? 2001 by the American Society of Ichthyologists and Herpetologists
Copeia, 2001(1), pp. 270–273
Buccal Expansion during Hissing in the Puff Adder, Bitis arietans
BRUCE YOUNG, JADE JAGGERS, NANCY NEJMAN, AND NATHAN J. KLEY
Videoradiographic analyses were made of hissing in puff adders (Bitis arietans).
During the hiss the larynx remains relatively stationary immediately adjacent to the
internal nares. The exhalatory portion of the hiss is characterized by a distinct
expansion of the caudal buccal cavity, including a depression of the hyoid and di-
vergence of the cornua. This buccal expansion is hypothesized to be an epiphenom-
enon of intraoral pressure generated by the exhalatory airstream of the hiss.
defensive repertoire of snakes (for reviews see
Mertens, 1946; Carpenter and Ferguson, 1977;
Greene, 1988). These localized bodyexpansions
may be horizontal (such as ‘‘hooding’’ in Naja;
Young and Kardong, 1989) or vertical (such as
throat expansion in Ptyas mucosus; Young et al.,
1999a); the plane of expansion generally cor-
relates with the main visual axisof the potential
predator (Greene, 1979; Senter, 1999). Al-
though many snakes use respiratory mecha-
nismsfor generalized bodyexpansion (e.g., Kin-
ney et al., 1998; Young et al., 1999b), the spe-
cialized defensive displaysappear to result from
differential contributionsof the cranial ribsand
the anterior portion of the respiratory tract
(Young et al., 2000).
The specializationsof the anterior respiratory
tract, which produce defensive visual displays,
may also result in unusual acoustic properties
(Young, 1991b; Young et al., 1999a). Most de-
fensive sounds produced by snakes have a sim-
ple acoustic structure characterized by very low
levels of frequency and amplitude modulation
and little or no temporal patterning (Young,
1997, 1998b). Manysnakessuch asHeterodonpla-
tyrhinos(Young and Lalor, 1998) and Daboia rus-
selii (Young, 1998a) are obligate nasal hissersin
which the exhalent airstream is always passed
through the internal nares. Experimental anal-
yses of hissing in another obligate nasal hisser,
the puff adder (Bitis arietans), revealed that the
larynx plays a passive role during sound pro-
duction, remaining patent throughout the
sound-producing portions of the hissing cycle
(Young et al., 1999b).
The larynx of snakes is structurally simple
(Kardong, 1972a,b; Young, 2000) and with the
exception of Pituophismelanoleucus(Young et al.,
1995) shows few anatomical specializations.
Changes in the relative position of the larynx
within the oral cavity during the hiss and/ or
changes in the dimensions of the buccal cavity
itself could result in a resonance effect and a
XPANSION of the body, particularly the an-
terior portion, is a common feature of the
visible distension of the buccal cavity similar to
what has been described as a defensive display
in Psammophis (Werner, 1985). Recent studies
using cineradiographyand videoradiographyon
squamates have provided documentation of in-
trabuccal processes relating to chemosensory
searching (Young, 1990, 1991a), defensive dis-
plays(Belset al., 1995), preytransport and swal-
lowing ( Janoo and Gasc, 1992; Cundall, 1995;
Kley and Brainerd, 1996), drinking (Bels and
Kardong, 1995), and ventilation (Owerkowiczet
al., 1999). In this study, we used videoradiogra-
phy to study intrabuccal processes associated
with defensive displays in the puff adder, B. ar-
MATERIALS AND METHODS
The snakesused for thisstudywere long-term
captives maintained in the venomous snake
room at Lafayette College at a temperature of
29–32 C, with a 12:12 L:D photoperiod, and a
diet of prekilled mice. All animal maintenance
and experimental procedures comply with ex-
isting guidelines for both live reptiles and ven-
omous snakes. We recorded x-ray video data
from five adult puff adders (B. arietans) with
snout–vent lengths (SVLs) ranging from 74.5–
The specimenswere individuallyanesthetized
by exposure to ice until the cessation of inde-
pendent movement. Once immobile, the spec-
imen was placed on a bed of ice and the mouth
held open with a surgical retractor. A soft ap-
plicator stick was used to repeatedly smear pow-
dered barium sulfate (BaSO4) onto the epithe-
lial lining of the larynx. Additional barium sul-
fate was placed into the caudal portion of one
of the nasal passageways. Any stray barium sul-
fate was rinsed and wiped from the oral cavity
prior to returning the specimen to normal tem-
perature for recovery from the anesthesia. One
day after the application of the barium marker
to the larynx, the water bowl wasremoved from
271 YOUNG ET AL.—BUCCAL EXPANSION IN BITIS
tansduring the onset (A) and termination (B) of the
exhalatory phase of the defensive hiss. Approximately
two seconds separates these two images. Note the dis-
tinct expansion of the buccal floor in (B).
Lateral images of a 128 cm SVL Bitis arie-Fig. 2.
tans during the onset (A) and during (B) the exhal-
atory phase of the defensive hiss. Note the expansion
of the buccal floor, and the depression and diver-
gence of the hyoid (arrow).
Frontal images of a 128 cm SVL Bitis arie-
the snake’s cage, and no further water was pro-
vided for one week prior to data acquisition.
The snakes were transported to the radio-
graphic facility at the Museum of Comparative
Zoology, Harvard University for videoradiogra-
phy. During transport and data collection, the
snakeswere kept at temperaturesfrom 25–30 C.
During data collection, the specimens were
placed individually into 52.5 ? 40 ? 22.5 cm
plastic containers with secure lids. One end of
the plastic container opened into a detachable
filming chamber. Two filming chambers were
made to accommodate animals of different siz-
es; both were 30 cm long and 11 cm high, but
one was 5 cm wide and the other 10 cm wide.
Both filming chamberswere made of Plexiglas?,
but each had a partial wooden floor. Defensive
behaviors were evoked either by motion of one
of the researchersor through direct stimulation
of the caudal end of the animal. Many of the
specimens were subsequently removed and
placed in appropriately sized clear Plexiglas?
tubes for additional data collection. Following
videoradiography, each snake was placed in a
tank of warm water to ensure hydration and was
subsequently given water ad libitum.
Videofluorscopy was performed using a Sie-
mens radiographic unit equipped with a Sire-
con image intensifier. X-ray videos were record-
ed at 30 fps on a Sony DCR VX1000 digital vid-
eo camera. The x-ray source and image inten-
sifier were aligned in a lateral position, and the
distal portion of the filming chamber or Plexi-
glas? tube was positioned against the image in-
tensifier. Although most of the videographic
data were recorded in lateral projection, the
filming chambers were large enough that the
snake could fully turn its head, affording us a
frontal perspective. Video sequences were
downloaded directly from the Sony digital cam-
era to a PowerMac G3 computer via a Radius
MotoDV Firewire card.
Multiple hisses were obtained from four of
the B. arietans; a total of 48 hisses were exam-
ined. During each hiss, the larynx appeared to
remain stationary in a protracted position near
the level of the internal nares. Although our
marker system did not allow us to quantify the
contact between the larynx and the internal na-
res, there wasno evidence for intrabuccal move-
ment of the larynx during sound production.
During the terminal portion of each exhalatory
hiss, there was a marked depression of the cau-
dal portion of the buccal floor (Fig. 1). In the
larger specimens, this buccal expansion lasted
approximately two seconds. This buccal expan-
sion was extensive enough that the hyoid ex-
tended ventral to the lower jawsand the cornua
diverged laterally (Fig. 2). Although not quan-
tified, the extent of buccal expansion appeared
to be related to the volume of air exhaled with
each hiss and, thus, probably with air pressure
as well. Although some buccal expansion was
272COPEIA, 2001, NO. 1
observed in each hissing B. arietans, it was most
pronounced in the largest specimen.
The combined use of videoradiography and
radiopaque barium markers permitted clear vi-
sualization of the larynx and other features of
the buccal cavity, thereby documenting the rel-
ative spatial stability of the larynx during sound
production in B. arietans. This technique also
provided clear evidence of buccal expansion as-
sociated with sound production (Figs. 1–2).
This expansion may represent an unusual form
of buccal pump in which exhalatory air is
pulled into the buccal cavity then redirected ei-
ther externally or back into the lung. Although
buccal pumps are known in reptiles (Owerkow-
icz et al., 1999) and other terrestrial vertebrates,
they normally function to pump in fresh inhal-
atory air not to expel exhalatory air (Brainerd,
1994). Although we consider it unlikelythat this
isa buccal pump, further experimental dataare
necessary to test this hypothesis.
Rather than an active buccal pump, this buc-
cal expansion may represent the passive result
of increased air pressure in the buccal cavity.
Puff adders move considerable volumes of air
during defensive hisses, particularly during the
exhalatory phase (Young et al., 1999b). If the
larynx does not form an airtight seal with the
internal nares, the resistance created bythe nar-
row diameter of the nasal passageways (relative
to the larynx) could force some of the exhalent
airstream into the oral cavity. Because B. arietans
keep the mouth closed during hissing, thispres-
surized air could cause expansion of the caudal
portion of the oral cavity, which is distended
similarly during prey transport. This hypothesis
would explain why the buccal expansion isseen
only during exhalation and why the extent of
buccal expansion appeared correlated with the
volume of exhaled air associated with each de-
fensive hiss. Furthermore, the duration of the
observed buccal expansions (approximately 2
sec) is in close agreement with the duration of
the exhalatory phase of the hiss of B. arietans
(mean 1.54 sec, range ? 1.2–2.2 sec; Young et
al., 1999b). A similar pattern of buccal expan-
sion has been described in Psammophis aegyptius
The use of exhalatory air pressure for body
expansion, such as we hypothesize, occurs in
the buccal region of B. arietans, is rather com-
mon in snakes (Noble, 1921; Carpenter and
Ferguson, 1977; Greene, 1988), and may be ac-
tive as well as passive (Young et al., 2000). The
buccal expansion in B. arietans is functionally
isolated from the respiratory-based expansion
of the puff adder’s body, which also occursdur-
ing defensive displays. Thisgeneral bodyexpan-
sion isproduced through movementsof the ribs
(Young et al., 1999b), and deflation of the body
is synchronous with expansion of the buccal re-
gion. Viewed without the assistance of videora-
diography, the buccal expansion of B. arietansis
not dramatic; indeed, it doesnot appear to have
been previously described. In part, this may be
explained by the defensive posture adopted by
B. arietans in which the snout is angled down
toward the ground, completely obscuring the
As a defensive display, this buccal expansion
in B. arietans is quite unusual. Body expansion
is generally interpreted as a way of making the
animal appear more intimidating by increasing
the visible surface of the snake (Greene, 1979;
Senter, 1999). Terrestrial snakes that increase
the dimensions of the head during defensive
displays typically do so in the horizontal plane
(e.g., Young et al., 1999c). Given the modest ex-
ternal evidence of buccal expansion, and the
defensive posture that obscures the buccal re-
gion, we consider it more likely that the buccal
expansion in B. arietans is an epiphenomenon
of the dramatic hisses produced by this species
rather than a true defensive behavior in which
the body is inflated for intimidation.
The authors thank the Academic Research
Committee (ARC) and the Department of Bi-
ology of Lafayette College for their kind sup-
port of this project. F. A. Jenkins was kind
enough to give us access to the videoradi-
ographic equipment, and T. Owerkowicz lent us
his technical expertise. Protocols employed in
this study were approved by the IACUC of La-
BELS, V. L., AND K. V. KARDONG. 1995. Water drinking
in snakes: evidence for an esophageal sphincter. J.
Exp. Zool. 272:235–239.
, J.-P. GASC, V. GOOSSE, S. RENOUS, AND R. VER-
NET. 1995. Functional analysisof the throat display
in the sand goanna Varanus griseus (Reptilia: Squa-
mata: Varanidae). J. Zool. Lond. 235:95–116.
BRAINERD, E. L. 1994. The evolution of lung-gill bi-
modal breathing and the homology of vertebrate
respiratory pumps. Am. Zool. 34:289–299.
CARPENTER, C. C., AND G. W. FERGUSON. 1977. Varia-
tion and evolution of stereotyped behavior in rep-
tiles, p. 335–554. In: Biology of the Reptilia. Vol. 7.
273YOUNG ET AL.—BUCCAL EXPANSION IN BITIS
C. Gans and D. Tinkle (eds.). Academic Press, New
CUNDALL, D. 1995. Feeding behaviour in Cylindrophis
and itsbearing on the evolution of alethinophidian
snakes. J. Zool. Lond. 237:353–376.
GREENE, H. 1979. Behavioural convergencein thede-
fensive displays of snakes. Experientia 35:747–748.
. 1988. Antipredator mechanisms in reptiles,
p. 1–152. In: Biology of the Reptilia. Vol. 16. C.
Gans and R. Huey (eds). Alan R. Liss, New York.
JANOO, A., AND J.-P. GASC. 1992. High speed motion
analysis of the predatory strike and fluorographic
study of oesophageal deglutition in Vipera ammody-
tes: More than meets the eye. Amphib.-Reptilia 13:
KARDONG, K. V. 1972a. Morphologyof therespiratory
system and its musculature in different snake gen-
era (Part 1) Crotalus and Elaphe. Gegenb. Morph.
. 1972b. Morphology of the respiratorysystem
and itsmusculature in different snake genera (Part
2) Charina bottae. Ibid. 117:364–376.
KINNEY, C., G. ABISHAHIN, AND B. A. YOUNG. 1998.
Hissing in rattlesnakes: redundant signaling or in-
flationary epiphenomenon? J. Exp. Zool. 280:107–
KLEY, N. J., AND E. L. BRAINERD. 1996. Internal con-
certina swallowing: a critical component of alethin-
ophidian feeding systems. Am. Zool. 35:81A.
MERTENS, R. 1946. Die Warn-und Droh-reaktionen
der Reptilien. Senck. Naturf., Abh. 471:1–108.
NOBLE, G. K. 1921. Snakes that inflate. Nat. Hist. 21:
OWERKOWICZ, T., C. G. FARMER, J. W. HICKS, AND E. L.
BRAINERD. 1999. Contribution of gular pumping to
lung ventilation in monitor lizards. Science 284:
SENTER, P. 1999. The visibility hypothesis: an expla-
nation for the correlation between habitat and de-
fensive displays in snakes. Herpetol. Rev. 30:213.
WERNER, Y. L. 1985. Defensive behavior in a boigine
snake: first record of throat inflation in Psammophis.
Israel J. Zool. 33:69–71.
YOUNG, B. A. 1990. Is there a direct link between the
ophidian tongue and Jacobson’s organ? Amphib.-
. 1991a. Evaluating hypothesesfor thetransfer
of stimulus particles to Jacobson’s organ in snakes.
Brain Behav. Evol. 41:203–209.
. 1991b. The morphological basis of ‘‘growl-
ing’’ in the King cobra, Ophiophagushannah. J. Exp.
. 1997. A review of sound production and
hearing in snakes, with a discussion of intraspecific
acoustic communication in snakes. J. Penn. Acad.
. 1998a. How to hiss loudly: narial flaring and
acoustic amplification in Russell’sviper (Daboia rus-
selii). Hamadryad 23:103–110.
. 1998b. On the acoustic biologyof snakes. Lit.
. 2000. The comparative morphology of the
larynx in snakes. Acta Zool. 81:177–193.
, AND K. V. KARDONG. 1989. The functional
morphology of hooding in the Asiatic cobra. Am.
, AND J. LALOR. 1998. Sound production in the
eastern hognose snake, Heterodon platyrhinos (Ser-
pentes: Colubridae): Does it snore? Amphib.-Rep-
, S. SHEFT, AND W. YOST. 1995. Sound produc-
tion in Pituophis melanoleucus (Serpentes: Colubri-
dae) with the first description of a vocal cord in
snakes. J. Exp. Zool. 273:472–481.
, J. SOLOMON, AND G. ABISHAHIN. 1999a. How
many ways can a snake growl? The morphology of
sound production in Ptyasmucosusand itspotential
mimicry of Ophiophagus. Herpetol. J. 9:89–94.
, N. NEJMAN, K. MELTZER, AND J. MARVIN.
1999b. The mechanics of sound production in the
puff adder, Bitisarietans(Serpentes: Viperidae) and
the information content of the snake hiss. J. Exp.
, J. LALOR, AND J. SOLOMON. 1999c. The com-
parative biomechanicsof an ophidian defensive be-
havior: head triangulation in hognose snake (Het-
erodon) and egg-eating snake (Dasypeltis). J. Zool.
, N. NEJMAN, AND J. JAGGERS. 2000. Snakesthat
inflate: the functional morphology of a defensive
(BAY, JJ, NN) DEPARTMENT OF BIOLOGY, LAFAY-
ETTE COLLEGE, EASTON, PENNSYLVANIA 18042;
AND (NJK) ORGANISMIC AND EVOLUTIONARY
BIOLOGY PROGRAM, UNIVERSITY OF MASSACHU-
SETTS, AMHERST, MASSACHUSETTS 01003. E-
mail: (BAY) email@example.com. Send re-
print requests to BAY. Submitted: 20 March
2000. Accepted: 24 July 2000. Section editor:
R. E. Gatten Jr.