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Herpetologia Petropolitana, Ananjeva N. & O.Tsinenko (eds.), pp. 171 ­ 173

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ON THE MORPHOFUNCTIONAL PECULIARITIES OF THE JAW APPARATUS OF OPHIOPHAGOUS ELAPID SNAKES AND ON THE SOME STAGES IN EVOLUTION OF ELAPIDAE A. Y. Sokolov
1

Keywords: Reptilia, Serpentes, Elapidae, Calliophis, Bungarus, Maticora, jaw apparatus, functional morphology.

INTRODUCTION Jaw elongation is an important specialization for swallowing prey of large diameter in most alethinophidian snakes (Macrostomata). Thus the inability of many specialized snake-eating species of elapids (species of the genera Calliophis, Maticora, Bungarus, Micrurus, and some others) to gape widely (despite a macrostomatan skull) is surprising. The evolution of limited gape may relate to their selection of narrow and elongate prey, but the reasons for the appearance deserve special consideration.

MATERIAL AND METHODS Prey capture and swallowing were observed in Calliophis macclellandi (one specimen). Fresh heads of three specimens of Bungarus multicinctus, two specimens of Calliophis macclellandi and two specimens of Maticora bivirgata were studied by layer-by-layer dissection of muscles under low magnification using an MBC-2 binocular microscope. Cranial kinesis was studied. The interaction with prey was modeled and functional analysis was made. These data were compared with similar data obtained from other elapids (Acanthophis praelongus, Naja kaouthia, and N. pallida) feeding on larger diameter prey and with species of other groups, besides Elapidae, that feed on large diameter prey (Sokolov, 2001a, 2001b).

RESULTS AND DISCUSSION Earlier (Sokolov, 2001a, 2001b) it was shown, that the classical snake-like prey-transport mechanism of alternately engaging the left and right side has a significant fault when the prey is large in diameter. The cause is using protractor muscles which are fastened on the braincase. The efficiency of the mechanism decreases when prey di1

Department of Vertebrate Zoology, Faculty of Biology, M. V. Lomonosov Moscow State University, Vorobyevy Gory, 1, k. 12, 119992 Moscow, Russia; E-mail: apophis@hotbox.ru.

ameter increases. Apparently unilateral transport evolved as a critical specialization of a limbless mud-dwelling snake ancestor to feeding on earthworms or leeches. The swallowing of hard immobile prey alive required advance on the prey by fixed steps. This stage made the snake jaw apparatus plastic (the prey is not crushed [broken] by jaws before entry into the esophagus). After transition to feeding on vertebrates colubroid snakes did not lose the plesiomorphic prey-transport mechanism and only later after transition to feeding on thick vertebrates classical mechanism was supplied by other prey-engaging mechanisms, faultless in swallowing prey of large diameter (other protracting muscles are used in the beginning of step on prey surface). For example advanced Elapidae use the pterygoideus muscle to protract the lower jaw when the teeth of the upper jaw have been fixed on the surface of prey. Specialization for feeding on elongate vertebrates was the first stage of vertebrate-feeding transition and as such, the basal prey-transport mechanism was sufficient. Many specialized snake-eating elapids can use the basal mechanism only (m. pterygoideus has "henophidian" organization and attachment peculiarities). But unlike leeches and earthworms killing or immobilizing little elongate vertebrates is not so hard. The ability to inflict a powerful bite on vital centers of the body, especially on the head or not far from it, is quite important. Some snake-eating snakes, including elapids try to restrain prey using their jaws. During the bite the kinetic upper part of the skull becomes rigid. This is achieved by caudally directed forces applied to the palatomaxillary arches (especially to the maxillae -- see Fig. 1) and quadrates and generated by contraction of the palatine retractor muscle (Mrp), m. pterygoideus (Mpt), m. adductor mandibulae externus posterior (Maeps), m. neurocostomandibularis (Mncm), and possibly m. cervicomandibularis (Mcm). These muscles create a "bowstring-like" effect and fix the skull construction in the maximally retracted position (see Cundall and Irish, 1989, for a similar effect in Casarea). In this situation the adductor muscles, especially the powerful m. adductor externus medius (Maem), use the jaw apparatus in a crocodile-like man-


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Herpetologia Petropolitana, Ananjeva N. & O.Tsinenko (eds.), pp. 171 ­ 173

ner -- the jaw has a long lever arm. In low snake species with flattened skulls vertically oriented muscle fibers are relatively short and limit gape size. Thus in this construction Maem and Maeps apply vertically and caudally oriented forces to the lower jaw. The compressor of the venom gland (Mcgl) is made of most unnecessary as adductor portion -- m. adductor externus anterior. The pressing of skull is (forces generated during jaw adduction are) effectively transmitted on to the fang which is situated under or near the prefrontal bone which is fixed in a vertical po-

sition. The fang can be used in a mammal-like manner -- in perforating some bone structures, the braincase for example. The inflowing of venom through the fang can lead to rapid immobilization of the victim. The analysis of the jaw apparatus of many other elapid species suggested that adaptation occurred during the evolution of family Elapidae. Analysis of the literature (e.g., Haas, 1930; Cundall and Green, 2000) about functional morphology and feeding peculiarities also infer that proteroglyphic sea-snakes experienced modifications of the jaw apparatus similar to

Calliophis macclellandi
Mcgl Mcm Prefrontal Quadrate Fang

Bungarus multicinctus
(some muscles have been extracted) Maem Prefronal bone

Maeps

Mncm

Maem Maxilla Mpt Maeps

Maxilla

Jaw joint Mpt

Scheme of the creation of caudally directed forces during the bite (model object is the jaw apparatus of Bungarus multicinctus)
Force of the conttruction of some caudally orientd fibers of Maeps and Maem (M) M+R Q P
1 1

Mrp contraction force (Mrp)

P

2

Caudally directed forces, applied to the maxilla
Prey Force of prey's reaction (R1) Q P
2

M P Mrp + P
1

rp

1

Quadrate's reaction (R2) Jaw joint-retracting force Q = M + R1 + R2 M+R
1

M

R

1

P1 and P2 forces of contraction of the different fibers of Mpt
Fig. 1.


Herpetologia Petropolitana, Ananjeva N. & O.Tsinenko (eds.), pp. 171 ­ 173

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those of serpent-eating elapids but associated with eel-eating in hydropiids and laticaudids. It is surprising that in this aspect proteroglyph snakes appear to have became venomous before so famous "typical ophidian" specialization to "thick prey-swallowing" (in skull of Calliophis and Maticora with "aniliid-like" proportions the quadrate is short and vertically oriented, postorbital part of braincase and jaws equally elongated, only Bungarus has more elongated jaws and elongated slanted quadrate). The snakeeating (or eel-eating in sea-snake case) can be interpreted like preadaptation to appearance of "thick object swallowing" mechanism typical for the advanced proteroglyph snakes which uses pterygoideus muscle. In specialized jaw apparatus of snake-eating elapids the contracted powerful pterygoideus muscle can break quadrate branch of pterygoid bone which is very slender. Thus the disconnection of pterygoid and quadrate with pterygoideum shortening (hyperstreptostylic movability) became very useful. Than the immobilization of the skull front part used for fang's fixation (it often takes place) results in decreasing of classical prey-engaging mechanism efficiency. Probably besides dolichophagy stage in evolution of the majority of elapid snakes also took place specialization to feeding on small vertebrate victims (several small victims as alternative to one long) which does not require to reconstruct so effective and formidable jaw apparatus. Its result is the look of the majority elapid specimen as active hunters, slender snakes. It is also easy to assume, that the transition from earthworm-eating to vertebrate-eating specialization on some stage could cause not only the snake-eating elapid's jaw apparatus, able "to switch on regime of rigidity," but also could cause simpler transformation -- the significant decreasing or loss of kinetism by some primitive snakes (a lot of Anlioidea and extinct Dinillysidae) which causes fossil skull preservation to be more probable. They refused from asymmetrical prey-engaging movements of toothed bones to swallow the prey and use outward support. Elongation of the jaws and postorbital

part of the braincase in akinetic or oligokinetic skulls can be accounted for by usefulness of significant lever for adductor muscles. It must be mentioned that the hypothesis that very early snakes used powerful jaws for killing elongate, heavy prey, has already been suggested by some authors (Greene, 1983; Mushinsky, 1987). But my hypothesis about worm-eating specialization of their limbless ancestor [see above and (Cundall and Green, 2000)] and lability of snake jaw apparatus can explain why using powerful jaws did not go beyond the process of prey-killing and why snakes swallow their prey entirely unlike amphisbaenians, which tear off and swallow peaces of large prey.

REFERENCES
Cundall D. and Irish F. J. (1989), "The function of the intramaxillary joint in the Round Island boa, Casarea dussumieri," J. Zool. (Lond.), 217, 189 ­ 207. Cundall D. and Greene H. W. (2000), "Feeding in snakes," in: Schwenk K. (ed.), Feeding: Form, Function, and Evolution in Tetrapod Vertebrates, Acad. Press, San Diego, pp. 293 ­ 333. Greene H. W. (1983), "Dietary correlates of the origin and radiation of snakes," Am. Zool., 23, 431 ­ 441. Haas G. (1930), "эber die Schadelmechanik und die Kiefermusculatur einiger Proteroglypha," Zool. Jb. Anat. C, 52(2), 347 ­ 404. Mushinsky H. R. (1987) "Foraging ecology," in: Siegel R. A., Collins J. T., and Novak S. S. (eds.), Snakes: Ecology and Evolutionary Biology, McGraw Hill, pp. 302 ­ 334. Sokolov A. Yu. (2001a), "On the morphological peculiarities of jaw apparatus of snakes Booidea, Colubroidea, and Acrochordoidea on the basis of the analysis of interaction with super-large prey," in: The Problems of Herpetology. Proc. of 1th Meeting of the Nikolsky Herpetol. Soc., Pushchino ­ Moscow [in Russian]. Sokolov A. Yu. (2001b), Morphofunctional Peculiarities of the Jaw Apparatus of Snakes Booidea, Colubroidea, and Acrochordoidea in Connection with Trophical Adaptations. Ph.D. Thesis, Izd. MGU, Moscow [in Russian].