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Studies in Herpetology, Rocek Z. (ed.) PP- 219 - 222 Prague 1986

Phyletic Relationships Among Viperine Snakes

Brian GROOMBRIDGE

IUCN Conservation Monitoring Centre,

219 /c/ Huntingdon Road, Cambridge CBS ODL, United Kingdom
This paper is a very brief summary of a survey of the morphology of vipers, in par-
ticular the Old World vipers lacking facial pits, intended to elucidate their phyletic in-
terrelations /topics touched on here are treated in Groombridge, 1980, and in prepa-
ration/.
Vipers collectively are clearly distinguished as strictly monophyletic by details of
the venom injection system. They fall into two primary groups comprising the monotypic
Azemiops and all other vipers; the former retains primitive features variously modified
in the latter, apparently a monophyletic group. Amongst these, the six species of Night
Adders Causus, inhabiting forest and savannah in sub-Saharan Africa, are phonetically
highly distinct. They share eight derived features: form of supranasal sac,
scale surface mierosculpture, hemipenial morphology, pulmonary artery pattern, loss
of maxillary-postorbital ligament, area of M. pterygoideus origin, form of compound
bone, form of ectopterygoid.
The genus Causus may be the sister group of other viper ines and crotalines. In almost
all snakes, and thus probably primitively in vipers, the M.hyotrachealis takes origin
from the hyoid; this is retained in Azemiops and Causus but in other vipers the muscle
fibres have shifted their origin off the hyoid and merge with the deep face of the M. neu-
rocostomandibularis. This suggests that viperines other than Causus, and pit vipers,
together form a strictly monophyletic group. Similarly, in most caenophidians there is
no elaboration of the posterior margin of the superficial palate; this is also true of
Azemiops and Causus, but other viperines and pit vipers are derived in possessing a
median choanal papilla, usually bifurcate /this interpretation is somewhat complicated
by the fact that the papilla is very small and intraspecifically variable in two viperine
species, probably a secondary reduction/.
Viperines other than Causus are distinguished as monophyletic by the ventral course
of the facial carotid artery; in all other caenophidians including other vipers the artery
passes dorsal to the mandibular nerve as it emerges from the prootic. The ventral course
is also found in scolecophidians and henophidians but, on the basis of differences in detail
and a consideration of other characters, I interpret the condition in viperines other than
Causus as a derived reversal -to the primitive snake condition. The Crotalihae are readily
distinguished as monophyletic by the possession of the facial sensory pit, with its associa-
ted modifications.
Considering the overall morphology of the four distinct groups of vipers, and the evi-
dence for the cladistic relations between them, I suggest it is most appropriate to re-
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cognise Azemiops, Causus, other vipers lacking pits, and pit vipers, each as a subfamily
of the Viperidae.
Among the Viperinae /sensu stricto/ it is possible to distinguish four major groups,
each of which appears, with varying degrees of probability, to be monophyletic. These
are: Bitis species, the Atheris group, the Eurasian group /notably Vipera/, and Echis-
Cerastes.
Species assigned to Bitis /mainly south and east African forms/ ai"e united by four
uniquely derived features: the form of the supranasal sac, of the ectopterygoid, of the
laterodorsal process of the septomaxilla, and scale surface microsculpture. Within the
genus the Kenyan highland form worthingtoni seems to be sister taxonjto the remainder,
distinguished by: postorbital-prootic contact, scalation of the snout region, anterior
ridge of the septomaxilla, and maxilla-prefrontal form.
The Atheris group /of central and east Africa/, comprising the monotypic Adenorhinos
barbouri, "Atheris' superciliaris and 'A* hindii, and true arboreal Atheris species,
is distignuished by scale surface morphology /further modified in hindii/ and by loss
of the lateral /maxillary/ branch of the M. retractor pterygoideus. The species super-
ciliaris is distinguished by the form of the palatine-pterygoid articulation and the pos-
session of a long intra-pulmohary bronchus, and, apparently primitively, has a distinct
supraocular scale. The remaining members of the group share four derived features:
hemipenial form, division of rostral scale, presence of naso-rostral, reduction of vo-
merine process of premaxilla. Among this group, hindii and true Atheris share one
derived feature, regular transverse scale row duplications, but Adenorhinos and Atheris
share two, extreme reduction of the vomerine process, hemipenial form. Since the
scale row feature has evolved elsewhere in vipers it seems likely that Adenorhinos is
more closely related to true arboreal Atheris than to hindii. The true Atheris are dis-
tinguished by: highly attenuated body form, with high ventral and subcaudal counts,
short and wide head plan, and typically square shape gular scales.
The two problem species superciliaris and hindii have in the past been treated as
members of Vipera, of Bitis, and most recently and reasonably, of Atheris /Marx & Rabb,
1965/. However the three main points of similarity with Atheris are all primitive for vi-
pers in general and thus no evidence for the proposed relationship. The same authors
propose that barbouri, for which they erected the new genus Adenorhinos, is not closely
related to Atheris; on the contrary I suggest they are monophyletic although the former
/a little known snake from the forested highlands of south Tanzania, possibly an inver-
tebrate feeder/ is phenetically highly distinct. It is illogical to recognise barbouri as a
monophyletic genus while assigning the almost equally distinct superciliaris and hindii
to Atheris; a reasonable compromise is to recognise two further genera for the former
two species and restrict application of Atheris to the slender arboreal forms.
The Eurasian group, comprising Vipera, Pseudocerastes and Eristicophis, is not
readily characterised in cladistic terms - the presence of a naso-rostral scale /further
modified in one section/ is one possible derived feature - but the species do share a
strong phonetic similarity. There are congruent trends in at least a dozen characters
in which the smaller European Vipera are atone extreme, apparently the most primitive,
while the mid-East and Asian forms are at the other.
Within the Eurasian radiation, Vipera xanthina/and closely related forms bornmuelleri,
latifii, raddei, and others described very recently/, alsopalaestinae, the lebetina complex,
russelli, Pseudocerastes and Eristicophis, not only differ from the smaller forms in
being generally mid-East rather than European in distribution, but share derived features
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of nasal and dorsal head scalation, reduction or loss of the occipital head of the M.
depressor mandibulae and presence of an anterior azygous vein /apparently a reversal/.
The last five taxa are distinguished from xanthina and related forms by a derived pre~
frontal form and by size increase; two monophyletic branches can be distinguishad within
this cluster, palaestinae and russelli on one hand, lebetina, Pseudocerastes and Eristi-
cophis on the other. The former pair are defined by head colour pattern, nasal scalation
and shape, and reduction or loss of peritoneal pigment. The latter share some derived re-
semblances, including features of head shape and scalation, scale surface microsculpture
and trunk pattern. Marx & Rabb syaoaymise Pseudocerastes with Vipera but this is not
appropriate ; the former shares over a dozen clearly derived features with Eristicophis,
including a unique form of supranasal sac /the three such structures in vipers differ in
form and innervation and are non-homologous/. Obst /1983/ uses Gray's name Daboia
for all these large Vipera and Pseudocerastes /Eristicophis was not discussed/. 1 had
considered but rejected its revival for palaestinae and russelli, or the latter alone;
I would reject Obst's usage since it obscures relationships between Vipera, Pseudoce-
rastes and Eristicophis.
Echis and Cerastes are distributed in warm deserts from the Sahara to Arabia, with
Echis extending to central and south Asia. On balance they appear to be closely related,
although phenetically rather distant. They share an identical and derived scale surface
morphology, also modifications of the flank scales whereby they form an oblique array
with serrated scale keels used to generate sound during warning display /shared in part,
however, with certain Atheris species/. The venoms also appear to be very similar since
Echis antivenom will effectively neutralise Cerastes venom.
There are no clear uniquely derived characters that link any of these four viperine
groups; it would be convenient to recognize each as a tribe of the Viperinae /sensu
stricto/. Two possible derived states shared by Echis, Cerastes, the Atheris group and
Bitis are; presence of densely reticulate scale microsculpture and a much reduced an-
gular-splenial; a further common factor /although extrinsic and thus of no cladistic sig-
nificance/ is their distribution, centred to the Afro-Arabian tectonic plate. The Echis
-Cerastes group is both geographically and phenetically intermediate between the Afri-
can Atheris and Bitis groups and the Eurasian radiation. However, on balance it seems
that Eehis and Cerastes are more closely related to the African Atheris and Bitis groups,
and are perhaps closest to Atheris.
Vipers may have arisen in Eurasia in the later Oligocene, perhaps 30 million years
ago. There was much fauna! exchange across tropical forest corridors between Eurasia
and Africa around the OHgocene/Miocene transition, the time of the first known viperid
fossils. Azemiops and Causus may be remnants of this first radiation, while viperines
and crotalines differentiated in parallel with the spread of steppe vegetation in Eurasia.

REFERENCES
GROOMBREDGE, B. /1980/: A phyletic analysis of viperine snakes. - Council for Natio-
nal Academic Awards, unpublished PhD thesis.
MARX, H., RABB, C. B. /1965/: Relationships and zoogeography of the viperine snakes
/family Viperidae/. - Fieldiana, Zoology, 44 /21/ : 161-206.
OBST, F. J. /1983/: Zur Kenntnis der Schlangengattung Vipera /Reptilia, Serpentes,
Viperidae/. - Zool. Abh. Mus. Tierk. Dresden, 38 /13/ : 229-235.
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AZEMIOPS CAUSUS IVIPERINES! GROTALINES

BITIS ECHIS ATHERIS ; EURASIAN I

GROUP CERASTES GROUP I GROUP

Fig. 1: Diagrams to show suggested phylogenetie relationships between: /A/ the four
major groups of Viperidae, /B/ the four major groups of Viperinae /sensu stricto/, and
/C/ species and species groups within the Eurasian radiation of viperines. /Further
discussion in Groombridge, 1980/.