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Research & Reviews: Journal of Zoological Sciences
New Species of
Apostolepis
(Serpentes, Dipsadinae, Elapomorphini)
from Bolivia, from the
Apostolepis borellii
Group
Thales Lema1 and Patrick Campbell2*
1Museu de Ciências e Tecnologia, Pontifícia Universidade Católica do Rio Grande do Sul, PO Box 1429,
Porto Alegre, RS 90619-900, Brazil
2Darwin Centre, Department of Life Sciences, Natural History Museum, Cromwell Road,
London SW7 5BD, UK
Research Article
Received date: 17/01/2017
Accepted date: 25/02/2017
Published date: 28/02/2017
*For Correspondence
Patrick Campbell, Darwin Centre, Department of
Life Sciences, Natural History Museum, Cromwell
Road, London SW7 5BD, UK, Tel: 02079425030.
E-mail: pdc@nhm.ac.uk
Keywords: Cerrado, borellii group; Santa Cruz,
Goiás, Mato Grosso, Mato Grosso do Sul, Brazil,
Bolivia
Abbreviations: AC: Anterior chin-shield; CC: Chin-
shields; CL: Cloacal; DO: Dorsal scale; FR: Frontal;
GR: Gular region; GU: Gular; IL: Infralabial; SL:
Supralabial; ME: Mental; MR: Mental region; NA:
Nasal; OC: Occipital (after the last SL does not
contact PA); PA: Parietal; PC: Posterior chin-shield;
PF: Prefrontal; PR: Preocular; PS: Postocular; PT:
Posterior temporal; PV: Preventral; RO: Rostral; SC:
Subcaudal; SL: Supralabial; SO: Supraocular; TE:
Terminal; VE: Ventral scale. Bilateral data are indi-
cated as right/left when necessary to indicate dif-
ferences between them. The measurements given
in millimeters were taken with a exible ruler and
digital caliper, and we used the following abbrevia-
tions: HEL: Head length; PVA: Portion of RO visible
from above; SPF: Suture inter-PF; SVL: Snout-vent
length; TAL: Tail length; TO: Total length; TRL: Trunk
length. The sex was determined following a base-
caudal incision.
ABSTRACT
Description of a new species of Apostolepis based on three
specimens labelled A. borellii from Bolivia in The Museum of Natural
History of London. The new species belongs to the borellii Group which
is at present only represented by the species A. borellii. This new species
differs from A borelii by the following characters: (a) snout with median
stripe (vs. immaculate); (b) supralabial blotch long (vs. short); (c) stripes
evident on brown background (vs. having a blackish brown background
with almost indistinct stripes) (d) ratio subcaudal by ventral scales low
(vs. high) (e) lower sides cream (vs. darkish and dotted). The species area
is Mato Grosso Plateau neighbouring the highlands of Bolivia in Cerrado
Domain. The species is similar to A. striata and A. serrana from which it
differs mainly by having nucho-cervical collars which is absent in the latter
species. These species are placed in a specialized group (borellii group)
while the phillipsae group is represented by A. phillipsae.
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INTRODUCTION
Three specimens housed in The Natural History Museum of London (BMNH) are determined as Apostolepís borellii Peracca
[1]. The redetermined specimen belongs to a new species. A. borellii was synonymized with Apostolepis nigroterminata Boulenger
[2] and following examination of the holotypes was revalidated [3] which is in litteris (submitted). The latter was allocated to the
nigrolineata group and A. borellii to an isolated group. The new species is more similar to another two species from the same
area, A. serrana Lema Renner and A. striata Lema. A. borellii is easily differentiated by having dark sides (Figures 1 and 2) and
in the other species the sides are an immaculate cream colour. Importantly A. phillipsae belongs to specic a group represented
by a single species, of which the major difference is the peculiar shape of the head. In a recent paper [3] reported on a visit to the
Universidade Federal de Mato Grosso collection the discovery of several unknown species, this proves that there still exists a rich
sample of unknown species from Serra do Amolar near Cuiabá Mato Grosso.
Figure 1. Holotype of Apostolepis borellii (MZUT.962), from Urucum Hill, Mato Grosso do Sul, Brazil.
MATERIALS AND METHODS
The Cerrado of western Brazil encompasses a variety of habitats with much altitudinal variation including plateaus
(“chapadas”) and mountain chains (“cordilleras”) on which there are savannahs, and/or growing forests. The area is on the Mato
Grosso Plateau covering central to western Brazil and continuing to neighboring Bolivia It is between two major rivers the Araguaia
at eastern end and the Paraguay at the western end. The Paraguay River bordering Brazil and Bolivia does not pose a signicant
barrier to reptile dispersal we expect the occurrence of similar herpetofauna on both sides as a result. The plateau of Chapada
dos Guimarães has vertical slopes. At the tops of each highland are elds and forests arborous savannas forested savannas, as
well as agriculture, and livestock. In the rainy seas ons October to November plus April to May oods are frequent. Rains are also
usually frequent from December to March. The dry season is from May to September with the driest period from June to August [4].
Santa Cruz de la Sierra, the capital of Santa Cruz department in eastern Bolivia, has a tropical savanna climate (Köppen: Aw) with
an average annual temperature of around 23 ºC (73 F). Although the weather is generally warm all year round cold winds called
"surazos" can blow in occasionally (particularly in the winter) from the Argentine pampas leading to a considerably and sudden
temperature drop. The months of greatest rainfall are January and February; the average annual rainfall is 912 mm (36 in).
Collection acronyms follow [5], except: UFMS Universidade Federal de Mato Grosso do Sul Campo Grande Mato Grosso do
Sul Brazil; MHNSM Museo de Historia Natural Universidad Mayor San Marcos Peru; UFMT Universidade Federal de Mato Grosso
Cuiabá Mato Grosso Brazil; UFRGS Universidade Federal do Rio Grande do Sul Porto Alegre Rio Grande do Sul Brazil.
RESULTS
Apostolepis underwoodi sp. n.
(Figures 2-11; Table 1)
Apostolepis borellii [1] Apostolepis nigroterminata [2].
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Figure 2. Holotype of Apostolepis borellii (MZUT.962), from Urucum Hill, Mato Grosso do Sul, Brazil.
Figure 3. Holotype of Apostolepis serrana (BMNH.1972.430), from Serra do Roncador, Mato Grosso, Brazil.
Figure 4. Holotype of Apostolepis striata (CHUNB.12794), from Vilhena, Rondônia, Brazil
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Figure 5. Holotype of Apostolepis underwoodi sp. b. (BMNH.1927.8.1.181) from Santa Cruz, Bolivia.
Figure 6. Holotype of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.181) from Santa Cruz, Bolivia.
Figure 7. Holotype of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.181) from Santa Cruz, Bolivia.
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Figure 8. Paratype 1 of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.180) from Santa Cruz, Bolivia.
Figure 9. Paratype 1 of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.180) from Santa Cruz, Bolivia.
Figure 10. Paratype 1 of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.180) from Santa Cruz, Bolivia.
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Figure 11. Paratype 2 of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.182) from Santa Cruz, Bolivia.
A. borellii A. serrana A. striata A. underwoodi A. underwoodi A. underwoodi
Specimens MZUT.962 BMNH.1972.430 CHUNB.12794 BMNH.1927.8180 BMNH.1927.8181 BMNH.1927.8182
Sex ♂ ♂ ♂ ♀ ♂ ♂
TOL 197 337 261 381.8 316.8 234.8
TAL 32 31 26 31.8 31. 8 24
R 6.2 10.9 10 12 10 9.8
SVL 165 306 287 350 285 210.8
R’ 0.194 0.101 0.091 0.091 0.112 0.114
VE 208 234 202 205 212 211
SC 32 33 26 27 28 31
R” 0.154 0.141 0.129 0.132 0.132 0.147
SL 3-4 3-6 3-6 3-6 3-6 3-6
WC 1.5-1 0 0 2 2-3 0.5
BC 0.5-1 0 0 1 1 0.5
LS dark immaculate immaculate immaculate immaculate spaced dots
TB 8/4 11/8 9/8 5/4 5/4 9/7
TE white white black/white black<white black<white black>>white
Snout white, blotch
on RO black sutures black white, blotch on RO white, blotch on RO white, blotch on RO
Table 1. Data comparison of the Apostolepis underwoodi sp. n. with species belonging to the Group borellii. Abbreviations: BC, number of dorsal
scales in black cervical collar; LS, lateral sides coloration; R, quotient TOL/TAL; R’, quotient TAL/SVL; R”, quotient SC/VE; SC, subcaudal scales;
SL, supralabial white scales forming blotch; SVL, snout-vent length; TAL, tail length; TB, number of dorsal and subcaudal scales in the tail blotch;
TE, terminal shield coloration (dorsal and subcaudal number); TOL, total length; VE, ventral scales; WC, number of DO in white collar.
Figure 12. Paratype 2 of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.182) from Santa Cruz Bolívia.
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Type-specimens: BMNH.1927.8.1.180, female, holotype; paratypes: BMNH.1927.8.1.181, holotype, male, and BMNH.1927.8.1.182,
male; from Buena Vista, Santa Cruz Department, Bolivia (17º27’32”S, 63º39’33”W), 398 m OLS) (Figure 14).
Localization of Bolivian specimens: These were captured in the department of Santa Cruz, highlands of western Cerrado at 416
m OLS. Climate: it is warm and tropical most of the year. Winters are short in the last two or three months of the year but can
suddenly get very cold. "Surazos" (southerly winds that blow in from Argentina) can reduce the temperature by as much as 30 de-
grees overnight. This extreme cold lasts only a few days at a time however the beautiful sub-tropical Santa Cruz climate is evident
throughout most of the year. Here the climate varies by geographical zone: temperate to cold in the western sierras and warm to
hot and humid as one descends down to the extensive plains.
Diagnosis: The species which are most similar are A. serrana Lema and Renner (Figure 3) and A. striata Lema (Figure 4) differing
from both, mainly by nucho-cervical collars absent in these species. Apostolepis aff. borellii is another species showing similari-
ties following analysis at the Universidade Federal de Mato Grosso do Sul campus Corumbá by Nelson R Albuquerque. The major
difference is the shape of the supralabial blotch triangular in the latter and trapezoidal in the new species.
DESCRIPTION OF HOLOTYPE
BMNH 1927.8.1.180, female Morphology: Head slightly elongate and slightly wider than neck; snout rounded not
projected. Tail stocky with TE conic not spinous.
Measurements: HEL 8.91; TRL 310; TAL 31.8; SVL 350; TOL 381.8; quotient (TAL/TOL), 0.091; quotient (TAL/SVL), 0.094. Eye
diameter, 0.91; distance eye to oral margin, 0.91; ratio eye/distance, 1, therefore the eyes are large. Head height: 3.12 (on PA
level), 1.35 (on NA level); head width 4.22 (on PA), 2.27 (on NA). Neck height, 3.16. Body width: 4.13 (neck), half trunk, 4.97; CL
region, 3.03; tail 3.03 (basis), 2.81 (half), and 1.36 (on last SC). Head shields: PA 3.63 (length), 1.57 (width); FR: 2.242 (length),
1.42 (width); PF: 1.43 (length), 1.41 (width); PA suture: 2.04; PF suture, 1.23; RO visible from above, 0.57; ratio PF suture/RO
above, 2.2.
Pholidosis: PT only at right; SL, 6/6, second and third entering the orbit; IL, 7/7, the rst four contacting AC; GU 6 an each side
and median. PV, 2; VE, 205; SC, 27; quotient SC/VE, 0.132. DO contacting TE, 6.
Colouration (in conservation, in 80% Industrial methylated spirit): Pileon darkish brown, densely marbled, with light brown on in-
ner parts of PA, extending to oral margin, crossing the eyes, and reaching the OC in nape black collar. PF is irregularly darkish in
posterior margins. FR is dark in the apex and in middle line. SO light, fading brown blotched; the NA outside the head cap. Snout,
mainly light cream in colour, with dark margins; the dark line between PF reaches the RO apex. Supralabial blotch is trapeze like,
from third to sixth SL. Pileon nuchal margin narrow (two DO, not one), forming sideburns, which reach the GR, where it is patchy.
White collar one DO long (narrow). Cervical collar patchy on lower sides, isolated from the vertebral stripe, where it is patchy (con-
taining a few black blotches, some of which situated between them). Mental region light, with black blotches on ME, and second
to fourth IL margins. GR disrupted by black nuchal collar. Vertebral stripe lineal, black running on the medial line of each DO.
Paravertebral stripe fading, as wide as half of fth DO row, more than half of the sixth DO row, with a dark margin. Lateral stripe
is darker than the paravertebral stripe, as wide as half of the fourth DO row, more than half of a third, of DO row, margined up by
black coloration. Light stripe situated between the paravertebral and pleural stripes, on half of fourth DO row; contrasting with
Figure 13. Paratype 2 of Apostolepis underwoodi sp. n. (BMNH.1927.8.1.182) from Santa Cruz Bolívia.
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blackish margins. Paraventral zone under pleural stripe is immaculate cream as well as along the ventral side from head to tail.
Variation (Table 1) The female has a much shorter tail than the males, approximately twelve to ten times. The RO is high,
with the portion visible from above, being greater than half of suture length of PF. Each PF is large, with long sides, meeting nasal
shield. The SO are short and wide, trapeze-rectangular like. The FR is pentagonal elongate, with anterior apex larger than the
posterior, length larger than the distance to snout tip, and a little wide anterior. Each PA is wide and both joined in V-shape. The
Figure 14. Map of South America showing the localization of the specimens examined several species of Apostolepis. Key: A. borellii (white
circle), A. underwoodi sp. n. (black circle), A. aff. borellii (double circle); A. nigroterminata (white triangle), A. serrana (black square), and A.
striata (white square).
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NA is short and high like an equilateral triangle, and contacting the PR which is lozenge like. PS is angled and circles the orbit.
The fth SL is the largest and looks like an inverted trapeze. The VE varies from 205 to 212 and is reduced in number in females
compared to males (205 to 211 and 212), and SC almost equal to males (27 to 28 and 31), this differs from the majority of
species, the trunk of females is longer than it is in males.
Colouration: Pileon uniformly black. Snout usually a light brown, only one specimen is white (Figures 5-13); usually with
black stripe on suture of PF and median line of rostral but can be partial. Pileon nuchal margin very narrow (one dorsal scale),
extending down, usually forming sideburns, rarely reaching gular region, never forming a complete collar; with salience on last
SL level, narrowing white collar. White collar as long as two DO. The black oblique band from the pileon running across the eye,
reaching the oral margin (rst to third SL). Cervical collar present, being narrow; one specimen with vestigial with anterior at
extremity of pleural stripes enlarged. Supralabial blotch long, trapeze like, triangular, from posterior margin of third SL to anterior-
lower margin of the sixty SL, with up parts of SL black. Background colour light brown, with ve dorsal dark brown stripes, the
vertebral scales and the pleurals are blackish brown; a light lineal stripe between paravertebral and pleural, usually present,
contrasting against the darkish superior margin of the pleural. Vertebral stripe is lineal, on the median line of vertebral DO row,
occurring in almost all striped species. The paravertebrals fades on half sixty, and half fty DO rows, presenting darker lineal
margins, fading to tail, where they disappear. The pleural is, usually, the widest stripe; they are dark brown, with the upper margin
blackish on half of fourth DO row. The general formula for the stripes is (considering dorsal area from the sixty to rst DO rows):
½+VI+1/2 V (paravertebral), 1/2V (vertebral), ½ IV+1/2 III (pleural), II or II+I (dotted). The underside of the pleural stripes is
cream, immaculate, or with serial dark dots on the second DO row. Tail blotch is as long as seven to ve DO. TE mostly or fully
white. The colouration in life is a dominant brown colour, with dark brown stripes; the areas under the pleural stripes snout labials
and ventral are white. A narrow light stripe occurs between the pleural and paravertebral stripes creating a contrast with these
stripes; this occurs frequently in almost all of the ve-striped species of this genus.
Etymology: The name is a homage paid in memory to Garth Underwood, eminent herpetologist and a good friend of senior
author with whom many memorable discussions on tropical African snake were enjoyed.
DISCUSSION AND CONCLUSIONS
Harvey[2] determined the specimens from Bolivia and the holotype of A. borellii, as A. nigroterminata. The specimens
housed in the BMNH are hereby revealed as new species (A. underwoodi). The others (USNM.280371, MNKP.472, MNKP.942;
CM.2909*, MNKM.2909, UMMZ.44687, UTA.44687, UMMZ.60773, ZFMK.66375, UMMZ.67962), have not been examined by
the authors. However, according to the difference in biome (Amazonas x Cerrado) and the little data provided so far, these may
not be considered A. nigroterminata. The UTA.44687, from which two gures was presented, one a drawing and the other a
photograph, clearly shows a difference between the specimens; the supralabial blotch is long in the photo (as opposed to short),
as it is in A. underwoodi. This specimen is from Santa Cruz, just like the specimens we examined (BMNH.1927.8.1.180-182).
Harvey put the differences down to polymorphism, without giving a full explanation. The specimens examined from Cerrado
differs from the holotype of A. nigroterminata, mainly by general morphology they are much slender in body form as opposed to
the latter which has a much stockier form head to tail. This aspect of the morphology is peculiar to Amazonian species belonging
to the nigrolineata Group. Furthermore strong differences between the two biomes Cerrado and Amazonia are another reason to
separate these species. The A. nigroterminata (holotype, and FMNH.39646), specimens are from the Ayacucho Riverbank in the
deep valleys of the Peruvian plateau at eastern and southern slopes respectively covered with Amazonian Forest. A photo of a
neonate A. nigroterminata was taken in Madre de Dios bordering Brazil in the Amazonas and Acre states of the Amazonian Forest.
A specimen found dead on the road (DOR) in the slopes of Cuzco, southern Peru which is also an area of importance home to
tropical rainy forests, almost bordering Bolivia[6].
We also examined several other specimens from the UHE Manso currently still under study with the senior author. An initial
determination is inconclusive and it could be that they belong to an unknown species maybe two. All these specimens plus A.
underwoodi are similar in morphology and colouration and we believe that they all belong to the borellii Group [7].
There are two species from the Brazilian Cerrado, Apostolepis serrana Lema and Renner and Apostolepis striata Lema [8]
which are very similar to A. underwoodi. The comparison of these species allow for a reallocation of these two species from the
phillipsae Group to the borellii Group which is presented in a separate paper (in litteris) showing the phylogeny of the Group in
plesiomorphy stage but apomorphy in relation to the quinquelineata and nigrolineata Groups easily differentiated by the absence
of a tail blotch in the former. The determination of the species located in the Group borellii can be accomplished by use of the
following short key:
Key to species known of borellii Group:
1a. Lower sides of body dark ..............................................................................................A. borellii
b. Lower sides of body light, sometimes with some dots ................................................................2
2a. Nucho-cervical collars present .....................................................................................................3
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b. Nucho-cervical collars absent ......................................................................................................4
3a. Supralabial blotch trapeze like ...............................................................................A. underwoodi
b. Supralabial blotch triangular .................................................................................A. aff. borellii
4a. Snout black; supralabial blotch extending to rostral; ventrals in 202; terminal black above ..…..............…...A. striata
b. Snout light, with median black stripe; ventrals in 234; terminal white ........................A. serrana
VOUCHER SPECIMENS
1. The specimens examined are indicated by an asterisk.
2. Apostolepis borellii---Brazil: Mato Grosso do Sul; Urucum Mountain (MZUT.962*).
3. Apostolepis aff. borellii---Brazil: Mato Grosso: Chapada dos Guimarães, UHE Manso River (MCP.11372, 14524, 14525).
4. Apostolepis nigroterminata---Peru: Ayacucho, La Mar, in Sivia, Apurimac River valley, 760 OSL (FMNH.39646*). Lo-
reto, D.O.R. (MHNSM.005). Ucayali Valley: Callaria, ville and tributary of Ucayali River, between Poznan and Caballococha
(BMNH.1946.1.9.77*).-
5. Apostolepis serrana---Brazil: Mato Grosso; Serra do Roncador, Rio das Mortes (BMNH.1972.430*).
6. Apostolepis striata---Brazil: Rondônia: Vilhena (CHUNB.12794*).
7. Apostolepis underwoodi n. sp.---Bolivia: Santa Cruz: Buena Vista (BMNH.1927.8.1.180*, 1927.8.1.181, 1927.8.1.182*).
ACKNOWLEDGEMENTS
To Christine Strüssmann for allowing examination of the UFMT herpetological collection; Gláucia Maria F Pontes, for allow-
ing examination of MCP specimens; Alexandre Bamberg de Araújo, for allowing examination of UnB specimens, and hospitality in
Brasilia, DF; and to Marco Antonio de Freitas for photos, and published data.
REFERENCES
1. Parker HW. Notes on reptiles and batrachians from Matto Grosso and E Bolivia. Ann Mag Nat Hist. 1928;10:96-99.
2. Harvey M. Revision of Bolivian Apostolepis (Squamata: Colubridae). Copeia 1999;388-409.
3. Martins LA and Lema T. Elapomorphini (Serpentes Xenodontinae) do Brasil sudoeste. Neotrop Biol Conserv 2015;10:93-
102.
4. Alho CJR. Paisagens e enfoques. In: Alho CJR Fauna silvestre da região do Rio Manso MT. ELETRONORTE and IBAMA
Brasília DF. 2000;19-29.
5. Sabaj-Pérez MH. Standard symbolic codes for institutional resource collections in herpetology and ichthyology: American
Society of Ichthyologists and Herpetologists. Washington DC, USA, 2014-15.
6. Carrillo-de-Espinoza N and Icochea J. Lista taxonómica preliminar de los reptiles vivientes del Peru. Publicaciones del
Museo de Historia Natural Universidad Nacional Mayor de San Marcos Zoología. 1995;49:1-27.
7. Conceição PN. Os habitats da area de inuência do APM Manso. In: Alho CJR Fauna silvestre da regio do rio Manso MT.
ELETRONORTE and IBAMA Brasília, DF. 2000;31-127.
8. Lema T. Geographical distribution of chromatic patterns in elapomorphine snakes (Colubridae), and species groups.
Comunic Mus Cienc Tecnol PUCRS Zool. 2003;16:17-37.
