Jaws that snap: control of mandible movements in the ant Mystrium

Ants of the genus Mystrium employ a peculiar snap-jaw mechanism in which the closed mandibles cross over to deliver a stunning blow to an adversary within about 0.5 ms. The mandible snapping is preceded by antennation and antennal withdrawal. The strike is initiated by contact of the adversary with mechanosensory hairs at the side of the mandible, and is powered by large yet slow closer muscles whose energy is stored by a catapult mechanism. Recording of closer muscle activity indicates that the mandibles are not triggered by any fast muscle. Instead, we suppose that activity differences between the left and right mandible muscles imbalance a pivot at the mandible tip and release the strike. The likelihood for the strike to occur can be modulated by an alarm pheromone. The presence of specialized sensilla and of a complex muscle receptor organ shows that the mandibles are also adapted to functions other than snapping and suggests that the force of the mandible can be finely adjusted for other tasks.     

The fast mandible strike in the trap-jaw ant Odontomachus

Ants of the ponerine genus Odontomachus employ a trap-jaw mechanism that allows them to instantaneously close their long, sturdy mandibles to catch prey or to defend themselves. Photoelectric scanning has revealed that these trap-jaws can be closed in less than 0.5 ms and that they decelerate before they collide with each other. The mandible strike is released in a reflexlike action when particular trigger hairs are touched. This reflex takes 4 to 10 ms and is probably the fastest reflex yet described for any animal. This speed is based on a catch mechanism in the mandible joint that keeps the extended mandibles open during contraction of the powerful closer muscle and allows the potential energy it produces to be stored within cuticular elements, apodemes, and the closer muscle itself. During a strike a relatively small specialized trigger muscle unlocks the catch, instantaneously releasing the stored energy to accelerate the mandible.     

The control of mandible movements in the ant Odontomachus

Ants use their mandibles to manipulate many different objects including food, brood and nestmates. Different tasks require the modification of mandibular force and speed. Besides normal mandible movements the trap-jaw ant Odontomachus features a particularly fast mandible reflex during which both mandibles close synchronously within 3 ms. The mandibular muscles that govern mandible performance are controlled by four opener and eight closer motor neurons. During slow mandible movements different motor units can be activated successively, and fine tuning is assisted by co-activation of the antagonistic muscles. Fast and powerful movements are generated by the additional activation of two particular motor units which also contribute to the mandible strike. The trap-jaw reflex is triggered by a fast trigger muscle which is derived from the mandible closer. Intracellular recording reveals that trigger motor neurons can generate regular as well as particularly large postsynaptic potentials, which might be passively propagated over the short distance to the trigger muscle. The trigger motor neurons are dye-coupled and receive input from both sides of the body without delay, which ensures the synchronous release of both mandibles.     

Mandible movements in ants.

Ants use their mandibles for almost any task, including prey-catching, fighting, leaf-cutting, brood care and communication. The key to the versatility of mandible functions is the mandible closer muscle. In ants, this muscle is generally composed of distinct muscle fiber types that differ in morphology and contractile properties. Fast contracting fibers have short sarcomeres (2-3 microm) and attach directly to the closer apodeme, that conveys the muscle power to the mandible joint. Slow but forceful contracting fibers have long sarcomeres (5-6 microm) and attach to the apodeme either directly or via thin thread-like filaments. Volume proportions of the fiber types are species-specific and correlate with feeding habits. Two biomechanical models explain why species that rely on fast mandible strikes, such as predatory ants, have elongated head capsules that accommodate long muscle fibers directly attached to the apodeme at small angles, whereas species that depend on forceful movements, like leaf-cutting ants, have broader heads and many filament-attached fibers. Trap-jaw ants feature highly specialized catapult mechanisms. Their mandible closing is known as one of the fastest movements in the animal kingdom. The relatively large number of motor neurons that control the mandible closer reflects the importance of this muscle for the behavior of ants as well as other insects.     

Motor control of the mandible closer muscle in ants

Despite their simple design, ant mandible movements cover a wide range of forces, velocities and amplitudes. The mandible is controlled by the mandible closer muscle, which is composed of two functionally distinct subpopulations of muscle fiber types: fast fibers (short sarcomeres) and slow ones (long sarcomeres). The entire muscle is controlled by 10-12 motor neurons, 4-5 of which exclusively supply fast muscle fibers. Slow muscle fibers comprise a posterior and an antero-lateral group, each of which is controlled by 1-2 motor neurons. In addition, 3-4 motor neurons control all muscle fibers together. Simultaneous recordings of muscle activity and mandible movement reveal that fast movements require rapid contractions of fast muscle fibers. Slow and subtle movements result from the activation of slow muscle fibers. Forceful movements are generated by simultaneous co-activation of all muscle fiber types. Retrograde tracing shows that most dendritic arborizations of the different sets of motor neurons share the same neuropil in the subesophageal ganglion. In addition, fast motor neurons and neurons supplying the lateral group of slow closer muscle fibers each invade specific parts of the neuropil that is not shared by the other motor neuron groups. Some bilateral overlap between the dendrites of left and right motor neurons exists, particularly in fast motor neurons. The results explain how a single muscle is able to control the different movement parameters required for the proper function of ant mandibles.     

Modulation in the feeding prey capture of the ant-lion, Myrmeleon crudelis

Ant-lions are pit-building larvae (Neuroptera: Myrmeleontidae), which possess relatively large mandibles used for catching and consuming prey. Few studies involving terrestrial arthropod larva have investigated prey capture behavior and kinematics and no study has shown modulation of strike kinematics. We examined feeding kinematics of the ant-lion, Myrmeleon crudelis, using high-speed video to investigate whether larvae modulate strike behavior based on prey location relative to the mandible. Based on seven capture events from five M. crudelis, the strike took 17.60 ± 2.92?msec and was characterized by near-simultaneous contact of both mandibles with the prey. Modulation of the angular velocity of the mandibles based on prey location was clearly demonstrated. M. crudelis larvae attempted to simultaneously contact prey with both mandibles by increasing mean angular velocity of the far mandible (65 ± 21?rad?sec(-1) ) compared with the near mandible (35 ± 14?rad?sec(-1) ). Furthermore, kinematic results showed a significant difference for mean angular velocity between the two mandibles (P<0.005). Given the lengthy strike duration compared with other fast-striking arthropods, these data suggest that there is a tradeoff between the ability to modulate strike behavior for accurate simultaneous mandible contact and the overall velocity of the strike. The ability to modulate prey capture behavior may increase dietary breadth and capture success rate in these predatory larvae by allowing responsive adjustment to small-scale variations in prey size, presentation, and escape response.     

Fast and Powerful: Biomechanics and Bite Forces of the Mandibles in the American Cockroach Periplaneta americana

Knowing the functionality and capabilities of masticatory apparatuses is essential for the ecological classification of jawed organisms. Nevertheless insects, especially with their outstanding high species number providing an overwhelming morphological diversity, are notoriously underexplored with respect to maximum bite forces and their dependency on the mandible opening angles. Aiming for a general understanding of insect biting, we examined the generalist feeding cockroach Periplaneta americana, characterized by its primitive chewing mouth parts. We measured active isometric bite forces and passive forces caused by joint resistance over the entire mandibular range with a custom-built 2D force transducer. The opening angle of the mandibles was quantified by using a video system. With respect to the effective mechanical advantage of the mandibles and the cross-section areas, we calculated the forces exerted by the mandible closer muscles and the corresponding muscle stress values. Comparisons with the scarce data available revealed close similarities of the cockroaches’ mandible closer stress values (58 N/cm2) to that of smaller specialist carnivorous ground beetles, but strikingly higher values than in larger stag beetles. In contrast to available datasets our results imply the activity of faster and slower muscle fibres, with the latter becoming active only when the animals chew on tough material which requires repetitive, hard biting. Under such circumstances the coactivity of fast and slow fibres provides a force boost which is not available during short-term activities, since long latencies prevent a specific effective employment of the slow fibres in this case.     

Sensory feedback in the control of mouthpart movements in the desert locust Schistocerca gregaria

ABSTRACT. When imposed movements were applied to one or both mandibles of the desert locust, Schistocerca gregaria , the other mouthparts moved in synchrony with the mandibles. This occurred in the presence or absence of food, and when the mandibles were driven at a higher or lower frequency than that seen during normal feeding. Electromyogram recordings from the mandibular closer muscles revealed bursts of activity at the same frequency as the imposed movement. This activity occurred during mandibular closing. Burst length was a function of driving wavelength. At low driving frequencies (less than 0.5 Hz), smaller bursts were seen prior to the longer closing burst; a series of similar small bursts was seen when the mandibles were held in the open position. When one mandible was driven, closer muscle activity was largely confined to that side. In the presence of food, however, activity was seen in both closer muscles. A possible mechanism for this is described. After destruction of the campaniform sensilla on the ventral surface of the mandibles, the bursts of activity in the mandibular closers, seen when the mandibles were held open, were replaced by continuous activity. This suggests that the function of these sensilla is to inhibit motor output to the closer muscles when the tension becomes high. When feeding on relatively incompressible food the closer muscle burst length increased, although chewing frequency did not alter. This effect was also produced by loading the mandibles artificially. A model for the feedback control of this behaviour is proposed.     

Mandible strike: the lethal weapon of Odontomachus opaciventris against small prey

In order to study both the hunting efficiency and the flexibility of their predatory behavior, solitary hunters of the trap-jaw ant Odontomachus opaciventris were offered small prey (termites, fruit flies and tenebrionid larvae), presenting different morphological or defensive characteristics. The monomorphic hunters showed a moderately flexible predatory behavior characterized by short capture sequences and a noteworthy efficiency of their mandible strike (76.7-100% of prey retrievals), even when presented with Nasutitermes soldiers. Contrary to most poneromorph ants, antennal palpation of the prey before the attack was always missing, no particular targeted region of the prey's body was preferred, and no 'prudent' posture was ever exhibited. Moreover, stinging was regularly performed on bulky, fast moving fruit flies, very scarcely with sclerotized tenebrionid larvae, but never occurred with Nasutitermes workers or soldiers despite their noxious chemical defense. These results suggest that, whatever the risk linked to potentially dangerous prey, O. opaciventris predatory strategy optimizes venom use giving top priority to the swiftness and strength of the lethal trap-jaw system used by hunters as first strike weapon to subdue rapidly a variety of small prey, ranging from 0.3 to 2 times their own body size and from 0.1 to 2 times their weight. Such risk-prone predatory behavior is likely to be related to the large size of O. opaciventris colonies where the death of a forager might be of lesser vital outcome than in small colony-size species.     

Functional design and prey capture dynamics in an ecologically generalized surfperch (Embiotocidae)

Kinematic and electromyographic analyses of prey capture in two species of surfperch (Embiotocidae) reveal differing abilities to modulate strike activity in response to different prey types. Both the black perch, Embiotoca jacksoni, and the shiner perch, Cymatogaster aggregata, demonstrate stereotyped and conserved neuromuscular and kinematic activity in suction feeding. A distinguishing anatomical trait in this family, the interopercular shelf, enhances the coupling of hyoid movement with mandibular depression. Analyses of variance suggest a preprogrammed motor output that is ballistically launched for suction generation, with the possibility of more plasticity in latter phases of the strike. While the trophically limited shiner perch displays a stereotyped repertoire of this one strike pattern, very small prey, larger conglomerates of these, and large distinct prey elicit three modulated patterns in the black perch. Functional characteristics that enable the ecologically generalized black perch to exploit a variety of prey types include energy–conserving modulatory ability, behavioural flexibility in utilizing a conserved suction–generating programme, and the addition of specialized winnowing and spitting activity.     

Reconstruction of cranial and hyobranchial muscles in the triassic temnospondyl Gerrothorax provides evidence for akinetic suction feeding

The cranial and hyobranchial muscles of the Triassic temnospondyl Gerrothorax have been reconstructed based on direct evidence (spatial limitations, ossified muscle insertion sites on skull, mandible, and hyobranchium) and on phylogenetic reasoning (with extant basal actinopterygians and caudates as bracketing taxa). The skeletal and soft‐anatomical data allow the reconstruction of the feeding strike of this bottom‐dwelling, aquatic temnospondyl. The orientation of the muscle scars on the postglenoid area of the mandible indicates that the depressor mandibulae was indeed used for lowering the mandible and not to raise the skull as supposed previously and implies that the skull including the mandible must have been lifted off the ground during prey capture. It can thus be assumed that Gerrothorax raised the head toward the prey with the jaws still closed. Analogous to the bracketing taxa, subsequent mouth opening was caused by action of the strong epaxial muscles (further elevation of the head) and the depressor mandibulae and rectus cervicis (lowering of the mandible). During mouth opening, the action of the rectus cervicis muscle also rotated the hyobranchial apparatus ventrally and caudally, thus expanding the buccal cavity and causing the inflow of water with the prey through the mouth opening. The strongly developed depressor mandibulae and rectus cervicis, and the well ossified, large quadrate‐articular joint suggest that this action occurred rapidly and that powerful suction was generated. Also, the jaw adductors were well developed and enabled a rapid mouth closure. In contrast to extant caudate larvae and most extant actinopterygians (teleosts), no cranial kinesis was possible in the Gerrothorax skull, and therefore suction feeding was not as elaborate as in these extant forms. This reconstruction may guide future studies of feeding in extinct aquatic tetrapods with ossified hyobranchial apparatus. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Mandible allometry in extant and fossil Balaenopteridae (Cetacea: Mammalia): the largest vertebrate skeletal element and its role in rorqual lunge feeding

Rorqual whales (crown Balaenopteridae) are unique among aquatic vertebrates in their ability to lunge feed. During a single lunge, rorquals rapidly engulf a large volume of prey‐laden water at high speed, which they then filter to capture suspended prey. Engulfment biomechanics are mostly governed by the coordinated opening and closing of the mandibles at large gape angles, which differentially exposes the floor of the oral cavity to oncoming flow. The mouth area in rorquals is delimited by unfused bony mandibles that form kinetic linkages to each other and with the skull. The relative scale and morphology of these skeletal elements have profound consequences for the energetic efficiency of foraging in these gigantic predators. Here, we performed a morphometric study of rorqual mandibles using a data set derived from a survey of museum specimens. Across adult specimens of extant balaenopterids, mandibles range in size from ～1–6 m in length, and at their upper limit they represent the single largest osteological element of any vertebrate, living or extinct. Our analyses determined that rorqual mandibles exhibit positive allometry, whereby the relative size of these mandibles becomes greater with increasing body size. These robust scaling relationships allowed us to predict mandible length for fragmentary remains (e.g. incomplete and/or fossil specimens), as we demonstrated for two partial mandibles from the latest Miocene of California, USA, and for mandibles from previously described fossil balaenopterids. Furthermore, we showed the allometry of mandible length to body size in extant mysticetes, which hints at fundamental developmental constraints in mysticetes despite their ecomorphological differences in feeding styles. Lastly, we outlined how our findings can be used to test hypotheses about the antiquity and evolution of lunge feeding. © 2012 The Linnean Society of London     

A test of adaptive hypotheses: Mandibular traits,nest construction materials,and feeding habits in neotropical social wasps (Vespidae,Polistinae)

Summary. The success of many behaviors in hymenoptera depends on the shape and structure of their mandibles. Neotropical social wasps exhibit variation in the shape of their mandibles; both the type of material used in the nest construction and the food sources have been proposed as selective forces that explain that variation. These hypotheses were studied using Independent Contrast analyses and combined tests of significance between: nine mandibles traits, the type of nest material and food source types. Necrophagy and short fiber use are derived conditions in the subfamily that have evolved five times each, while the use of long fibers and live prey are primitive conditions. The mandible structures appear related to the nest fiber type but not to necrophagy. Particularly, species that use long fibers have bigger internal dorsal tooth, longer internal ventral tooth, and shorter and more curved mandibles. Similar results were obtained by including plant hairs as a third nest material type. These findings open related questions for groups of social insects where studies on evolution of mandibles have emphasized food sources.Received 23 November 2003; revised 9 March 2004; accepted 21 April 2004.     

Interhabitat and instream movements of large Atlantic salmon parr in a Newfoundland watershed in winter

Radio‐telemetry was used to investigate movement of large, mainly mature male (80%) Atlantic salmon Salmo salar parr in Stoney River, Newfoundland during early winter (November; water temperature 6·0 ± 0·1° C) and mid‐winter (January to February; 0·8 ± 0·0° C). Site fidelity of parr in early winter was low. Parr moved between fluvial and lacustrine habitats and were active throughout the diel cycle. Parr caught in fluvial habitats in mid‐winter were smaller and younger than parr caught in early winter. Site fidelity of parr in mid‐winter was greater than in early winter. Parr in mid‐winter moved between fluvial and adjacent small lacustrine habitats, but avoided a larger pond inhabited by large piscivorous fishes. Instream movement rates in mid‐winter were lower than in early winter and occurred primarily during hours of darkness (dawn, dusk and night). Fluvial habitats were relatively stable and ice‐free throughout the study periods. These results suggested that large Atlantic salmon parr utilize a variety of habitats and remain active throughout the winter, even under stable environmental conditions.     

A cineradiographic and electromyographic study of mastication in Tenrec ecaudatus

Regular chewing was studied in the specialized Malagasy insectivore Tenrec ecaudatus with the aid of precisely correlated electromyography of the main adductors, digastrics, and two hyoid muscles and cineradiography for which metallic markers were placed in the mandibles, tongue, and hyoid bone. During the power stroke the body of the mandible moves dorsally and medially. The medially directed component of movement at this time is greatly increased by simultaneous rotation of the mandible about its longitudinal axis. The highly mobile symphysis, spherical dentary condyle, loss of superficial masseter muscle and zygoma, and the simplified zalamnodont molars all appear to be related to the large amount of mandibular rotation that occurs during occlusion. The balancing side lateral pterygoid muscle (inferior head) apparently shifts the working side mandible laterally during the last part of opening and the first part of closing. The working side temporalis and the superficial masseter muscle are both responsible for the shift back to the midline. The temporalis is usually active to the same extent on the working and balancing sides during the power stroke. The level of activity (amplitude) of the temporalis and duration of the power stroke increase with harder foods. Whenever soft foods are chewed, the superficial masseter is only active on the working side; whenever foods of increasing hardness are chewed, its level of activity on the balancing side increases to approach that of the working side. Mandibular rotation is greatly reduced when hard foods are chewed.     

Electrofishing and salmonid movement: reciprocal effects in two small montane streams

The effects of electrofishing on salmonid movement and of salmonid movement on electrofishing‐derived abundance estimates were studied in two streams in western Montana, U.S.A. Electrofishing increased emigration of salmonids from study reaches for 1 day, but not for succeeding days, whereas immigration to study reaches was unaffected. Movement of most emigrating fishes was downstream. On these small streams, electrofishing did not appear to cause fishes to flee during sampling. Numbers of salmonids migrating between mark and recapture runs were small relative to the fish abundance estimates in study reaches, usually much less than the 95% CL for those estimates, thus disregarding movements of marked fishes from the study reaches would have produced small positive biases in abundance estimates. Overall, for this suite of salmonid species in mid‐summer in these streams, the effects of electrofishing on fish movement and of fish movement on abundance estimates were minor.     

The limits of elaboration: curved allometries reveal the constraints on mandible size in stag beetles

Many studies have demonstrated the adaptive advantage of elaborate secondary sexual traits, but few if any have shown compelling evidence for the limits to the elaboration of these traits that must exist. We describe such evidence in the exaggerated mandibles of stag beetles. In 1932, Huxley showed that the slope of the allometric relationship between mandible length and body size in some stag beetles declines in the largest males. We show that this curvature is most pronounced in species with relatively long mandibles, consistent with the hypothesis that the decrease in slope is caused by the increasing costs of large mandibles, which ultimately limit their size. Increasing depletion of resources in the prepupa and pupa by the rapidly growing mandibles is the most likely way in which these costs are manifested. The curved allometries have two components: intraspecific mandible allometry is steepest among small males of the species with the longest mandibles, but shallowest among the largest males of those same species. These patterns suggest that selection continues to favour positive allometry in species that invest relatively more in weaponry despite the limits to mandible exaggeration being reached in the largest males.     

Determination of the diet of the stone curlew (Bwhinus oedicnemus) by faecal analysis

The value of faecal analysis for estimating the composition of the diet of stone curlews was assessed by examination of the faeces of a captive bird fed on a measured diet. Remains of soft–bodied prey were under–represented in the faeces but the results could be adjusted to allow for this. Estimation of the size of prey was possible by measurement of remnants such as earthworm chaetae and insect mandibles. In some types of prey large specimens left more remnants than small ones and a correction was devised to allow for this. Regurgitated pellets contained large, hard remains and there was no trace of some important prey types such as earthworms. A method is described for estimating the composition of the diet of the wild stone curlews from counts of prey remains in their faeces.     

Landscape structure influences the use of social information in an insectivorous bat

In anthropogenic landscapes, aerial insectivores are often confronted with variable habitat complexity, which may influence the distribution of prey. Yet, high mobility may allow aerial insectivores to adjust their foraging strategy to different prey distributions. We investigated whether aerial-hunting common noctules Nyctalus noctula adjust their foraging strategy to landscapes with different habitat complexity and assumingly different prey distribution. We hypothesized that the movement behaviour of hunting common noctules and changes of movement behaviour in reaction towards conspecifics would depend on whether they hunt in a structurally poor cropland dominated landscape or a structurally rich forest dominated landscape. We tracked flight paths of common noctules in northeastern Germany using GPS loggers equipped with an ultrasonic microphone that recorded foraging events and presence of conspecifics. Above cropland, common noctules hunted mainly during bouts of highly tortuous and area restricted movements (ARM). Bats switched from straight flight to ARM after encountering conspecifics. In the forested landscape, common noctules hunted both during ARM and during straight flights. The onset of ARM did not correlate with the presence of conspecifics. Common noctules showed a lower feeding rate and encountered more conspecifics above the forested than above the cropland dominated landscape. We conjecture that prey distribution above cropland was patchy and unpredictable, thus making eavesdropping on hunting conspecifics crucial for bats during search for prey patches. In contrast, small scale structural diversity of the forested landscape possibly led to a more homogeneous prey distribution at the landscape scale, thus enabling bats to find sufficient food independent of conspecific presence. This suggests that predators depending on ephemeral prey can increase their foraging success in structurally poor landscapes by using social information provided by conspecifics. Hence, a minimum population density might be obligatory to enable successful foraging in simplified landscapes.