oral sensory papillae in sea snakes

Oral Sensory Papillae in Sea SnakesAuthor(s): Barry BurnsSource: Copeia, Vol. 1969, No. 3 (Aug. 29, 1969), pp. 617-619Published by: American Society of Ichthyologists and Herpetologists (ASIH)Stable URL: http://www.jstor.org/stable/1441942 .

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HERPETOLOGICAL NOTES

ORAL SENSORY PAPILLAE IN SEA SNAKES.-Terrestrial snakes have two primary centers for the reception of olfactory stimuli: the nasal structure and Jacobson's organ. The latter, believed to be the primary oral chemo-receptor, connects to the roof of the mouth and is innervated by the medial olfactory nerve (Papez, 1929). Most snakes have a highly flexible, protrusible tongue which may be waved vigorously in the air and then retracted, depositing odoriferous compounds in the bilateral grooves of Jacob- son's organ (Wilde, 1938).

Little is known of the way in which sea snakes perceive chemical stimuli. The slower diffusion rates of molecules in water pre- sumably require some adaptations in the basic chemo-receptive system. This paper de- scribes a previously unreported system of oral sensory papillae, which appear as prominent villiform elevations of the epidermis (Fig. 1). The papillae lie parallel to the tooth rows in bilaterally symmetric rows on the oral surfaces, and there appears to be no con- sistent relationship between the spacing of the individual papillae and the teeth.

Three specimens each of Pelamis platurus (60 cm), Hydrophis ornatus (70 cm), and Laticauda colubrina (70 cm) and one speci-

men of Hydrophis melanocephalus (85 cm) were used in the study. All specimens were fixed in 7% formalin. For histological exami- nation, individual papillae were dissected from the mandibular region of H. ornatus and P. platurus, dehydrated in isopropyl alcohol, embedded in paraffin and sectioned at 6 ,. The mounted sections were stained with hematoxylin and eosin and a silver technique (Bodian, 1936). The head of one specimen of P. platurus, exclusive of the lower jaw, was decalcified for 4 hr in 2N HC1 and frontal sections were cut at 15 ,. Innervating nerves were traced in gross dis- section and in the serial sections of the head, proving to be maxillary and mandibular branches of the trigeminal (N V). The nerve bundle to an individual papilla branches slightly before reaching the epidermis and the individual fibers appear to taper rapidly upon entering the epidermis, thereby making it difficult to determine the exact manner in which the receptor cells are innervated (Fig. 2). Many fibers were also observed to pro- gress for a short distance horizontally prior to penetrating the basement membrane. Structures resembling taste buds, connecting to the surface through a small pore, were seen in many papillae (Fig. 2A, D).

Fig. 1. Dorsal view of the lower jaw of Pelamis platurus, showing an enlarged photograph of the lateral aspect with a row of papillae (P) medial to the mandibular tooth row. Pigmentation is apparent in the majority of papillae and in irregular patterns on the oral surfaces. The tracheal opening and the tongue can be seen along the mid-line of the jaw in the drawing. Scale represents 1 mm.

617



COPEIA, 1969, NO. 3

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Fig. 2. Views of papillae from Pelamis platurus and Hydrophis ornatus. A. Sagittal section of papilla from mandibular region of P. platurus, showing differentiation of basal epidermal cells into rod-shaped configurations (R), and a structural discontinuity (arrow) in the surface epithelium over- lying a small region of vertically oriented cells. Pigmentation is seen as a dermal aggregation of melanophores (M) and the ascending nerve (N) medial and deep. Hematoxylin and eosin. (Scale = 0.25 mm.) B. Sagittal section of papilla from palatal region of P. platurus. Ascending nerve branches in the dermal evagination. Bodian silver technique. Magnification as in A. C. Detail of area outlined in B, showing one type of "receptor cell" (R) and melanophore (M). (Scale = 30 /I.) D. Papilla from maxillary region of H. ornatus with a structure (circled) resembling a taste bud and connecting to the surface through a pore (P). Hematoxylin and eosin. (Scale= 0.15 mm.)

The papillae in the upper and lower jaws are positioned on the buccal wall of the maxillary and mandibular tooth rows, and on the labial wall of the palatal tooth row. The numbers of papillae showed some bi-

lateral asymmetry, perhaps due to difficulty in counting since these structures decrease in size posteriorly. Due to the small number of specimens examined, the numbers of papillae in each species can only be approxi-

618



HERPETOLOGICAL NOTES

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B. Laticauda colubrina D. Hydrophis melanocephalus

Fig. 3. Views of oral surfaces of four species of sea snake, showing distribution of papillae. (Lower jaw to left.) Papillae, represented by black dots, are medial to the maxillary (MX) and mandibular (MD) tooth rows, and lateral to the palatal (PT) tooth row. The internal choanae (IC) and tracheal opening (TR) are also shown. Approximate position of the fang (F) in each species is given. Jacobson's organ lies directly opposite the tongue in each specimen. Approximate numbers of papillae are as follows: A. MX(13-16), PT(28-30) and MD(18-22). B. MX(9-10), PT(19-20) and MD(19-24). C. MX(15-16), PT(23-25) and MD(18-22). D. MX(5-7), PT(21-23) and MD(18-20).

mated. The form and number of the papillae do appear to warrant gross taxonomic distinction (Fig. 3). Dermal pigmentation was only found in two species (P. platurus and L. colubrina) and its significance is uncertain.

Two terrestrial snakes (Pituophis catenifer and Crotalus cerastes) were examined under a binocular dissecting microscope and similar well developed papillae were found. These were unpigmented and less prominent. Al- though the functional value of these papillae is uncertain at present, it seems that they may be widely distributed in snakes and show dif-

fering degrees of development. Specimens were generously provided by

Dr. George V. Pickwell, NUWC, San Diego. I thank Dr. Carl Gans for providing addi- tional specimens of P. platurus, and dis-

cussing the manuscript; Dr. Eric Barham, NUWC, San Diego, and Dr. Richard

Etheridge, San Diego State College, for ad-

vice and encouragement. Work was per- formed under U. S. Navy Ship Systems Com- mand SR 104-03-01, Task 0588 at NUWC, San Diego. The material in this paper re- flects the opinion of the author only, and does not necessarily represent the official view of the U. S. Navy Department.

LITERATURE CITED BODIAN, D. 1936. A new method for staining

nerve fibers and nerve endings in mounted paraffin sections. Anat. Rec. 65:89-97.

PAPEZ, J. W. 1929. Comparative neurology. Hafner Publ. Co., New York.

WILDE, W. S. 1938. The role of Jacobson's organ in the feeding reaction of the common garter snakes (Thamnophis sirtalis sirtalis). J. Exp. Zool. 77:445-465.

BARRY BURNS, Bioacoustics and Marine Biol-

ogy Branch, Marine Environment Division, NUWC, San Diego, California 92132. Pres- ent address: Department of Psychology, Uni- versity of Waterloo, Waterloo, Ontario, Canada.

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oral sensory papillae in sea snakes

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