JOURNAL OF MORPHOLOGY 171:321-353 (1982)

Mastication in the Tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia): Structure and Activity of the Motor System

G. C. GORNIAK, H. I. ROSENBERG, AND CARL GANS Division of Biological Sciences, The university of Michigan, Ann Arbor, Michigan 48109

ABSTRACT The masticatory pattern of Sphenodon punctatus, the sole re- maining rhynchocephalian, now restricted to islands off the coast of New Zealand, has been analyzed by detailed anatomy, cinematography, cinefluoroscopy, and electromyography. Food reduction consists of a closing, crushing bite followed by a propalineal sliding of the dentary row between the maxillary and palatine ones. The large, fleshy tongue can be protruded to pick up small prey, and also plays a major role in prey manipulation. The rotational closing movement of the j aw, sup- porting the basic crushing movement, is induced by the main adductor musculature. It is followed by a propalineal anterior displacement relying heavily on the action of the M. pterygoideus. The fiber lengths of the several muscles reflect the extent of shortening. The most obvious modification appears in the M. pterygoideus, which contains a central slip of pinnately arranged short fibers that act at a period different from that of the rest of the muscle; their action increases the power during the terminal portion of the propalineal phase. This also allows the animal to use its short teeth in an effective shearing bite that cuts fragments off large prey. The action of single cusped dentary teeth acting between the maxillary and palatine tooth rows provides a translational crushing-cutting action that may be an analog of the mammalian molar pattern. However, this strictly fore-aft slide does not incorporate capacity for later development of lateral movement.

As the sole Recent representative of the a base line for comparisons among order Rhynchocephalia, the tuatara Spheno- lepidosaurians. don punctatus has been the subject of a dis- Lepidosaurians feed in various ways and proportionately large number of anatomic their varied feeding behaviors are reflected in studies (see Dawbin, '62; Robb, '73). The skull the structures they use. Snakes swallow their of Sphenodon differs from that of other lepi- prey whole by means of alternating, unilateral dosaurians in being fully diapsid. A quadrato- movements of their highly kinetic skulls (Cun- jugal bone, a squamosal-jugal brace, and a dall and Gans, '79; Gans, '61).Amphisbaenians fixed quadrate are retained, although there is bite into their prey, ripping pieces loose by ro- some question about the degree of cranial tation of the body (Gans, '74). Herbivorous kinesis (Versluys, '12; Kuhn-Schnyder, '54; lizards crop vegetation, then swallow it with Ostrom, '62; Iordansky, '66; Rieppel, '78). Both minimal reduction (Throckmorton, '76). Car- the dentitional pattern (Robinson, '76) and the nivorous lizards chew small food items cephalic musculature (Haas, '73; Poglayen- (Frazzetta, '62)or utilize inertial feeding to bolt Neuwall, '53) show further differences. Earlier down large prey (Gans, '61). Neither the occur- investigations, both descriptive and func- rence nor the absence of cranial kinesis cor- tional, relied on preserved material. More re- relates clearly with particular feeding cently, field investigations (Crook, '75; Gans, strategies. '82) and laboratory studies of living specimens The skull of Sphenodon differs from those of (e.g., Hill and Dawbin, '69; McDonald and Recent lizards because it has two fixed and Heath, '71; Gans and Wever, '76, Ireland and parallel rows of teeth on each side of the upper Gans, '77) have begun to increase our under- standing of the physiology and behavior of the Work carried out while H.I. Rosenberg was Visiting Associate Pro- tuatara (Robb, '77). The present report of the fessor at The University of Michigan on leave from the Department of relation of cranial architecture, musculature, Biology, University of Calgary, Calgary, Alberta, Canada. This paper is dedicated to the memory of George Haas in apprecia- and dentitional patterns to feeding behavior tion of his profound contributions to the cephalic anatomy of Recent and muscle action in the tuatara provides and fossil reptiles.

0362-252518211713-0321$09.000 1982 ALAN R. LISS. INC. 322 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS jaw. The lateral teeth of each set lie on the The animal (female; weight 242 gm;snout- medial edge of the maxilla and the medial ones vent length 22.1 cm) used for myologic anal- on the lateral edge of the palatine; between ysis had died of a protozoan infection that left them they form a narrow tooth-fringed channel its muscles relaxed. Fixation was in 10% for- into which the mandibular tooth row closes. malin about 2 hr. after death (timerequired for The teeth are subtriangular in profile, with the postmortem veterinary examination). An esti- bases fused in series along each row. Recon- mate of muscle weight, fiber and sarcomere structions have suggested that sphenodontids lengths, and muscle architecture (Table 1) of reduce their food by powerful, relatively slow the major masticatory muscles was obtained shearing bites (Gunther, 1867; Robinson, '73). by 1)dissecting out the preserved muscles (on The origin of the difference between food one side), 2) weighing each three times (being processing by Sphenodon and lizards appar- blotted dry between each weighing), 3) immers- ently dates back to the pre-Triassic separation ing each in 30% nitric acid for three to five between sphenodontid rhynchocephalians and days to dissolve the connective tissue, and 4) carnivorous prolacertilians (Robinson, '73). then placing them in 50% glycerol. The fiber The latter probably used weak, relatively fast, arrangement of the muscles was then traced piercing bites. The dichotomy of masticatory from camera lucida projection on a Wild dis- patterns seems to have been sharpened further secting microscope. The length of five entire as the lizards lost the quadratojugal arcade fibers from adjacent positions within the mus- and mobilized their quadrate bones (strep- cle was measured on a millimeter scale and ocu- tostyly); this permitted the swallowing of lar micrometer on a dissecting microscope. relatively larger prey. Sphenodon has a fully Several fibers were then placed in glycerol on a diapsid skull with a fixed quadrate and is ap- microscope slide and examined under oil im- parently unable to increase the lateral distance mersion. The overall length of 20 sets of 10 sar- between the jaw joints. It apparently compen- comeres was measured for part of each muscle sates for the limited size of the bolus that may by means of a calibrated micrometer located in be swallowed by subdividing larger prey into the ocular. The muscles were then washed with manageable pieces. water and 70% alcohol, air-dried, and weighed Through the courtesy of the government of to obtain dry weights of the fiber masses. New Zealand, four living specimens of Sphenodon were available for study. We here describe how Sphenodon capture and masti- Behavioral observations and movement cate different prey and how the major muscles records then drive their jaws. Analysis of some of the Specimens were observed while they were smaller muscular components is relegated to a housed individually in large (lm X lm X lm), second study. screened, glass-fronted cages located in an air- conditioned room maintained at 15"-17"C and illuminated for 12-hr. periods by both GroLux MATERIALS AND METHODS and white fluorescent lamps. A heat lamp Specimens available focused on one corner of the cage provided a The following animals were used in this basking site. Tuataras were fed crickets, study: For osteology, AMNH 75705, AMNH cockroaches, and newly born mice that had 89835, CU 8568; for myology, two preserved been dusted with Pervinal vitamin powder. but partially dissected (brains removed for Fresh drinking water and pans large enough to neuroanatomic study) heads (CG 5369, 5370) let the animals immerse themselves were and one intact specimen (CG 5321); for obser- always available. vation of feeding movements three living For detailed observations of feeding, specimens (two females, one male; weight tuataras were temporarily transferred to range 582-822 gm; CG 5320, 5322, 5323); the smaller cages or a table top and then condi- last two were used for the electromyography. tioned to accept food manipulated by hand. Chilled crickets (length: 2.0-2.4 cm; weight: 0.3-0.6 gm) and cockroaches (length 2.8-3.0 Dissection cm; weight: 0.5-0.7 gm), as well as newly born Photographs of all stages of dissection (length: 3.5-4.0 cm; weight: 2.1-2.4 gm) and served as a basis for illustrations and descrip- juvenile mice (length: 5.5-6.0 cm; weight: tions. Contrast between muscle and the sur- 6.1-7.0 gm), were offered individually to facil- rounding connective tissue was increased by itate observation and cinematography. use of an iodine solution (Bock and Shear, '72). Feeding sequences were filmed on 16-mm film Muscle terminology follows Haas ('73). with a strobe-synchronized camera (Gans, '66) SPHENODON MASTICATION 323 using either direct lateral or biangular lateral- pation. Because of the high risk to the animal frontal (mirror) views. Cineradiographs of one involved, we recorded from the small and deep- specimen were taken at the Museum of Com- ly positioned muscles of the head in only one parative Zoology of Harvard University specimen. The activity of the infrahyoid and (courtesy of Professor F. Jenkins) with a suprahyoid muscles and of the muscles of the Siemens cinefluoroscopy unit operated at 50 tongue is excluded. kV and 120 mA. The Siemens image intensifier Electrodes formed of 0.076-mm Teflon- was filmed with an Auclair 16-mm camera at insulated stainless steel wire (Medwire Corp.) about 50 frames per second. All films were ana- were inserted through the skin and into each lyzed with a Lafayette 16-mm analytical pro- muscle via 25-gauge hypodermic needles (see jector and a Vanguard motion analyzer. Gans and Gorniak, '80, for details of electrode construction). The outside ends of the elec- Mercury strain gauge records trodes were soldered to Teflon-insulated silver During many of the feeding sequences, a ver- wires placed into PE tubing or to earphone tically directed mercury strain gauge was wires (later experiments) that were connected placed on one side of the head. Patches of to cables leading to the preamplifiers by Am- Velcro were attached by contact adhesive to phenol Mighty-Mite circular connectors. The the skin over the postorbital-squamosal bar coating of the connecting wires was fixed to and to the midventral surface of the lower jaw. the animal by short patches of Velcro. This Complementary patches of Velcro were kept the leads from shifting and relieved strain bonded to each end of the gauge. The gauge on the electrodes. was then placed so that it was under slight ten- EMG signals were amplified by means of sion when the mouth was closed. Tektronix 122 and 26A2 preamplifiers and Honeywell 117 amplifiers. EMG signals, Electrom yogruphy strobe photocell outputs, and those from the EMGs were recorded from those mercury strain gauge amplifier were stored on masticatory muscles into which electrodes a Honeywell 5600 intermediate-band tape could be placed using bony landmarks and pal- recorder and simultaneously displayed on a

TABLE 1. Wet and dry whole muscle weights (in grams) and ranges of the fiber lengths (in mm) of the major masticatory muscles of Sphenodon Weights Muscles Wet Dry Fiber length N' M. depressor mandibulae 0.49 0.11 anterior portion 8.0-21.0 45 posterior portion 23.0-29.0 35

M. adductor mandibulae externus superficialis 0.90 0.35 anterior portion 7.0-18.0 50 posterior portion 10.0-15.0 50

M. adductor mandibulae externus medialis MAMEM-a 0.50 0.10 9.0-13.0 70 MAMEM-b 0.34 0.06 12.0-17.0 75 MAMEM-c 0.20 0.05 13.0-15.0 100

M. adductor mandibulae externus profundus 0.10 0.04 5.0-11.0 180

M. pseudotemporalis superficialis 0.54 0.12 8.0-18.0 105

M. pseudotemporalis profundus 0.18 0.06 14.0-17.0 100

M. pterygoideus typicus dorsalmost (deep) portion 0.08 0.02 5.0-10.0 80 middle portion 1.65 0.57 medial part 17.0-18.0 70 lateral part 7.0-15.0 70 ventrolateral portion 0.30 0.08 18.0-20.0 40

M. pterygoideus atypicus 0.11 0.05 16.0-17.0 60

'N equals number of fibers measured. 324 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS

Tektronix 565 oscilloscope and a Gould (Brush mandibulae externus profundus (N =4); M. 481) multichannel chart recorder. pseudotemporalis superficialis (N = 15); M. Animals were anesthesized by an intra- pseudotemporalis profundus (N =5); M. muscular injection of Brevital Sodium (Eli Lil- pterygoideus atypicus (N =4) and the super- ly; dosage: 1.2 mglkg of body weight). After ficial (N =26) and deep (N =19) parts of the they had recovered from anesthesia, the condi- medial half of the middle portion of the M. tioned animals were placed on a grounded pterygoideus typicus, as well as the superficial stainless steel tray (moistenedwith saline solu- (N =5) and deep(N =5) parts of the lateral half tion) that was fixed in front of the chart re of the middle portion and the ventrolateral por- corder. A movie camera recorded a lateral view tion of the M. pterygoideus typicus. of the animal and the chart record showing EMG signals, a transducer signal, and a 1-Hz RESULTS time signal. General Frameby-frame projection of films allowed Detailed descriptions of the skull (Romer, measurement of the displacement of the lower '56), dentition (Robinson, '76), and cephalic jaw. Velocity and acceleration were deter- musculature (Byerly '25; Haas, '73) of Sphen- mined, first graphically and later by means of a odon are already available. However, we here computer. The displacement record was also provide a brief description of the dentition and correlated with muscular activity and descriptions of the muscles from which record- transducer signals. Up to seven simultaneous ings were made including their fiber lengths EMGs were digitized and processed by a (Table 1) in order to provide a foundation for Hewlett Packard 21MX minicomputer to ob- the interpretation of the movements they gen- tain the number of spikes and their average erate. Sarcomere lengths from different mus- amplitude for intervals correlated with the cine cles are equivalent at 2.6 pm. Measurements of frames. Digitized records were stored on cas- fiber and sarcomere lengths are for one speci- sette tape and then displayed on a Tektronix men and one side only. 4051 Graphic Display System with 4662 Descriptions of the dentition and myology digital plotter. Previous studies suggest that are followed by a description of the feeding the product of the number of spikes times their movements observed when Sphenodon chews amplitude correlates best with tension (Gor- crickets, cockroaches, and mice of various niak and Gans, '80);hence, this value was plot- sizes. Descriptions of the muscular activities ted for each muscle as a bar graph. The plot recorded during reduction sequences are then showed individual records as a percentage of presented. the maximum value for each feeding sequence. Percentage graphs allow intersequence com- Dentition parisons even though the level of amplification Sphenodon has a mandibular and maxillary of EMGs has not been controlled in some ex- pair of canine-like teeth and a maxillary pair of periments. Recent studies show that EMGs incisor-like teeth. The large canine-like man- thus recorded and analyzed are highly dibular teeth lie just posterolaterally to the repeatable (Gans and Gorniak, '80). mandibular symphysis; the smaller maxillary We here report on 80 feeding sequences com- teeth lie posterior to the mandibular ones and bining EMG and strain gauge records, as well are each preceded by three small conical teeth. as on additional observations of EMGs All of these canine-like teeth are larger than without synchronized displacement record- the remaining marginal teeth. In frontal view, ings. Fifty-five of the feeding sequences were the mandibular canines slant slightly laterally filmed, and 31 of these contain strobe- and in lateral view slightly posteriorly; the triggered photocell outputs. EMGs with si- maxillary canines extend directly ventrally. multaneous movement records were obtained Both anterior and posterior surfaces of the from the following muscles (N= the number canine-like teeth are rounded, whereas their of reduction sequences): anterior (N = 17) and medial and lateral surfaces are relatively flat. posterior (N =38) portions of the M. depressor The upper pair of incisor-like teeth protrudes mandibulae; anterior (N =8) and posterior straight downward from the premaxilla; these (N=8) portions of the M. adductor mandibulae are the largest teeth. Each of the more externus superficialis sensu stricto; posterior teeth generally has two pointed anteromedial (N=59), posterior (N =14) and cusps, a small medial (which may be absent) ventrolateral (N =6) portions of the M. adduc- and large lateral one. The anterior and lateral tor mandibulae externus medialis; M. adductor surfaces of these teeth are rounded, the SPHENODON MASTICATION 325 posterior surface is flat, and the medial surface less than that of all the adductors (com- shows a sharp edge. In frontal projection, each pressors) combined. Appparently, the com- tooth lies well medial to the quadratoarticular pressors are capable of generating the greatest joint; the lateral margins of the teeth line up forces. with the lateral margins of the palatine tooth rows and their medial margin ends just medial M. depressor mandibulae (MDM; Figs. 1,2) to the inner surface of the pterygoid flange. The posterior fibers of the M. depressor man- When the jaws are closed, the maxillary dibulae originate from the dorsoposterior por- incisor-like teeth lie anterior to the mandibular tion of the parietal and dorsal posteriormost symphysis and anteromedial to the canine-like part of the squamosal, and the anterior fibers mandibular teeth; neither pair contacts the originate from the posterior aspect of the dor- other. sal process of the squamosal; some deep Sphenodon also has maxillary, palatine, and anterior fibers also originate from a middorsal mandibular (dentary) marginal teeth. These section of connective tissue. The sharp dif- teeth are triangular in lateral view and increase ference in the origin and the difference in fiber in size as one proceeds posteriorly along the lengths (Table 1) between the posterior half of tooth row. The medial side of the maxillary and the muscle and the anterior half suggests that mandibular teeth and the lateral side of the the MDM may have an anterior and posterior palatine teeth are flat; the opposite side is subdivision, even though there is no obvious rounded. The rounded surface of the maxillary connective tissue plane separating them. and palatine teeth flattens posteriorly, meets The posterior fibers first run laterad and the flat surface of the tooth and forms a sharp slightly ventroposteriorly and then curve posterior edge; their anterior surface is sharply posteriorly near the lower margin of rounded. In contrast, both the anterior and the dorsal temporal fossa. These fibers curve posterior surfaces of the mandibular teeth are around the posterior end of the jaw and insert rounded. The maxillary and palatine teeth on its ventral surface. The anterior fibers run slant slightly posteriorly, whereas the man- ventroposteriorly and slightly laterad and dibular teeth slant anteriorly. then insert on the posterolateral end of the jaw. The maxillary, palatine, and mandibular The superficial posterior and anterior fibers in- tooth rows diverge posterolaterally from the sert more ventrally on the mandible than the symphysis. The palatine teeth lie parallel to deeper fibers. The dorsal third of the depressor the posterior half of the maxillary tooth rows, is thin, the middle third relatively thick, and forming a narrow trough between them. This the ventral third tapers towards the insertion. trough is slightly wider posteriorly than Loose connective tissue attaches the medial anteriorly. The posterior mandibular teeth fit surface of the dorsal two-thirds of the muscle snugly within this trough and this fit restricts to underlying structures, whereas the ventral lateral movements of the mandible when the third is relatively free. teeth are occluded. The lengths of the superficial fibers of the an- terior portion of the MDM (range 19-21 mm) MYO@Y are greater than those of its deep fibers (range Weights 8-15 mm). In the posterior portion, the lengths The air-dried weights of the masticating of the superficial and deep fibers are similar muscles of one side totaled 1.61 gm (wet (superficial: range 25-29 mm; deep: range weights, blotted, totaled 5.39 gm). The M. 23-25 mm), and their lengths are greater than depressor mandibulae makes up 6.8% of the those of the anterior portion. In both parts, the total dry weight, the M. pterygoideus atypicus lengths of the superficial and deep fibers in- 3.170, and the entire M. pterygoideus typicus crease as one proceeds posteriorly; the increase 41.6%. The remaining 48.5% comprises the is greatest in the deep fibers of the anterior superficial, medial, and deep adductors. The portion. M. adductor mandibulae externus medialis makes up 13.0% of the total, the M. adductor M. adductor mandibulae externus superficialis mandibulae externus superficialis 21.7%, the sensu stricto (MAMES; Figs. 1,2) M. pseudotemporalis superficialis 7.570, the The M. adductor externus superficialis sen- M. pseudotemporalis profundus 3.7%, and the su stricto fills the lateral part of the ventral M. adductor mandibulae externus profundus temporal fossa and forms a bulge on the lateral 2.5%. Thus, even though the M. pterygoideus surface of the posterior part of the lower jaw. It typicus is the largest single muscle, its mass is is covered by the lower temporal fascia and is 326 G.C.GORNIAK, H.I. ROSENBERG. AND C. GANS

MDM MAYEM MPSTS

MIMD \ MAMES

MAMEM-c

MAMEP ‘MAMES SPHENODON MASTICATION 327 not immediately visible after removing of the sert on the basal aponeurosis that lies deep to skin. The MAMES originates from the medial the MAMES. This aponeurosis is the insertion surfaces of the postorbital and squamosal; the for several other adductors of the lower jaw, anterior one-fourth of the origin is fleshy, the and transmits the forces to the dorsal margins deep portion of the middle half is fleshy, and of the coronoid and postcoronoid portion of the the superficial part aponeurotic (the lower jaw. The bulk of the MAMEM fills the aponeurosis is wide anteriorly and tapers dorsal temporal fossa. It is difficult to see its posteriorly), and the posterior one-fourth of the individual heads, as the ventral half of the origin is aponeurotic. The fibers pass in a muscle is covered by loose connective tissue, posteroventrad and slightly laterad direction by the MAMES, and by the upper temporal dorsal and medial to the jugal. Ventral to the bar. In vivo, the components of the MAMEM jugal the fibers curve medially to insert along may be located relative to the bony landmarks. the lateral surface of the dentary, posterior to Haas ('73)lists five heads of the MAMEM (but the mandibular tooth row. The most super- only diagrams four); there appears to be a ficial fibers insert most ventral and the deepest discrepancy between the labels used in his text fibers most dorsal on the dentary. description of the MAMEM and those in his The superficial anteriormost fibers of the diagrams. Only three (a-c) heads were found in anterior one-fourth of the MAMES show the the present study and their labels follow the longest fiber lengths (range 17-18 mm) and de- convention used in the diagrams. crease thereafter (13-14 mm), whereas the The anteromedial head of the MAMEM underlying deep fibers of this part are short (MAMEM-b) originates as a set of laterally (range 7-10mm). As one proceeds posteriorly and slightly anteriorly directed fibers from the through the middle half of the MAMES, the dorsolateral surface of the parietal. A short length of the superficial fibers originating from distance from their origin, the superficial the wide aponeurosis first decreases to 11-12 fibers of the anterior head curve sharply to run mm but then increases to 14-15 mm as the nearly straight ventrad and slightly anterior- aponeurosis tapers. In contrast, the length of ly; the deeper fibers curve less sharply than the the deep fibers of this portion first increases to superficial ones and the deepest run nearly 12-14 mm and then decreases to 10-12 mm straight ventrolaterad. The superficial and posteriorly. In the posterior one-fourth of the deep fibers taper ventrally to insert on an MAMES, there is no significant difference bet- anterodorsal extension of the basal apo- ween the lengths of the superficial and deep neurosis with the anterior fibers inserting dor- fibers. The lengths of these fibers range bet- sal to the posterior ones. The lengths of the ween 10-12 mm anteriorly and 8-9 mm superficial and deep fibers of the anterior por- posteriorly. tion of the MAMEM-b are similar (12-14 mm). In the posterior portion, the deep fibers (15-17 M. adductor mandibulae externus medialis mm) are slightly longer than the superficial (MAMEM; Figs. 1, 2) ones (14-16 mm) but both are longer than The compound M. adductor mandibulae ex- those anteriorly. ternus medialis lies posterior to the M. The posterior head (MAMEM-c) originates pseudotemporalis superficialis. The muscle as a set of fibers that runs in a markedly has fleshy origins, but all of its subdivisions in- anterolaterad direction from the dorsal, pos- terolateral surface of the parietal and the an- terodorsal surface of the squamosal. The Fig. 1. Sphenodon punctatus. Top: Lateral view of dis- section after removal of skin and connective tissues. Note superficial fibers then curve sharply ventrad, that adductor muscles are bound by the dorsal and ventral continue anteriorly, and pass deep to the post- arches of the diapsid skull. Middle: Lateral view of dissec- orbital bar and the MAMES. The deep fibers of tion after removal of both bony arches and most of the the MAMEM-c run anteriorly and nearly MAMES. Note the subdivisions of the MAMEM and how this bulky muscle tapers to insert onto the thin basal apo- straight ventrolaterad. The superficial and neurosis. Bottom: Lateral view of the dissection after re- deep fibers converge ventrally to form a thin moval of both bony arches, most of the MAMES, and dis- muscular sheet; the anterior fibers form the an- placement of the MAMEM. Note the large MPSTS and the terior part of this sheet and the posterior fibers relations of the maxillary (V2)and mandibular (V3)branches of the trigeminal nerve. MAMEM, M. adductor mandibulae the posterior part. The anterior part inserts externus medialis; MAMEP, M. adductor mandibulae exter- dorsal to the posterior part on the lateral sur- nus profundus; MAMES. M. adductor mandibulae externus face of the anterior and central portion of the superficialis; MDM, M. depressor mandibulae; MIMD, M. basal aponeurosis. In the anterior part of the intermandibularis; MLAO, M. levator anguli oris; MPSTS, M. pseudotemporalis superficialis: MPTA. M. pterygoideus MAMEM-c, the deep fibers (14-15 mm) are atypicus. slightly longer than the superficial ones (13-14 328 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS

MA~ES MPSTP

Fig. 2. Sphenodon ponctatus. Top: Lateral view of skull. maxilla; MPSTP, M. pseudotemporalis profundus; n, nasal; Note fully diapsid skull having two temporal fenestrae com- p, parietal; pf, postfrontal; pl, palatine; pm, premaxilla; PO, pletely encircled by bone. Bottom: Lateral view of the skull postorbital; pr, prootic; prf, prefrontal; pt, pterygoid q, (withlower arch removed) and lower jaw. The sites of attach- quadrate; qj, quadratojugal; sq, squamosal. For com- ment of cephalic muscles are indicated. at, articular; BA, pleteness, we show attachment sites of the M. levator anguli basal aponeurosis; c, coronoid process; d, dentary; e, oris (MLAO) and the M. retractor anguli oris (MRAO). epipterygoid; f, frontal; is, interorbital septum; j, jugal; m. Other abbreviations as in Figure 1. SPHENODON MASTICATION 329 mm). However, the lengths of the superficial However, as one moves posteriorly the lengths and deep posterior fibers are similar to each of both the superficial and deep fibers increase other (14-15 mm) and similar in length to the and become similar to each other (superficial: deep fibers of the anterior portion. 10-11 mm; deep: 9-11 mm). The largest part of the MAMEM is the ven- trolateral head (MAMEM-a) that originates M. pseudotemporalis superficialis (MPSTS; from the posterolateral and posteroventral sur- Figs. 1, 2) face of the parietal and from the anterior sur- The anterodorsal portion of the M. pseudo- face of the dorsal process of the squamosal. temporalis superficialis is visible in the an- The superficial fibers initially run in a marked- terior corner of the dorsal temporal fossa, but ly anterolateral direction, then curve sharply most of the muscle lies deep to the MAMEM. ventrad, continuing anteriorly to pass deep to The maxillary division of the trigeminal nerve the postorbital bar and MAMES. The deep (V,) crosses the lateral face of the MPSTS and fibers curve less than the superficial, running the mandibular branch of the trigeminal nerve nearly straight ventrolateral and slightly an- (V,) lies against its posterior margin. teriorly. The superficial fibers insert on the lat- The MPSTS originates from the posterior eral surface and deep fibers on the medial sur- part of the postfrontal, the anterolateral part face of the anterior and central portion of the of the parietal, and the dorsoposterior part of basal aponeurosis just ventral to the insertion the epipterygoid. Its anterior fibers initially of the anterior and middle heads. The anterior pass ventrad and slightly anterolaterad dorsal fibers of the MAMEM-a also insert dorsal to to the postorbital, but then curve medially the posterior ones. The fibers of the anterior deep to the postorbital to run nearly straight part of the MAMEM-a are shorter than those ventrad. The anterior fibers converge to insert of the posterior part (anterior: 9-11 mm; on the medial surface of a tendinous extension posterior: 11-13 mm). However, the lengths of of the anterior part of the basal aponeurosis. the superficial and deep fibers of the anterior The central and posterior fibers also run ven- part are similar to each other as are those of the trad and slightly laterad dorsal to the postor- posterior part. bital and then curve slightly medially ventral to it. However, the orientation of these fibers M. adductor mandibulae externus profundus becomes progressively more anteriad as one (MAMEP; Figs. 1,2) moves caudally. The central fibers insert onto The M. adductor mandibulae externus pro- the anterior tendinous extension, ventral and fundus lies deep to the MAMEM and posterior posterior to the anterior fibers. The posterior to the M. pseudotemporalis superficialis. It fibers insert directly onto the medial surface of has a lateral head originating from the postero- the anterior and central portion of the basal lateral surface of the prootic and a medial head aponeurosis. The most superficial of the an- originating from its anterolateral surface. The terior, central, and posterior fibers insert most fibers of the lateral head pass ventrad and an dorsally and the deepest fibers most ventrally, teriorly to converge onto a flat tendon, insert- The superficial anteriormost fibers of the ing on the medial surface of the posterior part MPSTS are longer than the deep ones (super- of the basal aponeurosis. The anterior fibers of ficial: 17-18 mm; deep: 14-15 mm). As one the medial head run almost directly ventrad to moves posteriorly, the lengths of the super- join the tendon of the lateral head. The pos- ficial fibers remain relatively constant until terior fibers of the medial head pass ventrad the posterior margin of the MPSTS, where the and slightly anteriorly to insert directly on the fiber lengths decrease to 15 mm. In contrast, basal aponeurosis posterior to the insertion of the length of the deep fibers first increases its anterior fibers and those of the lateral head. (15-17 mm) but then decreases (11-8 mm) as The anterior superficial fibers of the lateral the posterior border of the muscle is reached. head of the MAMEP are slightly shorter than the anterior deep fibers (superficial: 7-8 mm; M. pseudotemporalis profundus (MPSTP; deep: 8-9 mm). As one proceeds posteriorly, Fig. 2) the length of the superficial fibers decreases The M. pseudotemporalis profundus is com- (5-6 mm), whereas the lengths of the deep posed of a long lateral and a short medial part fibers remain relatively constant. The anterior and lies between the MPSTS and the epiptery- superficial fibers of the medial head are also goid bone. The mandibular branch of the tri- slightly shorter than those of its deep counter- geminal nerve separates the posterior margin parts (superficial: 6-7 mm; deep: 7-8 mm). of the MPSTP from the anterior margin of the 330 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS

M. adductor mandibulae externus profundus. pterygoid and the ventromedial process of the The lateral part originates deep to the anterior quadrate. Its superficial (i.e., ventral) fibers portion of the MPSTS from the ventroanterior originate from the pterygoid by an aponeu- region of the parietal and the dorsoanterior rosis, whereas the deeper fibers attach direct- part of the epipterygoid. The medial part of the ly. The middle portion of the MPTT may be MPSTP lies deep to the lateral part and orig- subdivided into medial, intermediate, and lat- inates from the anterior part of the epip- eral parts and each of these into superficial and terygoid and the posterior part of the mem- deep fiber layers. branous braincase. The fibers of the lateral The superficial fibers of the medial part show part pass ventroposteriorly and slightly lat- a parallel arrangement. These fibers first run erad, whereas those of the medial part pass posteromedially and slightly ventrad; there- posterolaterad and slightly ventrad. The after they curve posterolaterad toward the lateral and medial parts join near the upper ventroposterior margin of the mandible. The margin of the mandible and the fibers then run superficial fibers of the intermediate part also ventroposteriorly and slightly laterad to insert show bundles of parallel fibers that initially on the ventromedial surface of the dentary, pass caudad, then turn sharply ventrad and ventral to the coronoid process. slightly laterad to the ventral margin of the The lengths of the anteriormost and posteri- mandible; thereafter they curve sharply ormost fibers of the lateral part are similar caudad and slightly ventrolaterad. The deep (14-15 mm), as are the lengths of the anterior fibers of both these parts are parallel and pass and posterior fibers of the medial part (14-15 straight posterolaterad and slightly caudad. mm). However, the fibers in the middle of the Both superficial and deep fibers of the medial lateral part are longer (16-17 mm) than those and intermediate parts converge posteriorly to at its anterior and posterior margins. insert on the medial surface of the posterior end of the lower jaw, just anterior to the inser- M. pterygoideus typicus (MPTT; Fig. 3) tion of the dorsal portion of the MPTT. The bulky M. pterygoideus typicus has a As one moves farther laterad, the fiber complicated internal architecture. It may be arrangement of the MPTT changes from a par- subdivided into 1)a dorsalmost (deep)portion, allel to a bipinnate one. This change in fiber ar- 2) a middle portion, and 3) a ventrolateral one. rangment is not obvious from a superficial ven- Haas's brief description (1973) of this muscle tral view, as the middle portion of the MPTT is only mentions its several bony points of at- covered partially by the ventrolateral portion. tachment. Haas ('73) does not describe this change in the The dorsalmost (deep)portion of the MPTT MPTT of Sphenodon and no such condition fills the ventral half of the space lying medial has been mentioned for the MPTT of to the pterygoid and pterygoid wing of the Uromastyx aegyptius (Throckmorton, '80), quadrate. The muscle originates from the an- Varanus exanthematicus, Ctenosaura similis, terodorsal region of the medial surface of the and Tupinambis nigropunctata (Smith, '80). pterygoid. From here its fibers run sharply This bipinnate arrangement marks the ventrad and curve slightly posterolaterally to boundaries of the distinct lateral one-third of insert on the dorsal surface of the postero- the MPTT. This lateral part is further subdi- medial end of the lower jaw by means of fine vided into a lingual and buccal half by the tendons and fleshy attachment. insertion sites of the fibers. The medialmost fi- The fibers of the dorsalmost portion of the bers of the lingual half are long, curve posterio- MPTT are short dorsally and ventrally and laterally, and insert near its posterior end. As long in the center of the muscle. As one moves one continues toward the plane of insertion, dorsally, the length of the fibers increases from the fibers curve less and their lengths gradual- 5-6 mm (ventral) to 8-10 mm but then de- ly decrease as they insert farther anteriorly creases to 6-7 mm. along this plane. The fibers of the buccal half The middle portion is the bulkiest part of the run ventromedial to meet those of the lingual MPTT. It bulges ventrally from the two sides half; the more posterior insert more posteriorly to form a deep, narrow ridge in the roof of the than the anterior fibers. The lengths of the posterior part of the oral cavity. The middle fibers of the buccal half are equivalent to each portion of the MPTT originates from the ven- other. tral and medial surface of the ectopterygoid- The ventrolateral portion of the MPTT has a pterygoid process (pterygoid flange), the tendinous origin from the lateral and ventral medial margin and ventroposterior half of the aspect of the ectopterygoid-pterygoid process. SPHENODON MASTICATION 33 1

Pm

Fig. 3. Sphenodonpunctatus. Top: Ventral view of skull view of the middle portion of the MPTT with the ventro- and right half of lower jaw. Note the close proximity of the lateral portion displaced. Note the shape and fiber arrange- coronoid process of the lower jaw and the pterygoid flange ment of the MPTT. The numbers give the lengths of the and the arrangement of maxillary and palatine tooth rows. fibers (in mm) in the regions indicated. a. angular: bo, basioc- Bottom: Ventral view of the dissection after removal of the cipital; bs, basisphenoid ec, ectopterygoid; MPTT, M. ptery- intermandibular and throat musculature. The cross-hatched goideus typicus; ps, parasphenoid s. stapes; v, vomer. Other areas represent sites of attachment of the MPTT. Ventral abbreviations as in Figure 2. 332 G.C.GORNIAK. H.I. ROSENBERG. AND C. GANS

Its fibers first pass ventrolaterally and slight- when they are repositioning it between the ly caudad to the ventral margin of the mandi- jaws, and during the terminal phase, just prior ble; they then curve posterolaterally to run to swallowing. along the ventral margin up to the posterior Reducing movements. Reducing move- third of the jaw, where they insert on its ments usually comprise groups of two to four medial, ventral, and ventrolateral surfaces. cycles during which the prey is positioned be- The ventralmost fibers insert most posteriorly tween the teeth on one side of the head. In each on the mandible and the medial and lateral fi- cycle, the mouth first opens slowly and then bers anteriorly. The fiber lengths for the dif- continues to open more rapidily until max- ferent regions of the middle and ventrolateral imum gape for the cycle is reached. It next portions are shown in Figure 3. closes rapidly and then slows down as the food is contacted. During slow closing, the mandi- M. pterygoideus atypicus (MPTA; Figs. 1,2) ble first continues to move upward and then The M. pterygoideus atypicus is the largest moves anteriorly. The mouth then opens of the deep jaw muscles. It originates ventral slightly and the mandible remains immobile to the eye on the dorsal surface of the palatine until the start of the next cycle. During these and can be exposed by elevating the eye and its reduction cycles, strain gauges placed at right loose connective tissues. The lateralmost fi- angles to the tooth row generate a double- bers originate most anteriorly and the medial- peaked output (see below). most most posteriorly. Its fibers pass caudad Changes in the size of the prey do not pro- and slightly dorsolaterad, bridging the gap be- duce fundamental changes in mandibular tween the posterior end of the palatine and the movement. However, the horizontal and ver- pterygoid. From here they continue caudad, tical excursions of the head are greatest when passing medially through a slightly rounded large prey is being reduced. Also the duration depression in the ectopterygoid-pterygoid pro- of certain phases of the masticatory cycle then cess. After bending through about 80°, they increases. continue posteroventrad to insert on the Repositioning movements. Food is shifted medial surface of the lower jaw, just ventral posterolaterad during the individual chewing and posterior to the coronoid bone. The lateral- cycles of a group. Subsequently, it is reposi- most fibers insert anteriorly and the medial- tioned between the tooth rows of the same or most posteriorly. The fiber lengths of the the opposite side. At the start of a reposi- MPTA (16-17 mm) are relatively constant tioning movement, the mouth opens farther from its medial to lateral margins. than during reducing movements. The tongue shifts the food as the mouth opens and dis- Feeding movements places it anteriorly and laterally. Reposition- Introduction ing movements produce single peaks of greater General terminology. A feeding sequence amplitude and duration than chewing cycles consists of prey capture, mastication, and on the strain gauge records. Occasionally, the swallowing. Mastication is subdivided into food may be repositioned without a significant reducing, repositioning, and terminal phases. change in the pattern of chewing movements. Each single swing of the mandible, starting Terminal movement. At the very end of a with opening of the mouth and continuing reduction sequence, the tongue moves the food through closing, is referred to as a cycle. Each towards the back of the oral cavity. In such ter- cycle is divided into phases defined by obvious minal movements, the mouth opens slightly changes in the movement pattern. wider and longer than it does during chewing Preliminary information about muscular ac- cycles. Strain gauge records show a single peak tivity is provided by the externally visible of relatively long duration. movements of the jaws and tongue and by the bulging muscles, specifically of the Mm. ad- Feeding on crickets and cockroaches ductor mandibulae externus medialis (dorsal Capture. Tuataras respond to moving prey temporal fossa) and superficialis (ventral tem- by cocking their head towards it. While they poral fossa) and the M. depressor mandibulae. ordinarily ignore motionless prey, they may in- The bulky tongue is highly mobile, plays an im- gest it after it has been moved around with portant role in capture and manipulation of tweezers. food, and is visible whenever the mouth is When a (hungry) tuatara notices insects open. Individual cycles of masticatory phases moving on the ground, it points its head to- differ when the animals are reducing the food, wards the prey, opens the mouth, and then SPHENODON MASTICATION 333 everts the tongue. The tongue first lifts slight- axis through the quadrate. During the fast- ly out of the buccal floor and then begins to opening phase (2), the lower jaw rotates open protrude; during this movement its dorsal sur- more rapidly; but the entire jaw also moves face remains straight and the tongue appears posteriorly. Cineradiographs show that the thin in profile (Fig. 4B). As the tongue pro- retroarticular process of the mandible con- trudes beyond the symphysis, its upper sur- tinues to rotate, but simultaneously translates face curves. The middle of the tongue then posteriorly along the articular surface of the seems to be pushed upward and forward, but quadrate. The fast opening phase ends with the anterior portion appears to be fixed to the the mouth wide open and with the retroar- symphysial region so that the tongue starts to ticular process shifted posteriorly in the man- double back under itself (Fig. 4C). The head dibular fossa. continues to move towards the prey and cine- During the fast-closing phase (3),the mandi- radiographs show that the hyoid (supporting ble first rotates closed rapidly and only the trachea and posterior lingual portion) is decelerates when the teeth contact the food. protracted. This protraction of the hyoid The anterior shift of the mandibular tip at the moves the posterior aspect of the tongue to- end of fast closing is so minor that the articular wards the symphysis. process shows no obvious translation in cine- During capture, the sticky dorsal surface of radiographs. Next follows the distinct the anterior portion of the tongue rotates crushing phase (4). The dorsal and lateral ad- around the symphysis to lie ventrally. The ven- ductor masses on the working side of the head trally directed surface is pushed against the bulge obviously and one may hear chitin being food (Fig. 4D) by a combination of tongue fractured. During the crushing phase, the man- eversion and the forward and downward move- dible slowly rotates toward closure; it also ment of the head (Fig. 4E). Hyoid, tongue, and moves slightly forward as the retroarticular adherent prey are then withdrawn into the oral process both rotates about the quadrate and cavity (Fig. 4F) and the mouth closes. translates anteriorly. During the shearing Reducing movements. Retraction of the phase (5), the mandible obviously moves tongue pulls the adherent prey into the mouth, anteriorly; food held fixed against the max- where it generally comes to rest partially illary and palatine tooth rows is sheared by the across one set of tooth rows; two to three pre- mandibular row acting like a saw. Large food liminary masticatory or immobilizing cycles items tend to be rotated slightly and the skin follow. The tongue then repositions the cricket of the mouth adjacent to the food is pulled taut posteriorly near the corner of the mouth and during this propalineal (anteriad) shift. The between either set of teeth, after which masti- shearing phase lasts until the mandible drops cation proper begins. The cricket generally re- slightly and moves slightly posteriorly, sepa- mains in a fixed position relative to the upper rating the upper and lower teeth. During the jaw for two to four masticatory cycles. Occa- resting phase (6),the lower jaw remains slight- sionally, propalineal shearing movements of ly depressed until the start of the slow opening the lower jaws shift the cricket slightly phase of the next cycle. anteriad. The cricket is then repositioned by During the crushing phase, the muscles the tongue either to the same or the opposite bulge noticeably out of the dorsal temporal side as the mouth opens; two to three more fossa. Normally the food is asymmetrically po- masticatory cycles follow. Such groups of sitioned; the muscles of the working side then cycles occur repeatedly during a reduction se- bulge slightly earlier and more obviously than quence. Increasing amounts of secretion do those on the balancing side. During the fast- become visible around the cricket and it be- closing and crushing phases, muscles on the comes reduced to a saliva-covered, mushy working side also bulge slightly out of the ven- mass after approximately 15 chewing cycles. tral temporal fossa. Muscles of the anterior A masticatory cycle (Figs. 5, 6) may be sub- portion of the ventral fossa begin to bulge dur- divided into six phases: 1)slow-opening, 2) fast ing fast closing; those of the posterior portion opening, 3) fast-closing, 4) crushing, 5) shear- bulge next, during the crushing phase. ing, and 6) resting; all are best described from Records from the strain gauge (Fig. 6) cross- lateral views (Fig. 5). ing the gape reflect the jaw movements during During the slow opening phase (l),the lower a chewing cycle as a double-peaked curve; the jaw first rotates open slowly. Cineradiographs first peak is larger than the second. The rise of show that the retroarticular process of the the first peak correlates with the start of fast mandible simply rotates about a transverse opening, the peak indicates the transition from 334 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS

Fig, 4. Sphenodon punctatus capturing a cricket. Suc- manipulated by a plastic rod to attract the tuatara and elicit cessive frames (24 framesisec.) from a 16-mm, strobe-ex- feeding within a circumscribed area. This procedure was posed film. An immobilized (chilled) cricket was used in most recording sessions. fast opening to fast closing, and the signal placements occur during the slow opening and returns to base line at the end of the fast shearing phases, nor do the strain gauges in- closing phase. The small secondary peak is pro- dicate anteroposterior movements and the duced by the bulging of the dorsal adductor relative opening of the mouth during the mass and consequently correlates with the resting phase. crushing phase. The relative height of this In general, the length of all phases, except secondary peak is higher on the working than for the resting one, decreases as does the excur- on the balancing side. No strain gauge dis- sion of the jaws throughout a reduction se- SPHENODON MASTICATION 335

B

5 !&

Fig. 5. Sphenodonpunctatus. Displacement of lower jaw represents the bulgingof the working side adductors during during a chewing cycle traced from 16-mm movie. Arrows crushing and shearing phases. The insert shows the path of indicate the movement of the jaw between frames as food is the tip of the mandible relative to the head during a reducing reduced between the left tooth rows. The vertical bars cross- cycle. 1. slow-opening phase: 2, fast-opening phase; 3, fast- ing the labial zone are painted reference markers indicating closing phase; 4, crushing phase: 5, shearing phase. the extent of the propalineal shift. The stippled area W aw c's

VERTICAL VERTICAL V ERT IC AL DISPLACEMENT DISPLACEMENT DISPLACEMENT

- rcm I

w SPHENODON MASTICATION 337 quence. Neither direct observations nor anal- there is less propalineal displacement of the ysis of films suggests that the mandible moves mandible during terminal cycles than during laterally, or that the lower jaws rotate about masticatory ones; the path of the mandibular their long axes. tip shows only a slight anteroposterior dis- The lower jaws reach maximum opening ve- placement when the mouth opens and closes. locity during the initial one-third of the fast During the fast opening phase, the mandible opening phase (Fig. 7). The velocity then and its articular process show only a slight smoothly reverses to a maximum closing value posterior translation and during the crushing that occurs during the first one-third of the and shearing phases only slight anterior trans- fast-closing phase. Maximum closing veloci- lation. There are usually five terminal cycles at ties tend to be greater than or equal to (rarely the end of a reduction sequence. less than) maximum opening velocities. Maxi- Mandibular displacement during terminal mum opening acceleration of the lower jaws oc- cycles is similar to that during reducing ones. curs at the start of fast opening and the two- to Maximum opening velocity occurs during the three-times greater maximum closing accelera- last one-third of jaw opening, and maximum tion is reached at the start of the fast closing closing velocity takes place during the first phase. one-third of closing. Maximum opening ac- Repositioning movements. Insects are re- celeration coincides with the start of fast open- positioned every three to five cycles. Reposi- ing and the two-times-greater maximum clos- tioning cycles occur about 100 msec. after the ing acceleration coincides with the start of fast end of the shearing phase of the previous re- closing. duction cycle; the resting phase before a re- positioning cycle is only 40% as long as that Feeding on mice between two reduction cycles. General. Sphenodon ingests newly born As the mouth begins to open, the tongue mice in the same way that it does crickets and twists towards the working side to contact and roaches. Portions of the feeding pattern slide the cricket off the double tooth rows. The change during ingestion of juvenile mice. mouth opens wider than during a chewing cy- Tables 2 and 3 show changes in reducing move- cle and the tongue arches dorsally, first center- ments among reduction sequences for crickets, ing the cricket in the oral cavity and, as the roaches, and juvenile mice. mouth closes, repositioning it laterally for the Capture and immobilization. Sphenodon first cycle of the next chewing sequence. captures mice by biting them and obtaining a As the mandible reaches a wide open posi- secure grip with the anterior teeth. The tongue tion during repositioning, the skin covering plays no role during capture nor is it pro- the dorsal temporal fossa sinks inward slightly truded. After capture, mice are shifted grad- but then rises and straightens during the fast- ually deeper into the mouth by inertial move- closing phase. Strain gauge records do not ments of the head. These involve a rapid drop show a secondary peak. of the mandible with a simultaneous upward Terminal movements. As the cricket be- and forward movement of the head relative to comes crushed, it is gradually worked posteri- the prey. The mouth then snaps closed and the orly to the central region of the oral cavity; head again moves downward. Captured mice reduction cycles then pass smoothly into ter- are generally positioned transversely in the minal ones. mouth across the tooth rows of both sides. Terminal movements are characterized by Coincident with or following the capture and dorsal and anterior arching of the tongue posterior shift, Sphenodon makes a series of which usually rubs against the roof of the crushing bites that kill the mouse. The tooth mouth (and collects food from it). During this rows on both sides are used simultaneously movement the lingual tip extends beyond the and the prey is not repositioned as long as it re- anterior margin of the maxillary tooth row. mains centrally located in the mouth. Repos- The tongue (and hyoid) then retract, carrying itioning occurs by rapid lateral movements of the food into the buccal cavity. The mouth the head (with a simultaneous opening cycle) opens slightly wider and for a longer interval and effectively shifts the prey to the side op- during terminal cycles than during masti- posite to that towards which the head moves. catory cycles. Both during capture and during inertial move The dorsal adductor musculature does not ments Sphenodon rotates its skull slightly dor- bulge obviously (sothe strain gauge records do sad around the head joint; this occurs coinci- not show a secondary peak). Furthermore, dent with mandibular depression. 4 4 4 5 4 W - W ?, 00 T T i \ \

4 -

300 t

4 t WORKING REPOSITION4 LEFT LEFT REPOSITION RIGHT RIGHT REPOSITION SIDE Fig. 7. Sphenodon punctntus. Vertical displacement graphs of the tip of the mandible (relative to the head) when (filmed at 24 frames per sec.). velocity, and acceleration tuatara reduces a cricket. SPHENODON MASTICATION 339

TABLE 2. Comparison of masticatory cycles when Sphenodon chew crickets, cockroaches, and juvenile mice' Total number Duration of Duration of Bites per of bites per Duration repositioning terminal Food second sequence of bite' movements' movements' Crickets 0.84 f 0.13 21.2 f 3.39 502.6 f 80.4 709.3 f 98.4 891.7 f 305.5 (N=190) (N=12) (N=50) (N=23) (N=16)

Cockroaches 0.83 f 0.87 32.0 f 5.63 620.7 i 140.6 831.9 f 151.3 1072.2 f 180.4 (N=130) (N= 9) (N=50) (N=31) (N=20) Juvenile mice 0.55 f 0.06 38.4 t 4.82 877.4 f 187.4 1391.1 i 237.4 1300.5 f 398.9 IN=192) IN= 5) (N=42) IN=15) IN=ll)

'Bites are defined as the start of slow opening to the start of the resting phase. Data are mean k SD. 'Milliseconds.

TABLE 3. Duration (msec.)of the six phases of masticatory cycles when Sphenodon chew crickets, cockroaches, and juvenile mice' Slow- Fast- Fast- Food N opening opening closing Crushing Shearing Resting Crickets 10 141.04 i 29.5 95.53 -t 20.5 82.00 f 20.5 68.06 f 20.5 63.55 f 21.6 232.06 f 114.0 (21%) (14%) (12%) (10%) (9%) (34%)

Cockroaches 10 145.55 f 41.4 86.51 f 13.5 77.08 f 13.5 63.96 f 21.3 63.55 f 21.6 264.04 f 134.5 (21%) (12%) (11%) (9%) (9%) (38%) Juvenile mice 10 414.51 k 116.4 132.02 f 18.0 113.57 f 18.0 86.51 f 13.5 91.02 t 27.1 843.37 2 203.4 (25%) (8%) (7%) (5%) (5%) (50%)

'Number in parenthesis directly below each mean equals the duration in percentage of the entire cycle. N equals numher of cycles

Reducing mouements. At the start of re- Protruding limbs and even the heads of mice duction, the mice are shifted inertially to one will then be cut off, but the severed portions side of the mouth by rapid mouth opening with are not picked up and only the part in the coincident lateral shifts of the head. Simulta- mouth is ingested. This observation may ex- neously, mice tend to be shifted posteriorly as plain the comments that decapitated petrels the head moves forward relative to the prey. were found in areas inhabited by tuataras The mice are repositioned inertially after each (Crook, '75). set of four to seven cycles. The tongue is not noticeably involved in the manipulation of Electromyography - Capture large prey during these early stages of As the mouth starts to open, the anterior and mastication. posterior portions of the M. depressor man- As reduction of mice proceeds, movements dibulae (MDM) begin to fire bilaterally. The of the mandible resemble those during the re- anterior portion first reaches its maximum duction of crickets. However, reduction of level and continues at this level until the mice differs by upward movements of the en- mouth is almost completely open. However, tire head as the mouth opens, and downward the posterior portion first reaches a 25-30% movements as it closes; the head also tilts level, becomes more active to a 50-6070 level, towards the balancing side during the first half and then reaches its maximum level near the of a reduction sequence. Thereafter, head end of opening. As the mouth reaches a wide- movements cease, only the lower jaw cycles, open position, the anterior portion of the M. ad- and the tongue becomes involved in the manip- ductor mandibulae externus superficialis ulation of the food. During terminal cycles, the (MAMES) starts to fire at a 20-2570 level. tongue protrudes but does not arc upward as it Both portions of the MDM first become less does during the reduction of crickets; nor does active and then silent as the mouth starts to it appear to rub against the roof of the mouth. close. Portions of mice may remain outside of the Closing of the mouth is accompanied by in- mouth during most of the reduction sequence. creased activity in the anterior portion of the 340 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS

MAMES and by the start of activity in the M. adductor mandibulae externus super- posterior portion of the MAMES, the antero- ficialis sensu strict0 (MAMES). The anterior medial and posterior portions of the M. adduc- and posterior portions of the MAMES are ac- tor mandibulae externus medialis, the M. pseu- tive asymmetrically during reduction cycles dotemporalis superficialis, as well as the super- and the level of activity is greater for the mus- ficial and deep parts of the middle portion of cle on the working than on the balancing side. the M. pterygoideus typicus. All of these ad- Maximum voltage is 0.86 mV for the anterior ductors become more active during closing and portion and 2.28 mV for the posterior one. attain maximum activity when the teeth con- As the mouth starts to close, the anterior tact and then crush (or penetrate) the prey. portion of the MAMES of the working side Thereafter, the adductors become less active begins to fire at a 20-3070 level (Fig. 8). Activi- as the mouth is closed and then silent as it ty increases during c!osing to reach levels of opens slightly and stops moving. All of these 90-100% on the working side and 40-6070 on adductors, as well as the MDM, remain silent the balancing side during the crushing phase. as the mouth stays motionless, even though Activity of the MAMES of the working side crickets and cockroaches lie partially across then drops to 0-30% as the lower jaw starts to one set of lower teeth and juvenile mice across move anteriorly during the shearing phase. both sets. However, the posterior portion of the MAMES is silent until the start of the crushing phase. Electromyography - Reduction The level of activity then builds rapidly to M. depressor mandibulae (MDM). The M. 70-100% on the working side and then depressor mandibulae of the working and decreases sharply to below 40% as the balancing sides are active bilaterally and sym- crushing phase ends. The posterior portion of metrically during the opening phase of a reduc- the muscle is generally silent during the shear- tion cycle. However, the pattern of activity ing phase. Both portions of the MAMES are differs between the anterior and posterior por- silent during the resting and opening phases of tions of this muscle. Maximum voltages are a reduction cycle. 1.84 mV for the anterior and 2.32 mV for the During repositioning cycles, the anterior posterior portion. portion of the MAMES starts to become active The anterior portion of the MDM starts to at a 10-20% level at the end of the fast-opening fire at a 10-15% level at the beginning of the phase and throughout the fast-closing phase. slow-opening phase and continues to fire at Unless the repositioning cycle has placed food this level throughout this phase; the posterior between the tooth rows, the activity remains portion remains silent. At the start of the fast- at 20-50% during the next crushing phase. opening phase, activity of the anterior portion When food has been positioned between the reaches 40-60%, increases to 80-100% about teeth, the MAMES becomes more active, midway through the fast-opening phase, and reaching 70-100% during the crushing phase. then drops to 20-30% as the lower jaw reaches M. adductor mandibulae externus medialis its furthest ventral excursion (Fig. 8).The pos- (MAMEMI. The anteromedial (-b-),posterior terior portion of the MDM becomes active at a (-c-),and ventrolateral (-a-)heads of the M. ad- 40-6070 level and maintains this level ductor mandibulae externus medialis are throughout fast opening. Both portions of the bilaterally and asymmetrically active during a MDM become silent once the mouth reaches reduction cycle, and the level of activity is the wide-open position and remain inactive greater for the head on the working side than during the fast-closing, crushing, shearing, for that on the balancing one. Activity de- and resting phases. creases as the food is reduced, as it is reposi- Activity of both the anterior and posterior tioned, and during terminal cycles. Maximum portions of the MDM is greater at the start voltage is 1.74 mV for the anteromedial, 2.48 than at the end of a reduction sequence and mV for the posterior, and 1.94 mV for the ven least during terminal cycles. When food is re- trolater al head. positioned, the start and cutoff of activity in All heads of the MAMEM of the working both the anterior and posterior portions are and balancing sides are silent at the start of similar to those seen during a reduction cycle. closing; those of the balancing side remain However, the level of activity of the posterior silent throughout the fast-closing phase. How- portion reaches 100% during the repositioning ever, as the teeth approach the food late in the movements, which is more than 40% greater fast-closing phase, all three portions of the than its maximum activity level during reduc- working side start to fire at a 20-3070 level tion cycles. (Fig. 8). Their activity increases rapidly at the SPHENODON MASTICATION 34 1

go BALANCING v) 5 10 3V

20

MDM g: anterior 'OOi25 A MDM 75 posterior 50 3 100125 I- i MAMES 75 anterior 50

= MAMEM 75 Wm -a- 4 5 25 3 MAMEM 75 W -b- I::] 1 c 1 Y 25 In v, MAMEM75 L -c- 0 'I:]25

W 100 7 (3 MAMEP 75

s 25 2 W 50 MPSTS nW 25 ,

25

TIME II I I II I II I I1 I I Ill I I1 I I I I I1I I I II II I II I II I1I I I1 I Ill 11 I I II I1 I Ill 40 rnsedunit

Fig. 8. Sphenodon punctatus. Synthetic summary of a cricket. Muscle abbreviations as in Figure 1. The numbers sequence of vertical displacements of the lower jaw and bar (1-61 along the displacement graph indicate the six phases of graphs of the percentage of the number of EMG spikes a reduction cycle. times the mean spike amplitude when a tuatara reduces a 342 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS start of the crushing phase, reaching 70-100%. (MPSTP). The M. pseudotemporalis profun- Activity of the posterior and ventrolateral dus of the working side is more active than heads then drops to a 40-60% level and the that on the balancing side. Maximum voltage anteromedial one to a 50-70% level as this is 0.71 mV. phase ends. The posterior and ventrolateral The MPSTP of the working side begins to portions of the MAMEM of the working side fire at the start of the crushing phase. Activity show a 10-20% level of activity at the start of increases rapidly toreach 75-100% at the start the shearing phase, whereas the anteromedial of the shearing phase but then decreases rapid- portion shows a 20-4070 level. The three heads ly to 20-3070 at the end of shearing. The then become silent and remain so through the MPSTP of the balancing side fires later and is resting phase. Activity of the anteromedial active for a shorter period than the muscle of and ventrolateral portions of the balancing the working side. Activity of the balancing side builds to a 30-4070 level at the start of the side MPSTP begins at the end of the crushing crushing phase, increases to 50-60Y0, and then phase and increases rapidly to a 60-80% level drops to 0-10% as the crushing phase ends; ac- early during the shearing phase; it rapidly tivity of the posterior head first increases drops to zero near the end of shearing. The rapidly to 50-6070 and then drops to a 30-40% MPSTP of both the working and balancing level. They become silent at the start of the sides are inactive during the resting and open- shearing phase and remain so throughout the ing phases. resting and opening phases. M. pterygoideus typicus (MPTT). Both the M. adductor mandibulae externus profundus superficial and deep medial parts of the middle (MAMEP). The M. adductor mandibulae ex- portion of the M. pterygoideus typicus of the ternus profundus is bilaterally active during a working and balancing sides are active asym- reduction sequence. Activity is greater on the metrically. The level of activity of both parts is working side than on the balancing one and de greater for the working than for the balancing creases on both sides as the food becomes re- side and activity decreases as the food is re- duced. Maximum voltage is 1.28 mV. duced. Maximum voltage is 1.86 mV for the su- The muscles on both sides start to fire at a perficial medial part, 1.90 mV for the super- 20-40Y0 level at the start of fast closing (Fig. ficial deep part, 1.46 mV for the superficial 8). Activity increases to 50-6070 and reaches lateral part, 1.54 mV for the deep lateral part, 90-100% on the working and 60-8070 on the and 1.30 mV for the ventrolateral part. balancing side during the last half of the The superficial medial part of the middle por- crushing phase. Thereafter, activity decreases tion of the MPTT of the working side begins to bilaterally to a 0-30% level during the first fire at a 10-30% level during the fast-closing half of the shearing phase. Both muscles are si- phase (Fig. 9). Activity increases during the lent during the resting phase. crushing phase to reach 70-100% at the start M. pseudo temporalis s u perficialis of the shearing phase, then decreases rapidly (MPSTS). The M. pseudotemporalis super- to 10-25% at the end of this phase, and ceases ficialis of the working side is more active than at the start of the resting phase. The deep the MPSTS of the balancing side, which shows medial part of the MPTT of the working side variable activity during reduction cycles. Both begins to fire later than the superficial one, on- sides also show variable and low levels of ac- ly starting to show a 20-40% level of activity tivity during terminal cycles. Maximum during the crushing phase. Activity increases voltage is 1.72 mV. throughout the crushing phase and reaches The MPSTS of both the working and balanc- 70-100% at the start of the shearing phase. ing sides are silent at the start of closing and The deep part rapidly becomes less active to during the fast-closing phase of reduction 10-30Y0 and is silent throughout the resting cycles. The MPSTS of the working side be- phase, comes active at the start of the crushing phase. The superficial medial part of the middle por- Activity increases rapidly to 80-100% and tion of the MPTT of the balancing side shows then drops quickly to below 50%, to end at the an activity pattern similar to but of lower start of the shearing phase (Fig. 8). Simultan- amplitude than that of the working side. How- eously, the MPSTS of the balancing side is ac- ever, the deep part of the MPTT of the balanc- tive at a 20-40% level. Both sides are silent ing side is active later than that of the working throughout the shearing, resting, and opening side. For the deep part of the balancing side, phases. activity starts during the last half of the M. pseudo temporalis pro fundus crushing phase and then increases rapidly to SPHENODON MASTICATION 343 reach 40-60% at the start of the shearing superficial medial and lateral parts and the phase. Activity then decreases rapidly and deep lateral part and the ventrolateral portion ceases at the start of the resting phase. of the MPTT now are silent during closing of The superficial and deep lateral parts of the the mouth and active when it opens. The super- middle portion of the MPTT of the working ficial medial and lateral parts become active at side fire asymmetrically (Fig. 9). The super- a 10-2570 level at the end of the resting phase, ficial lateral part begins to fire at a 10-40% continue through slow and fast opening at a level at the start of the crushing phase. Activi- 20-60% level, and end as the mouth starts to ty then increases during the first part of the close. The deep lateral part and the ven- shearing phase, reaches 80-100% near the end trolateral portion become active at the start of of shearing, and decreases rapidly thereafter. the resting phase and remain so through slow The deep lateral part of the working side is ac- opening. tive at a 10-30% level during the fast-closing M. pterygoideus atypicus (MPTA). The M. phase, remains so during crushing, increases pterygoideus atypicus of the working and to 70-100% during the shearing phase, but balancing sides are active during the fast- then decreases rapidly to a 0-2070 level. closing, crushing, and shearing phases of a re The superficial lateral part of the balancing duction cycle. However, the activity level of side begins to fire at the start of shearing. Ac- the working side MPTA is greater than that of tivity first increases rapidly to 20-30% and the balancing side MPTA. Maximum voltage then decreases rapidly at the end of shearing. is 1.06 mV. The deep lateral part of the balancing side The MPTA of the working side begins to fire shows an activity pattern similar to the work- at a 20-30% level during the fast closing (Fig. ing side but at a lower level. Both the super- 9). Activity then increases to 50-75% during ficial and deep lateral parts of the working and the first part of the crushing phase and then balancing side are silent during the resting and reaches maximum near the end of crushing and opening phases. the start of the shearing phase. During shear- The ventrolateral portion of the MPTT is ac- ing, the activity level remains high (60-75%) tive throughout most of a masticatory cycle but then decreases rapidly as the shearing but at varying activity levels. The ven- phase ends. Activity of the MPTA of the trolateral portions of the working and balanc- balancing side initially reaches a 15-2070 level ing sides show similar activity patterns; how- during fast closing. Activity thm increases ever, the activity levels of the working side slightly to 30-40% during crushing and re- muscle are greater than those of the balancing mains so during the first part of the shearing side. phase; it then drops to zero as shearing ends. The ventrolateral portion of the working side Both the MPTA of the working and balancing shows two bursts of activity as the mouth side are inactive during the resting and open- closes and variable low level activity during ing phases and during terminal cycles. the resting phase. The first burst of activity begins at the start of fast closing. Activity in- DISCUSSION creases rapidly to 40-60%, but then decreases Masticatory pattern rapidly to 0-20% during crushing. This de- General creased level is followed by a second burst dur- The dentition of Sphenodon is functionally ing which the activity level reaches maximum heterodont. As already noted (Robinson, ’76), at the start of the shearing phase. Activity the large anterior (successional)marginal teeth then decreases to 10-20% as the shearing are analogous to canines. As none of the acre phase ends. The ventrolateral portions remain dont teeth are replaced and new teeth develop active at a level varying between zero and 25% at the rear of the series, the tooth series retains during the resting phase. a sequence of teeth that show size increases During terminal cycles, the activity pattern from front to rear. of the medial and lateral parts of the middle However, the size increase is uneven; thus portion of the MPTT, as well as the ven- Robinson’s reference (’76) to “successional,” trolateral portion differ from that during chew- “remnant hatchling,” and “additional” dental ing (Fig. 9). The deep medial part starts to fire regions. As earlier stated by Gunther (1867), at a 5-2070 level at the start of the shearing old individuals still retain the small remnant phase and continues throughout the resting hatchling teeth anteriorly; as these teeth be- phase at a 20-50% level and into the start of come smaller, wear marks gradually develop slow opening at a 5-20% level. In contrast, the on the dentary itself (Robinson, ’76).The wear 344 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS a 0 F pe W>

Y MPTT loo middle 7550- 4 a med ia I 25 suDerficiaI 1L

medial deep 25

superficial

lateral 25 deep

ven tro - lateral 25

25

TIME -/ I1 I I I1 II II I Ill IllI I IIIIII 40 msec/unit

Fig. 9. Sphenodon punctatus. Synthetic summary of the when a tuatara reduces a cricket. Note the difference in the percentage of the number of EMG spikes times the mean activity pattern of the MPTT and the absence of activity of spike amplitude of the different portions of the M. the MPTA during a terminal cycle. The numbers along the pterygoideus typicus IMPTI') and M. pterygoideus atypicus displacement graph indicate the six phases of a reduction IMPTA) on the working side and during a terminal cycle cycle. of these anterior teeth increases the vertical mits adult animals to impale larger prey. The distance between the upper and lower tooth few small remnant hatchling teeth provide a rows in this region; more important, it in- rough contact surface that will hold large prey; creases the effective height of the enlarged SUC- however, such prey must be repositioned be- cessional teeth (which show less wear) and per- fore reduction. In adult Sphenodon, the small SPHENODON MASTICATION 345 surface area of the remnant hatchling teeth to be greater on the dorsal (two rows of teeth) limits their shearing capacity and thus this than on the ventral (asingle row) surface. Con- section is not used during reduction of large sequently, the stress level will be much larger prey. on the ventral side. This arrangement assures Our X-ray movies of feeding sequences sug- that the mandibular rather than the maxillo- gest that Sphenodon lacks cranial kinesis and palatine teeth will first perforate uniform prey. this observation agrees with some reports The effects of mandibular deceleration and the (Versluys, ’12; Kuhn-Schnyder, ’54; Jollie, ’60). closing forces will differ depending upon the However, Romer (’56)described a movable ar- position of the food. If the bolus moves with ticulation between the basipterygoid process the mandible, deceleration forces will decrease of the basisphenoid and the pterygoid. Iordan- the differential. If the tongue holds the bolus sky (’66)considered a special metakinesis as a against the palate, the forces will enhance it. possible feature of the tuatara skull. One As shear during sliding movements is again should realize that even cineradiographs of greater on the mandibular than on either the lizards with kinetic skulls have not provided maxillary or palatine rows, the cutting action measurable displacement of bones because of will also begin on the mandible. The asym- the limited resolution of available methods metry of anteroposterior edges becomes criti- (Throckmorton,’76). Whatever the condition in cal during the propalineal translation at the juvenile animals (Ostrom, ’62), manipulation of end of crushing; the anteriad shift of the man- skulls and of living adults shows no trace of dible then exposes the food to the sharply slop- cranial kinesis. [Since the preparation of this ing vertical aspects of the three tooth rows. report, one of us (C.G.)was able to examine two This angulation increases the probability that living specimens, each younger than 5 years. the cusps will hook into surface irregularities Neither showed any capacity for palatal of the prey; the forward slide of the mandible motility.] thus induces localized shear and cutting. The pattern of food reduction seen in In interpreting any of the several patterns Sphenodon would seem to represent an inter- seen, it remains critical to remember that the esting and important variant in the develop- stress induced and the strain effected in the ment of reptilian masticatory patterns. It is a prey surface will be less when more teeth or a rather specialized behavior, as most living rep- greater cutting surface contact the prey; other tiles use their feeding apparatus as an “organ things being equal, prey deformation or rup- of prehension” (Davis, ’61). The most signifi- ture is thus greatest for the cutting element cant aspect is probably indicated by that has fewest contact points. This, of course, Robinson’s comments (’76)about the “poor oc- assumes that the translational movement oc- clusal relationships.” One could even modify curs while the teeth are pressed together, as this comment to state that Sphenodon lacks they are in Sphenodon. Should the prey be im- occlusion of the kind seen in mammals. The paled on the dentary or held against it by the tooth rows do not meet but interdigitate. A tongue, it might then be slid past the palatine staggered interdigitation of tooth positions tooth array and its inertia would enhance rasp- may occur among the individual teeth of other ing or cutting of its surface. reptiles (crocodilians are a good example), but The crushing and shearing phases shown by Sphenodon shows an interdigitation of tooth Sphenodon have a markedly different signif- rows, rather than of individual teeth. On each icance for the two food types tested. In dealing side of the mouth, the food is contacted by two with the exoskeleton of relatively large hard sets of teeth onits dorsal and one set onits ven- prey, the closing movement must effect a ma- tral surface. The close approximation of the jor force so that the teeth will induce initial pterygoid flanges and coronoid processes as- penetration at high angles of incidence among sures that the mandible can only move parallel teeth and prey. This initial perforation by the to the upper tooth rows. The food object is thus crushing action weakens the exoskeleton, as it exposed to short-distance bending or shear, provides stress-concentrating points; the the effect of which differs with the consistency shearing phase then rips apart the armor. Al- of the prey. Consequently, we have here a food- though we did not test prey items with truly handling system unique in vertebrates. heavy exoskeletons, the large orthopterans The static forces applied to the dorsal and and beetles ingested by tuataras in the wild ventral tooth rows differ only slightly (the lat- probably represent the kinds of prey for which ter is greater by the mass of the bolus). this process in critical. However, the toothlprey contact area is likely For soft prey, the relative significance of 346 G.C.GORNIAK. H.I. ROSENBERG. AND C. GANS these two phases of each masticatory cycle dif- larger, less worn, and better able to perform fers. The initial bite then serves not only to the slicing action. There may be a trade-off as crush and incapacitate prey but also to fold up very large prey would, when placed between the soft tissues, compressing them against the the posteriormost teeth, require a very wide internal skeleton. To make the propalineal gape and thus place the crushing muscles into shearing movement effective, the direct a less advantageous portion of the length-ten- crushing force must continue to be applied; sion curve. This may be the reason why some thus compressors may be seen to fire at full of the dorsalmost crushing muscles (M. ad- level during the beginning of the sliding move- ductor mandibulae externus medialis, M. pseu- ment. (Continuation of compression during dotemporalis superficialis) have relatively long shearing may be visualized by considering the fibers that curve ventrolaterally and only start use of a sharp knife to cut a folded piece of to fire effectively after the mouth has partially fabric resting on a wooden block. If the blade closed. The placement of the pterygoid presses the fabric against the block, and then muscles suggests that, their activity should slides along the surface, all pleats and folds not shift on the length-tension curve, as dis- will be separated simultaneously. If the knife placement is relatively independent of gape only presses the cloth against the block in (see below). some regions, only these will be separated, the loose cloth will stretch and a much longer hor- Capture izontal movement is required for its separa- Sphenodon uses different approaches to cap- tion.) Thus, the effectiveness of cutting is ture small and large prey. Small prey are re markedly increased by holding the dorsal and trieved by rapid movement of the tongue, ventral tooth rows together during the slide. pulled into the back of the mouth and bitten in- The crushing also permits more rapid ap- itially between the cheek teeth. Large prey are proach of teeth to the internal skeleton of the captured by moving the head toward them, prey. When Sphenodon reduces adult birds or biting them while the tongue remains at rest mice, the relativeIy short mandibular cusps are and impaling them on the incisor-like succes- unlikely to reach bone until several shearing sional teeth. The difference may involve strokes have occurred. several factors. The combination of the crush-induced hold- Small prey are relatively flat and their bodies ing action and of the differential stress levels tend to be close to the ground; this would force noted at the upper and lower tooth rows have the tuatara to bend its neck sharply in order to major effects on the length of the stroke need- bring the jaws into position for the bite. Most ed for penetration. As the jaws close, the dis- small prey, such as crickets and cockroaches, tance between them decreases. This changes are also very mobile and acceleration of the the force application to the bolus from long tongue is less costly (and hence likely to be bending to shear and increases the risk of local more rapid) than that of the entire head. The failure of the integument and of the soft tis- adhesive mechanism for prey capture is in- sues in the prey. The greater local stresses im- herent in the dorsal surface of the tongue and posed by the mandibular teeth are more likely is reflected in its long, densely packed papillae to exceed the elastic limit of the prey than are and mucous cells (Gabe and Saint Girons, '64); the lower stresses induced where the bolus con- these give the tongue the appearance of a deep- tacts the upper jaw. Thus, the bolus is likely to pile carpet. Sphenodon rarely uses its tongue hang on the palatal surface and cutting will be during the capture of large and slowly crawling concentrated between bolus and mandibular prey, such as juvenile mice. Sphenodon then teeth. This means that the full anteriad stroke moves its snout close to the prey, opens its of the mandible induces a cut at a single site of mouth, and shifts it into position for a bite. The a fixed prey item. It assures maximal utiliza- projecting successional teeth will hold the soft tion of the rather limited capacity of the man- prey, even when the initial bite does not other- dible for propalineal movement. wise incapacitate it. Thus, Sphenodon cap Both the crushing and the shearing mech- tures prey with a pattern reflecting prey size, anism make the continuous posterior shift of configuration, and mobility. the prey advantageous. First of all, posterior Transport of prey also reflects its size, shift of the prey improves the effective me weight, and texture. Small prey is transported ment arm of the jaw. Secondly, the acrodont by the tongue; large prey is shifted by inertial dentition only adds additional cusps at the movements of the head. Large prey occupies rear; this assures that the posterior teeth are much of the oral cavity and thus limits move SPHENODON MASTICATION 347 ments of the tongue. Also, feathered and the anterior part of the tongue by passing it be furred prey provide poor surfaces for lingual tween the tips of the upper and lower jaws, and adhesion. then clean the floor and roof of the mouth by arcing the tongue and moving it posteriorly. Reduction After mice are reduced, Sphenodon again uses Sphenodon reduces both small and large the jaws to clean the tongue first but then uses prey with similar mandibular movements. Two the tongue to clean only the floor of the mouth. factors that may explain this stereotyped pat- Perhaps the fluid content of mice does not tern of movement are: 1)the limited degrees of adhere to the roof of the mouth, eliminating freedom of the cranial joints force the move- the need to clean it; also most cutting action ments to follow a set path, and 2) the activity takes place along the ventral surface of the pattern of the muscles generating the move- Prey. ments remains relatively constant throughout Myology and electromyography reduction sequences. General In Sphenodon, the degrees of freedom of the mandible are indeed limited by the position of The review of Haas ('73) indicates that the the tooth rows and the close approximation of head muscles of Sphenodon are similar to the pterygoid flanges and coronoid processes; those of a generalized lizard, but retain some this would by itself tend to produce the repeat- indications of arrangements primitive among able movement pattern observed. However, reptiles. The tuatara differs from squamates in even though the pattern of movement remains having an anterior M. pterygoideus atypicus. relatively constant, other aspects of the Also the separation among adjacent muscles is masticatory cycle, such as motor activity, less pronounced in Sphenodon than in lizards change with food type (Tables 2,3); so does the or snakes (Haas,'73). The latter condition may degree of head and tongue movement. Thus, reflect an absence of mobility among cranial whereas mandibular excursion is stereotyped elements, but it also raises the question because of the constraints of the hard tissues whether the muscular separation is retained and absence of intracranial movement from an earlier form with a less rigid skull. Al- (kinesis),the size and consistency of the food ternatively one may ask whether the described have significant effect on movements of the subdivisions are real or based upon expecta- head and tongue. tions derived from the study of squamates. For Throckmorton ('76)suggested that the slow instance, the two posteriormost portions of the opening may be assisted by gravity. However, M. adductor mandibulae externus medialis duration of the slow-opening phase during may be defined morphologically and have reduction of juvenile mice (weight 6-7 gm) is slight differences in fiber direction (and fiber twice that during reduction of crickets (0.3-0.6 length); however, their activity shows no sig- gm). If slow opening were gravity-assisted, it nificant differences. In contrast, the M. de- would be more rapid during the reduction of pressor mandibulae and M. adductor mandib- heavier than of lighter prey items. ulae externus superficialis sensu stn'cto are not The duration of the slow-openingphase does morphologically separated into distinct por- reflect the size of the food. Obviously, large tions, but their sections do differ in fiber length prey occupies more space within the oral cavi- and in activity pattern. ty than does small prey. Perhaps, as there is In Sphenodon, the anterior movement of the less space to manipulate it, the risk of loss is lower jaw during the shearing phase is an im- greater. However, prolongation of the slow- portant component of mastication. The M. opening phase increases the length of time the pterygoideus typicus is the largest single mus- prey is secured and decreases the risk of losing cle and its anteroposterior line of action directs it. By opening the mouth slowly and for a short the forces primarily anteriorly and to a small distance (beyond the diameter of prey), degree vertically and horizontally, even when Sphenodon can quickly snap it closed to keep the mouth is wide open. Thus, although the prey from slipping out of the mouth. MPTT is active during crushing, its maximum activity levels during reduction occur during Terminal the shearing phase, when movement of the During terminal movements, Sphenodon lower jaw follows the main line of action of the uses its tongue to clean the oral cavity in two muscle. Furthermore, the fixed quadrate of different ways. After reduction of crickets and Sphenodon would keep the main line of action cockroaches, Sphenodon seems first to clean of the MPTT in a constant anteroposterior 348 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS line. Smith (’80)notes the forward movement of bulae (MDM).The nearly vertical path of these the quadrate and activity of the M. pter- fibers to their insertion just posterior to the ygoideus of Varanus during closing. She quadratoarticular joint would simply rotate argues that a movable quadrate lets the M. the mandible about the quadratoarticular pterygoideus function as an adductor during joint, opening the mouth straight downward. ingestion, and moves the lower jaw anteriorly In the herbivorous lizard Uromastyx the during biting. However, Sphenodon also has a MDM inserts at the caudal end of the lower large M. pterygoideus, which clearly facilitates jaw, well posterior to the jaw joint; it is silent the generation of large forces during the shear- during slow opening (Throckmorton, ’78).This ing phase. Even though the M. pterygoideus of position and activity pattern are similar to Varanus may assist in closing the mouth, its those of the posterior portion of the MDM in size and primarily anteroposterior line of ac- Sphenodon. These results suggest that those tion suggest additional functions. Size and fibers of the MDM lying close to the joint may position indicate that the muscle would tend to induce slow opening of the mouth, whereas generate large propalineal forces during the those lying farthest away from the joint induce bite. These would be less important in shifting fast opening. Consequently, studies on rep- the lower jaw than in maintaining its position tilian feeding should examine not only various relative to the midline when prey is struggling subdivisions of the complex adductors, but or being shaken. also different areas of comparatively simple muscles, such as the MDM. Capture During a reduction cycle, the activities of the The activity pattern of most of the muscles superficial and deep adductors and the ptery- studied differs between the times during which goids allow them to be classified into three Sphenodon makes a capture bite and those in functional groups (Fig. 10). The first is the clos- which it engages in reduction cycles. These dif- ingcompressor group. It consists of the M. ad- ferences seem to reflect the need to 1) open the ductor mandibulae externus superficialis, the mouth rapidly during the capture bite (sothat M. adductor mandibulae externus profundus, the tongue can be quickly protruded), and 2) and the M. pseudotemporalis superficialis. The then to snap the mouth closed to secure and second group is the compressor-shear group. It kill the prey. Opening for a bite proceeds uni- consists of the M. pseudotemporalis profundus formly and fast; the slow-opening phase char- and the M. pterygoideus atypicus. The third acterizing reduction, terminal, and reposition- group is the shear group and it consists of the ing cycles is then absent. Consequently, both M. pterygoideus typicus. Group 1 generates portions of the M. depressor mandibulae be- closing forces that initially close the mouth come active bilaterally; in contrast, only the and then compress or crush the prey. Group 2 anterior portion of the muscle is active during generates compressive forces during crushing slow opening. The simultaneous firing at the but continues to apply these forces during start of opening not only rotates the mandi- shearing. Simultaneously, group 3 induces bles, but also induces posterior translation of anteriorly directed forces on the lower jaw and the fossa on the condyle, so that the mandible the food is compressed and sheared by action drops most rapidly. of groups 2 and 3. The activity levels of the ad- The closing movement is similarly distinct. ductors apparently reflect instantaneous local Not only do the various adductors fire more changes in tension due to changes in the con- symmetrically during capture than during a re- sistency and position of the bolus during duction bite, but the M. pterygoideus im- reduction cycles. mediately becomes active symmetrically. It Olson (’61)contrasted the concepts of “static contributes to the closing component and thus pressure” and “kinetic inertial” systems of jaw accelerates the jaw and adds to its impact, but mechanics. In the former the adductor muscles it also induces maximum propdined action at exert maximum force when the mouth is nearly the very beginning of closure. This brings the closed and thoroughly reduce the food. In the successional teeth into opposed position so latter, the adductors supposedly exert max- that they approach each other before closure, imum forces when the mouth is wide open, food rather than at the end of the shearing phase. is not reduced and the muscles apparently function for prey capture. In Sphenodon, the Reduction activity level of the adductors generally sup- In Sphenodon,slow opening is generated by ports the concept of a “staticpressure” system. the anterior portion of the M. depressor mandi- However, the activity levels generated by the SPHENODON MASTICATION 349

Fig. 10. Sphenodon punctatus. Lateral view of the skull groups. 1, Closing-compressor group; 2, compressor-shear showing a summary of the three mechanical adductor group: 3, shear group.

adductors of both the working and balancing these thus differ from activities recorded in sides change from bite to bite during a reduc- Sphenodon during reduction. These differing tion sequence; presumably these muscles res- activity patterns seem to relate to the degree pond to changes in the position and texture of to which the quadrate can move. In the bolus. (This pattern is equivalent to that Uromastyx, the guadrate is held only by supra- shown by some masticating mammals.) Thus, temporal and pterygoid. Thus, action of the the present results support the hypothesis of a MDM and MPTT not only moves the mandible “staticpressure” system only in that forces ex- about the quadrate but also increases mandib- erted by the adductors during an individual ular excursion by movement of the quadrate it- bite are greatest when the mouth is nearly self; these muscles may also function to stabi- closed. However, they conflict with the lize the quadrate. In Sphenodon, the quadrate hypothesis in that the forces generated by the is fixed and mandibular movements are re- adductors during a bite are not the maximum stricted to the quadratoarticular joint. Con- forces that these muscles are capable of exer- sequently, the activity patterns of at least the ting, nor are the forces generated then MDM and MPTT are apparently affected by equivalent among bites of a reduction se the degree of cranial kinesis. Unfortunately, quence. The concept of “maximum ” force in- we still lack detailed descriptions of feeding volves too many variables to be meaningful in movements and the activity patterns of the this context. other masticatory muscles in Uromastyx In the reduction cycles of Uromastyx aegyp- aegyptius or other lizards that show varying tius, the M. depressor mandibulae (MDM) is degrees of cranial kinesis. Thus, comparisons active when the mouth closes and the deep por- relating the degree of intracranial movements tion of the M. pterygoideus (MPTT) is active and the activity patterns of the masticatory when the mouth opens (Throckmorton, ’76); muscles are premature. 350 G.C.GORNIAK. H.I. ROSENBERG, AND C. GANS

Terminal teresting pattern emerges. The first example is given by the anterior and posterior portions of The fibers of the middle portion of the M. the M. depressor mandibulae. The fibers of the pterygoideus typicus (MPTT) lie anteropos- anterior portion are shorter than the posterior teriorly when the mouth is closed; activation of ones. The anterior portion also inserts close to these fibers would then tend to pull the mandi- the quadratomandibular joint and thus has a ble directly anteriorly. During terminal cycles, short moment arm. This anterior portion fires activity of the ventrolateral and medial and la- during slow opening, inducing initial separa- teral deep parts would bring the tips of the up- tion of teeth from the bolus. The muscle then per and lower jaws into close approximation, appears to be close to its resting length; how- but would not generate significant closing ever, the length-tension relation may not be forces on the mandible. Such activity, while particularly critical, as the muscle is then ac- the anterior part of the tongue pushes against tive only at a low level. Initially the teeth are the aligned tips of the jaws during terminal still embedded in the food and the muscle in- cycles, allows the mouth gradually to open duces pure rotation. After the start of the fast- while conforming to the shape of the pro- opening phase, muscular activity increases truding tongue; the incisor-like teeth are then and contributes to further opening; however, rubbed against the surface, cleaning the at this time the muscle incurs a slight relative tongue. lengthening as the mandible is translated pos- The fiber direction of the medial and lateral teriorly at the jaw joint: this might improve superficial parts of the MPTT suggests that it would also tend to move the mandible anterior- the length-tension relationship. The more posterior portion of the M. ly when the mouth is closed and that it would depressor mandibulae not only has a longer maintain the closed position. However, during terminal cycles the superficial part of the lever arm and much greater bulk, but has markedly longer fibers than the anterior por- MPTT is active coincident with the M. depres- tion. The former is active only when the mandi- sor mandibulae (MDM) as the mouth opens. ble is being rapidly depressed, inducing both Simultaneously, activity of the ventrolateral rotation and translation. Quite clearly the and lateral deep parts increases. Their actions much greater length of its fibers reduces form a bilateral force couple. These parts of the relative shortening and retains the muscle in MPTT and the MDM insert as a sling on the the advantageous portion of the length-tension posterior end of the articular. Upward pull by curve. the MDM rotates the mandible about the Similar patterns are seen in the fast-closing quadrate while the anterior pull of the MPTT and crushing movements. The anteriormost limits posterior translation of the mandible. portions of the MAMES have long fibers and Consequently, the mandible opens by simple the MAMEP has relatively short ones, al- rotation, accounting for the decrease in pro- though both muscles start the fast-closing palineal movement during terminal cycles. movement. The MAMEP has arelatively short lever arm, but the fibers of the MAMES lie su- perficially along the side of the face and have a Fiber length relationships relatively long lever arm. Toward the end of While the fiber lengths of the muscles con- fast closing (before the cusps reach firm con- sidered in this study differ by a ratio of almost tact with the prey), one notes the start of ac- 6 to 1, the extreme lengths are represented by tivity 1) of the posterior portion of the only three muscles. The dorsalmost (deep)por- MAMES, 2) of the three portions of the tions of the M. pterygoideus typicus and the MAMEM, and 3) of the MPTS. Four of these M. adductor mandibulae externus profundus five muscles show similar and relatively nar- have the shortest fibers and the posterior por- row ranges in fiber lengths, and the other tion of the M. depressor mandibulae has the (MPTS) shows a wide range. The MAMEM-a longest ones (Table 1).However, most muscles has the shortest; fibers and lever arm of the show a wide range of fiber lengths, with the ex- MAMEM complex; the posterior portion of the ception of such muscles as the M. pterygoideus MAMES also has shorter fibers and lever arm atypicus. Fiber lengths generally differ within than the anterior one. The short fibers of the subdivisions. This variability emphasizes the MPTS reach from the parietal straight ventral- importance of sampling many sites before ly to the basal aponeurosis, whereas its long assuming that the fiber length is constant. fibers curve laterad and then run ventrad. The When the fiber lengths are viewed in relation long fibers of the MAMEM also curve ventro- to their position and activity times, a very in- laterally and will in the resting position form SPHENODON MASTICATION 35 1 an angle of close to 40" in their course. Ap- reduction cycle is affected by the size of the parently these curving fibers are much food object. Similarly, the activity levels of the straighter when the mandible is fully de- adductors reflect the size and position of the pressed. Thus, those adductors in which the di- bolus. The increased adductor activity, when rection of action is straight dorsoventral have food is in contact with the teeth, suggests that short fibers and those in which the path of the the timing and level of adductor activity are muscle incurs a curve to a more posteriorly controlled by an oral afferent feedback system. displaced origin have long ones. Furthermore, Whether this feedback system is similar to in spite of their different origins, the lengths of that of mammals remains subject to test. The most fibers of the MAMEM and MPTS are present observations suggest the likelihood similar, though the latter has a group of deeply that the afferent information on the size and placed, short fibers. These similarities appear position of the bolus is derived from the sense to be achieved by the attachment of these organs of the tongue. muscles on various continuations of the basal The masticatory muscles of Sphenodon do aponeurosis rather than directly on the mandi- not have to restrain the jaw movements to the ble. propalineal plane, as the mechanical con- In the M. pterygoideus typicus (MPTT)the straints preclude lateral movements. In lizards origin of the fibers varies, whereas all of them with cranial kinesis, the muscles presumably insert in close juxtaposition. Thus, there is a have a greater role in guiding the movements regional change in fiber arrangement from of the jaw and in stabilizing cranial elements long-fibered parallel to short-fibered bipinnate. during the bite. One would expect more com- The long-fibered portion is apparently capable plex control systems in such cases. of greater absolute shortening than the short- In spite of this mechanical simplicity, the fibered one. It is activated before the short one neural control mechanism in Sphenodon ap- and induces the initial propalineal forces dur- pears to be relatively complex. Olfactory cues ing shearing. In contrast, the short fibers in- mediate the prey attack response and visual duce the forces at the end of the shearing cues are used to steer the capture of prey. The phase. The long, medial fibers would also in- size and position of the bolus are monitored duce a medial component to the force, which during reduction and will affect the activity of may be disadvantageous for generating propa- the masticatory, lingual, and nuchal mus- lineal movement. The medial component would culature. These oral sensory signals steer not shift the jaw very slightly toward the working only the overall food handling, but are ob- side at the start of shearing when the teeth are viously responsible for differences between the slightly separated. However, the line of action EMG patterns of successive cycles. of the short, lateral, bipinnate fibers is nearly straight anteriorly and parallel to the Phylogeny toothrows. Thus, at the end of the shearing phase these fibers tend to keep the lower teeth The capacity for inducing not only per- aligned between the upper rows while forating and crushing forces but for applying generating a final thrust to shear the food. The shear in an anterior-posterior direction may be fiber arrangement and parallel arrangement of critical in the further development of long and short fibers do raise some questions sphenodontid dentition, as well as in that of about preliminary firing patterns that may the rhynchosaurs (which may or may not be re- bring the fibers to a length at which stimula- lated to Sphenodon: Carroll, '77; Sill, '71). tion will induce effective action. These animals tend to widen the maxillary- palantine tooth area in which each row is corn- Neural control posed of an array of variously shaped teeth. The mandibular tooth row is much narrower Little is known about the neural mechanism and its teeth perhaps larger, a pattern that has controlling the feeding movements of lizards been variously ascribed to adaptation to a her- and of the activity patterns of the muscles bivorous diet. Cutting action by the upper generating them. Almost all work on the teeth would presumably require that the food neural control of mastication has been carried object move past them. This cutting action out on mammals (Dubner and Kawamura, '71; could occur only if the prey were impaled on Gans et al., '78). Three observations relate dentary teeth and cutting-slippage occurred generally to control systems and may deserve against the palatal surface. The effect here brief mention. would be equivalent to those achieved when The duration of the different phases of a the tooth cusps are widened and serve as slic- 352 G.C.GORNIAK, H.I. ROSENBERG, AND C. GANS ing or shaving devices while they move at right More important, the avoidance of the need for angles to the prey. a precise matching bite eliminated any tenden- Although this study does not deal with cy for later development of different kinds of fossils to any significant extent, the pattern in “molar occlusions.” The dentition in the sphen- Sphenodon permits some very interesting odontid upper jaw may be conceived as a mam- speculations. Most textbooks argue that malian molar row with a medial separation. It heterodonty and complex tooth shapes are presumably represented a significant advance characteristic of mammals and absent in Re- over a general crushing bite, but the solution cent reptiles. While this is an overstatement adopted may have blocked the path to continu- (Edmund, ’69), the pattern of mandibular ing development. movement is obviously more complex in modern mammals. The nature of the complexi- ACKNOWLEDGMENTS ty generally reflects translatory movements between the tooth rows. The preserved specimens derive from the col- Such translation has apparently arisen a lections of the American Museum of Natural number of times independently. Thus, it oc- History (AMNH, R.G. Zweifel), that of Cornell curs in turtles (Gaffney, ’75), in Sphenodon, University (CU, H. Pough), and the Carl Gans and presumably within the therapsid-mam collection at Ann Arbor (C.G.). We thank malian transition. In each case, this horizontal curators for facilitating loans and Dr. R.G. movement apparently involves sliding along Northcutt for the gift of dissected specimens. the craniomandibular joint and is independent We acknowledge grant BMS 71 01380 from of the phenomenon of cranial kinesis. The lat- the U.S. National Science Foundation (C.G.), ter primarily reflects movement between and grant DHEW-PHS-G-IROlDE05112from the about the occipital, the medial, and the nasal National Institutes of Health (C.G. and portions of the braincase, as well as between G.C.G.), and grant A-6062 from the Natural the variously fixed dental arcades and the Sciences and Engineering Research Council of quadratic suspension of the mandible. Canada (H.R.). Cinefluoroscopy was carried While translatory movements do occur in out at the Museum of Comparative Zoology some turtles, the broad crushing surfaces and facility of Dr. F.A. Jenkins with the assistance continuous cutting edges of the Testudines of Miss E. Gordon. We thank B. Clark, C. would involve few problems with occlusion. Leonard, and T. Scanlon for their aid with the The occlusion of dental arrays is assumed to be experiments; T. Rizki for provision of a refer- much more difficult to develop and in- ence; F. de Vree and A.P. Russell for comments vestigators have predicated a complex series on the manuscript; J. Beach and J. Fetcho for of stages with gradual development of addi- developing the computer software; and D. tional cusps and basins (Peyer, ’68). Luce and Teryl Lynn for preparing the ana- The solution found by the Rhynchocephalia tomic illustrations. (and rhynchosaurs) appears to reflect a rather simple avoidance of the occlusion problem. The teeth need never contact, and the wear marks LITERATURE CITED between them are as likely to reflect interac- Bock, W.J., and C.R. Shear (1972) A staining method for tion of tooth and prey as grinding of tooth on gross dissection of vertebrate muscles. Anat. Anz. 130:222-227. tooth. The system is effective even when the Byerly, T.C. 11925) The myology of Sphenodon puntatum. inter-row distance changes. Local variants in U. Iowa Stud. Nat. Hist. 11/6):3-51. tooth shape have much less effect than do Carroll, K.L. (19771 The origin of lizards. In S.M. 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