Neuromuscular control of prey capture in frogs.

While retaining a feeding apparatus that is surprisingly conservative morphologically, frogs as a group exhibit great variability in the biomechanics of tongue protraction during prey capture, which in turn is related to differences in neuromuscular control. In this paper, I address the following three questions. (1) How do frog tongues differ biomechanically? (2) What anatomical and physiological differences are responsible? (3) How is biomechanics related to mechanisms of neuromuscular control? Frog species use three non-exclusive mechanisms to protract their tongues during feeding: (i) mechanical pulling, in which the tongue shortens as its muscles contract during protraction; (ii) inertial elongation, in which the tongue lengthens under inertial and muscular loading; and (iii) hydrostatic elongation, in which the tongue lengthens under constraints imposed by the constant volume of a muscular hydrostat. Major differences among these functional types include (i) the amount and orientation of collagen fibres associated with the tongue muscles and the mechanical properties that this connective tissue confers to the tongue as a whole; and (ii) the transfer of intertia from the opening jaws to the tongue, which probably involves a catch mechanism that increases the acceleration achieved during mouth opening. The mechanisms of tongue protraction differ in the types of neural mechanisms that are used to control tongue movements, particularly in the relative importance of feed-forward versus feedback control, in requirements for precise interjoint coordination, in the size and number of motor units, and in the afferent pathways that are involved in coordinating tongue and jaw movements. Evolution of biomechanics and neuromuscular control of frog tongues provides an example in which neuromuscular control is finely tuned to the biomechanical constraints and opportunities provided by differences in morphological design among species.     

Prey location,biomechanical constraints,and motor program choice during prey capture in the tomato frog, <Emphasis Type="Italic">Dyscophus guineti</Emphasis>

This study investigated how visual information about prey location and biomechanical constraints of the feeding apparatus influence the feeding behavior of the tomato frog, Dyscophus guineti. When feeding on prey at small azimuths (less than ± 40°), frogs aimed their heads toward the prey but did not aim their tongues relative to their heads. Frogs projected their tongues rapidly by transferring momentum from the lower jaw to the tongue. Storage and recovery of elastic energy by the mouth opening muscles amplified the velocities of mouth opening and tongue projection. This behavior can only occur when the lower jaw and tongue are aligned (i.e., within the range of motion of the neck). When feeding on prey at large azimuths (greater than ± 40°), frogs aimed both the head and tongue toward the prey and used a muscular hydrostatic mechanism to project the tongue. Hydrostatic elongation allows for frogs to capture prey at greater azimuthal locations. Because the tongue moves independently of the lower jaw, frogs can no longer take advantage of momentum transfer to amplify the speed of tongue projection. To feed on prey at different azimuthal locations, tomato frogs switch between alternative strategies to circumvent these biomechanical constraints.     

Mechanical properties of sea-urchin lantern muscles: a comparative investigation of intact muscle groups in Paracentrotus lividus (Lam.) and Stylocidaris affinis (Phil.) (Echinodermata, Echinoidea)

The jaw apparatus, or lantern, of sea-urchins contains five pairs of retractor and protractor muscles which are responsible for lantern displacement. Using intact retractor or protractor groups, the force-length relations of these muscles were compared in two taxonomically distant species, Paracentrotus lividus and Stylocidaris affinis. The total contractile forces generated by the muscles can be resolved into vertical and horizontal components. It was found that the vertical component of the retractors is maximal at a lantern position which is significantly lower (i.e. more protruded) in Paracentrotus than in Stylocidaris. Total forces generated by the retractors were in both species maximal at or above the lantern `resting positions'. In Paracentrotus alone, the total force-displacement curves tended to be bimodal. It is hypothesized that the retractors of Paracentrotus contain two populations of muscle fibres, one adapted for jaw opening and one for lantern retraction. No significant differences in the properties of the protractors of the two species could be identified. The lantern of Paracentrotus is more mobile than that of Stylocidaris and is able to exploit a wider range of food sources. This investigation has shown that the force-length relations of the lantern muscles match their differing working conditions. Accepted: 3 November 1997     

Feeding specializations of the Mexican burrowing toad, Rhinophrynus dorsalis (Anura: Rhinophrynidae)

Of the several, unrelated anuran taxa that feed underground, the Neotropical pipoid, Rhinophrynus dorsalis , seems to be the most specialized ant- and termite-feeder. The snout is covered with a curious and apparently unique epidermal armour. The buccal and oesophageal linings are ornately folded. The lips effect a double closure along the long, wedgeshaped, edentate maxillary arch. Peculiar submandibular glands seem to enhance the seal of the lips. The results of morphological, cinematographic, and muscle stimulation studies reveal that Rhinophrynus has a mechanism of tongue protrusion basically distinct from that of other frogs that project their tongues by means of a lingual flip. In Rhinophrynus , the intrinsic tongue muscles act to stiffen the organ, exerting hydrostatic pressure on the fluid contents of the lingual sinus. Actual protrusion of the tongue through the buccal groove involves shifting the organ forward via protraction of the hyoid by muscles extrinsic to the tongue—a mode that is unique among anurans and one highly suited for securing small insect prey in subterranean burrows.     

Comparison of isometric contractile properties in hindlimb extensor muscles of the frogs Rana pipiens and Bufo marinus: functional correlations with differences in hopping performance

The leopard frog (Rana pipiens) is an excellent jumper that can reach high take-off velocities and accelerations. It is diurnal, using long, explosive jumps to capture prey and escape predators. The marine toad (Bufo marinus) is a cryptic, nocturnal toad, typically using short, slow hops, or sometimes walking, to patrol its feeding area. Typical of frogs with these different locomotor styles, Rana has relatively long hindlimbs and large (by mass) hindlimb extensor muscles compared to Bufo. We studied the isometric contractile properties of their extensor muscles and found differences that correlate with their different hopping performances. At the hip (semimembranosus, SM), knee (peroneus, Per) and ankle (plantaris longus, PL), we found that Rana's muscles tended to produce greater maximum isometric force relative to body mass, although the difference was significant only for PL. This suggests that differences in force capability at the ankle may be more important than at other joints to produce divergent hopping performances. Maximum isometric force scaled with body mass so that the smaller Rana has relatively larger muscles and force differences between species may reflect size differences only. In addition, Rana's muscles exhibited greater passive resistance to elongation, implying more elastic tissue is present, which may amplify force at take-off due to elastic recoil. Rana's muscles also achieved a higher percentage of maximum force at lower stimulus inputs (frequencies and durations) than in Bufo, perhaps amplifying the differences in force available for limb extension during natural stimulation. Twitch contraction and relaxation times tended to be faster in Rana, although variation was great, so that differences were significant only for Per. Fatigability also tended to be greater in Rana muscles, although, again, values reached significance in only one muscle (PL). Thus, in addition to biomechanical effects, differences in hopping performance may also be determined by diverse physiological properties of the muscles.     

Metamorphosis and evolution of feeding behaviour in salamanders of the family Plethodontidae

Plethodontid salamanders capture prey with enhanced tongue protraction relative to other salamander taxa, yet metamorphosing plethodontids are hypothesized to be constrained relative to direct-developing plethodontids in their degree of tongue evolution (protraction length and velocity) by the presence of a larval stage in development. In this biphasic life history the hyobranchial apparatus serves the conflicting functions of larval suction feeding and adult tongue protraction. The deletion of the larval stage removes one of the conflicting functions and has thus permitted direct-developing plethodontids to circumvent this constraint and evolve extremely long tongues, which in some species can be projected to 80% of body length. To evaluate this constraint hypothesis and explore taxonomic diversity of feeding behaviours, we studied feeding in larvae, adults and metamorphosing individuals of seven species of metamorphosing plethodontids from the basal taxa Desmognathinae and Hemidactyliini using direct observations, high-speed videography and kinematic analysis. We found that larval plethodontids suction feed, but feeding is suspended entirely during metamorphosis, and aquatic adults do not suction feed. Adults have exapted the terrestrial modes of tongue and jaw prehension for aquatic prey capture. These findings substantiate the premise that suction feeding and tongue protraction are conflicting functions, and thus our results support the constraint hypothesis. Plethodontid adults have evolved their extreme tongue protraction ability at the expense of adult suction feeding. The rapid metamorphosis that characterizes plethodontids may be an adaptation that minimizes the non-feeding period imposed by the evolution of derived tongue protraction in adults. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 134 , 375–400.     

Feeding Motor Patterns in Anurans: Insights from Biomechanical Modeling

During feeding in anurans, the mouth opens while the tongue,which is attached to the mandible at the front of the mouth,rotates forward. Due to the relative simplicity of its anatomyand the complexity of its motion, tongue protraction in frogspresents an ideal system for exploring the neural control ofmultijoint movements. In this study, we used a forward dynamic,rigid body model with four segments and two muscles to investigateopen loop control of tongue protraction in the Australian white-lippedtree frog, Litoria caerulea. Model parameters include the massdistribution, initial position and initial angular velocityof each segment and the anatomy and physiology of each muscle.Model variables include the level of muscle activation at eachtime step and impulsive torques to open and close the mouth.The model gives X,Y coordinates of each segment and joint anglesat each time step as output. The model was tested using scaled,normalized EMG signals and impulsive joint torques to predictthe paths of the lower jaw tip and tongue tip. Predicted pathswere compared to experimentally observed paths using Pearsonproduct-moment correlation coefficients. Simulations demonstratethat the genioglossus muscles likely play a minor role, if any,in determining the trajectory of the tongue in most anurans.Most of the force for tongue protraction comes from angularmomentum transferred to the tongue by the opening jaws. In anurans,tongue protraction is dynamically stable and will occur as longas the musculoskeletal elements are in the correct initial position.     

Kinematics of prey capture in the tailed frog Ascaphus truei (Anura: Ascaphidae)

The kinematics of prey capture by Ascaphus truei was investigated. High-speed films (100 fps) of 13 successful and one unsuccessful prey capture sequences from six adult frogs were analysed. Ascaphus , the sister group of all living frogs, shares several aspects of feeding kinematics, including rotation of the tongue pad about the mandibular symphysis and mandibular bending during mouth opening and closing, with more derived frogs such as Bufo marinus. The times required for tongue retraction, mouth opening and closing are similar in Ascaphus and Bufo. However, because Bufo is much larger and protracts its tongue much farther than Ascaphus , the velocities of tongue retraction, mouth opening and mouth closing are relatively lower in Ascaphus than in Bufo. Differences in prey capture between Ascaphus and Bufo marinus are (1) the distance of tongue protraction is less in Ascaphus (±0.5 cm) than in Bufo (c. 2 cm); and (2) lunging of the whole body is more pronounced in Ascaphus. Prey capture is highly variable in Ascaphus. An intraoral transport sequence is sometimes (7 of 14 observations) inserted into the prey capture cycle before the completion of mouth closing. The gape cycles range from 80–150 ms for sequences with no oral transport and from 130–280 ms for sequences with oral transport. Also, the time required for tongue retraction is significantly longer in the unsuccessful capture attempt. This variability is generally greater than that observed during prey capture in salamanders, and suggests that frogs and salamanders may differ in the importance of sensory feedback in coordinating prey capture.     

Season and testosterone affect contractile properties of fast calling muscles in the gray tree frog Hyla chrysoscelis

In anurans, circulating levels of androgens influence certain secondary sexual characteristics that are expressed only during the breeding season. We studied the contractile properties of external oblique muscles (used to power sound production) in a species of North American gray tree frog, Hyla chrysoscelis, during the breeding season and also in testosterone-treated captive males and females after the breeding season. Compared with the muscles of breeding-season males, the trunk muscles of postbreeding-season males have 50% less mass, 60% longer twitches, and 40% slower shortening velocities. Testosterone levels similar to those found in breeding-season male hylid frogs restore the contractile speed and mass of male trunk muscles and also convert the small slow trunk muscles of females into larger fast-contracting muscles. We conclude that androgens likely play a key role in altering the contractile properties of these muscles in males during the annual cycle, allowing them to operate in the breeding season at the frequencies required to produce the characteristic rapidly pulsed calls of this species. Females as well as nonbreeding-season males do not produce advertising calls, and therefore the slower muscles found in these animals may allow more economic operation of these muscles. The effects of testosterone on female trunk muscles indicate the potential of this hormone in contributing to the sexual dimorphism in size and contractile properties of these muscles, but this dimorphism is likely due to the interaction of more than one hormone.     

Functional anatomy of the luring apparatus of the deep-sea ceratioid anglerfish <Emphasis Type="Italic">Cryptopsaras couesii</Emphasis> (Lophiiformes: Ceratiidae)

The osteology and myology of the illicial apparatus of Cryptopsaras couesii were examined in an effort to elucidate function. The apparatus consists of two bones, a tiny illicial bone, completely enveloped by tissue of the esca, and an extremely long supporting pterygiophore that lies within a deep groove on the dorsal surface of the head. The anterior end of the pterygiophore emerges on the tip of the snout from between the frontal bones, while the posterior end, encased in a dermal sheath when the illicial apparatus is retracted, emerges on the back just anterior to the dorsal caruncles. Five pairs of muscles control movement of the illicial apparatus: small, short erectors and depressors control movement of the illicial bone, while extremely long inclinators, protractors, and retractors control movement of the pterygiophore. The protractors and retractors of C. couesii are more robust and much longer than those of other lophiiforms, indicating that the pterygiophore of this species has an exceptionally wide range of movement in the anterior and posterior plane. Moreover, these muscles wind around the pterygiophore in opposite directions, a unique anatomy that suggests that C. couesii extends and retracts the pterygiophore by rotation.     

The role of hypoglossal sensory feedback during feeding in the marine toad, Bufo marinus.

Behavioral observations demonstrate that bilateral deafferentation of the hypoglossal nerves in the marine toad (Bufo marinus) prevents mouth opening during feeding. In the present study, we used high-speed videography, electromyography (EMG), deafferentation, muscle stimulation, and extracellular recordings from the trigeminal nerve to investigate the mechanism by which sensory feedback from the tongue controls the jaw muscles of toads. Our results show that sensory feedback from the tongue enters the brain through the hypoglossal nerve during normal feeding. This feedback appears to inhibit both tonic and phasic activity of the jaw levators. Hypoglossal feedback apparently functions to coordinate tongue protraction and mouth opening during feeding. Among anurans, the primitive condition is the absence of a highly protrusible tongue and the absence of a hypoglossal sensory feedback system. The hypoglossal feedback system evolved in parallel with the acquisition of a highly protrusible tongue in toads and their relatives.     

Isometric contractile properties and instantaneous stiffness of amphibian skeletal muscle in the temperature range from 0 to 20 degrees C

The isometric contractile properties of frog (Rana pipiens) and toad (Bufo bufo) sartorii have been studied over the temperature range from 0 to 20 degrees C. The isometric twitch tension was found to vary considerably between these two species and between muscles in the same species. Between 0 and 4 degrees C there was very little change in maximum isometric twitch tension. Between 4 and 12 degrees C several muscles from frog or toad showed a potentiation of twitch tension whereas others showed a decline. Over this temperature range the toad sartorii consistently demonstrated a greater potentiation. By 12 degrees C a steady decline in twitch tension in both muscles was seen as the temperature range the toad sartorii consistently demonstrated a greater potentiation. By 12 degrees C a steady decline in twitch tension in both muscles was seen as the temperature approached 20 degrees C. The maximum isometric tetanic tension recorded between 18 and 20 degrees C increased fractionally to an average of 1.504 +/- 0.029 (n = 4) for frog sartorii and to 1.377 +/- 0.008 (n = 5) for toad sartorii. The time to peak twitch tension and the half-relaxation time decreased markedly with an increase in temperature. Moreover, the half-relaxation time was reduced by a greater proportion than the time to peak twitch tension. Measurements of instantaneous stiffness by controlled velocity releases from the plateau of isometric tetani revealed that the large increase in isometric tetanus tension as the muscle was warmed was not accompanied by a corresponding increase in the total number of active cross-bridges. The possibility that a decreased availability of intracellular Ca2+ ions at the contractile sites contributing to the fall of isometric twitch tension at elevated temperatures is discussed. The possibility exists that at elevated temperatures a change inthe intrinsic contractile ability of the muscle occurs which produces an increased tension per cross-bridge.     

Contractile properties of feline genioglossus, sternohyoid, and sternothyroid muscles.

Despite a wealth of information about the respiratory behavior of pharyngeal dilator muscles such as the genioglossus, sternohyoid, and sternothyroid muscles, little is known about their contractile and endurance properties. Strips of these muscles (as well as of the diaphragm) were surgically removed from anesthetized cats and studied in vitro at 37 degrees C. The isometric contraction times of the muscles were 38 +/- 1, 31 +/- 1, 28 +/- 2, and 35 +/- 1 ms for genioglossus, sternothyroid, sternohyoid, and diaphragm, respectively. Contraction times were significantly longer for the genioglossus than for the sternohyoid and sternothyroid muscles and significantly longer for the diaphragm than for the sternohyoid muscle. Twitch-to-tetanic ratios were largest for the diaphragm and lowest for the sternohyoid muscle, and the force-frequency relationship of the sternohyoid was most rightward positioned and that of the diaphragm was most leftward positioned. During repetitive stimulation, the decrement in force was greatest for the diaphragm and least for the genioglossus muscle, with the force loss of the two hyoid muscles being intermediate in magnitude. The Burke fatigue index was significantly greater for the genioglossus than for the diaphragm, despite similar tension-time indexes during repetitive stimulation. These data indicate heterogeneity among pharyngeal dilator muscles in their contractile and endurance properties, that certain pharyngeal dilator muscle properties differ from diaphragmatic properties, and that pharyngeal muscles have relatively fast contractile kinetics yet reasonable endurance characteristics.     

Resource competition triggers the co-evolution of long tongues and deep corolla tubes

Background

It is normally thought that deep corolla tubes evolve when a plant''s successful reproduction is contingent on having a corolla tube longer than the tongue of the flower''s pollinators, and that pollinators evolve ever-longer tongues because individuals with longer tongues can obtain more nectar from flowers. A recent model shows that, in the presence of pollinators with long and short tongues that experience resource competition, coexisting plant species can diverge in corolla-tube depth, because this increases the proportion of pollen grains that lands on co-specific flowers.

Methodology/Principal Findings

We have extended the model to study whether resource competition can trigger the co-evolution of tongue length and corolla-tube depth. Starting with two plant and two pollinator species, all of them having the same distribution of tongue length or corolla-tube depth, we show that variability in corolla-tube depth leads to divergence in tongue length, provided that increasing tongue length is not equally costly for both species. Once the two pollinator species differ in tongue length, divergence in corolla-tube depth between the two plant species ensues.

Conclusions/Significance

Co-evolution between tongue length and corolla-tube depth is a robust outcome of the model, obtained for a wide range of parameter values, but it requires that tongue elongation is substantially easier for one pollinator species than for the other, that pollinators follow a near-optimal foraging strategy, that pollinators experience competition for resources and that plants experience pollination limitation.     

THE ADDUCTOR AND RETRACTOR MUSCLES OF THE VELIGER OF PECTEN MAXIMUS (L.) (BIVALVIA)

In Pecten maximus (L.), retractor and adductor muscles becomefunctional in the early veliger larva. The twelve-day-old veligerhas four pairs of velar retractors, three pairs of retractorsattached to the posterior body wall and an anterior adductor.The pediveliger has in addition, pedal retractor muscles anda posterior adductor. The retractors consist of striated muscle:the adductors have both smooth and striated portions. The retractorsattach near the hinge, branch to a greater or lesser extent,then attach to specific areas of the velum, posterior body walland foot. Some features of the branching and of the dispositionof points of attachment form a pattern which exhibits mirrorsymmetry about the plane between the two shell valves. Thispattern is characteristic of the species. It is deduced thatretraction and protraction of the velum result from co-ordinatedsequences of muscle contractions. ^*Present address: Forest Products Research Centre, P.O. Box1358, Boroko, Papua New Guinea. (Received 15 June 1984;     

Diet breadth,coexistence and rarity in bumblebees

Factors that determine the relative abundance of bumblebee species remain poorly understood, rendering management of rare and declining species difficult. Studies of bumblebee communities in the Americas suggest that there are strong competitive interactions between species with similar length tongues, and that this competition determines the relative abundance of species. In contrast, in Europe it is common to observe several short-tongued species coexisting with little or no evidence for competition shaping community structure. In this study we examine patterns of abundance and distribution in one of the most diverse bumblebee communities in Europe, found in the mountains of southern Poland. We quantify forage use when collecting nectar and pollen for 23 bumblebee species, and examine patterns of co-occurrence and niche overlap to determine whether there is evidence for inter-specific competition. We also test whether rarity can be explained by diet breadth. Up to 16 species were found coexisting within single sites, with species richness peaking in mountain pasture at ~1,000 m altitude. Results concur with previous studies indicating that the majority of pollen collected by bumblebees is from Fabaceae, but that some bee species (e.g. B. ruderatus) are much more heavily dependent on Fabaceae than others (e.g. B. lucorum). Those species that forage primarily on Fabaceae tended to have long tongues. In common with studies in the UK, diet breadth was correlated with abundance: rarer species tended to visit fewer flower species, after correcting for differences in sample size. No evidence was found for similarity in tongue length or dietary overlap influencing the likelihood of co-occurrence of species. However, the most abundant species (which co-occurred at most sites) occupied distinct dietary niche space. While species with tongues of similar length tended, overall, to have higher dietary niche overlap, among the group of abundant short-tongued species that commonly co-occurred there was marked dietary differentiation which may explain their coexistence.     

Fiber types and some contractile properties of extensor digitorum longus and soleus muscles in different animal species

We studied the fiber types and contractile properties of the extensor digitorum longus (EDL) and soleus (SOL) muscles from young adult mice, rats and guinea pigs, and the correlation between these two parameters. Individual fibers in both muscles were classified as fast-twitch glycolytic (FG), fast-twitch oxidative glycolytic (FOG) or slow-twitch oxidative (SO) fibers according to Peter et al., and type II B, II A, or I fibers according to Brooke & Kaiser. Contractile properties were measured in situ at 37 degrees C. The isometric twitch contraction time (CT) and one-half relaxation time (1/2 RT) tended to be shortened in proportion to the area occupied by type II fibers, and type II B fibers. However, the differences between CT and fiber types were not always uniform among the three species. The CT of the rat EDL, in spite of its higher proportion of type II B fibers about 10% was the same as that of the guinea-pig EDL. The SOL of the mouse, composed of about 50% type I (SO) fibers, had a CT about as short as that of the EDL. In the case of the classification by Peter et al., the relationship between the percentage of subgroups of fast-twitch fibers and the CT or 1/2 RT, but not the resistance to fatigue, was not obvious. The resistance to fatigue tended to be enhanced in proportion to the area occupied by FOG in the EDL and by SO (type I) in the SOL. These results suggest that the contractile properties of individual fibers identified histochemically are distinct among animal species, producing interspecies differences in fiber types along with different contractile properties. However, it may be possible to compare the difference between fiber types and CT or 1/2 RT in the classification based on the pH lability of myosin ATPase, and also the difference between fiber types and resistance to fatigue in the classification based on the oxidative enzyme.     

The roles of visual and proprioceptive information during motor program choice in frogs

Previous studies have shown that leopard frogs, Rana pipiens, use tongue prehension to capture small prey and jaw prehension to capture large prey. After hypoglossal nerve transection, the frogs fail to open their mouths when attempting to feed on small prey, but open their mouths and capture large prey. Here, we investigate how visual information about the prey and proprioceptive information from the tongue interact to influence the motor program choice. Using pieces of earthworm of various sizes, we found that Rana exhibits two different behavior patterns based on prey size. The frogs captured the 1.5-cm prey using tongue prehension, whereas 2.0-cm and larger prey were captured using jaw prehension. After hypoglossal transection, the frogs never opened their mouths when they tried to feed on 1.5-cm prey. When feeding on 3.0-cm and larger prey after transection, they always opened their mouths and captured the prey using jaw prehension. When offered 2.0-cm prey, they alternated randomly between opening and not opening the mouth. Therefore, deafferentation changed the pattern of motor program choice at the behavioral border. This implies that afferents from the tongue interact with visual input to influence motor program choice.