The role of modified teeth in the function of prolonged bites in Hierophis viridiflavus (Serpentes: Colubridae)

Abstract

The role of modified teeth in the function of prolonged bites in Hierophis viridiflavus (Serpentes: Colubridae). Analysis of the maxillary, palatine, pterygoid, and dentary bones of the Western Whipsnake, Hierophis viridiflavus carbonarius, revealed the presence of grooves and ridges in the teeth on the four dentiferous bones. Enlarged and modified rear teeth were found on the posterior maxillaries, separated by alveolar diastema and aligned differently from the anterior maxillary teeth. In both live and dissected specimens, Duvernoy's gland, associated with the production of toxins, surrounds the rear maxillary teeth, which deliver the secretions produced by the gland. These characters, plus the infliction of prolonged bites, facilitate the subduing of prey. The morphology of the palatomaxillary arch places H. viridiflavus in the group of opisthoglyphous colubroids, whose modified fangs facilitate the inoculation of secretions, considered a "primitive form of venom." Other species of large sympatric colubroids were also examined, and some analogous structures were observed.

Full text

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Phyllomedusa - 22(2), December 2023
Received 08 August 2023
Accepted 30 October 2023
Distributed December 2023
The role of modied teeth in the function of prolonged
bites in Hierophis viridiavus (Serpentes: Colubridae)
Alessandro Paterna
OPHIS Museo Paleontologico e Centro Erpetologico, 64100 Teramo, Italy. E-mail: alessandro.paterna@hotmail.com.
Phyllomedusa 22(2):121–130, 2023
© 2023 Universidade de São Paulo - ESALQ
ISSN 1519-1397 (print) / ISSN 2316-9079 (online)
doi: http://dx.doi.org/10.11606/issn.2316-9079.v22i2p121-130
Abstract
The role of modied teeth in the function of prolonged bites in Hierophis viridiavus
(Serpentes: Colubridae). Analysis of the maxillary, palatine, pterygoid, and dentary
bones of the Western Whipsnake, Hierophisviridiavuscarbonarius, revealed the presence
of grooves and ridges in the teeth on the four dentiferous bones. Enlarged and modied
rear teeth were found on the posterior maxillaries, separated by alveolar diastema and
aligned dierently from the anterior maxillary teeth. In both live and dissected specimens,
Duvernoy’s gland, associated with the production of toxins, surrounds the rear maxillary
teeth, which deliver the secretions produced by the gland. These characters, plus the
iniction of prolonged bites, facilitate the subduing of prey. The morphology of the
palatomaxillary arch places H. viridiavus in the group of opisthoglyphous colubroids,
whose modied fangs facilitate the inoculation of secretions, considered a “primitive form
of venom.” Other species of large sympatric colubroids were also examined, and some
analogous structures were observed.
Keywords: Duvernoy’s glands, Modied fangs, Opisthoglyphous, Western Whipsnake.
Resumo
O papel dos dentes modicados em mordidas prolongadas de Hierophis viridiavus
(Serpentes: Colubridae). A análise dos ossos maxilares, palatinos, pterigóides e dentários de
Hierophisviridiavuscarbonarius revelou a presença de sulcos e cristas nos dentes dos quatro ossos
dentíferos. Dentes posteriores ampliados e modicados foram encontrados nos maxilares posteriores,
separados por diástemas alveolares e alinhados de forma diferente dos dentes maxilares anteriores.
Tanto nos espécimes vivos como nos dissecados, a glândula de Duvernoy, associada à produção de
toxinas, circunda os dentes maxilares posteriores, que liberam as secreções produzidas pela glândula.
Essas características, além da inição de mordidas prolongadas, facilitam a dominação da presa. A
morfologia do arco palatomaxilar coloca H. viridiavus no grupo dos colubróides opistóglifos, cujas
presas modicadas facilitam a inoculação de secreções, consideradas uma “forma primitiva de
veneno”. Outras espécies de grandes colubróides simpátricos também foram examinadas, e algumas
estruturas análogas foram observadas.
Palavras-chave: Glândula de Duvernoy, Opistoglifodonte, Presas modicadas, Serpentes.

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Introduction
When we nd ourselves in front of a snake,
the rst and most common need is to establish
whether it is venomous. The Western Whipsnake,
Hierophis viridiavus (Lacépède, 1789), the
subject of this study, is a colubrid species that is
widespread in Italy and southern France, in
addition to adjacent countries including
Switzerland, Croatia, and Spain (Kreiner 2007).
It occurs in Germany as an introduced
allochthonous species (Paterna 2023). To date,
this snake is considered a non-venomous
colubrid (Sindaco et al. 2006, Kreiner 2007, Di
Nicola et al. 2021) or aglyphous, meaning that it
does not possess a venom fang model similar to
those of opisthoglyphous colubrids or real venom
glands. The opisthoglyphous dentition is
characterized by the presence of enlarged and
modied rear maxillary teeth (Weinstein et al.
2011) and postocular glands called Duvernoy’s
glands, which produce venom in several species
(Rodriguez-Robles 1994, Lumsden 2004). Other
authors have stated that the Western Whipsnake
is equipped with such glands, and the toxicity of
this species has been demonstrated (Phisalix and
Caius 1916). Cases in which adult humans
reported clinical complications after the bite of
this snake have been reported (Weinstein et al.
2011, Dutto et al. 2015).
Following observations of live specimens of
H. viridiavus carbonarius in the eld, as well
as observing the presence in the palatomaxillary
arch of a gland located near the posterior
maxillary tooth, I performed dissections and
microscopy of the jaws of deceased specimens
and other sympatric colubroid species for
comparison.
Materials and Methods
The samples used in the osteological
investigation came from three adult males and
two females of Hierophisviridiavuscarbonarius
that were found dead on the road in the Abruzzo
region, Italy, in spring and summer 2023. An
adult male Zamenis longissimus (Laurenti, 1768)
and a subadult female Natrix helvetica (Lacépède,
1789), roadkills from the same region, were used
for comparison. Bones of the specimens were
prepared at OPHIS Museo Paleontologico e
Centro Erpetologico (Teramo, Italy) using
surgical tools and sodium hypochlorite. From
each specimen the two maxillary bones, the two
palatines, the two pterygoids, and the two
dentaries were examined. Shed teeth from
captive bred Elaphe quatuorlineata Lacépède,
1789, originally from Apulia, Italy, were
collected from live specimens at OPHIS.
Microphotographs of the cranial bones and teeth
were taken using a stereomicroscope Nikon
SMZ1500 together with a Digital Sight DS-2Mv
camera at the Faculty of Veterinary Medicine of
the University of Teramo.
Live specimens of H. viridiavus, Z.
longissimus, E. quatuorlineata, Hemorrhois
hippocrepis (Linnaeus, 1758), and N. helvetica,
part of the OPHIS collection, were used for in
vivo anatomical comparisons. Photographic
material of the latter was obtained with a Sony
α6000 digital camera, while photos of the cranial
bones of H. viridiavus were obtained with a
Nikon Coolpix P510.
Results
Microscopy of the Dentiferous Bones
In prepared samples of Hierophisviridiavus
carbonarius, minor sulci and crests were found
in the teeth of all four dentiferous bones. The
maxillary teeth have a depression on the lingual
surface that is longitudinally incised by a thin
groove (Figure 1A), while the mid-posterior
teeth have a deeper canal-like fossa posteriorly
(Figure 1B). Pterygoid teeth have a basal fossa
and a distal ridge in the labial wall (Figure 1C).
Palatine teeth present a slight depression labially
located as the nutritive alveolar foramina and a
thin ridge on the lingual surface. Additional
isolated furrows are present in the teeth of the
maxilla and the pterygoid (Figure 1D). The most
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Phyllomedusa - 22(2), December 2023
anterior teeth in the dentaries feature a small
fossa close to the edge of the crown and a distal
second fossa (Figure 1E). The posterior teeth of
the dentary also feature slight lingual depressions
and a mesial cutting edge.
The most posterior teeth of the maxillae are
distinguishable, even by eye, as longer and
thicker than all other teeth (Racca et al. 2020).
The alveoli of the two posterior teeth are adjacent
to each other but separated by a diastema from
the anterior one, for a length slightly shorter than
that of an alveolus corresponding to the
ectopterygoid process (Figure 1F). Here the
maxillary arch presents a deviation of about 20°
labially, positioning the enlarged teeth o-axis
from the anterior teeth, which are uniformly
placed with the same interdental space to the
rostral extremity of the maxilla. The anterior
maxillary teeth, and the teeth present in the other
three dentiferous bones, show a lingulolabially
compressed base and an anteroposteriorly
backwards-bent crown that gives the entire tooth
a shark n-shaped silhouette. This laterally
compressed shape is also observable in the
alveoli of the maxilla, while the two last
separated alveoli display a circular alveolar
margin (Figure 1F).
These two posterior teeth dier from the rest
in the morphology of the crown. Mesially a
sulcus/canal is present, delimited by two ridges
running along the entire length of the tooth from
the base of the crown to its apex (Figure 2).
Labially, in the basal half of the tooth, a triangular
fossa is delimited by two prominent ridges,
converging in a “V” shape, which reach the
crown’s tip. A second longitudinal fossa is
located labiodistally after the posterior one of the
two ridges that border the basal fossa. In the
distal half of the teeth, the intervals between the
mesial sulcus and the fossae highlight the four
ridges that converge at the apex of the crown,
giving the tooth a star-shaped section in lingual
view (Figure 2). Rugosities occur on the
projected surface of the central ridges in the
basal half. In the two rear maxillary teeth, the
basal portion in contact with the bone appears
more compact, with a more circular section,
widening like a bulb before resuming the “sharp”
shape. At the base of the last maxillary tooth, a
small portion of the root is visible. Here the
nutritional foramen assumes the shape of an
inverted teardrop, where the angled lower end
culminates directly in the crown, which is
consequently indented. A slight longitudinal
groove twice as long as the nutritional foramen
originates from this notch. This condition is
absent in the other maxillary teeth, in which the
nutritional foramen is usually circular in shape
and located at the base of the root.
Dissection
The head of a roadkilled adult male Hierophis
viridiavus carbonarius was dissected; scales
and skin were removed dorsally and laterally. In
lateral view Duvernoy’s gland is visible at the
posterior end of the maxilla, anteriorly reaching
and surrounding the two rear maxillary teeth
(Figure 3). The posteriormost maxillary tooth
emerges from the gland at the apex of the crown,
visible in both lateral and ventral views. Also in
lateral view, dorsoposteriorly in contact with
Duvernoy’s gland, is the Harderian gland,
delimited ventroanteriorly by the ectopterygoid
and the postocular (Figure 3).
In Vivo Observations
During eld studies (Paterna 2015, unpubl.
data) and while observing captive specimens of
Hierophis viridiavus carbonarius, two reddish
to purplish glands at the posterior ends of the
maxillae were observed at the level of the sixth
supralabial scale (Figure 4A). These glands
correspond to the position of Duvernoy’s glands
observed in the dissected skull in both lateral
and ventral view. Such glands are visible in vivo
in both adult and juvenile specimens. The glands
are easily distinguished from the surrounding
mucosa by color variation. The tip of the rear
maxillary tooth emerges from the cu of tissue
and can be further uncovered by moving the
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Phyllomedusa - 22(2), December 2023
Figure 1. Stereomicroscope pictures of the groove details in the teeth of the dentiferous bones in specimens of
Hierophis viridiflavus carbonarius from Abruzzo, Italy. (A) Adult female, right maxillary tooth in lingual
view. (B) Adult male, maxillary tooth in distal view. (C) Adult female, right pterygoid teeth in lingual view.
(D) Detail of the lingual groove in the right maxillary tooth of an adult female. (E) Adult female, anterior right
dentary tooth in lingual view. (F) Photo of the toothless right maxilla in an adult male in ventral view.
A B
C
E
D
F
mucosa rostrodorsally. Anterolaterally to this,
corresponding with the maxillary deviation
occurring between the line of the two rear and
the anterior teeth, it is possible to distinguish a
pocket, which is more easily identiable in
younger specimens.
In the other species examined (Zamenis
longissimus, Elaphe quatuorlineata, Hemorrhois
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Figure 2. Stereomicroscope pictures in varied contrast of a left rear maxillary tooth in mesiolingual view from an adult
male of Hierophis viridiflavus carbonarius from Abruzzo, Italy.
Figure 3. Dissected skull of an adult male Hierophis
viridiflavus carbonarius from Abruzzo, Italy.
Abbreviations: dg, Duvernoy’s gland; dn,
dentary; ep, ectopterygoid; fr, frontal; hg,
Harderian gland; mx, maxilla; ns, nasal; pf,
prefrontal; pm, premaxilla; po, postocular; qd,
quadrate; rmt, rear maxillary tooth; sr,
surangular.
hippocrepis, and Natrix helvetica), the above
characters were found only in H. hippocrepis
(Figure 4B). As in the case of H. viridiavus,
these characters were more readily observed in
juveniles. Photographs of H. viridiavus, H.
hippocrepis, and Z. longissimus (Figure 4C)
demonstrate the presence or absence of the
gland.
Distinctive Features in the Dentition of the Species
More or less obvious furrows and ridges are
found in the dentiferous bones of Zamenis
longissimus and Natrix helvetica (Figure 5A–F).
Enlarged maxillary teeth have been found in N.
helvetica, in which the rear maxillary teeth share
the “blade tooth” morphology. The posteriormost
tooth, saber-shaped, exhibits a distal carina and
a smaller mesial one (Figure 5A). The other
maxillary teeth also feature slight keels but are
more tapered and undulated (Figure 5C). In Z.
longissimus, the anterior maxillary teeth are
larger and longer than the posterior teeth. In the
maxillae of these two species, the alveoli and
consequentially the teeth, are aligned without
any relevant diastema, unlike Hierophis
viridiavus. Elaphe quatuorlineata exhibits long
maxillary teeth (Figure 5G, H), with the
posteriormost featuring a mesial longitudinal
sulcus in the distal half of the crown (Figure
5G).
Discussion
Hierophis viridiavus is known to bite if
handled, and its bite is prolonged with repeated
chewing-like movements of the jaws. Bites from
this species may produce temporary neurotoxic
symptoms in humans (Weinstern et al. 2011,
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Phyllomedusa - 22(2), December 2023
Figure 4. Details of Duvernoy’s gland and rear maxillary teeth in the palatomaxillary arch of (A) an adult female
Hierophis viridiflavus carbonarius, and (B) a young male Hemorrhois hippocrepis. (C) Palatomaxillary arch
of an adult male Zamenis longissimus. Abbreviations: g, cuff of gland; p, pocket; rf, rear fang.
Dutto et al. 2015) and severe neurotoxic and
hemotoxic symptoms leading to death in small
mammals (Phisalix 1922). The teeth of Hierophis
viridiavus carbonarius exhibit ridges and
grooves both of which confer a better grip during
the bite (Oliveira et al. 2016) and transmit mixed
oral secretions to the penetrated tissues.
Young and Kardong (1996) examined the
teeth of the four dentiferous bones of 661 snake
species including 739 colubrid specimens.
Although species names and numbers of
individuals of each species were not provided,
some information may be obtained from this
study. Furrowed teeth were present in the anterior
maxilla in 0.5% of the individuals examined and
in the posterior maxilla in 1% of the specimens.
In 1% the furrowed teeth were in the palatine, in
2% the pterygoid, and in 5% the dentary. Only
three opisthoglyphous species were named:
Ahaetulla prasina preocularis (Taylor, 1922),
Boiga cyanea (Duméril, Bibron and Duméril,
1854), and Rhachidelus brazili Boulenger, 1908,
in which furrows were reported in the anterior
half of the maxilla. Of the 36 specimens of
colubrids examined that exhibited furrowed
teeth, these teeth occurred in both the palatine
and the pterygoid in 5 (14%) of the specimens
(Young and Kardong 1996). Hierophis
viridiavus exhibited furrowed teeth in all four
dentiferous bones, and according to Young and
Kardong (1996) this condition is present in very
few colubrid or colubroid species.
The heterodonty found within the maxillary
teeth and the morphology of the maxillary bone
place H.viridiavus within the opisthoglyphous
snakes. Not only does this species have separated
and enlarged posterior maxillary teeth but also
these teeth are characterized by the presence of
prominent grooves and ridges. Elongate maxillary
posterior teeth, together with well-dened
Duvernoy’s glands, represent a pre-adaptation to
the subduing of prey, from which venom glands
evolved for rapid killing (Kardong 1982). Other
studies consider Duvernoy’s gland not dierent
from the venom glands present in elapids and
viperids (Weinstein and Kardong 1994, Fry et al.
2008). Contrary to the venom glands present in
solenoglyphous and proteroglyphous snakes, the
duct of Duvernoy’s gland is not directly
channeled into the teeth, but rather leads into a
dened space or cu around one or more teeth
(Zalisko and Kardong 1992, Kardong and Lavin-
Murcio 1993); in H. viridiavus these are the
two posteriormost maxillary teeth. In the
dissected specimen, these enlarged teeth are
completely surrounded by Duvernoy’s gland,
leaving only the apex of the crown visible. When
a prey animal is bitten, the mucous membrane
comes into direct contact with the surface of the
tegument, which, following the compression
Paterna
A B C

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Phyllomedusa - 22(2), December 2023
Figure 5. Stereomicroscope pictures of the dentiferous bones of the colubrid species investigated. (A) Natrix helvetica
lanzai, rear maxillary tooth in lingual view. (B) Natrix helvetica lanzai, rear maxillary tooth in mesial view.
(C) Natrix helvetica lanzai, maxillary teeth in lingual view. (D) Natrix helvetica lanzai, left dentary in lingual
view. (E) Zamenis longissimus, left maxillary teeth in lingual view. (F) Zamenis longissimus, left dentary teeth
in lingual view. (G) Elaphe quatuorlineata quatuorlineata, rear maxillary tooth in mesial view. (H) Elaphe
quatuorlineata quatuorlineata, maxillary tooth in distal view.
A
C
G
E
B
D
H
F
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Phyllomedusa - 22(2), December 2023
generated by the bite, causes the secretion of
Duvernoy’s glands to be released directly on the
wound. The pressure of the bite unsheaths the
rear maxillary teeth from the mucosa, and the
secretion enters the bite along the ridges and
grooves of the teeth. The eectiveness of the bite
is augmented by the grooves present in other
teeth and by the masticating action of the
prolonged bite. In addition, the pockets located
labially to the enlarged maxillary teeth may
accumulate the secretions of Duvernoy’s glands,
as in the American water snake Nerodia sipedon
(Linnaeus, 1758) (Ranayhossaini 2010). Substantial
amounts of secretions inside the mouth of H.
viridiavus were observed, especially in adult
specimens.
The above constitute mechanisms that
maximize the amount of secretion in a “low
pressure” system (Taub 1967, Kardong and
Lavin-Murcio 1993, Weinsten et al. 2013),
lacking muscular insertions in the venom glands
typical of snakes with anterior venom fangs. The
bite and neurotoxicity of the secretion may play
an important role in predation by H.viridiavus,
which takes a wide variety of prey (Filippi et al.
2003, Mondino et al. 2022) despite that it cannot
be considered a “constrictor” snake.
Dentition in Other Species
Enlarged and modied rear maxillary teeth
were found in Natrix helvetica lanzai. Although
dierent from the teeth of Hierophisviridiavus,
its fangs resemble those observed in several
opisthoglyphous colubrids (Weinstein et al. 2011).
Natrix helvetica (Natrix natrix sensu lato), along
with H. viridiavus, has been considered an
aglyphous ophid (Sindaco et al. 2006, Kreiner
2007, Di Nicola et al. 2021) even though the
clinical consequences of its bite in humans has
been documented (Gardner-Thorpe 1967, Satora
2004, GläßerTrobisch and Trobisch 2008).
Analogous glands to those surrounding the
rear maxillary teeth of H.viridiavus have been
observed in the palatomaxillary arch of
Hemorrhois hippocrepis. Cases of mild local
eects following the bite of the congeneric
Hemorrhois algirus and Hemorrhois nummifer
are present in literature (Mamonov 1977, Malik
1995, Weinstein et al. 2011, Kazemi et al. 2023).
Conclusion
Several unsuspected characters in the upper
jaws of Hierophis viridiavus that are involved
in the inoculation of salivary secretions,
especially those produced by Duvernoy’s glands,
were found. These morphologies are linked to
the predisposition of this species to inict
prolonged, “chewing” bites, a widespread and
distinctive behavior of this snake among the
Italian ophidian fauna. The morphology of the
maxillary bone places this species within the
opisthoglyphous snakes, equipped with modied
fangs apposite for the transmission of secretions
that can be considered a “primitive form of
venom.” The presence of grooves on most teeth
suggests that H.viridiavus should be considered
polyglyphous, rather than aglyphous. Grooves
were observed in the four dentiferous bones of
other European species, although it is uncommon
within colubroids. Among the Italian fauna, the
opisthoglyphous species occur in limited
northern border areas and small islands in the
south (Sindaco et al. 2006), making H.viridiavus
an exception within the large “aglyphous”
colubrids on the mainland.
Similar inoculation systems were observed in
the large European colubroids Natrix helvetica
and Hemorrhois hippocrepis; the presence of
Duvernoy’s glands and neurotoxic secretions
have previously been documented in both genera
(Phisalix 1922, Ovadia 1984, Jackson 2003,
Weinstein et al. 2011).
Although changing the status of H.
viridiavus from harmless to humans is not
recommended, special attention should be given
not only to this species, but to the entire
Palearctic whipsnake/racer complex (sensu Nagy
et al. 2004) and the genus Natrix. All these
species possess morphology capable of delivering
toxic bites.
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Phyllomedusa - 22(2), December 2023
Acknowledgments
I thank Luca Palazzese for his help, time, and
use of the instrumentation of the Laboratories of
the Veterinary Medicine Faculty of Teramo. I
thank Associate Editor Ross D. MacCulloch,
Editor-in-Chief Jaime Bertoluci, and anonymous
reviewers for their comments and opinions of
this study.
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