ArticlePDF Available

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

Authors:
  • OPHIS Museo Paleontologico e Centro Erpetologico

Abstract and Figures

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.
Content may be subject to copyright.
121
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.
122
Phyllomedusa - 22(2), December 2023
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
Paterna
123
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
ModiedteethinHierophis viridiavus
124
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
Paterna
125
Phyllomedusa - 22(2), December 2023
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,
ModiedteethinHierophis viridiavus
126
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
127
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
ModiedteethinHierophis viridiavus
128
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.
Paterna
129
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.
References
Di Nicola, M. R., L. Cavigioli, L. Luiselli, and F. Andreone.
2021. Anbi & Rettili d’Italia - Edizione Aggiornata.
Latina. Edizioni Belvedere. 576 pp.
Dutto, M., I. Ineich, F. Serre-Collet, M. Goyon, and R.
Bédry. 2015. Trois cas de morsures du Colubridé
Hierophis viridiavus (Lacépède, 1789). Bulletin de la
Société Herpétologique de France 156: 55–62.
Filippi, E., M. Capula, and L. Luiselli. 2003. Dietary shifts in
the Western Whip Snake Coluberviridiavus Lecépède,
1789 of the small Mediterranean island of Ustica
(Squamata: Serpentes: Colubridae). Herpetozoa 16: 61–
66.
Fry, B. G., H. Scheib, L. van Weerd, B. A. Young, J.
McNaughtan, S. F. R. Ramjan, R. E. Poelmann, and J. A.
Norman. 2008. Evolution of an arsenal: structural and
functional diversication of the venom system in the
advanced snakes. Molecular & Cellular Proteomics
2008: 215–246.
Gardner-Thorpe, C. 1967. Snakebite poisoning. British
Medical Journal 26: 558.
Gläßer-Trobisch, A. and D. Trobisch. 2008. Bissunfall bei
einer Ringelnatterfütterung. Elaphe 16: 59–61.
Jackson, K. 2003. The evolution of venom-delivery systems
in snakes. Zoological Journal of the Linnean Society
137: 337–354.
Kardong, K. V. 1982. The evolution of the venom apparatus
in snakes from colubrids to viperdis & elapids. Memórias
do Institudo de Butantan 46: 105–118.
Kardong, K. V. and P. A. Lavin-Murcio. 1993. Venom
delivery of snakes as high-pressure and low-pressure
systems. Copeia 1993: 644–650.
Kazemi, S. M., M. H. Jahan-Mahin, T. Mohammadian-Kalat,
M. S. Hosseinzadeh, and S. A. Weinstein. 2023. Local
envenoming by the coinsnake or Asian racer, Hemorrhois
nummifer and mountain racer or leopard snake,
Hemorrhois ravergieri (Serpentes: Colubridae, Colubrinae)
in Iran: a reminder of the importance of species
identication in the medical management of snakebites.
Toxicon 226: 107070.
Kreiner, G. 2007. The Snakes of Europe. Frankfurt am Main.
Edition Chimaira. 317 pp.
Lumsden, N. G., B. G. Fry, R. Manjunatha Kini, and W. C.
Hodgson. 2004. In vitro neuromuscular activity of
‘colubrid’ venoms: clinical and evolutionary implica-
tions. Toxicon 43: 819–827.
Malik, G. M. 1995. Snake bites in adults from the Asir region
of southern Saudi Arabia. American Journal of Tropical
Medicine and Hygiene 52: 314–317.
Mamonov, G. 1977. Case report of envenomation by the
mountain racer, Coluber ravergieri in USSR. The Snake
9: 27–28.
Mondino, A., J. Crovadore, F. Lefort, and S. Ursenbacher.
2022. Impact of invading species on biodiversity: diet
study of the green whip snake’s (Hierophis viridifavus,
L. 1789) in Switzerland. Global Ecology and
Conservation 38: e02239.
Nagy Z. T., R. Lawson, U. Joger, and M. Wink. 2004.
Molecular systematics of racers, whipsnakes and
relatives (Reptilia: Colubridae) using mitochondrial and
nuclear markers. Journal of Zoological Systematics and
Evolutionary Research 42: 223–233.
Oliveira, L., R. R. Scartozzoni, S. M. Almeida-Santos, C. Jared,
M. M. Antoniazzi, and M. G. Salomão. 2016. Morphology
of Duvernoy’s glands and maxillary teeth and a possible
function of the Duvernoy’s gland secretion in Helicops
modestus Günther, 1861 (Serpentes: Xenodontinae). South
American Journal of Herpetology 11: 54–65.
Ovadia, M., 1984. Embryonic development of Duvernoy’s
gland in the snake, Natrix tessellata (Colubridae).
Copeia 1984: 516–521.
Paterna, A. 2015. Morphological traits of hatchlings of the
Western Whip snake Hierophis viridifavus (Lacépède,
1789) from a central Italian population. Russian Journal
of Herpetology 22: 179–187.
Paterna, A. 2023. Intraspecifc oophagy in Hierophis
viridifavus (Serpentes: Colubridae) during oviposition
in a controlled environment. Phyllomedusa 22: 29–35.
Phisalix, M. 1922. Animaux Venimeux et Venins. Volume 2.
Paris. Masson et Cie. 1512 pp.
Phisalix, M. and F. Caius. 1916. Propriétés venimeuses de la
salive parotidienne chez des Colubridæ aglyphes des
genres Tropidonotus Kuhl, Zamenis et Helicops Wagler.
Bulletin du Muséum National d’Histoire Naturelle
22: 213–218.
ModiedteethinHierophis viridiavus
130
Phyllomedusa - 22(2), December 2023
Racca, L., A. Villa, L. C. M. Wencker, M. Camaiti, H. A.
Blain, and M. Delno M. 2020. Skull osteology and
osteological phylogeny of the Western Whip snake
Hierophis viridiavus (Squamata, Colubridae). Journal
of Morphology 281: 808–836.
Ranayhossaini, D. J. 2010. An Investigation of the
Hemotoxicity of the Duvernoy’s Gland Secretionof the
Northern Water Snake (Nerodia sipedon). Pennsylvania
State University Schreyer Honors College. 26 pp.
Rodriguez-Robles, J. A. 1994. Are the Duvernoy’s gland
secretions of colubrid snakes venoms? Journal of
Herpetology 28: 388–390.
Satora, L. 2004. Bites by the grass snake Natrix natrix.
Veterinaryand Human Toxicology 46: 334–334.
Sindaco R., G. Doria, E. Razzetti, and F. Bernini. 2006.
AtlantedegliAnbiedeiRettilid’Italia. Firenze. Societas
Herpetologica Italica. Edizioni Polistampa. 792 pp.
Taub, A. M. 1967. Comparative histological studies on
Duvernoy’s gland of colubrid snakes. Bulletin of the
American Museum of Natural History 138: 1–50.
Weinstein, S. A, J. White, D. E. Keyler, and D. A. Warrell.
2013. Non front-fanged colubroid snakes: a current
evidence based analysis of medical signicance. Toxicon
69: 103–13.
Weinstein, S. A., D. A. Warrell, J. White, and D. E. Keyler.
2011. “Venomous” Bites from Non Venomous Snakes. A
Critical Analysis of Risk and Management of “Colubrid”
Snake Bites. Waltham. Elsevier Inc. 364 pp.
Weinstein, S. A. and K. V. Kardong. 1994. Properties of
Duvernoy’s secretions from opisthoglyphous and
aglyphous colubrid snakes. Toxicon 32: 1161–1185.
Young, B. A. and K. V. Kardong. 1996. Dentitional surface
features in snakes (Reptilia: Serpentes). Amphibia-
Reptilia 17: 261–276.
Zalisko, E. J. and Kardong, K. V. 1992. Histology and
histochemistry of the Duvernoy’s gland of the brown
tree snake Boiga irreguluria (Colubridae). Copeia
1992: 791–798.
Editor: Ross D. MacCulloch
Paterna
... Melanistic specimens have been reported from the island of Alonissos (Cattaneo, 1998;Broggi, 2010;Kalogiannis, 2021). In this study we analysed the dentiferous bones of three specimens of D. caspius from this last-mentioned locality, focusing specifically on the morphology of the maxillae, to verify the presence of the traits recently described in the close taxa Hierophis viridiflavus (Lacépède, 1789) and Hemorrhois hippocrepis (Linnaeus, 1758), attributable to an opistoglyphous dentition (Paterna, 2023). ...
... The two teeth may work as a single functional unit (Knox & Jackson, 2010), and such as in Helicops modestus, the mesio-distal contact point between the two overlapping teeth could act as a lateral canal in which the oral secretions flow during the biting/chewing action (Oliveira et al., 2016). These posterior teeth, as in the case of H. viridiflavus (Paterna, 2023), are covered by a cuff/sheath visible in the palatomaxillary arch in live specimens (Fig. 8). These cuffs are easily recognizable due to their morphology and different coloration compared to the surrounding mucosa. ...
... These cuffs are easily recognizable due to their morphology and different coloration compared to the surrounding mucosa. In H. viridiflavus these are located medially to the Duvernoy's gland, which converges ventrally towards the posterior maxillary teeth (Paterna, 2023). ...
Article
Full-text available
The analysis of the dentiferous bones, in particular of the maxillae of the Caspian whipsnake Dolichophis caspius, reveals the presence of features typical of opisthoglyphous colubroids. Modified teeth are present in the posterior extremities of the maxillae, morphologically different from the anterior ones, from which they are separated by an alveolar diastema. In correspondence of such diastema, the maxillary bone deviates ventrally, positioning the rear teeth inferiorly than the anterior ones. As in other opisthoglyphous species, such characteristics are also visible in the palatomaxillary arches of in vivo individuals, as the rear maxillary teeth are covered by cuffs/sheaths which are easily recognizable from the surrounding mucosa. Presence of such traits was also found in the congeneric Dolicohphis jugularis and Dolichophis schmidti, and discussed in the other western Palearctic whipsnakes and racers species, suggesting that such adaptations may be developed in common ancestors from which such clade originated.
Article
Non-front-fanged snakes (NFFS) have long been overlooked by snake venom research, likely due to most of them being considered non-medically relevant for humans. The paucity of information about composition and activities of NFFS venoms and oral secretions makes it difficult to assess whether a given species can inflict medically significant bites. Here, we provide a review of the information currently available about the symptoms/signs elicited by bites from European NFFS, aiming to offer a foundation for understanding the threat they pose in terms of snakebite. Despite an overall limited amount of available data for most of the considered taxa, the genus Malpolon is notable for its capacity to cause local and systemic envenoming, including neurotoxic symptoms. Bites by other genera like, Hemorrhois, Hierophis, Natrix, Platyceps, Telescopus, and Zamenis are mainly associated with local symptoms, but the extent of their medical significance remains unclear. Our findings suggest that, although bites from European NFFS generally cause only mild effects, the potential occurrence of systemic effects from some species cannot be ruled out. Considering the above, any bite by European NFFS should receive professional medical evaluation in order to ensure patient safety and appropriate management, as well as detailed documentation facilitating construction of an accurate medical risk profile for the species.
Article
Full-text available
Intraspecific oophagy in Hierophis viridiflavus (Serpentes: Colubridae) during oviposition in a controlled environment. Following the observation of adult pairs of the Western Whipsnake, Hierophis viridiflavus, in a controlled environment, two distinct but related phenomena were observed: egg deposition and predation of freshly laid eggs by the male. Data about deposition, number and morphology of the eggs, hatching and offspring are presented and compared with the literature. The episode of oophagy is described, confirming the inclination to predate snake eggs and intraspecific oophagy in this species.
Article
Full-text available
Next-generation sequencing is increasingly used in conservation biology to resolve complex interactions between species, either diet or gut parasites studies. We applied a recent long metabarcoding method to elucidate the green whip snake’s (Hierophis viridiflavus) prey consumption based on DNA extracted from stomach contents. Illegally introduced in Canton of Vaud (Switzerland), three populations of the green whip snake have strongly developed in two regions, East (Chablais) and North. We suspect that this introduced species is threatening part of the local herpetofauna, especially the Asp viper and the Western green lizard in this region. Consequently, an extermination program has been implemented from 2016 to mitigate Hierophis viridiflavus expansion and its impact arising from its generalist diet. Stomach contents of 94 individuals removed from introduction sites were analysed by long metabarcoding. Our study revealed the consumption of 67 prey belonging to 9 species, primarily small mammals and reptiles. The recurrent presence of two parasitic nematodes was also discovered. Although cannibalistic behaviour could not be highlighted with this approach, a scavenging behaviour was suspected based on the presence of an insect used in forensic entomology (Calliphora vicina). These results confirm the opportunistic feeding behaviour of Hierophis viridiflavus and its ability to predate on threatened species. Although 86.6% of preys were not listed on the Swiss Red List, the impact on the Asp viper population can be important (up to 20% of consumed preys) and could partially explain its strong decline.
Article
Full-text available
We investigated the gross anatomy, histology and ultrastructure of Duvernoy's glands and scanning electron microscopy of maxillary teeth of Helicops modestus, as well as its prey-handling behavior in laboratory. We later compared this histology with other species of Hydropsini. Duvernoy's glands are located in the post-ocular region, immediately behind the supralabial gland. Each gland is connected to a pair of ungrooved rear fangs by a vestibule from which the secretion is drained. Histological analysis showed that the gland is wrapped by a layer of connective tissue and consists of a glandular body formed by prismatic cells organized in acini and a duct lined with columnar cells. The prismatic cells are positive to PAS and bromophenol blue, indicating glycoprotein content, whereas the columnar ductal cells are positive to PAS and alcian blue pH 2.5, indicating the presence of acid mucous. Transmission electron microscopy showed electron-dense, heterogeneous granules in the prismatic cells, whereas the granules of the columnar cells were electron-luscent and homogeneous. The Duvernoy's glands of H. modestus are more similar to those of H. angulatus than any other species analyzed. Observations of prey-handling behavior showed that H. modestus strikes and holds fish in its mouth while repeatedly carrying out bilateral raking motions with both maxillae. Ingestion starts headfirst. We observed only a single episode of constriction. Snakes usually swallowed fish alive but clearly immobilized, suggesting that the primary function of the Duvernoy's secretion is associated with the quiescence/immobilization of the fish prey.
Article
Full-text available
A western whip snakes’ communal nesting site has been discovered in central Italy. The morphological characteristics, differences and anomalies of the hatchlings of this species are described. The results of body weight and size showed different values to historical data. Sexual dimorphism has been observed in the number of ventrals and subcaudals, as well as in the size and weight of the specimens. Differences, anomalies and malformations in the head scutellation have been observed in 16% of the examined specimens. The photographic material allowed a classification of five different main types of head pattern. The data are provided in tables and diagrams.
Article
In Iran, there are approximately 4500-6500 snakebites per year, but fortunately only 3-9 of these are fatal. However, in some population centers such as Kashan city (Isfahan Province, central Iran), approximately 80% of snakebites are attributed to "non-venomous" snakes that are often comprised of several species of non-front-fanged snakes (NFFS). NFFS comprise a diverse group that constitute approximately 2900 species belonging to an estimated 15 families. We report here two cases of local envenoming from H. ravergieri, and one from H. nummifer that occurred in Iran. The clinical effects consisted of local erythema, mild pain, transient bleeding and edema. Two victims experienced progressive local edema that distressed the victims. The medical team's unfamiliarity with snakebites contributed to the incorrect clinical management of one victim including the contraindicated, ineffective provision of antivenom. These cases provide further documentation about local envenoming caused by these species, and also emphasize the need for regional medical personnel to receive increased training in order to improve familiarity with the local snake fauna and evidence-based snakebite management.
Article
The skull osteology of Hierophis viridiflavus is here described and figured in detail on the basis of 18 specimens. The sample includes specimens from the ranges of both H. viridiflavus viridiflavus and H. viridiflavus carbonarius as well as specimens not identified at sub-specific level. The main characters that define H. viridiflavus in comparison to the parapatric congeneric species Hierophis gemonensis are wide maxillary diastema, basioccipital crest well distinct in three lobes and basioccipital process well marked. The foramina of the otoccipital and prootic, and the basioccipital process of the basioccipital are among the most ontogenetically variable characters, as indicated by two juvenile specimens included in the sample. A specimen-level phylogenetic analysis including H. gemonensis and other outgroups (overall 6 species, 26 specimens, 64 skull characters) recovered all H. viridiflavus specimens in one clade, indicating the presence of a clear phylogenetic signal in the applied characters. However, the resolution within the H. viridiflavus clade is poor the monophyly of H. viridiflavus carbonarius was retrieved, but not that of Hierophis v. viridiflavus. Probably due to the relatively high variability, the skull morphology does not support the recently proposed specific status of the two subspecies. K E Y W O R D S intraspecific variation, ontogenetic variation, specimen-level phylogeny
Article
This book is the first significant contribution to thoroughly examine the potential hazards associated with snakes of the former family, Colubridae. This family contained >65% of living snake species (approximately 3,000 taxa) and has recently been split into multiple families. Many of these snakes produce oral secretions that contain toxins and other biologically-active substances. A large variety of these snakes figure in the pet industry, yet little documented information or formal study of their potential medical importance has been published. Therefore, although the possible medical importance of many of these species has been subjected to speculation since the mid-nineteenth century, there is a limited amount of useful descriptive information regarding the real hazard (or lack thereof) of snakes belonging to this diverse, artificial family. There is a need for "one-stop shopping" offering information regarding their possible toxicity and clinical relevance as well as recommendations for medical management of their bites. This book is the first synthesis of this information and includes evidence-based risk assessment, hazard rankings and specific recommendations regarding important species, many common in captivity. Fills a gap in the toxinological, medical and herpetological literature by providing a comprehensive review of this entire assemblage of snakes, with particular attention given to their capacity, real or rumored, to cause harm to humans A patient-centered, evidence-based approach is applied to analyzing documented case reports of bites inflicted by approximately 100 species. Clinical management of medically significant bites from non-front-fanged colubroids is methodically reviewed, and specific recommendations are provided.