Table Of Content1
An Overview of the Artificial
Assemblage, the Colubridae:
A Brief Summary of Taxonomic
Considerations
The taxonomy of this former assemblage is in dynamic transition and subject to
frequent and often conflicting recommended rearrangement. This very large artifi-
cial grouping often functioned as a sort of “disposal depot” (colloquially known as
a “taxonomic garbage can” or “rag bag”) for taxa of unestablished affinities. This
resulted in the incorrect assignment of many diverse and phylogenetically unrelated
ophidian species. For over 30 years, numerous taxonomists have devoted increasing
attention to resolving this complex issue by using methods involving morphologi-
cal (based on osteology, dentition, hemipenal morphology, lepidosis/meristics, etc.)
or molecular (analysis of nuclear or mitochondrial DNA sequences—sometimes
inferred from ribosomal RNA sequences—allozyme electrophoresis, immunodif-
fusion, etc.) methods or, less commonly, combined morphological and molecular
systematics (Cadle, 1988; Dessauer et al., 1987; Dowling et al., 1983, 1996; Heise
et al., 1995; Jenner and Dowling, 1985; Kraus and Brown, 1998; Lawson et al., 2005;
Pinou et al., 2004; Vidal et al., 2000, 2007, 2010; Zaher, 1999; Zaher et al., 2009).
Discussion of the current status of these ongoing reassignments is far too volumi-
nous to detail here. However, some recommended changes are summarized in Table
1.1. Analyses of previous taxonomic assignments have increasingly been subject
to more of a “splitting” (e.g., division of a given species, genus, subfamily, or family
into separate entities) approach, rather than “lumping” these together. For instance, the
crayfish-eating snakes (Regina spp.) of the tribe Thamnophiini are polyphyletic, and the
Thamnophiini itself has at least three major clades (Alfaro and Arnold, 2001). Ongoing
phylogenetic investigations will probably modify numerous subfamilies, genera, and
re-define existing lineages (Hedges et al., 2009; Pyron et al., 2011). It should be noted
that several medically important species have been recently reassigned. For example,
Vidal et al. (2007) and Zaher et al. (2009) recommended raising the previous subfamily,
Natricinae, to a full family, Natricidae (see Table 1.1). This family contains Rhabdophis
tigrinus and R. subminiatus, two species that have inflicted fatal or life-threatening bites
(Section 4.2). Such reassignments reinforce the call for the use of precise and current
taxonomy in clinical toxinology (Wüster et al., 1998). Some species can be reassigned;
this can lead to controversy and confusion in the literature. For example, historically, the
front-fanged mole vipers, burrowing asps, or stiletto snakes (Atractaspis spp., approxi-
mately 18 species; Plate 1.1A), were first considered viperids or elapids, then reassigned
to the colubrid subfamily, Aparallactinae (the centipede-eating snakes), then placed in
“Venomous” Bites from Non-Venomous Snakes. DOI: 10.1016/B978-0-12-387732-1.00001-4
© 2011 Elsevier Inc. All rights reserved.
2 “Venomous” Bites from Non-Venomous Snakes
Table 1.1 Summary of Proposed Taxonomic Reassignments for the Superfamily
Colubroidea and Other Medically Relevant Taxaa,b
Superfamily Colubroidea
Colubridae
Colubrinae (including Boiga, Dispholidus, Hierophis, Platyceps, Thelotornis)*
Grayiinae
Calamarinae
Dipsadidae
Dipsadinae (including Leptodeira, Sibynomorphus)*
Heterodontinae (Heterodon)*
Xenodontinae (including Alsophis, Boiruna, Clelia, Hydrodynastes, Phalotris, Philodryas,
Tachymenis)*
Natricidae (including Natrix, Rhabdophis, Thamnophis)*
Pseudoxenodontidae
Superfamily Elapoidea
Elapidae
Elapinae
Hydrophiinae
Lamprophiidae
Atractaspidinae*
Lamprophiinae
Psammophiinae* (including Malpolon)
Pseudoxyrhophiinae
Superfamily Homalopsoidea
Homalopsidae (including Cerberus, Homalopsis, Enhydris)*
Superfamily Viperoidea
Viperidae
Azemiopinae
Causinae
Crotalinae
Viperinae
a Taxa discussed in the text are marked with an asterisk.
b Further revision of the Colubroidea is underway and may modify the relationships shown here. For instance, Pyron
et al. (2011) supported the earlier definition of the Colubroidea, and thus recognized the subfamily status of a number of
clades. This includes the Natricinae, rather than the full family, Natricidae as assigned by Vidal et al. (2007), and Zaher
et al. (2009).
An Overview of the Artificial Assemblage, the Colubridae 3
(A) (B)
(C)
Plate 1.1 (A–C) Mole viper, burrowing asp, or stiletto snake (Atractaspis spp.). These unusual
fossorial snakes have long been subject to taxonomic revision. They possess notably enlarged,
canaliculated fangs that are freely rotatable on the maxilla. This makes manual handling impossible
as gripping these snakes behind the head in the conventional manner allows a penetrating jab from
the laterally highly mobile fang(s) (Plate 1.1A, A. fallax, Kenya; Plate 1.1B, West African mole
viper; slender burrowing asp, A. aterrima, Nigeria; Plate 1.1C, fangs from Reinhardt’s burrowing
asp; variable burrowing adder; itiuiu, A. irregularis, Niangara, Congo). Their venoms contain a
wide array of components, including multiple isoforms of cytotoxins and novel vasoconstrictor
peptides (e.g., sarafotoxins). Envenomations may be severe; life-threatening cases are well-
documented. Current taxonomic reassignments have recommended placement of these snakes from
their own family Atractaspididae into a subfamily, Atractaspidinae, of the Lamprophiidae, thereby
including one other taxonomically problematic front-fanged genus, Homoroselaps. However,
some investigators consider Homoroselaps spp. as members of the Elapidae. Many little-known
colubroids remain of uncertain taxonomic affinity (see text). Photos copyright to David A. Warrell
(Plate 1.1A and B) and Arie Lev (Plate 1.1C; AMNH specimen #12355).
their own family, Atractaspididae (Underwood and Kochva, 1993). These distinctive
snakes are now assigned by some investigators to the superfamily Elapoidea, as a sub-
family (Atractaspidinae) of the Lamprophiidae (www.reptile-database.org/; see Table
1.1). The lamprophiids include a number of species that are commonly kept in captivity.
Among the approximately 8-12 genera (depending on the author [s]) grouped within
the atractaspidids are taxa with mid-maxillary enlarged, grooved, and noncanaliculate
4 “Venomous” Bites from Non-Venomous Snakes
(B)
(A) (C)
Plate 1.2 (A–C) Maxilla and enlarged posterior maxillary teeth of the Natal black snake
(Macrelaps microlepidotus). The natural history of this rare semifossorial species is poorly
known. A non-front-fanged colubroid, it has traditionally been grouped with the unusual front-
fanged genus, Atractaspis (see text). There are a number of anecdotal cases of bites by this
species. Unfortunately, there is no documented clinical review of any of these victims. Effects
have allegedly included loss of consciousness and possible cranial nerve involvement, but
further information is required in order to critically evaluate the potential hazard associated
with bites from this uncommon species. As illustrated in the comparison of two specimens
in Plate 1.2A, the most posterior maxillary teeth are markedly enlarged and gently recurved.
They contain a shallow groove that extends along almost the entire medial-posterior surface
of the tooth (the position of the groove from an antero-lateral view is indicated by the arrow
in Plate 1.2B). The groove is visible (arrows) in Plate 1.2C. The uppermost specimen in Plate
1.2A is AMNH #5897; the other specimen in Plate 1.2A and Plate 1.2B and C is AMNH
#18227. See Appendix E for locality data; photos copyright to Scott A. Weinstein.
dentition (e.g., the Natal black snake, or Natal swartslang, Macrelaps microlepidotus,
Plate 1.2A–C), and front-fanged (“proteroglyphous”) canaliculated morphology (e.g.,
the dwarf garter snakes, Homoroselaps spp.), with Atractaspis spp. exhibiting markedly
enlarged distensible canaliculated fangs (Plate 1.1B and C) and notably elongated venom
glands. Deufel and Cundall (2003) noted the similarities between unilateral fang use in
Atractaspis and unilateral “slashing envenomation by some rear-fanged snakes.” However,
the loss of pterygoid teeth and associated maxillary movement resulted in the inability of
Atractaspis spp. to perform “pterygoid walk” prey transport.1 These authors remarked
1 “Pterygoid walk” prey transport refers to the alternating pterygoidal movements employed during active
deglutition of a seized prey item. This generally advances the maxillae, thereby drawing the grasped prey
into the snake’s esophagus, and facilitates swallowing.
An Overview of the Artificial Assemblage, the Colubridae 5
that “Atractaspis spp. appear to represent the evolutionary endpoint of a functional
conflict between envenomation and transport in which a rear-fanged envenomating
system has been optimized at the expense of most, if not all, palatomaxillary transport
function” (Deufel and Cundall, 2003). Therefore, although all of the fossorial and/or
nocturnal genera included in this group share many traits: slender body form with short
tails, and lacking a loreal scale; possessing smooth, shiny scales; relatively small heads
and eyes (Shine et al., 2006; see Plate 1.1A), and their monophyly is supported by
morphological and molecular data (McDowell, 1986; Underwood and Kochva, 1993;
Vidal et al., 2008; Zaher, 1999; Zaher et al., 2009), some genera possess markedly dif-
ferent dentitional morphology that notably influences their potential medical impor-
tance. Bites from Atractaspis spp. have caused serious envenomings (Kochva, 1998;
Kurnick et al., 1999; Wagner et al., 2009; Warrell et al., 1976a), while the medical
importance of uncommonly encountered genera such as Homoroselaps and Macrelaps
is unclear. Bites from M. microlepidotus have been reported to cause loss of conscious-
ness, and the species is considered “potentially lethal” by some authors (Vitt and
Caldwell, 2008), although all of these cases are anecdotal, without any formal medi-
cal evaluation or verification (Branch, 1982; Chapman, 1968; FitzSimons, 1919, 1962;
FitzSimons and Smith, 1958; Visser and Chapman, 1978). FitzSimons (1919) stated
that M. microlepidotus bites were insignificant, and Chapman (1968) described a bite
with minimal local effects. Similarly, the single well-documented bite from a dwarf-
spotted garter snake (Homoroselaps lacteus) consisted of only local pain and edema
(Branch, 1982). Thus, the atractaspidids are a distinctive series of snakes assigned to a
shared taxonomic status on the basis of strong morphological and molecular systematic
evidence. However, this taxonomy has placed together several species previously con-
sidered either “colubrids,” elapids, or viperids. Therefore, the revised biological classi-
fications of many species previously considered part of the “Colubridae” may result in
reassignments that can impact their perceived clinical importance by altering previous
taxonomic relationships, or by formulating new perceptions on the basis of relation-
ships to newly reassigned taxa.
It must be noted that to date, some of these reassignments (such as those involving
Atractaspis spp.) are not universally adopted or recommended by consensus and
may be subject to further changes or returned to their previous classification(s).
Therefore, the clinician must be proactive in seeking a thorough biological history
(through consultation with a knowledgeable toxinologist or professional herpetolo-
gist and/or via current literature) for any colubroid of unknown clinical importance
involved in a medically significant bite. This may provide clues about the potential
medical importance of the species involved as derived from observations of bites by
related taxa. It emphasizes the need for careful verification of recommended taxo-
nomic reassignments prior to their publication and general adoption. Such a standard
may frustrate taxonomists eager to achieve recognition of their findings, but this cau-
tion may also temper incorrect, premature assertions that can affect categorization of
an “envenomed” patient.
2
Differences Between Buccal Gland
Secretion and Associated Delivery
Systems of “True” Venomous
Snakes and “Colubrid” Snakes:
Low- Versus High-Pressure Gland
Function and Canaliculated Versus
Solid Dentition
A half-truth, like half a brick, is always more forcible as an argument than a whole
one. It carries better.
Stephen Leacock
2.1 Basic Considerations Regarding Gland Structure and
Function
The functional morphology of venom glands in “front-fanged” or “true” venomous
snakes (viperids, elapids, and atractaspidids) differs notably from the gland appara-
tus and associated dentition of other colubroids. An unknown number of these spe-
cies lack their homologous counterpart, the Duvernoy’s gland (Kardong, 1996; Taub,
1966; Weinstein and Kardong, 1994; Weinstein et al., 2010; Zalisko and Kardong,
1992). Taub (1967) reported that about 17% (approximately 30 species) of colubrid
snakes studied (120 genera, 180 species) lacked evidence of Duvernoy’s glands and,
in some discrete groups, as many as 90% examined lacked these glands.
Most Duvernoy’s glands lack any significant storage capacity, exhibit a duct sys-
tem distinguishable from that of venom glands of front-fanged snakes, and usually
have no direct striated muscle insertion to pressurize the fundus of the gland. The
consequence is a low-pressure secretion-injecting system (Kardong, 1996; Kardong
and Lavin-Murcio, 1993; Taub, 1967; Weinstein and Kardong, 1994; Weinstein et al.,
2010). Figure 2.1 (Panels A–C) illustrates the basic functional morphology of a typical
Duvernoy’s gland with its limited muscle attachment and associated dentition. Some
members of the tribe, Dispholidini (Section 4.3), are exceptions to this, as they do
have some limited striated muscle attachment on the gland fundus and thereby have
“Venomous” Bites from Non-Venomous Snakes. DOI: 10.1016/B978-0-12-387732-1.00002-6
© 2011 Elsevier Inc. All rights reserved.
As As
Cg
As
As
(A) (D)
Ld
Cld Se
Lu
Pd
Cc
Md
Oe Vg Avg
(B) (E)
Mx
Md Sd
Pk
Fs
Ep Ep
G
F F
(C) (F)
Figure 2.1 Comparison of a Duvernoy’s gland system in an “opisthoglyphous”
(“rear-fanged” non-front-fanged) snake (left) and a venom gland system in a model
“proteroglyphous” or “solenoglyphous” snake (right). Panel A. In the non-front-fanged
(“opisthoglyphous”) snake, Duvernoy’s gland (shaded) is located in the temporal region.
Adjacent striated muscles (e.g., adductor superficialis) run medially past the gland, but usually
are not directly attached. Dispholidus typus is an exception to this, as it does have limited muscle
attachment to the gland. Panel B. A cross-sectioned view of the Duvernoy’s gland that reveals
the arrangement of the internal duct system draining the extensive parenchyma. A single duct
departs from a small, central cistern within the gland, and runs to a cuff of oral epithelium
surrounding the posterior maxillary tooth (F). Panel C. When the posterior maxillary tooth
penetrates the integument of the prey or human victim, the cuff of the oral epithelium remains
on the surface, thereby receiving Duvernoy’s secretion, which flows around the tooth that may
(as depicted here) or may not be grooved (an “open system” with inherently low pressure).
Panel D. The venom gland (shaded) of this model proteroglyphous or solenoglyphous snake
includes a main venom gland, main duct accessory venom gland, and secondary duct that empty
into the base of the canaliculated (hollow) fang. Striated jaw muscles (e.g., adductor externus
superficialis in “proteroglyphous” elapids or compressor glandulae in “solenoglyphous”
viperids) act directly upon the venom gland to raise the intraglandular pressure and send a pulse
of venom from the gland through the duct to the fang. Panel E. A sagittal view of the venom
gland reveals the secretory epithelium, and extensive storage reservoir of venom. Panel F. When
the fang penetrates the integument of the prey, the attachment of the venom duct to the fang
tightens in order to maintain the relatively high-pressure head, and venom passes down the
hollow core of the fang to be delivered deeply into the tissues (a “closed system” with inherently
high pressure). Abbreviations: jaw muscles, adductor mandibulae externus superficialis (As),
compressor glandulae (Cg), accessory venom gland (Avg), central cistern (Cc), common lobular
duct (Cld), epithelium of prey integument (Ep), fang or enlarged maxillary tooth (F), fang sheath
(Fs), groove on surface of maxillary tooth (G), lobular duct (Ld), lumen holding secretory
product (Lu), main duct (Md), maxilla (Mx), oral epithelium (Oe), pocket of oral epithelium
around tooth (Pk), primary venom duct (Pd), secondary venom duct (Sd), secretory epithelium
(Se), main venom gland (Vg). After Weinstein and Kardong (1994) used with permission.
Low- Versus High-Pressure Gland Function and Canaliculated Versus Solid Dentition 9
some pressurization of the system (Fry et al., 2008; Taub, 1966; Weinstein et al., 2010).
The muscle insertion into the venom glands typical of front-fanged snakes exerts a
high-pressure head (often in excess of 30 psi; Kardong, 2009) facilitating rapid deliv-
ery of a significant volume of pre-stored venom bolus through the associated venom
ducts and canaliculate fangs (Figure 2.1, Panels D–F) that may be fixed (essentially,
permanently erect, “proteroglyphous,” Plate 2.1A–E) or erectile with varying mobility (or,
distensibility) according to size or species (“solenoglyphous,” Plate 2.2A; Kardong,
(A) (B)
Plate 2.1 (A and B) Fangs of the common Asian cobra (Naja naja). The fixed, erected,
canaliculated fangs are representative of the “proteroglyphous” dentition present in the Elapidae.
Many elapid species have short fangs, but some such as the coastal taipan (Oxyuranus scutellatus)
have long, slightly recurved fangs. Many elapid venoms contain multiple isoforms of postsynaptic
or presynaptic neurotoxins. These venoms may be delivered less deeply than those administered
by the often larger fangs of viperids, but this does not decrease their in vivo lethality.
(A) Profile of fangs of Naja naja, Sri Lanka.
(B) Close-up of fang of Naja naja, North India. Note the elongated oval-shaped bevel
(arrows) that closely resembles that of a hypodermic needle. The canaliculated (hollow or
containing a lumen) morphology facilitates deep injection of venom into the integument of
prey or human victim (see text).
(C) Fangs of the yellow-lipped sea krait (Laticauda colubrina), Madang, Papua New
Guinea. Hydrophiine sea snakes and laticaudiines (sea kraits) exhibit the “proteroglyphous”
dentition associated with high-pressure venom glands. Bites from laticaudiines are rare, but
may be life threatening when they occur (see text).
(D) Yellow-lipped sea krait (Laticauda colubrina), Madang, Papua New Guinea. While
hydrophiine sea snakes are ovoviviparous, the laticaudiines are oviparous, and come ashore
to lay their eggs in rock crevices. Their venoms contain postsynaptic neurotoxins (e.g.,
erabutoxins), and phospholipases A myotoxins.
2
(E) Close-up view of fangs of the olive sea snake (Aipysurus laevis), Roebuck Bay, Western
Australia. The fixed canaliculated fangs of this hydrophiine sea snake are closely set (arrows),
probably to establish a firm grip on struggling prey and possibly increase the likelihood of effective
venom delivery to the fishes of multiple niches belonging to at least 17 families and six different
morphological types that comprise a major part of the diet of this species (Heatwole and Cogger,
1993). Aipysurus laevis also preys on crustaceans, cephalopods, and fish eggs. Plate 2.1A, C, and
D, photos copyright to David A. Warrell; Plate 2.1B, AMNH specimen #64418; and Plate 2.1E,
AMNH specimen #86176, photos copyright to Arie Lev.
10 “Venomous” Bites from Non-Venomous Snakes
(C) (D)
(E)
Plate 2.1 C–E (Continued)
1979; Weinstein and Kardong, 1994). Some elapids exhibit incomplete fang can-
nula without complete fusion of the venom duct groove (Bogert, 1943). None of the
known colubroids of the former colubrid assemblage possess such dentition. The teeth
associated with Duvernoy’s glands are never canaliculate (i.e., never with a lumen),
but instead are solid, often enlarged, and sometimes deeply grooved (Fry et al., 2008;
Weinstein and Kardong, 1994; Weinstein et al., 2010; Young and Kardong, 1996).
Duvernoy’s gland morphology may vary considerably among non-front-fanged
colubroid species, and enlarged teeth associated with glands may be present mid- [e.g.,
Pampas snake, boipemi, cobra espada comum (other names as well), Tomodon dorsa
tus, Plate 2.3A–D], or notably posterior (e.g., Malpolon monspessulanus, Plate 2.4A–C),
in the maxilla (Broadley and Wallach, 2002; Fry et al., 2008; McKinstry, 1978; Taub,
1967; Weinstein et al., 2010). Several medically important species (i.e., some members
of the tribe, Dispholidini, see Section 4.3) have multiple enlarged, deeply grooved pos-
terior maxillary teeth with modifications probably adapted for enhanced conduction of
secretions into inflicted bite wounds (Broadley and Wallach, 2002; Meier, 1981; Section
4.3). It is important to note that other medically important species (e.g., R. tigrinus and
Low- Versus High-Pressure Gland Function and Canaliculated Versus Solid Dentition 11
(A) (B)
Plate 2.2 (A) Tropical rattlesnake; Neotropical rattlesnake; cascabel; cascavel;
maraca-boia; numerous other names (Crotalus durissus collilineatus) (Brazil) with
fangs erected. Central and South American rattlesnakes have markedly variable venoms
among different populations. Some secrete venoms that contain the potent heterodimeric
presynaptic neurotoxin, crotoxin, historically, the first toxin isolated from any snake venom.
Other populations lack this toxin, and secrete venoms that only contain toxins common to
many Crotalus spp. (procoagulants, hemorrhagins, hypotensive peptides, and numerous other
components). Bites from these snakes can cause severe systemic envenoming. Given their
sizable fang structure, venom reservoir, and potent venom, fatalities are common. Note the
distensible, strongly recurved, canaliculated front-fangs typical of “solenoglyphous” dentition.
The fang on the right side of the photo is expressing a drop of venom at the fang aperture.
(B) Close-up view of Western diamondback rattlesnake (Crotalus atrox) anterior maxilla and
fangs. This specimen has fangs that contain a visible groove that corresponds with the venom canal
or lumen. Viperid and elapid fangs have significant morphological variability. Several hypotheses
have attempted to establish evolutionary models for the development of dentition adapted for
venom delivery. One of these suggests that selective apoptosis (programmed cell death) contributes
to the formation of a fang lumen, or an external groove (see text).
Plate 2.2A, photo copyright to David A. Warrell; Plate 2.2B, AMNH specimen #137173,
photo copyright to Arie Lev.
R. subminiatus) lack grooves in their enlarged posterior maxillary teeth (Section 4.3).
This supports the accuracy of Stejneger’s contention that the presence of a grooved “rear
fang” is not strictly necessary for the introduction of Duvernoy’s secretion into a bite-
inflicted wound (Stejneger, 1893).
Although their morphology is variable (Fry et al., 2008; Weinstein et al., 2010),
the typical storage capacity of venom glands also emphasizes the functional differ-
ence between these and Duvernoy’s glands (Figure 2.1). One notable aspect of this
difference is in the much broader range of potential venom yields from front-fanged
