Mandible Movements in Ants ଝ
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Comparative Biochemistry and Physiology Part A 131Ž. 2001 7᎐20 Review Mandible movements in ants ଝ Jurgen¨ PaulU Uni¨ersitat¨¨ Wurzburg, Theodor-Bo¨eri-Institut() Biozentrum , Lehrstuhl fur¨ Verhaltensphysiologie und Soziobiologie, Am Hubland, D-97074 Wurzburg,¨ Germany Received 13 January 2001; received in revised form 30 March 2001; accepted 3 April 2001 Abstract 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 sarcomeresŽ. 2᎐3 m and attach directly to the closer apodeme, that conveys the muscle power to the mandible joint. Slow but forceful contracting fibers have long sarcomeresŽ. 5᎐6 m 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. ᮊ 2001 Elsevier Science Inc. All rights reserved. Keywords: Adaptation; Biomechanics; Force; Insects; Morphology; Motor control; Muscle fiber types; Trap-jaw mechanisms; Velocity 1. Introduction brood care, carrying nestmates, transporting liq- uids and communicationŽ Holldobler¨ and Wilson, For the majority of insects, the mouthparts are 1990. Accordingly, ant mandibles have to per- the most important tools for almost any task. This form many different kinds of movements in terms is particularly true for the mandibles of ants. Ants of velocity, force output and precision. While employ their mandibles for fast or powerful ac- some tasks are common among ant speciesŽ e.g. tions like prey-catching, fighting, digging, leaf-cut- brood care. , others represent specific adaptations. ting, and also for delicate tasks such as grooming, Predators often have long jaws equipped with piercing teeth and sharp edges, whereas herbivo- rous ants have more compact mandibles suited ଝ This paper was originally presented as part of the ESCPB for the special task of processing plant material Congress symposium ‘Learning about the Comparative Ž.Gronenberg et al., 1997 . In many ant species, Biomechanics of Locomotion and Feeding’, Liege` July 26᎐27, 2000. however, the mandibles resemble a general type U Tel.: q49-931-888-4303; fax: q49-931-888-4309. found in many other insect groups: they are sturdy, E-mail address: [email protected]Ž J. shovel-like, non-segmented limbs. But mandible Paul. specialization is not only based on shape but also 1095-6433r01r$ - see front matter ᮊ 2001 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 5 - 6 4 3 3Ž. 0 1 00458-5 8 J. Paul rComparati¨e Biochemistry and Physiology Part A 131() 2001 7᎐20 depends on the speed of movement and on the closer muscle is much larger than the opener force the jaws can generate. Catching elusive prey muscle. In large species or in large individuals of obviously requires different movement character- polymorphic speciesŽ Holldobler¨ and Wilson, istics and tactics than cracking seeds. 1990. , the mandible closer occupies up to two- Force and velocity of a limb movement depend thirds of the entire head capsule volumeŽ. Fig. 1a . on the muscles and the accessory structures that The proportion of the mandible closer muscle control the particular limb. In ants, the mandible volume in relation to the head capsule volume design is simple. It conforms to the common decreases with decreasing size of the antŽ. Fig. 1a . mandible organization of other hymenopterans In small species or small individuals, the mandible Ž.Snodgrass, 1935, 1956 : the mandibles are con- closer muscle only fills approximately 25% of the nected to the head capsule by a hinge joint, head capsuleŽ. Fig. 1a . The reason for this allo- movable only in a single planeŽ inwardsrout- metric correlation is that other organs and struc- wards. , operated by only a single closer and tures within the head take up relatively more opener muscle on each side of the head. Even space when the head capsule volume decreases ᎐ though opener closer muscle co-contraction may Že.g. antennal, labial, and maxillary muscles; Fig. occur, the mandible closer muscle is much larger 1b; Paul and Roces, 1999. Most notably, the and the key to the versatility of mandible func- brain is relatively larger in small antsŽ Jaffe and Ž. tions Gronenberg et al., 1998a . All the fast, Perez, 1989. However, the mandible closer is the forceful, or delicate mandible movements are largest muscle in any ant worker, even in very generated by the mandible closer muscle. small species or individuals. Because of its relative simplicity and its great In almost all ants, the mandible closer muscle behavioral relevance, this movement system is is composed of two morphologically distinct types very well suited for studying adaptive muscle mor- of muscle fibersŽ Gronenberg et al., 1997; Paul phology, biomechanics, and motor control. This and Gronenberg, 1999. : fibers with short sar- review gives an overview of the diversity of ant comeresŽ. sarcomere length 2᎐3 m and fibers mandible movements and the underlying mecha- with long sarcomeresŽ. 5᎐6 m . As a general nisms considering an evolutionary context by rule, in long sarcomeres, more myosin᎐actin comparing species adapted to different lifestyles. cross-bridges act in parallelŽ Huxley, 1974; Tregear and Marston, 1979; Cooke, 1997. There- 2. Muscle fiber types and general morphology of fore, fibers with long sarcomeres generate larger the mandible closer muscle forces. In muscle fibers with short sarcomeres many units simultaneously shorten in series, re- In ants, as in most other animals, the mandible sulting in a high contraction velocityŽ Jahromi Fig. 1. Allometric correlations between mouthpart muscle and head capsule volumes in ants. Data points represent single individuals of various ant species, respectively Ž Atta sexdens, Camponotus rufipes, ns4; Diacamma sp., Ectatomma ruidum, Harpegnathos saltator, Leptothorax sordidulus, ns3; Pachycondyla ¨illosa, Myrmecia sp., ns2.Ž. a The relative volume of the mandible closer muscle increases with increasing head capsule volume Ž.rs0.76315; P-0.0001 .Ž b. The relative volumes of the labial adductor, abductor, maxillary adductor, and abductor decrease with increasing head capsule volume Ž.rsy0.75849; P-0.0001 . J. Paul rComparati¨e Biochemistry and Physiology Part A 131() 2001 7᎐20 9 and Atwood, 1969, 1971; Lang et al., 1977. This 1999. The main body of the apodeme is a mas- correlation between sarcomere length and con- sive sclerotized structure, which funnels the forces tractile properties of a muscle fiber has been of all closer muscle fibers into the mandible. The shown in many different studiesŽ O’Connor et al., apodeme base gives rise to apodeme collaterals. 1982; Stephens et al., 1984; Gunzel¨ et al., 1993; Typically, three branches project from the Taylor, 2000. Hence, muscle fibers with short apodeme base posteriorly into the closer muscle: sarcomeres are fast contracting fibers, whereas a central principal branch and two accessory long sarcomeres indicate slow but forceful muscle branches, a median and a lateral one. The most fibers. Ultrastructural observations and consider- significant alteration of the basic design is the ations support this classification of muscle fiber introduction of apodeme filaments. Bundles of types in antsŽ proportion and density of myofila- such filaments, each of which connects exclusively ments, mitochondria, sarcoplasmatic reticulum, to a single muscle fiber, may replace the acces- and thickness of z-discs; van Leeuwen, 1991; sory branches entirely although the basic organi- Gronenberg et al., 1997. However, absolute val- zation can still be discerned. ues of sarcomere lengths and other structural The muscle fiber types of the ant mandible properties do not always accurately predict physi- closerŽ fast directly attached, slow directly and ological performance of muscle fibers in filament-attached fibers. are arranged in bundles arthropodsŽ Costello and Govind, 1983; Silverman of like fibersŽ Gronenberg et al., 1997; Paul and et al., 1987; Gunzel¨ et al., 1993. A causal rela- Gronenberg, 1999. In all ants studied, the tionship between the characteristics of the mandible closer muscle is thus composed of sub- mandible movement and the electrical activity of units that each comprises only a single muscle particular muscle fiber types has been established fiber type and occupies characteristic positions Ž.Paul and Gronenberg, submitted . In conclusion, within the head capsuleŽ. Fig. 2 . While the rela- the mandible closer muscle of ants is composed tive and absolute size of each muscle fiber group of two different sets of fibers: slow but forceful differs across species and in some cases between muscle fibersŽ. sarcomere length 5᎐6 m and individuals of different body size, the relative probably less forceful but fast onesŽ sarcomere position of the different muscle fiber bundles is length 2᎐3 m.. very similar in different speciesŽ. Fig. 2 . These In arthropods, muscle fibers attach to the ex- typical positions of the muscle fiber types possess oskeletonŽ. e.g. the thorax or head capsule di- functional significanceŽ see below; Paul and Gro- rectly via a deeply serrated area of adhesion nenberg, 1999. between the muscle fiber and the cuticleŽ Neville, In contrast to the mandible closer of ants, 1975a,b.