Prey Transport Mechanisms in Blindsnakes and the Evolution of Unilateral Feeding Systems in Snakes1

Home , Alethinophidia, Anomalepididae, Anomalepis, Anomochilus, Leptotyphlops, Ophidia

AMER.ZOOL., 41:1321±1337 (2001)

NATHAN J. KLEY2 Organismic & Evolutionary Biology Program, University of Massachusetts, Amherst, Massachusetts 01003

SYNOPSIS. Most snakes ingest and transport their prey via a jaw ratcheting mechanism in which the left and right upper jaw arches are advanced over the prey in an alternating, unilateral fashion. This unilateral jaw ratcheting mechanism differs greatly from the hyolingual and inertial transport mechanisms used by lizards, both of which are characterized by bilaterally synchronous jaw movements. Given the well-corroborated phylogenetic hypothesis that snakes are derived from lizards, this suggests that major changes occurred in both the morphology and motor control of the feeding apparatus during the early evolution of snakes. However, most previous studies of the evolution of unilateral feeding mechanisms in snakes have focused almost exclusively on the morphology of the jaw apparatus because there have been very few direct observations of feeding behavior in basal snakes. In this paper I describe the prey transport mechanisms used by representatives of two families of basal snakes, Leptotyphlopidae and Typhlopidae. In Leptotyphlopidae, a mandibular raking mechanism is used, in which bilaterally synchronous ¯exions of the lower jaw serve to ratchet prey into and through the mouth. In Typhlopidae, a maxillary raking mechanism is used, in which asynchronous ratcheting movements of the highly mobile upper jaws are used to drag prey through the oral cavity. These ®ndings suggest that the unilateral feeding mechanisms that characterize the majority of living snakes were not present primitively in Serpentes, but arose subsequently to the basal divergence between Scolecophidia and Ale- thinophidia.

INTRODUCTION highly reduced tongue that lacks a frictional Three fundamental modes of intraoral surface (McDowell, 1972; Schwenk, 1988). prey transport are recognized within Squa- Finally, snakes use gnathic (jaw-based) mata. Most lizards use a hyolingual trans- transport mechanisms, in which kinetic el- port mechanism, in which cycles of tongue ements of the jaw apparatus are used to protraction and retraction serve to ratchet ratchet prey into and through the mouth prey through the mouth and towards the (Cundall and Greene, 2000). While both pharynx (Smith, 1984; Herrel et al., 1996; hyolingual and cranioinertial transport are Schwenk, 2000). In some lizards, however, common among tetrapods, gnathic transport this lingual ratcheting mechanism is aug- mechanisms are unique to snakes (Bramble mented or replaced by a cranioinertial and Wake, 1985). transport mechanism, in which rapid move- Nearly all of what is currently known ments of the entire head are used to propel about gnathic transport in snakes derives prey through the oral cavity (Gans, 1969; from studies of taxa belonging to Macro- Bramble and Wake, 1985). This mode of stomata (Fig. 1), a large and diverse clade intraoral transport is of particular impor- that includes approximately eighty-®ve per- tance in varanid lizards (Smith, 1986; Elias cent of the more than 2,500 species of ex- et al., 2000), which share with snakes a tant snakes (McDiarmid et al., 1999). These studies have shown that most macrostomatans ingest and transport their prey via a 1 From the Symposium Motor Control of Vertebrate ``pterygoid walk'' mechanism (Boltt and Feeding: Function and Evolution presented at the An- nual Meeting of the Society for Integrative and Com- Ewer, 1964), in which reciprocating ratch- parative Biology, 3±7 January 2001, at Chicago, Illinois. eting movements of the medial upper jaw 2 E-mail: [email protected] arches, combined with lateral rotations of 1321 1322 NATHAN J. KLEY

mechanism that he termed ``snout shifting'' in the anilioid Cylindrophis (Fig. 1). Like the pterygoid walk, snout shifting involves unilateral movements of the toothed elements of the upper jaws, combined with side-to-side movements of the entire head, which together serve to advance the head over the prey. However, the upper jaws in Cylindrophis (and in other anilioids) remain tightly bound to the ventral elements of the bony snout (e.g., vomers, septomaxillae) by several short, robust ligaments. These ligaments prevent extensive translational movements of the jaws such as those which are associated with the pterygoid walk in macrostomatans. Independent movements of the upper jaws are instead achieved through lateral rotations of the entire snout complex about the nasofrontal articulation (prokine- sis; Frazzetta, 1962) and independent translational movements of the left and right FIG. 1. Phylogenetic hypothesis of relationships of septomaxilla-vomer complexes to which the major groups of snakes, modi®ed from Tchernov the upper jaws are bound (rhinokinesis; et al. (2000). Interrelationships of the three scoleco- Cundall and Shardo, 1995). Thus, in certain phidian families (Leptotyphlopidae, Typhlopidae and Anomalepididae) after Cundall et al. (1993). Fossil respects, Cylindrophis represents an inter- taxa are indicated by a dagger (²). mediate functional stage between lizards and macrostomatan snakes (Cundall, 1995); despite retaining a tight connection between the entire head about the cranio-vertebral the upper jaws and the snout (as in lizards), joint, serve to advance the snake's head prey is transported via a unilateral jaw over its prey (Dullemeijer, 1956; Albright ratcheting mechanism (as in macrostoma- and Nelson, 1959a, b; Frazzetta, 1966; Kar- tans). dong, 1977; Cundall and Gans, 1979; Cun- The discovery of snout shifting in Cylin- dall, 1983; Kardong, 1986). Because this drophis, and its likely presence in other an- unilateral jaw ratcheting mechanism differs ilioids such as Anilius (Gans, 1961; Cun- greatly from both the hyolingual and cran- dall, 1995), suggests that the pterygoid ioinertial transport mechanisms of lizards walk is unique to Macrostomata, but that (Kardong and Berkhoudt, 1998; Cundall, the unilateral jaw displacement pattern 1995), its origin has been somewhat enig- common to both snout shifting and the pter- matic, and there have thus been numerous ygoid walk is primitive for Alethinophidia attempts made to determine the evolution- (Fig. 1). Whether this unilateral jaw dis- ary steps through which it arose (e.g., Gans, placement pattern is unique to Alethinophi- 1961; Rieppel, 1980; Lee et al., 1999; Kar- dia is unknown, however, because the feed- dong and Bels, 2001). However, most stud- ing mechanisms of the three families of ies that have addressed the evolutionary or- blindsnakes (Scolecophidia; Fig. 1) have re- igin of unilateral feeding mechanisms in mained largely unknown (Kardong et al., snakes have been conducted from an almost 1997). The feeding behavior of these tiny, exclusively anatomical perspective because secretive snakes is known only from a few the actual feeding mechanisms used by bas- brief accounts (Smith, 1957; Reid and Lott, al snakes have remained largely unknown. 1963; Thomas, 1985; Webb and Shine, Recently, Cundall (1995) provided the 1993b; Kley and Brainerd, 1999), and thus ®rst detailed account of feeding behavior in a detailed understanding of feeding me- a basal snake, describing a prey transport chanics in the group is lacking. In this paper FEEDING IN BLINDSNAKES 1323

FIG. 2. Schematic diagram of the apparatus used for magni®ed high-speed videography.

I describe the prey transport mechanisms sunk into the ventral surface of the head, used by representatives of two families of feeding trials were recorded from a ventral Scolecophidia (Leptotyphlopidae and Ty- perspective. The snakes were fed in a clear phlopidae) in an effort to elucidate the phy- acrylic ®lming chamber (6 ϫ 13 ϫ 34 mm) logenetic origin of unilateral feeding mech- positioned above an inverted Nikon SMZ- anisms in snakes. U dissecting microscope that was coupled to a Kodak EktaPro high-speed video sys- MATERIALS AND METHODS tem. Feeding sequences were recorded at The blindsnakes used for this study were 250 fps (shutter speed, 1/500 sec) and then purchased from commercial herpetological transferred to S-VHS videotape using a suppliers. Feeding behavior was observed Panasonic AG-1970 VCR. Selected video in one species of Leptotyphlopidae (Lep- sequences were digitized using Adobe Pre- totyphlops dulcis (Baird and Girard), n ϭ miere software on a Power Macintosh G3 20) and two species of Typhlopidae (Ty- computer and jaw movements were ana- phlops lineolatus Jan, n ϭ 5; Rhinotyphlops lyzed frame-by-frame using NIH Image schlegelii (Bianconi), n ϭ 5). The snakes software. Additional feeding trials were re- were fed larvae and pupae of several spe- corded at 60 fps with a Sony DCR VX700 cies of ants (most frequently species of digital camera. Finally, several feeding tri- Camponotus, Formica and Acanthomyops) als for T. lineolatus were recorded using vi- collected in the vicinity of Amherst, Mas- deo¯uoroscopy. X-ray videos were record- sachusetts. Ant pupae ranged in size from ed at 60 fps using a Sony DCR VX1000 1.3 ϫ 3.0 mm to 3.4 ϫ 8.4 mm, while the digital camera that was coupled to a Sie- larvae were generally smaller, often less mens radiographic unit equipped with a Si- than 1 mm in diameter. recon image intensi®er. In these feeding tri- Feeding trials for 10 individuals of Lep- als, ant pupae were injected with an aque- totyphlops dulcis and 1 individual of Ty- ous barium sulfate solution so that they phlops lineolatus were recorded using mag- could be visualized throughout intraoral ni®ed high-speed videography (Fig. 2). transport and swallowing. (Unfortunately, all but one of the typhlopids The cranial morphology of all three spe- observed during this study refused to feed cies of blindsnakes was studied primarily under the conditions required for this tech- through microdissections and the examina- nique.) Several hundred feedings were re- tion of cleared and stained skeletal prepa- corded for each species. Because the mouth rations. Microdissections were performed in blindsnakes is subterminal and counter- on 5 Leptotyphlops dulcis,4Typhlops li- 1324 NATHAN J. KLEY neolatus and 3 Rhinotyphlops schlegelii to published elsewhere (Kley, in preparation). examine the myology of the jaw apparatus Descriptions of the cranial anatomy of other in each species. Because of the extraordi- species of Leptotyphlops are provided by narily small size of L. dulcis (2.2±3.0 mm Haas (1930, 1959), McDowell and Bogert head diameter, mean ϭ 2.6 mm), specimens (1954), List (1966), Brock (1932), and Ab- of this species were generally dissected in deen et al. (1991a, b, c). water or in 70% ethanol, and the entire head One of the most peculiar features of the of each specimen was frequently immersed jaw apparatus in Leptotyphlops dulcis is the in Lugol's iodine solution (Weigert's vari- complete lack of teeth in the upper jaws ation) to facilitate differentiation between (viz., the maxillae, palatines and ptery- closely apposed muscle layers (Bock and goids; Fig. 3A). Within Serpentes, this con- Shear, 1972). Following these dissections, 5 dition is unique to Leptotyphlopidae L. dulcis,3T. lineolatus and 2 R. schlegelii (Greene, 1997). Furthermore, the upper jaw were cleared and stained according to a pro- arches are relatively immobile due to tight tocol modi®ed from Hanken and Wassersug ligamentous connections between the max- (1981) and 2 L. dulcis,1T. lineolatus and illae and other elements of the rigid snout 1 R. schlegelii were prepared as dried skel- complex (especially the premaxilla and pre- etons using small dermestid beetle larvae. frontals). As a result, ratcheting movements The bones, cartilages, ligaments and joints of the upper jaws like those associated with of the jaw apparatus were examined and prey transport in alethinophidian snakes are manipulated in each of these skeletal prep- not possible in Leptotyphlops. Also, in con- arations under a Nikon SMZ-U stereo dis- trast to most alethinophidians, the ligamen- secting microscope. In addition, the heads tous connection between the posterior part of 3 specimens of L. dulcis were decalci- of the pterygoid and the distal part of the ®ed, dehydrated and embedded in low-vis- quadrate is extremely weak, visible only in cosity nitrocellulose (Thomas, 1983) and histological sections as a faint band of serially sectioned at 30 ␮m in transverse, loosely arranged connective tissue. Thus, frontal and sagittal planes. Sections were the lower jaw is functionally decoupled stained with Hematoxylin and Picro-Pon- from the upper jaws in Leptotyphlops. ceau (Humason, 1979; Thomas, 1983) and In contrast to the upper jaws, however, examined using a Zeiss Axioskop com- the lower jaw of Leptotyphlops bears teeth pound microscope to verify the relation- and is highly kinetic. The mandible itself is ships of cranial elements determined from relatively short and is suspended from the alcoholic and cleared and stained speci- braincase by the exceptionally long, antero- mens. ventrally directed quadrates (Fig. 3A). The proximal end of each quadrate articulates RESULTS with the braincase in a relatively loose slid- Magni®ed high-speed videography re- ing joint. A single row of four or ®ve teeth vealed that both Leptotyphlops dulcis and is present on each dentary, representing the Typhlops lineolatus ingest and transport only teeth in the skull. Because of the their insect prey using rapid jaw ratcheting somewhat cupped shape of the enlarged lat- mechanisms. However, the transport mech- eral ¯anges of the dentaries, these tooth anisms used by these species differ radical- rows are oriented nearly transversely across ly from one another, and neither resembles the anterior margin of the lower jaw (Fig. the unilateral jaw ratcheting mechanisms 3B, left). Moreover, each mandibular ramus used by alethinophidian snakes. is divided into separate anterior and posterior halves by a highly mobile intramandi- Leptotyphlops bular joint. This joint is formed by contact Morphology of the jaw apparatus. Only between the posterior end of the splenial, a brief description of the relevant structures which is closely applied to the ventromedial of the jaw apparatus of Leptotyphlops is surface of the dentary, and the anterior end presented here. A more detailed account of of the angular, which runs along the ventro- the cranial morphology of L. dulcis will be lateral surface of the compound bone (Fig. FEEDING IN BLINDSNAKES 1325

FIG. 3. Cranial morphology and jaw mechanics in Leptotyphlops dulcis. Drawings were made from a cleared and stained adult specimen. A. Left lateral view of the skull. Note the well-developed intramandibular (splenial- angular) joint and the absence of teeth on the upper jaw elements (pterygoid, palatine and maxilla). (The ventrally directed projections on the maxilla are features of the bone itself, and the size and form of these projections vary widely between individuals.) B. Ventral view of the lower jaw during protraction (left) and retraction (right). Note that during retraction, the dentary-splenial complex rotates medially about the intramandibular joint and also caudally about its own long axis. Abbreviations: a, angular; c, coronoid; cb, compound bone; d, dentary; m, maxilla; p, palatine; pt, pterygoid; q, quadrate; s, splenial. Modi®ed from Kley and Brainerd (1999).

3A). Because of the rounded articular facets The distal tips of the dentaries are round- on both the splenial and angular, and the ed and do not contact one another anteriorly reduced dorsal contact between the dentary (Fig. 3B). However, Meckel's cartilage, and post-dentary bones (e.g., coronoid and which persists throughout nearly the entire compound bone), the anterior half of each length of the lower jaw, provides a tight mandibular ramus (dentary ϩ splenial) is linkage between the mandibular rami. The capable of extensive rotation about the in- left and right halves of this cartilage exit tramandibular joint in all planes. However, the distal tips of the dentaries, curve dor- lateral and ventral rotations of the dentary- somedially, and fuse together to form a ro- splenial complex are checked by several bust cartilaginous nodule at the midline. ligaments that span the intramandibular This cartilaginous linkage severely limits joint. both lateral separation and independent an- 1326 NATHAN J. KLEY teroposterior excursions of the tips of the tal plane about the splenial-angular (intramandibular rami, but allows extensive ro- mandibular) joint. As a result of this move- tation between the left and right anterior ment, both the intramandibular joints and mandibular segments. In addition, this nod- the distal ends of the quadrates were forced ule of cartilage between the tips of the man- laterally. At the same time, however, each dibular rami serves as the site of origin for anterior mandibular segment was also ro- the extraordinarily robust median tendon of tated caudally about its own long axis (Fig. the M. genioglossus. A large slip of this 3B, right). The combined result of these muscle extends caudally beyond the lingual movements was that the transversely ori- sheath to insert onto the posteriorly posi- ented dentary tooth rows were rotated cau- tioned, Y-shaped hyoid which, on average, dally into the mouth, thereby dragging the is located between the 14th and 19th pre- prey toward the snake's esophagus. caudal vertebrae in Leptotyphlops dulcis. The rapid jaw movements associated This hyoid portion of the M. genioglossus with ingestion and prey transport in Lep- (a likely homologue of the M. mandibulo- totyphlops were usually augmented by syn- hyoideus II of lizards) is unique to Lepto- chronized movements of the anterior por- typhlopidae among snakes (Langerbartel, tion of the trunk. During jaw protraction, 1968; Groombridge, 1979). the neck was ¯exed slightly in the vertical Feeding mechanics and behavior. When plane, forming a shallow arch over the sub- presented with ant larvae and pupae, indi- strate. Then, during subsequent jaw retrac- viduals of Leptotyphlops dulcis quickly be- tion, the neck was straightened, thereby gan to exhibit characteristic frenzied feed- pushing the braincase anteriorly as the lowing behavior. The snakes began to feverish- er jaw was pulling the prey caudally. Thus, ly sway their heads and necks from side to as in alethinophidian snakes, movements of side in an attempt to locate potential food the anterior trunk supplement jaw move- items. Once the snout contacted an ant larva ments during prey transport in Leptotyph- or pupa, the snake would slide the ventral lops. In contrast to the concertina-like surface of its snout over the top of the prey movements seen in alethinophidians (Cun- until the prey item was positioned at or near dall, 1995; Kley and Brainerd, 1996; Moon, the front of the mouth. In some instances, 2000), however, axial bending during prey the snake would actually pin its prey transport in Leptotyphlops is restricted to against the substrate with its snout prior to the vertical plane. Finally, it should be em- initiating ingestion, but this was not a nec- phasized that while the ventro¯exion asso- essary pre-requisite for successful inges- ciated with prey transport in Leptotyphlops tion. Once the snake had positioned its may result in the prey being forced against mouth near the prey, it would then open its the substrate, this is neither a necessary nor mouth widely and grasp the prey between a common aspect of feeding behavior in its jaws. these snakes (contra Reid and Lott, 1963). In all feedings that were observed, Lep- Once the prey was transported to the rear totyphlops dulcis ingested and transported of the mouth, Leptotyphlops dulcis initiated ant larvae and pupae using a rapid mandib- swallowing with a forceful compression of ular raking mechanism (Kley and Brainerd, the pharynx. After the prey was forced into 1999). Immediately following mouth open- the esophagus through pharyngeal com- ing, the snakes initiated bilaterally synchro- pression, swallowing appeared to occur en- nous cycles of lower jaw ¯exion in which tirely through peristalsis. No axial bending the toothed anterior mandibular segments was observed during swallowing. were rapidly (2±3 Hz) rotated in and out of Muscular control of jaw movements. the mouth to drag prey into and through the Leptotyphlopid snakes are among the most oral cavity (Fig. 3B). This mandibular rak- highly miniaturized tetrapods. Even in the ing mechanism involved complex move- largest species of Leptotyphlops, maximum ments at the intramandibular joints. Each head diameter rarely exceeds 5 mm. Thus, anterior mandibular segment (dentary ϩ electromyography of head muscles in these splenial) was rotated medially in a horizon- snakes was not feasible. However, micro- FEEDING IN BLINDSNAKES 1327 manipulations of both fresh and cleared and the upper jaw arches bear teeth and are stained specimens provided useful, albeit highly mobile. limited, insight into the muscular control of In both Typhlops and Rhinotyphlops, the the mandibular raking mechanism. mandible is much longer than in Leptotyph- The results of these manipulations lops, and is suspended from the braincase strongly suggest that jaw retraction in Lep- via the relatively short quadrates (Fig. 4A). totyphlops is powered primarily by the long The dentary is greatly reduced and lacks and robust M. genioglossus, pars hyoidea, teeth, a condition that is unique to typhlo- which runs from the cartilaginous nodule pids among snakes. As in Leptotyphlops, between the distal tips of the mandibular the left and right halves of Meckel's carti- rami to the posteriorly positioned hyoid ap- lage are bound together by an expanded in- paratus. Indeed, by applying a caudally di- terramal cartilaginous nodule, an arrange- rected force to the tendon of the M. genio- ment which prevents independent move- glossus, the movements of the anterior ments of the left and right mandibular rami. mandibular segments that were observed However, in sharp contrast to the condition during feeding were replicated almost pre- seen in Leptotyphlops, there is extensive cisely. In contrast, jaw protraction in Lep- contact between the relatively long splenial totyphlops appears to be powered mainly by and the large, triangular coronoid. Thus, the the M. geniohyoideus. This complex strap intramandibular joint is bridged completely muscle has a lateral head, originating from by the splenial (Fig. 4A), and consequently, the lateral surface of the trunk muscles in the lower jaws of Typhlops and Rhinotyph- the cervical region, and a medial head, orig- lops are relatively rigid and akinetic. inating from the hyoid. Both heads con- In contrast to the lower jaw, the upper verge to insert via tendons onto the ventro- jaws of both Typhlops and Rhinotyphlops posterior surface of the dentary. The action are exceptionally kinetic. The maxillae lie of the M. geniohyoideus is to rotate the an- horizontally against the roof of the mouth terior mandibular segments laterally about with their transversely oriented tooth rows the intramandibular joints and also rostrally directed posteriorly (Fig. 4A, B, C), and are about their own long axes, thus rotating the suspended largely by ligaments and mus- dentary tooth rows outwards to their resting cles rather than through bony articulations. position. It is likely, however, that contrac- In particular, a robust ligament running tion of the M. intermandibularis complex from the canaliculate anterior end of the and elastic recoil of Meckel's cartilage also maxilla to the posterolateral margin of the contribute to jaw protraction. premaxilla (the premaxillo-maxillary ligament) anchors the anterior end of the max- Typhlops and Rhinotyphlops illa (Fig. 4A, C). Posteriorly, the maxilla is Morphology of the jaw apparatus. As for suspended by the M. retractor maxillae,a Leptotyphlops, only a brief description of large muscle that takes its origin from the the typhlopid jaw apparatus will be pre- lateral surface of the braincase and inserts sented here. More comprehensive treat- onto the posterodorsal surface of the max- ments of the cranial anatomy of other ty- illa. phlopid species are provided by Haas The palatine is the only bone that con- (1930), Smit (1949), List (1966) and Ior- tacts the maxilla directly. This bone has a dansky (1997). complex arched shape, with a medial pro- In nearly every major respect, the mor- cess that articulates with the posterolateral phology of the jaw apparatus of Typhlops margin of the vomer (Fig. 4C), and a lateral lineolatus was found to agree completely process that curves ventrally to insert into with that of Rhinotyphlops schlegelii. How- a shallow groove on the dorsal surface of ever, the jaw morphology of both of these the maxilla (Fig. 4B). Near the midpoint of taxa differs profoundly from that of Lep- the palatine, there is a slight ventral process totyphlops dulcis. Most signi®cantly, the that is embraced by the forked anterior end lower jaws of Typhlops and Rhinotyphlops of the pterygoid (Fig. 4C). As in Lepto- are toothless and relatively rigid, whereas typhlops, the pterygoid in Typhlops and 1328 NATHAN J. KLEY

FIG. 4. Cranial morphology and jaw mechanics in Typhlops lineolatus. Drawings were made from a cleared and stained adult specimen. A. Left lateral view of the skull. Note the horizontally positioned maxillae and the absence of teeth on the lower jaw. B. Dorsal view of the skull, showing the sliding articulation between the lateral process of the palatine and the dorsal surface of the maxilla. C. Ventral view of the skull, showing the articulation between the medial process of the palatine and the posterolateral edge of the vomer. Note the robust premaxillo-maxillary ligaments which anchor the anterior ends of the maxillae. D. Ventral view of the skull during maxillary raking, showing asynchronous retraction of the maxillae. The lower jaw has been removed to permit an unobstructed view of the upper jaws. Abbreviations: c, coronoid; cb, compound bone; d, dentary; m, maxilla; p, palatine; pml, premaxillo-maxillary ligament; pt, pterygoid; q, quadrate; s, splenial; v, vomer.

Rhinotyphlops is a long and slender bone ated a tactile search for individual prey that is widely separated from the quadrate items by rapidly sweeping its head from (Fig. 4C). Thus, the upper and lower jaws side to side in an erratic fashion as it pro- are functionally decoupled as in Leptotyph- gressed forward. Once the snake's head lops. In both Typhlops and Rhinotyphlops, contacted an ant larva or pupa, the snake the pterygoid is suspended from the ventral maneuvered its head so that its mouth was surface of the braincase by the robust M. positioned directly over the prey. The snake protractor pterygoidei, which originates would then open its mouth to initiate cap- from the ventral surface of the braincase ture and ingestion. and courses posteroventrally to ensheathe In all feedings that were observed, Ty- the posterior end of the pterygoid. phlops lineolatus and Rhinotyphlops schle- Feeding mechanics and behavior. Like gelii ingested and transported their prey us- Leptotyphlops, Typhlops and Rhinotyphlops ing a rapid maxillary raking mechanism. As exhibited somewhat frenzied feeding be- the mouth was opened over an ant larva or havior when presented with ant brood. pupa, the snake initiated ratcheting move- Soon after a snake detected the presence of ments of the upper jaws in which the prey (presumably via chemosensory cues toothed maxillae were rapidly (3±5 Hz) ro- obtained through tongue-¯icking), it initi- tated in and out of the mouth. These max- FEEDING IN BLINDSNAKES 1329 illary raking movements served to drag the tion, prey were frequently ¯ipped up over prey caudally into the mouth and towards the anterior margin of the lower jaw, an ac- the throat. tion that tended to align the long axis of the The jaw movements associated with prey with that of the snake's head. maxillary raking in Typhlops and Rhino- Unlike the smaller Leptotyphlops, Ty- typhlops were more variable than those in- phlops and Rhinotyphlops often ingested volved in the mandibular raking mechanism multiple prey items before swallowing of Leptotyphlops. Most frequently, both in- them. Once the pharynx was ®lled, the gestion and intraoral transport were char- snake initiated swallowing with a forceful acterized by asynchronous jaw movements contraction of the throat muscles immedi- in which the left and right maxillae were ately ventral to the pharynx, followed by protracted and retracted slightly out of wavelike muscular contractions propagated phase with one another (Fig. 4D). In some along the ventral surface of the neck. The instances, however, only a single maxilla prey was then rapidly propelled along the was used during ingestion. This generally remainder of the esophagus, presumably via occurred when a snake was attempting to peristalsis. Like Leptotyphlops, Typhlops ingest an ant larva or pupa that was posi- and Rhinotyphlops exhibited no axial bend- tioned to one side of its mouth rather than ing during swallowing. directly below it, or when a snake was try- Muscular control of jaw movements. ing to extract prey from a narrow, con®ned Several previous studies have analyzed the space. potential movements of the jaw apparatus Movements of the lower jaw were also in typhlopids and their muscular control somewhat variable. In the majority of feed- (Haas, 1930; Evans, 1955; Iordansky, ings observed, ingestion was completed 1997). However, all of these studies were with a single maxillary retraction. In such based exclusively on anatomical evidence. instances the lower jaw was abducted dur- My observations of feeding in live Ty- ing maxillary protraction and then adducted phlops lineolatus and Rhinotyphlops schle- during maxillary retraction. However, in- gelii, combined with the brief accounts of gestion of larger prey required several max- Thomas (1985) and Webb and Shine illary protraction-retraction cycles. In these (1993b) for Typhlops richardi and Rampho- instances, the lower jaw remained partially typhlops nigrescens, respectively, provide adducted throughout most of the maxillary some corroboration of the functional hy- protraction phase, presumably to prevent potheses generated through these morpho- the advancing maxillae from pushing the logical investigations. prey back out of the mouth. Finally, during High-speed video recordings of Typhlops the rapid ingestion of large numbers of rel- lineolatus reveal that the tooth-bearing pos- atively small prey, movements of the lower terior ends of the maxillae are rotated jaw were largely independent of upper jaw through an arc of greater than 90Њ during movements. Under these circumstances, the jaw protraction. Given that neither of the lower jaw generally remained abducted as muscles inserting onto the maxillae (M. re- the maxillae continued to rake prey into the tractor maxillae and M. pterygoideus) have mouth. In this manner, multiple prey items origins that are anterior to the maxillae, the were often ingested simultaneously. observed rotations of these elements are in- It should be emphasized that no appre- ferred to be produced indirectly through ciable protraction of the lower jaw was ever movements of the pterygoid and palatine observed in either Typhlops lineolatus or bones. As noted by Evans (1955), the ap- Rhinotyphlops schlegelii, and the mandible plication of an anteriorly directed force to was never used to scoop prey off of the the pterygoid causes the arched palatine to substrate as predicted by Iordansky (1981, pivot about its medial connection with the 1990, 1997). However, prey items that were vomer, resulting in the lateral process of the initially positioned unfavorably for ef®cient palatine being displaced anteriorly and ven- ingestion were in some instances reoriented trally, thereby erecting the maxilla. The by the mandible. During maxillary retrac- only muscle capable of producing this an- 1330 NATHAN J. KLEY terior translation of the pterygoid is the M. mechanisms that might be used by these protractor pterygoidei, which originates snakes: 1) suction feeding (Haas, 1964, from the ventral surface of the braincase 1968; Groombridge, 1979); 2) lingual trans- and courses posteroventrally to ensheathe port (McDowell, 1972); and 3) gnathic the caudal end of the pterygoid. Thus, as (jaw-based) transport (Haas, 1930, 1962, suggested by previous authors (Haas, 1964; 1964, 1968; Iordansky, 1981, 1997). Nei- Cundall and Rossman, 1993; Iordansky, ther suction feeding nor lingual feeding 1997), erection of the maxilla appears to have ever been documented in any snake occur through the action of the M. protrac- and I found no evidence for either in Lep- tor pterygoidei. totyphlops, Typhlops or Rhinotyphlops. In- My observations of the cranial muscula- stead, all three species observed during the ture of Typhlops lineolatus and Rhinotyph- course of the present study used their jaws lops schlegelii, together with those of Haas to capture, ingest and transport their insect (1930) for T. punctatus, T. lumbricalis and prey. However, both the mandibular raking Ramphotyphlops bituberculatus and those mechanism of Leptotyphlops and the max- of Iordansky (1997) for T. lumbricalis and illary raking mechanism of Typhlops and T. vermicularis strongly suggest that the Rhinotyphlops differ signi®cantly from the primary retractor of the upper jaw is the M. jaw ratcheting mechanisms of alethinophi- retractor maxillae. This is a very large dian snakes. muscle of uncertain homology (Lakjer, 1926; Haas, 1930, 1973) that is unique to Mandibular raking Typhlopidae. It has a broad origin over the The mandibular raking mechanism of lateral surface of the braincase and inserts Leptotyphlops differs profoundly from the onto the posterodorsal portion of the max- feeding mechanisms of other snakes in that illa. While other muscles are likely to par- prey is transported by bilaterally synchro- ticipate in upper jaw retraction (e.g., M. nous movements of the lower jaw rather pterygoideus and M. retractor pterygoidei), than by independent movements of the up- the size, position and ®ber orientation of the per jaws. Among the more than 2,500 liv- M. retractor maxillae, together with its di- ing species of snakes, mandibular transport rect insertion onto the maxilla, suggest that mechanisms are known elsewhere only in a it is largely responsible both for retracting small number of cochleophagous (snail-eat- the upper jaw and rotating the maxilla back ing) colubrids of the subfamilies Dipsadi- to its resting position. nae and Pareatinae (Cundall and Greene, 2000). In these taxa, the mandible is used DISCUSSION to pull snails from their shells. However, Although the foraging strategies (Wat- the snail extraction mechanisms used by kins et al., 1967; Gehlbach et al., 1971; these highly specialized colubrids involve Webb and Shine, 1992) and dietary habits unilateral ratcheting movements of the left (Punzo, 1974; Webb and Shine, 1993a; and right mandibular rami (Sazima, 1989) Webb et al., 2000; Torres et al., 2000) of and thus bear little resemblance to the bi- scolecophidian snakes have been studied in laterally synchronous mandibular raking some detail, the feeding behavior of these mechanism of Leptotyphlops. Furthermore, diminutive serpents has been known only bilaterally synchronous jaw movements are from a few brief accounts (Smith, 1957; generally restricted to prey capture in ale- Reid and Lott, 1963; Thomas, 1985; Webb thinophidians (e.g., Frazzetta, 1966; Kar- and Shine, 1993b; Kley and Brainerd, dong, 1974; Cundall, 1987; Cundall and 1999). The actual mechanisms by which Deufel, 1999). Only rarely do such move- blindsnakes capture, ingest, transport and ments occur during prey transport, and swallow their prey have remained largely when they do, it is only during the transi- unknown (Cundall and Rossman, 1993; tion between intraoral transport and swal- Greene, 1997). However, previous studies lowing, a period during which the prey is of the cranial morphology of scolecophidi- moved not by the jaws, but by concertina- ans have proposed three different feeding like movements of the trunk in the cervical FEEDING IN BLINDSNAKES 1331 region (Cundall, 1995; Kley and Brainerd, tween the feeding mechanisms of typhlo- 1996; Kardong and Berkhoudt, 1998). pids and alethinophidians relate to the mor- The muscle activity patterns associated phology and function of the upper jaws in with mandibular raking in Leptotyphlops the two groups. The vast majority of ale- remain completely unknown. Given the bi- thinophidian snakes have a continuous row laterally synchronous jaw movements that of relatively long, recurved teeth along each characterize this mechanism, it seems likely medial upper jaw arch. In most taxa, recip- that bilateral activation of the hypoglossal rocating translational movements of these muscles powering jaw retraction (M. genio- toothed palatopterygoid arches are primar- glossus, pars hyoidea) and protraction (M. ily responsible for transporting prey geniohyoideus) is involved. Regardless of through the oral cavity (Cundall and muscle activity patterns, however, move- Greene, 2000). In typhlopids, however, the ments of the lower jaw in Leptotyphlops are pterygoids and palatines are toothless and morphologically constrained to be bilater- translational movements of the pterygoids ally synchronous. As in typhlopids (Bellairs serve only to protract and retract the and Kamal, 1981; Young, 1998), the left toothed maxillae. Prey transport in typhlo- and right halves of Meckel's cartilage in pids is thus brought about exclusively Leptotyphlops extend beyond the distal tips through rotational movements of the highly of the mandibular rami and fuse together to mobile maxillae. form a robust interramal nodule of carti- Other important differences between the lage. This cartilaginous link between the feeding mechanisms of typhlopids and al- tips of the mandibular rami permits hinge- ethinophidians relate to the structure of the like rotations between the dentaries, but al- lower jaw and its functional association lows almost no lateral or anteroposterior with the upper jaws. In alethinophidian separation of the mandibular tips. In addi- snakes, the distal tips of the dentaries are tion, during jaw retraction, caudally direct- quite separate from one another and are ed forces generated through contraction of joined together only by highly variable ar- the M. genioglossus are distributed evenly rays of connective tissues (Young, 1998; between the left and right distal mandibular Bellairs, 1984). Although the biomechani- segments because this muscle originates cal properties of these interramal connec- from a median tendon that arises from the tive tissues have not yet been critically ex- interramal cartilaginous nodule. For these amined, in most taxa they permit consid- reasons, independent movements of the left erable separation between the distal tips of and right halves of the lower jaw are not the mandibular rami. Consequently, each possible in Leptotyphlops. half of the lower jaw can be protracted or retracted independently of the other. Fur- Maxillary raking thermore, due to a ligamentous connection Like mandibular raking in Leptotyphlops, between the caudal tip of the pterygoid and maxillary raking in Typhlops and Rhino- the quadratomandibular joint (the pterygo- typhlops represents a highly specialized quadrate ligament), unilateral movements mechanism for the rapid ingestion and of the upper and lower jaws on each side transport of large numbers of small insect of the head are at least partially coupled to prey. In contrast to mandibular raking, how- one another in most taxa (e.g., Albright and ever, maxillary raking bears at least some Nelson, 1959b; Cundall and Gans, 1979). similarity to the feeding mechanisms of al- In contrast, the interramal connection in ty- ethinophidian snakes. In particular, prey is phlopids is quite rigid. As noted previously transported into and through the mouth via by Bellairs and Kamal (1981), the two independent ratcheting movements of the halves of Meckel's cartilage are bound to- upper jaws. However, many more differ- gether in the interramal region by an en- ences than similarities can be found be- larged cartilaginous nodule, thereby pre- tween the feeding mechanisms of typhlo- venting independent movements of the left pids and alethinophidians. and right mandibular rami. However, the ri- Perhaps the most striking differences be- gidity of the lower jaw in typhlopids does 1332 NATHAN J. KLEY not impede movement of the upper jaws. of snakes. Finally, the sensory pathways in- Due to the relatively wide separation be- volved in the modulation of feeding kine- tween the pterygoid and quadrate and the matics in typhlopids remain unknown and loss of the pterygo-quadrate ligament (Ior- are likely to represent a pro®table line of dansky, 1997), the upper and lower jaws are inquiry in future studies of typhlopid feed- functionally decoupled in Typhlopidae. ing. Given that ingestion in Typhlops and Finally, it is important to emphasize that Rhinotyphlops is usually initiated only after the synchronization of jaw movements is the snake's snout has come into contact different in typhlopids and alethinophidi- with the prey, it seems likely that the integ- ans. Alethinophidians generally use unilat- umentary mechanoreceptors present on the eral ratcheting movements of their jaws to head scales of typhlopids (Aota, 1940; drag themselves forward over their prey Young and Wallach, 1998) represent an im- (Gans, 1961). The upper and lower jaws on portant source of sensory feedback during one side of the head are opened and pro- feeding. Denervation experiments could tracted, and then closed and retracted. provide insight into the role of these cuta- These movements are then mirrored by the neous tactile organs in modulating feeding contralateral jaws. In contrast, typhlopids behavior. most commonly drag prey into and through the mouth using asynchronous movements The origin of unilateral feeding in snakes of the upper jaws. That is, the maxillae are As discussed above, the leptotyphlopid protracted and retracted slightly out of mandibular raking mechanism and the ty- phase with one another rather than in an phlopid maxillary raking mechanism both alternating, reciprocating pattern. differ in signi®cant ways from the snout The neuromuscular control of maxillary shifting and pterygoid walk mechanisms of raking in typhlopids remains unexplored. anilioids and macrostomatans, respectively. Given the degree to which feeding kine- In particular, neither mandibular raking nor matics (especially patterns of maxillary maxillary raking are characterized by the protraction and mandibular abduction) are unilateral pattern of jaw displacement that modulated according to prey size and po- underlies the feeding mechanisms of ale- sition, it is likely that the motor patterns thinophidians. Although feeding behavior associated with maxillary raking exhibit in the third scolecophidian family, Anom- considerable variability as well. Unlike alepididae, remains entirely unknown, the Leptotyphlopidae, however, Typhlopidae close phylogenetic relationship between an- includes a small number of ``giant'' species omalepidids and typhlopids (Cundall et al., (e.g., Rhinotyphlops schlegelii, Typhlops 1993; Tihen, 1945; Robb and Smith, 1966; punctatus) that reach nearly 1 m in length List, 1966), and the similar form and posi- and more that 2.5 cm in diameter (Fitz- tion of the maxillae in these two families Simons, 1962; Roux-EsteÁve, 1974). Large (List, 1966), suggest that anomalepidids adults of such species might afford the op- also transport prey using a maxillary raking portunity to use electromyography to study mechanism. Furthermore, many of the mor- the activity of head muscles during feeding phological features that facilitate unilateral in these snakes. EMG data from typhlopids feeding in Alethinophidia (e.g., loose inter- would not only provide a more detailed un- ramal connection, kinetic snout, pterygo- derstanding of the maxillary raking mech- quadrate ligament, etc.) are absent in An- anism itself, but could also be compared omalepididae (Haas, 1964, 1968), as they with similar data from alethinophidian are in Leptotyphlopidae and Typhlopidae. snakes (e.g., Cundall and Gans, 1979; Kar- Thus, available evidence suggests that, dong and Berkhoudt, 1998) and scleroglos- among extant snakes, unilateral feeding is san lizards (e.g., Smith, 1982; Herrel et al., present only in Alethinophidia. 1999) in an attempt to elucidate the modi- When the feeding mechanisms of scole- ®cations in motor control patterns that were cophidian snakes are placed within a phy- associated with the shift to jaw-based prey logenetic context (Fig. 5), two hypotheses transport mechanisms in the early evolution emerge concerning the evolution of unilat- FEEDING IN BLINDSNAKES 1333

FIG. 5. The phylogenetic distribution of prey transport mechanisms in snakes. Phylogenetic hypothesis adapted from Tchernov et al. (2000) and Cundall et al. (1993). Fossil taxa are excluded. eral feeding: (1) unilateral feeding arose in trom and Schwenkmeyer, 1951). In con- the common ancestor of Anilioidea and trast, most alethinophidians feed on rela- Macrostomata (i.e., within Alethinophidia); tively large vertebrate prey (Greene, 1983, or (2) unilateral feeding arose in the com- 1997). It might therefore be inferred that mon ancestor of Scolecophidia and Alethin- unilateral transport evolved as an adaptation ophidia (i.e., it is primitive for Serpentes), for handling large and potentially danger- and was subsequently lost in Scolecophidia. ous prey, as this mode of transport ensures It is clear that the feeding mechanisms of that a constant grip is maintained on strug- blindsnakes are highly derived and doubt- gling prey as it is ratcheted through the less differ considerably from those of an- mouth. Indeed, many non-venomous colu- cestral snakes. Therefore neither of these broid snakes ingest and transport their prey two hypotheses can be strongly rejected while it is still alive, and in the case of large based on the morphological and behavioral colubrids such as Drymarchon, formidable data that are currently available. However, prey such as large rats and small rabbits can when the criterion of parsimony is used to be eaten safely in this manner (unpublished evaluate these hypotheses, the ®rst scenario observation, N.J.K.). However, constriction is favored over the second. For this reason, appears to have arisen very early in ale- I accept the hypothesis that unilateral feed- thinophidian evolution (Greene and Bur- ing evolved within Alethinophidia (Fig. 5). ghardt, 1978) and basal alethinophidians Why unilateral feeding mechanisms are rarely ingest their prey without ®rst killing unique to Alethinophidia remains unknown. it through suffocation. Thus, it appears un- Perhaps the most conspicuous difference in likely that unilateral transport arose as an feeding biology between Scolecophidia and adaptation for the transport of live, strug- Alethinophidia relates to the prey on which gling prey. these snakes feed. Scolecophidians feed It might also be hypothesized that the predominantly on social insects. In most unilateral pattern of jaw displacement seen species for which detailed dietary infor- in alethinophidians arose simply as a by- mation is available, ant larvae and pupae product of the structural modi®cations of represent the most important food resource the skull associated with the ingestion of (Webb and Shine, 1993a; Webb et al., large-diameter prey in these snakes. For in- 2000). In some species, termites are also stance, the liberation of the mandibular tips frequently consumed (Punzo, 1974; Bratts- has long been recognized as an important 1334 NATHAN J. KLEY morphological innovation in the early evo- modi®ed in association with the shift to a lution of snakes that served to increase po- unilateral jaw displacement pattern. tential gape size (Gans, 1961). However, loosening of the interramal linkage not only ACKNOWLEDGMENTS allowed the tips of the mandibular rami to I am grateful to E. L. Brainerd for her spread apart laterally, but also permitted the support, encouragement and assistance left and right halves of the lower jaw to be throughout this project. W. E. Bemis, K. protracted and retracted independently of Schwenk and E. J. Hilton provided valuable one another. Therefore, if mandibular lib- guidance during the preparation of histolog- eration occurred as a result of selection for ical sections. F. A. Jenkins and A. W. increased gape size, its role in unilateral Crompton kindly permitted me to use the transport would be interpreted as being ex- radiographic facility at the Museum of aptive rather than adaptive (sensu Gould Comparative Zoology. For the loan of spec- and Vrba, 1982). Like the adaptive hypoth- imens used for comparative purposes, I esis presented above, however, this exaptive thank J. Hanken and J. P. Rosado (Museum hypothesis seems unlikely in the light of of Comparative Zoology) and H. K. Voris available evidence. First, the evolution of and A. Resetar (Field Museum of Natural increased gape size in Alethinophidia has History). E. L. Brainerd, K. Schwenk and occurred primarily through structural mod- W. E. Bemis critically reviewed the manu- i®cations of the lower jaw, suspensoria and script. The lab in which this work was done intermandibular soft tissues (Gans, 1961; was supported by NSF IBN-9875245 to E. Lee et al., 1999; Cundall and Greene, L. Brainerd. 2000). In contrast, many of the modi®cations in cranial morphology that facilitate REFERENCES unilateral feeding have occurred in the up- Abdeen, A. M., A. M. Abo-Taira, and M. M. Zaher. per jaws, and therefore have had little effect 1991a. Further studies on the ophidian cranial os- on gape size. 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