Morphological and Functional Diversity of Ant Mandibles

This article was originally prepared by Chris A. Schmidt for the Tree of Life Web Project. Additional information that has been added is denoted by the text being preceded by a citation.

Introduction
Mandibles ("jaws") are a crucial tool for many insects, but perhaps in no insect group are they more highly utilized than in the ants (Formicidae). Ants use their mandibles for a diverse array of activities, and are thus constrained by the need to have mandibles which can fulfill a number of functions. Despite these constraints, ants have evolved a spectacular diversity of mandible shapes. This page describes and illustrates just a small sampling of this diversity. It begins with a description of the basic roles that mandibles play in the daily lives of ants. It then goes on to describe the basic morphology of an ant mandible and to show a few examples of both typical and somewhat unusual mandibles. The remaining sections (not yet developed) will describe further variations on the basic pattern, including mandibles specialized for prey capture, mandibular variation within a colony (allometric growth and caste systems, for example in the army ants), and mandibles specialized for warfare.

Manipulation of objects
Like most insects, ants lack grasping forelegs (such as those found in the Mantodea and Mantispidae) and compensate for this by using their mandibles as "hands." Ants use their mandibles to manipulate all sorts of objects, such as food particles of varying sizes (from very small to many times larger and heavier than the ant itself) and even liquids (e.g. water or honeydew suspended as a drop between the mandibles). Like other social insects, ants construct often elaborate nests, using their mandibles to dig into dirt or wood, and then again to carry the debris away. In contrast with most other social insects, however, ants have a system of cooperative brood care in which eggs and larvae are directly handled by attending workers. Attendants ("nurses") frequently move the brood to other nest chambers, for example in response to changes in humidity, damage to the nest, the presence of pathogens, or continued development of the brood. (Termites lack a larval stage, while the brood of most social wasps and bees develop in nest cells and are less frequently handled or moved than in ants.) Another fascinating use of mandibles in some ants is social carrying, in which one worker will physically carry another worker in its mandibles to aid in recruitment to a food source or new nest site.

Food processing
In addition to being used to transport food items, mandibles are also used to process the food. Carnivorous ants often use their mandibles to decapitate or dismember their prey, to facilitate feeding or storage. They also use their mandibles to tear, puncture, or grind their food.

Hunting and defense
Mandibles are also crucial to the hunting success of predatory ants. Mandibles can be wielded as formidable weapons in their own right, or as tools with which to grasp prey until a paralyzing sting can be delivered (a common strategy in the Ponerinae, most of which are solitary predators). Mass foraging predators (e.g. army ants, described below) use their mandibles to pin down prey from all sides while their nestmates dispatch it. A number of highly modified mandibles have evolved in response to the requirements of catching certain prey, especially those that are otherwise difficult to catch (e.g. collembolans). See the section on specialized predators below for several examples of such modifications.

Despite a common misconception, most ants lack painful bites (being too small to have any effect on human skin). Usually ant "bites" are actually the venomous stings of ants in certain subfamilies (most commonly the Myrmicinae, but also members of the Ponerinae, Myrmeciinae, Pseudomyrmecinae, and others, and perhaps most notoriously the bullet ant, Paraponera clavata). Some ants, however, can indeed inflict a painful bite on humans; among these are the African driver ants of the subfamily Dorylinae, which in great numbers are capable of killing large mammals solely through the action of their mandibles (Hölldobler and Wilson, 1990). Perhaps more important generally is the role of mandibles in defense against smaller predators and competitors, such as other ants. Many ants have a major worker caste ("soldiers") with large body size and massive mandibles (e.g. Eciton and Pheidole, described below). Such major workers can be truly formidable adversaries to their opponents. Some ants have evolved mandibles specialized for offense against other ants, including Polyergus, a genus of slave-making ants which uses its sickle-like mandibles to maim or kill Formica workers defending their brood (see below).

Ant Mouthparts
The basic mouthparts of insects include (from anterior to posterior) the labrum (upper lip), paired mandibles, paired maxillae, and the labium (lower lip) (Chapman, 1998). Both the maxillae and labium have sensory palps; the number of palp articles ("segments") are important characters in the identification of ant genera. The primitive condition in ants is believed to be 6-segmented maxillary palps and 4-segmented labial palps (written "6, 4"), but this number has frequently become reduced during the evolution of various ant lineages (Bolton, 2003). In addition, in some ants (e.g. Myrmecocystus) certain palp articles have become greatly elongated.

Typical Ant Mandibles
Like all pterygote insects, ant mandibles have two points of articulation with the head (such mandibles are termed "dicondylic") and are thus constrained to move transversely (Triplehorn and Johnson, 2005). A typical ant mandible is illustrated in Fig. 1. It is characterized by an outer, external margin (Fig. 1a) and an internal margin, which is further divided by the basal angle (Fig. 1d) into a basal margin (Fig. 1c) and a masticatory margin (Fig. 1b). From the masticatory margin arise a variable number of teeth and denticles (Fig. 1e).

Figure 1. Mandible of Pachycondyla havilandi (Ponerinae; South Africa), illustrating the basic external morphology of an ant mandible (points of articulation with the head not shown). a: external margin; b-e: parts of the internal margin: b: masticatory margin; c: basal margin; d: basal angle; e: teeth. Note the long transverse groove extending much of the length of the mandible; similar grooves and pits occur on the mandibles of many ants. Note also the row of setae along the masticatory border, another common feature of ant mandibles.

Ants primitively had short, curved mandibles with two teeth (apical and pre-apical) (Bolton, 2003). While many modern ants have basically this same mandibular morphology (although usually with additional teeth), a more typical groundplan is for the mandible to have an elongated masticatory margin and a prominent basal angle, giving the mandible a distinctive triangular shape. This type of mandible is illustrated in Figures 2-4, which show frontal views of three ants from distantly-related subfamilies.

Figure 2. Frontal view (left) and enlarged view of mandible (right) of Pachycondyla havilandi (Ponerinae; South Africa), showing the characteristic triangular mandibular morphology common to many ants.

Figure 3. Frontal view (left) and enlarged view of mandible (right) of a minor worker of Pheidole rhea (Myrmicinae; Arizona, USA), again showing the characteristic triangular mandibular morphology. The major worker of this species is illustrated below in the section on polyphenisms.

Figure 4. Frontal view (left) and enlarged view of mandible (right) of a media worker of Eciton sp. (Ecitoninae; Costa Rica), a Neotropical army ant. The major worker of this species has highly modified mandibles and is illustrated below in the section on polyphenisms.

Basic Mandible Variation
Two variations on this basic pattern are illustrated in Figures 5 and 6. Ectatomma tuberculatum (Fig. 5) has especially large mandibles, in which the masticatory margin has become greatly lengthened, and is lacking noticeable teeth except for at the apices. In contrast, the Amblyoponinae (illustrated here by Stigmatomma pallipes, Fig. 6) have long, straight mandibles lacking distinct basal and masticatory margins. In at least some species (including Stigmatomma pallipes), certain teeth are pronged, with two points. Additional variations in mandibular morphology are described in the following sections.

Figure 5. An example of variation on the basic mandibular form, Ectatomma tuberculatum (Ectatomminae; Costa Rica). Its masticatory margins are greatly lengthened and nearly toothless.

Figure 6. Another example of mandibular variation, Stigmatomma pallipes (Amblyoponinae; North Carolina, USA), whose mandibles lack a distinct basal angle and whose numerous teeth have an unusual forked appearance. Note also the row of clypeal teeth between the mandibles, a synapomorphy of this subfamily.

Morphology and Orientation
Lattke et al. (2018) - The mandibular morphology of the Protalaridris armata group contrasts with that of most other ant genera due to its upturned dorsal margin when seen laterally. In Hymenoptera the mandibular shape is typically crescent-shaped in lateral view and triangular in dorsal view. Ant mandibles, as in most insects, are dicondylate and this constrains mandibular movement along a transverse (laterally) oriented plane (Staniczek, 2000; Blanke et al., 2014). The abduction and adduction are produced by abductor and adductor muscles originating on the dorsal and lateral internal surface of the head capsule (Snodgrass, 1935; Grimaldi & Engels, 2005). Given the overwhelming dominance of the triangular – subtriangular mandible variants, it can be assumed this is a plesiomorphic and conserved general shape and an inversion of the mandibular apex from downturned to upturned should be rare. Deviations from this are the specialized linear mandibles of genera such as Acanthognathus; Anochetus; Daceton; Mystrium; Myrmoteras; Odontomachus, and Strumigenys, which are straight when seen laterally (Larabee & Suarez, 2014). Even rarer are the instances of “up-turned” (and always more or less elongated) mandibles.

Ants in the ponerine genus Harpegnathos have elongate upturned mandibles convergently shaped with those of Protalaridris. Both genera also share the presence of a large crescent-shaped basal ventral tooth with a convex anterior margin in lateral view. The monotypic genus Talaridris has an elongate scooped-shaped mandible but with a distinct ventral denticle that has a concave posterior margin when seen laterally. Besides these extant groups the extinct sphecomyrmicine genera Ceratomyrmex and Haidomyrmex also bear elongate mandibles with an upturned apical part and ventral tooth at the base (Perrichot et al., 2016). Long-mandibulate Strumigenys of the gundlachi group have relatively slender, tapering mandibles that in profile may be linear to weakly concave (Bolton, 2000: 176). Their mandibles differ from the aforementioned genera in lacking a basal ventral tooth and the dorsal concavity, when present, is feeble at best. The masticatory margin of triangular mandibles generally bear variously shaped teeth that lie in the same plane as the dorsal mandibular surface. This configuration is different in the ascrobicula group of Octostruma (see Longino, 2013a) and Protalaridris leponcei. Their mandibles are triangular but the masticatory margin bears a series of relatively large, irregularly sized teeth that protrude dorsomedially, clearly visible in lateral view. One of the preapical teeth of Protalaridris leponcei is particularly large compared with the others (Fig. 6a), and further enlargement may lead to the situation found in the remaining species of the genus. Such enlargement may be exemplified by an undescribed species Rhopalothrix UFV sp. 1 imaged in Antweb (2017; specimen UFV-LABECOL-000326). In the latter, the mandible bears a very large preapical tooth that rivals the mandibular shaft in size. If the mandibles in Protalaridris leponcei represent the plesiomorphic state within the genus, further enlargement of a dorsomedially projecting tooth might have proved advantageous for certain tasks, such as prey securement (Ohkawara et al., 2016). A tooth or denticle projecting from the basal mandibular angle is known in some species of Neivamyrmex (Borgmeier, 1955). Thus, the “upturned” part of the mandibles in the armata group could be derived from a preapical mandibular projection. That possibility is supported by the presence of a large incurved ventral tooth close to the mandibular base of in all these ants; this tooth may actually represent the original apical part of the mandible. Additionally, in the long mandible, only the part distal to the ventral tooth is distinctly upturned in Protalaridris, Talaridris, and Harpegnathos. The trap-jaw mandible in the genus Acanthognathus bears a slender and curved basal tooth or process (Gronenberg et al., 1998) that is anteriorly convex and with apical denticles, suggesting the possibility it may be the original mandible, but the morphology is much different than of the previously mentioned genera.

Our interpretation may also be useful for addressing enigmatic mandibular morphology in non-extant ants. What Barden & Grimaldi (2012: 8) interpret as the apical tooth of Haidomyrmex scimitarus may actually represent a hypertrophied preapical tooth whilst the apex of the so-called ventrobasal mandibular tooth (the posteriormost member of the basal teeth) is most probably the original apical mandibular tooth. Likewise, what is labelled as the basal tooth in Ceratomyrmex ellenbergeri (Fig. 1C in Perrichot et al., 2016) would be the principal mandibular shaft and the apical portion of the mandible would be a hypertrophied preapical tooth or projection. As in extant taxa, the upturned part of the mandibles in these early ants begins close to the “basal mandibular tooth”. Fig. 11 depicts our idea of what is the main mandibular shaft and what is the extension of the preapical dentition or margin.

The mandibles of Haidomyrmex and Ceratomyrmex were interpreted as being unlike anything present in modern ants (Barden & Grimaldi, 2016; Perrichot et al., 2016; Barden 2017) and even implying a vertical movement (Perrichot et al., 2016). In our interpretation, the mandibles of Haidomyrmecini possess analogues in extant genera and it is not necessary to postulate vertical mandibular movement which would imply a 90 degree twist of the mandibular condyles and associated radical structural modifications of the head capsule, mandibular apodemes, and muscles. Haidomyrmecine and Talaridris mandibles correspond to the planar type (sensu Keller, 2011), with the external surface facing laterally and the external margin facing ventrally, whilst mandibles in Protalaridris and Harpegnathos are torqued, with their external surface facing dorsally and the external margin facing laterally (Keller, 2011). What still makes haidomyrmecine mandibles remarkable is the length and the angle at which the dorsal tooth projects, almost perpendicular to the longitudinal axis of the body, something unseen in extant taxa. Hopefully, detailed phylogenies and careful comparative studies of closely related taxa with different mandibular morphology will help elucidate the developmental pathways of such transformations.

Trap-Jaws: Structure and Mechanisms
Gibson et al. (2018) - In ants, power-amplified trap-jaw mandibles have evolved independently at least four times. There is a single occurence in the subfamily Ponerinae, as expresssed in the sister genera Odontomachus and Anochetus.

The suite of structures involved and some details of the morphological structures and mechanics of trap-jaw ants differ from group to group, but in general they possess elongated mandibles locked open with a latch mechanism. This allows elastic strain energy to be stored within the head capsule as enlarged mandible closer (adductor) muscles contract. When inter-mandibular mechanosensory trigger hairs are stimulated, the latch is released by the contraction of fast-twitch muscles, allowing the mandibles to close extremely rapidly (Patek et al., 2006; Spagna et al., 2008; Larabee, Gronenberg & Suarez, 2017).

Most research on the functional morphology and strike kinematics of trap-jaw ants has focused on the genus Odontomachus. In this genus, the mandibles are held open by a latch formed through interactions between the basal condyle of the mandibles and the mandible sockets (Gronenberg et al., 1993). Elastic energy for the mandible strike is likely stored, in part, within enlarged mandibular apodemes, although the exact location of energy storage remains unknown (Gronenberg et al., 1993). Strikes are stimulated by contact with trigger hairs on the mandibles that connect to ‘giant’ sensory neurons (Gronenberg & Tautz, 1994). During a strike, Odontomachus mandibles reach peak maximum velocities between 35 and 67 m s-1, accelerate tens to hundreds of thousands times faster than gravity, and generate forces over 300 times the mass of an individual ant (Patek et al., 2006; Spagna et al., 2008). Due to the high force-to-body mass ratio of these mechanisms, some Odontomachus species use their mandibles to repel small intruders out of their nests (Carlin & Gladstein, 1989) and to perform horizontal or vertical jumps, which can increase survivorship during encounters with predators such as antlions (Patek et al., 2006; Spagna et al., 2009; Larabee & Suarez, 2015).

Odontomachus species typically rely on the crushing force of their mandibles alone for prey capture (Brown, 1976, 1978; De la Mora, Perez-Lachaud & Lachaud, 2008). Performance of mandible strikes is correlated with body size in Odontomachus (Spagna et al., 2008), with smaller species generally producing faster but less forceful strikes.

In Odontomachus, mandible strikes have been relatively well described and can occur in <0.15 ms and reach speeds of over 60 m s-1. Performance of mandible strikes is correlated with body size in Odontomachus (Spagna et al., 2008). Smaller species generally produce faster but less forceful strikes. Anochetus species, smaller and morphologically distinct from Odontomachus, offer an interesting opportunity to compare trap-jaw kinematics across a greater range of morphological variation.

Relative to Odontomachus, ants in the sister genus Anochetus are generally smaller, have a distinct head morphology, and frequently ambush and sting their prey when hunting. Two Anochetus species, Anochetus targionii and Anochetus paripungens, have mandible strikes that overall closely outperform but closely resemble those found in Odontomachus ruginodis, reaching a mean maximum rotational velocity and acceleration of around 3.7 x 104 rad s-1 and 8.5 x 108 rad s-2, respectively. This performance is consistent with predictions based on body size scaling relationships described for Odontomachus. Anochetus horridus and Anochetus emarginatus have slower strikes relative to the other species of Anochetus and Odontomachus, reaching mean maximum rotational velocity and acceleration of around 1.3 x 104 rad s-1 and 2 x 108 rad s2, respectively. This variation in strike performance among species of Anochetus likely reflects differences in evolutionary history, physiology, and natural history among species. Overall, the studied species followed a pattern of increasingly energetic strikes with larger body mass.

Taxonomic Considerations
Lattke et al. (2018) - There is a long history of ant genera established because of variances in mandibular morphology, with further studies forcing a taxonomic weeding out of excess names. Differences in mandibular morphology and antennal segmentation have traditionally been important in separating genera within the Basiceros and Strumigenys groups, but recent work has gathered convincing evidence to the contrary, especially in the latter genus.