceleration that induces this vestibulomotor response in individual frogs. These thresholds were recorded for several anuran species that cover a broad range of sizes and life styles. Interspecific variation in the magnitude of the thresholds, which correlated with the ecology and behavior of the species, was documented. Also an allometric relationship was observed between this threshold and body size; the larger the frog, the lower the threshold. In many species, the threshold value for reflexive vestibulomotor responses to angular acceleration was proportional to the -0.4 (+/-0.2) power of body mass. Physical dimensions of the semicircular canals determine, in part, vestibular sensitivity to angular acceleration. Hence changes with growth in the semicircular canals are believed to contribute to the slop&of -0.4. The biological significance of this allometry in vestibular responses is discussed and compared to trends in vestibular sensitivity and semicircular canal morphology of other vertebrate classes. 01999
COSPAR.
Published
by Elsevier Science Ltd.
INTRODUCTION The function and sensitivity of the vestibular organ should relate to the behavior and way of life of different animals. Amphibians were the first vertebrates to emerge from the aquatic world onto land and now occupy a large diversity of ecological niches. Behavioral responses to gravitational stimuli suggest that the sensitivity of the vestibular system may correlate with the ecology of different anuran species (Naitoh et al., 1994; Yamashita et al., 1997). Organogenesis of the vestibular system in anurans occurs largely before hatching (Whiteside, 1922). At metamorphosis, differentiation of the vestibular system is almost complete and the anuran is ready to function on land. Growth in size of the vestibular organ from the froglet to adult stage should correlate with changes in their vestibulomotor behavior, and the ecology of the species. In this paper we explore how changes in the sensitivity of this sensory organ correlate with the postmetamorphic growth of anurans of different ecologies. We also discuss how the coordination of sensory inputs and central processing may alter the vestibulomotor responses of different species. An understanding of the variation in vestibulomotor sensitivity among amphibians has implications to the potential use of these animals in future study of the function and adaptability of the vestibular system to unusual environments. METHODS Adults, tadpoles, and eggs of Hylajaponica, Rana nigromaculata, and Bufo japonicus were collected from field sites in Shimane and Kanagawa Prefectures, Japan. Bombina orientalis was bred for several generations in the laboratory. Tadpoles were fed boiled lettuce and spinach; froglets and adults ate mealworms, crickets, or beef liver. Temperature was maintained at 25 “C in the colony and at the time of the experiments. Yaw axis stimuli were applied to individual animals that were confined in a cylindrical vessel, which had a water soaked urethane foam sheet on the bottom to keep animals moist. The inner diameter of the vessel was >I50 % of snout-vent length of the animal examined. The vessel was placed on a stage that was rotated 2083
2084
M. Yamashita et al.
around the vertical axis by a stepping electric motor with a step angle of 0.0072 degrees. The time profile for rotation was computer controlled. Angular acceleration was kept constant for 10 sec. In order to keep the terminal velocity below a maximum of 200 degrees/set, the duration of acceleration was reduced at higher acceleration rates. The table was rotated at this steady speed for ten seconds, and decelerated at the same rate which it had been accelerated. The responses of the animals to accelerations were observed through a CCD video camera mounted above the stage. All observations were made in the dark, with infra-red light emitting diodes illuminating the animal. RESULTS Frogs and toads reacted to angular accelerations by turning their heads opposite to the acceleration, when the acceleration level exceeded a threshold value. When stimuli were strong, the frogs moved their whole bodies. At the same time, saccade motions of the head were displayed by certain species. Threshold values depended on both body size and species. The larger the animal’s mass, the lower the threshold observed. Intraspecific variation for this threshold is shown in Fig. 1 for four anuran species. The allometric relation between the threshold for response to an angular acceleration and body mass was found to fit a power function of - 0.4 (+/-0.2, depending on species). Interspecific variation in this threshold value was quite large when the animals were compared at normalized and Ranu nigromucufura showed the highest and the lowest threshold respectively. Threshold values for Bufoju~onicus and Bombinu oriettrulis were more dispersed but lay largely between the other two species. body masses. Hylujuponicu
01
1
IO
100
1000
Body Weight (g)
Fig. 1 Threshold of angular acceleration for vestibular response to yaw stimuli.
DISCUSSION Growth Process and Ailometrv of Vestibular Resuonses The body mass at maturity is almost three orders of magnitude higher for Bufojuponicus, and two orders higher for Ranu nigromuculuta, than immediately after metamorphosis. Even though differentiation of the anuran vestibular system is complete at metamorphosis, its physical size increases greatly with this postmetamorphic growth (Dempster, 1930). Sensitivity of the semicircular canals for vertebrates in general has been estimated by modeling their mechanism for sensing angular acceleration (Jones and Spells, 1963; Gauldie and Radtke, 1990; Muller, 1994; ten Kate er al., 1970). The models suggest that the frequency response and sensitivity of the system should depend largely on its size and the proportions of each part of
Vestibular Responses
2085
the sensory organ. In cases where the proportions are the same in different sized semicircular canals, the models predict that the physically larger canals should have the higher sensitivity for angular acceleration. That is consistent with our observed trend of a lower threshold for bigger animals, shown in Fig. 1. The relation between the size of the vestibular system and the body as a whole is a fundamental factor in quantitative analysis of the vestibular responses of animals at different body size. Allometric growth of the vestibular organ was examined and discussed for fishes by ten Kate et al. (1970) who concluded that the threshold of the vestibular response for fishes is independent on body size. However, Howland and Masci (1973) reported a 0.229 to 0.358 power function relationship of body mass to the radii of curvature in the semicircular canals of fishes. Jones and Spells (1963) as well elucidated a 0.095 power of body mass to the square of the internal radius of the canals, and 0.076 for radius of curvature, based on a large compilation of morphological data from many species and families of vertebrates. Based on the trend he found, Jones (1974) proposed a correlation between the speed of movement and the required sensitivity of the semicircular canals in animals of different sizes. Changes in the size and proportions of the vestibular system with postmetamorphic growth in anurans have not been described in detail. Anuran external proportions, however, change relatively little with growth; i.e., froglets are shaped like adult frogs. The size of the vestibular system during growth is determined in part by cranial growth. Postmetamorphic growth and remodeling of the cranium do not take place isometrically (Parker, 187 1). Inner parts, such as the semicircular canals, do not grow linearly with body length. The separation of the right and left inner ear can be used as an index to evaluate topological changes with growth. From X-ray imaging of the inner ear of frogs and toads at different size (Yamashita et al., 1996), the separation of the otolithic layers was found to be roughly proportional to the 0.6 power of body size (i.e., 0.2 power of body mass). It is reasonable to suspect that the physical dimensions of the semicircular canals may have a similar allometric relationship. From the theoretical prediction of vestibular sensitivity and its dependence on the physical dimensions of the sensory organ, the power of 0.2 on body mass might predict a power of more than -0.4 for the thresholds observed. The proportions, however, for the physical dimensions of the semicircular canal need not be the same during growth, even though the fundamental configuration and design of the organ are established before metamorphosis. Changes in the proportion of inner cross section of the canal, its radius of curvature, and the ratio of the diameters between the duct and ampulla section might explain the discrepancy. Central nervous system (CNS) suppression of vestibular responses may also influence the perceived sensitivity of the canals, predicted from their allometric relationships. As both prey and predator, frogs and toads have to contend with trade-offs in whether or not to move their heads. Moving the head to counter external acceleration may stabilize their visual field, but would reveal the anurans’ presences to predators. If the degree of CNS supression is enhanced during postmetamorphic growth, that would result in modification of the slope in the power function to less than expected but yielding improved sensitivity when grown. Observed allometry could be a combination of an increase in the sensitivity at the sensory organ and increased suppression of vestibulomotor behavior by the CNS during overall growth. Large dispersion of the threshold in some species, such as Bombina orientalis, might indicate variable suppression among individuals. Ecological Niche. & Intersoecific and Intrasnecific Variation We found the highest threshold value for angular acceleration in the vestibulomotor response of the arboreal species, Hylajaponica, compared to the terrestrial taxa. This difference in habitat corresponds to differences in the stability of the surfaces on which these animals perch and the dimensionality of their worlds (i.e., the arboreal niche is more three dimensional than the terrestrial one.) Arboreal species perch on surface, such as leaves on trees and blades of grasses. They experience unintentional movements of their body as the substrates on which they perch move in the wind. These species are equipped with toe-pads to help them hold onto mobile surfaces, and may be programmed to suppress vestibulomotor responses to angular acceleration. Terrestrial species, in contrast, are used to perching on stabler surfaces. Sensing an unintentional movement would be an alarming situation for these anurans. Hence, they should have high vestibular sensitivity (i.e., a low threshold), and for their own defense to whatever is moving them, they should not suppress their vestibulomotor responses. The functionality of the anuran’s vestibulomotor program evidently differs across species. This is reflected in the absolute size at metamorphosis and the ratio of their size at metamorphosis to that at maturity. The
M. Yamashitaet al.
2086
large spread in vestibular thresholds for the four taxa at their metamorphic sizes suggests that the animals are already committed to their distinctive ecological niches when they first emerge on land. In conclusion a variety of factors appear to affect the scaling of vestibular sensitivity in anurans. The differences ‘between species are substantial, but can be generally understood in the context of the environments in which they live. Knowledge of the differences in vestibulomotor responses of anurans has implication to the selection of species for future studies on the adaptation of animals to exotic accelerations. ACKNOWLEDGMENTS This study was supported by the ISAS Fund for Basic Experiments Oriented to Space Station Utilization. Wassersug’s space research has been supported by the Natural Science and Engineering Research Council of Canada, and the Canadian Space Agency. REFERENCES Dempster, W.T., The Morphology of the Amphibian Endolymphatic Organ, _I.Morph. Physiof., 50,7 I - 126 (1930). Gauldie, R.W., and R. L. Radtke, Using the Physical Dimensions of the Semicircular Canal as a Probe to Evaluate Inner Ear Function in Fishes, Comp. Biochem. Physiol., 96A, 199-203 ( 1990). Howland, H.C., and J. Masci, The Functional Allometry of Semicircular Canals, Fins and Body Dimensions in the Juvenile Centrarchid Fish, Lepomis gibbosus (L.), J. EmbryoE. up. Morph., 29, 72 l-743 ( 1973). Jones, G.M., The Functional Significance of Semicircular Canal Size, in Hundbook oj’Sensory Physiology WI, Vestibulur System, Part Z:Busic Mechanisms, ed, Kohnhuber, H.H., Springer-Verlag, 171- 184 (1974). Jones, G.M., and K. E. Spells, A Theoretical and Comparative Study of the Functional Dependence of the Semicircular Canal upon its Physical Dimension, Proc. Roy. Sot. B., 157,403-419 (1963). Muller, M., Semicircular Duct.Dimensions and Sensitivity of the Vertebrate Vestibular System, J. theor: Biol., 167,239-256 (1994). Naitoh, T., M. Yamashita, A. Izumi-Kurotani, S. Yokota, and R.J.Wassersug, Interspecific variation in the behavioral responses of frogs to exotic gravitational stimuli. ASGSB Bull., 8, 22 (1994). Parker, W.K., On the Structure and Development of the Skull of the Common Frog (Rana temporaria, L), Phil. Trans. Royal Sot. London, 161, 137-211 (187 1). ten Kate, J.H., H. H. Van Barneveld, and J. W. Kuiper, The Dimensions and Sensitivities of Semicircular Canals, J. Exp. Biol., 53, 501-5 14 (1970). Whiteside, B., The Development of the Saccus Endolymphaticus in Rana temporariu L., Amer. J. Anatomy, 30,23
l-266 (1922).
Yamashita, M., A. Izumi-Kurotani, Y. Mogami, M. Okuno, T. Naitoh, and R. J. Wassersug, The Frog Space (FRIS) Experiment Onboard Space Station Mir: Final Report and Follow-on Studies, Biol. Sci. Space, 11,3 13-320 (1997). Yamashita, M., T. Naitoh, R. J. Wassersug, A. Izumi-Kurotani, S. Kawamata, M. Suzuki, A. Shiraishi, Miyagi-Okamoto, Y. Okamoto, T. Takeshima, and Y. Takatsuki, X-ray Imaging of Otolithic Layer Anurans and Its Interspecific Variation, Space Utiliz. Rex, 13,77-80 (1996).
in in
Y. of
A& Space Res. Vol. 23, No. 12, pp. 2083-2086,1999 0 1999 COSPAR. Published bv Elsevier Science Ltd. AI1 rights reserved Printed in &eat Britain 0273-I 177/99 $20.00 + 0.00 PII: SO273-1177(99)00166-O
ALLOMETRY IN VESTIBULAR RESPONSES OF ANURANS M. Yamashital, T. Naitohz, A. Kashiwag? 1Institute of 2Department 3Laborator-y 4Department
, Y. Kondo3 and R.J. Wassersugd
Space and Astronautical Science, Sagamihara, Kanagawa 229-8510, Japan of Biological Science, Shimane University, Matsue, Shimane 690-8504, Japan for Amphibian Biology, Hiroshima University, Higashihiroshima, 739, Japan of Anatomy & Neurobiology, Dalhousie University, Halifax, NS B3H 4H7, Canada
ABSTRACT Frogs and toads turn either their heads or bodies opposite to angular accelerations applied around the yaw axis. Thresholds exist for the minimum angular acceleration that induces this vestibulomotor response in individual frogs. These thresholds were recorded for several anuran species that cover a broad range of sizes and life styles. Interspecific variation in the magnitude of the thresholds, which correlated with the ecology and behavior of the species, was documented. Also an allometric relationship was observed between this threshold and body size; the larger the frog, the lower the threshold. In many species, the threshold value for reflexive vestibulomotor responses to angular acceleration was proportional to the -0.4 (+/-0.2) power of body mass. Physical dimensions of the semicircular canals determine, in part, vestibular sensitivity to angular acceleration. Hence changes with growth in the semicircular canals are believed to contribute to the slop&of -0.4. The biological significance of this allometry in vestibular responses is discussed and compared to trends in vestibular sensitivity and semicircular canal morphology of other vertebrate classes. 01999
COSPAR.
Published
by Elsevier Science Ltd.
INTRODUCTION The function and sensitivity of the vestibular organ should relate to the behavior and way of life of different animals. Amphibians were the first vertebrates to emerge from the aquatic world onto land and now occupy a large diversity of ecological niches. Behavioral responses to gravitational stimuli suggest that the sensitivity of the vestibular system may correlate with the ecology of different anuran species (Naitoh et al., 1994; Yamashita et al., 1997). Organogenesis of the vestibular system in anurans occurs largely before hatching (Whiteside, 1922). At metamorphosis, differentiation of the vestibular system is almost complete and the anuran is ready to function on land. Growth in size of the vestibular organ from the froglet to adult stage should correlate with changes in their vestibulomotor behavior, and the ecology of the species. In this paper we explore how changes in the sensitivity of this sensory organ correlate with the postmetamorphic growth of anurans of different ecologies. We also discuss how the coordination of sensory inputs and central processing may alter the vestibulomotor responses of different species. An understanding of the variation in vestibulomotor sensitivity among amphibians has implications to the potential use of these animals in future study of the function and adaptability of the vestibular system to unusual environments. METHODS Adults, tadpoles, and eggs of Hylajaponica, Rana nigromaculata, and Bufo japonicus were collected from field sites in Shimane and Kanagawa Prefectures, Japan. Bombina orientalis was bred for several generations in the laboratory. Tadpoles were fed boiled lettuce and spinach; froglets and adults ate mealworms, crickets, or beef liver. Temperature was maintained at 25 “C in the colony and at the time of the experiments. Yaw axis stimuli were applied to individual animals that were confined in a cylindrical vessel, which had a water soaked urethane foam sheet on the bottom to keep animals moist. The inner diameter of the vessel was >I50 % of snout-vent length of the animal examined. The vessel was placed on a stage that was rotated 2083
2084
M. Yamashita et al.
around the vertical axis by a stepping electric motor with a step angle of 0.0072 degrees. The time profile for rotation was computer controlled. Angular acceleration was kept constant for 10 sec. In order to keep the terminal velocity below a maximum of 200 degrees/set, the duration of acceleration was reduced at higher acceleration rates. The table was rotated at this steady speed for ten seconds, and decelerated at the same rate which it had been accelerated. The responses of the animals to accelerations were observed through a CCD video camera mounted above the stage. All observations were made in the dark, with infra-red light emitting diodes illuminating the animal. RESULTS Frogs and toads reacted to angular accelerations by turning their heads opposite to the acceleration, when the acceleration level exceeded a threshold value. When stimuli were strong, the frogs moved their whole bodies. At the same time, saccade motions of the head were displayed by certain species. Threshold values depended on both body size and species. The larger the animal’s mass, the lower the threshold observed. Intraspecific variation for this threshold is shown in Fig. 1 for four anuran species. The allometric relation between the threshold for response to an angular acceleration and body mass was found to fit a power function of - 0.4 (+/-0.2, depending on species). Interspecific variation in this threshold value was quite large when the animals were compared at normalized and Ranu nigromucufura showed the highest and the lowest threshold respectively. Threshold values for Bufoju~onicus and Bombinu oriettrulis were more dispersed but lay largely between the other two species. body masses. Hylujuponicu
01
1
IO
100
1000
Body Weight (g)
Fig. 1 Threshold of angular acceleration for vestibular response to yaw stimuli.
DISCUSSION Growth Process and Ailometrv of Vestibular Resuonses The body mass at maturity is almost three orders of magnitude higher for Bufojuponicus, and two orders higher for Ranu nigromuculuta, than immediately after metamorphosis. Even though differentiation of the anuran vestibular system is complete at metamorphosis, its physical size increases greatly with this postmetamorphic growth (Dempster, 1930). Sensitivity of the semicircular canals for vertebrates in general has been estimated by modeling their mechanism for sensing angular acceleration (Jones and Spells, 1963; Gauldie and Radtke, 1990; Muller, 1994; ten Kate er al., 1970). The models suggest that the frequency response and sensitivity of the system should depend largely on its size and the proportions of each part of
Vestibular Responses
2085
the sensory organ. In cases where the proportions are the same in different sized semicircular canals, the models predict that the physically larger canals should have the higher sensitivity for angular acceleration. That is consistent with our observed trend of a lower threshold for bigger animals, shown in Fig. 1. The relation between the size of the vestibular system and the body as a whole is a fundamental factor in quantitative analysis of the vestibular responses of animals at different body size. Allometric growth of the vestibular organ was examined and discussed for fishes by ten Kate et al. (1970) who concluded that the threshold of the vestibular response for fishes is independent on body size. However, Howland and Masci (1973) reported a 0.229 to 0.358 power function relationship of body mass to the radii of curvature in the semicircular canals of fishes. Jones and Spells (1963) as well elucidated a 0.095 power of body mass to the square of the internal radius of the canals, and 0.076 for radius of curvature, based on a large compilation of morphological data from many species and families of vertebrates. Based on the trend he found, Jones (1974) proposed a correlation between the speed of movement and the required sensitivity of the semicircular canals in animals of different sizes. Changes in the size and proportions of the vestibular system with postmetamorphic growth in anurans have not been described in detail. Anuran external proportions, however, change relatively little with growth; i.e., froglets are shaped like adult frogs. The size of the vestibular system during growth is determined in part by cranial growth. Postmetamorphic growth and remodeling of the cranium do not take place isometrically (Parker, 187 1). Inner parts, such as the semicircular canals, do not grow linearly with body length. The separation of the right and left inner ear can be used as an index to evaluate topological changes with growth. From X-ray imaging of the inner ear of frogs and toads at different size (Yamashita et al., 1996), the separation of the otolithic layers was found to be roughly proportional to the 0.6 power of body size (i.e., 0.2 power of body mass). It is reasonable to suspect that the physical dimensions of the semicircular canals may have a similar allometric relationship. From the theoretical prediction of vestibular sensitivity and its dependence on the physical dimensions of the sensory organ, the power of 0.2 on body mass might predict a power of more than -0.4 for the thresholds observed. The proportions, however, for the physical dimensions of the semicircular canal need not be the same during growth, even though the fundamental configuration and design of the organ are established before metamorphosis. Changes in the proportion of inner cross section of the canal, its radius of curvature, and the ratio of the diameters between the duct and ampulla section might explain the discrepancy. Central nervous system (CNS) suppression of vestibular responses may also influence the perceived sensitivity of the canals, predicted from their allometric relationships. As both prey and predator, frogs and toads have to contend with trade-offs in whether or not to move their heads. Moving the head to counter external acceleration may stabilize their visual field, but would reveal the anurans’ presences to predators. If the degree of CNS supression is enhanced during postmetamorphic growth, that would result in modification of the slope in the power function to less than expected but yielding improved sensitivity when grown. Observed allometry could be a combination of an increase in the sensitivity at the sensory organ and increased suppression of vestibulomotor behavior by the CNS during overall growth. Large dispersion of the threshold in some species, such as Bombina orientalis, might indicate variable suppression among individuals. Ecological Niche. & Intersoecific and Intrasnecific Variation We found the highest threshold value for angular acceleration in the vestibulomotor response of the arboreal species, Hylajaponica, compared to the terrestrial taxa. This difference in habitat corresponds to differences in the stability of the surfaces on which these animals perch and the dimensionality of their worlds (i.e., the arboreal niche is more three dimensional than the terrestrial one.) Arboreal species perch on surface, such as leaves on trees and blades of grasses. They experience unintentional movements of their body as the substrates on which they perch move in the wind. These species are equipped with toe-pads to help them hold onto mobile surfaces, and may be programmed to suppress vestibulomotor responses to angular acceleration. Terrestrial species, in contrast, are used to perching on stabler surfaces. Sensing an unintentional movement would be an alarming situation for these anurans. Hence, they should have high vestibular sensitivity (i.e., a low threshold), and for their own defense to whatever is moving them, they should not suppress their vestibulomotor responses. The functionality of the anuran’s vestibulomotor program evidently differs across species. This is reflected in the absolute size at metamorphosis and the ratio of their size at metamorphosis to that at maturity. The
M. Yamashitaet al.
2086
large spread in vestibular thresholds for the four taxa at their metamorphic sizes suggests that the animals are already committed to their distinctive ecological niches when they first emerge on land. In conclusion a variety of factors appear to affect the scaling of vestibular sensitivity in anurans. The differences ‘between species are substantial, but can be generally understood in the context of the environments in which they live. Knowledge of the differences in vestibulomotor responses of anurans has implication to the selection of species for future studies on the adaptation of animals to exotic accelerations. ACKNOWLEDGMENTS This study was supported by the ISAS Fund for Basic Experiments Oriented to Space Station Utilization. Wassersug’s space research has been supported by the Natural Science and Engineering Research Council of Canada, and the Canadian Space Agency. REFERENCES Dempster, W.T., The Morphology of the Amphibian Endolymphatic Organ, _I.Morph. Physiof., 50,7 I - 126 (1930). Gauldie, R.W., and R. L. Radtke, Using the Physical Dimensions of the Semicircular Canal as a Probe to Evaluate Inner Ear Function in Fishes, Comp. Biochem. Physiol., 96A, 199-203 ( 1990). Howland, H.C., and J. Masci, The Functional Allometry of Semicircular Canals, Fins and Body Dimensions in the Juvenile Centrarchid Fish, Lepomis gibbosus (L.), J. EmbryoE. up. Morph., 29, 72 l-743 ( 1973). Jones, G.M., The Functional Significance of Semicircular Canal Size, in Hundbook oj’Sensory Physiology WI, Vestibulur System, Part Z:Busic Mechanisms, ed, Kohnhuber, H.H., Springer-Verlag, 171- 184 (1974). Jones, G.M., and K. E. Spells, A Theoretical and Comparative Study of the Functional Dependence of the Semicircular Canal upon its Physical Dimension, Proc. Roy. Sot. B., 157,403-419 (1963). Muller, M., Semicircular Duct.Dimensions and Sensitivity of the Vertebrate Vestibular System, J. theor: Biol., 167,239-256 (1994). Naitoh, T., M. Yamashita, A. Izumi-Kurotani, S. Yokota, and R.J.Wassersug, Interspecific variation in the behavioral responses of frogs to exotic gravitational stimuli. ASGSB Bull., 8, 22 (1994). Parker, W.K., On the Structure and Development of the Skull of the Common Frog (Rana temporaria, L), Phil. Trans. Royal Sot. London, 161, 137-211 (187 1). ten Kate, J.H., H. H. Van Barneveld, and J. W. Kuiper, The Dimensions and Sensitivities of Semicircular Canals, J. Exp. Biol., 53, 501-5 14 (1970). Whiteside, B., The Development of the Saccus Endolymphaticus in Rana temporariu L., Amer. J. Anatomy, 30,23
l-266 (1922).
Yamashita, M., A. Izumi-Kurotani, Y. Mogami, M. Okuno, T. Naitoh, and R. J. Wassersug, The Frog Space (FRIS) Experiment Onboard Space Station Mir: Final Report and Follow-on Studies, Biol. Sci. Space, 11,3 13-320 (1997). Yamashita, M., T. Naitoh, R. J. Wassersug, A. Izumi-Kurotani, S. Kawamata, M. Suzuki, A. Shiraishi, Miyagi-Okamoto, Y. Okamoto, T. Takeshima, and Y. Takatsuki, X-ray Imaging of Otolithic Layer Anurans and Its Interspecific Variation, Space Utiliz. Rex, 13,77-80 (1996).
in in
Y. of