Color variation in Apostolepis nigrolineata (Serpentes, Colubridae: Dipsadinae: Elapomorphini), and contribution to the knowledge of the nigrolineata group

Abstract

ABSTRACT Color variation in A. nigrolineata was observed after examination of a large sample. The juveniles have five-stripes, lower sides yellowish cream, snout white, several white blotches on the supralabials, as well as on the nuchal region and the region in which other species have a white collar. The adults become dark, with the paravertebral stripes fading and eventually disappearing; the lower sides become blackish, sometimes forming a stripe under the pleural strip; the snout also darkening and becomes blackish; the supralabial blotches are reduced to small one during ontogeny, being oval, or trapezoidal, under the eye; the nuchal blotches are also reduced to a pair of oval blotches. The background coloration varies from brown to reddish during development. Juveniles from western Maranhão and adjacent areas of Pará are generally darker. The nigrolineata group is restricted to the Amazonian Forest, with the exception of one species that occurs in the northeastern enclave, remnant of the last Quaternary glaciations. A. nigrolineata differs strongly from A. quinquelineata, the latter being plesiomorphic and the former, and apomorphic in relation to it.

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1
Author for correspondence: thalesdelema@gmail.com
Color variation in Apostolepis nigrolineata (Serpentes,
Colubridae: Dipsadinae: Elapomorphini), and contribution
to the knowledge of the nigrolineata group
ales Lema1, Albérico Nogueira de Queiroz2, Luciane Aldado Martins1
1 Vertebrate Systematic Laboratory, Museu de Ciências e Tecnologia, Pontifícia Universidade Católica do Rio
Grande do Sul, P. O. Box 1429, 90619-900, Porto Alegre, Rio Grande do Sul, Brazil.
2 Departamento de Arqueologia, Universidade Federal de Sergipe, Av. Marechal Rondon, s/n, 49100-000,
Jardim Rosa Elze, São Cristovão, Sergipe, Brazil.
Cuad. herpetol. 31 (2): 00-00 (2017)
R e cib i d o: 9 A g ost o 2 0 1 6
Revisado: 22 Diciembre 2016
Aceptado: 24 Abril 2017
Editor A so ciado: J. Go ld berg
ABSTRACT
Color variation in A. nigrolineata was observed aer examination of a large sample. e juve-
niles have ve-stripes, lower sides yellowish cream, snout white, several white blotches on the
supralabials, as well as on the nuchal region and the region in which other species have a white
collar. e adults become dark, with the paravertebral stripes fading and eventually disappearing;
the lower sides become blackish, sometimes forming a stripe under the pleural strip; the snout
also darkening and becomes blackish; the supralabial blotches are reduced to small one during
ontogeny, being oval, or trapezoidal, under the eye; the nuchal blotches are also reduced to a
pair of oval blotches. e background coloration varies from brown to reddish during develop-
ment. Juveniles from western Maranhão and adjacent areas of Pará are generally darker. e
nigrolineata group is restricted to the Amazonian Forest, with the exception of one species that
occurs in the northeastern enclave, remnant of the last Quaternary glaciations. A. nigrolineata
diers strongly from A. quinquelineata, the latter being plesiomorphic and the former, and
apomorphic in relation to it.
Key words: Amazonia; Ontogeny; Supralabial blotch; Collars; Tail blotch; Morphs.
Introduction
Apostolepis nigrolineata (Peters 1869) is the best-
represented Amazonian species in collections,
indicating that it might be abundant. By contrast,
its congeners, Apostolepis quinquelineata Boulen-
ger 1896, Apostolepis rondoni Amaral 1925 rev.,
Apostolepis nigroterminata Boulenger 1896, and
Apostolepis sp. are very scarce in collections. We
had the opportunity to examine a large sample of
A. nigrolineata in the Museu Paraense Emílio Go-
eldi (MPEG), the data of which were published by
Lema and Renner (1998). In that sample, Cúrcio
et al. (2011) detected another species, Apostolepis
nelsonjorgei Lema & Renner 2004. In this paper, we
selected the specimens determined as actually belon-
ging to A. nigrolineata, to record color variation in
the adults and also throughout development. Some
photos of living specimens are also added to facilitate
species identication. Apostolepis nigrolineata is the
most frequent species in the Amazon Domain. It is
sometimes mistaken for Apostolepis quinquelineata
Boulenger 1896, a species that is very dierent in
appearance, and has restricted distribution in nor-
thern Amazonas and adjacent lands. One dierence
between the two species is the absence of a tail blotch
in A. quinquelineata, which may be a regression. e
closest species to A. quinquelineata, is A. rondoni
Amaral 1925, which is revalidated mostly because
it has the tail blotch. One species of the group is
endemic to the Serra de Baturité, Ceará, being very
similar to A. nigrolineata, the main dierence being
the presence of very thin stripes which disappear in
adult stage (in litteris). Another species is Apostole-
pis nigroterminata Boulenger 1896, from Peru and
adjacent Brazil; it diers mainly by the presence of
nucho-cervical collars. Apostolepis nigrolineata was
analyzed by Felipe Cúrcio, from the University Fede-

2
Lema et al.  Apostolepis nigrolineata variation
ral de Mato Grosso (Cuiabá, Brazil), for a complete
taxonomic assessment (in litteris).
e variation of each specimen was recorded
in individual les (Lema and Renner, 1998) and the
generalized aspects were presented. Here, we present
the detailed aspects of variation color mainly the
supralabial blotch which varies much during ontoge-
nesis. e frequency of types and incidence of color
variation occurrence were not recorded because
variation is polymorphic in juveniles, becoming
established in the adults. Data of the specimens were
published in Lema and Renner (1998).
Materials and methods
Specimens were observed directly at the Labora-
tory of Vertebrate Systematic of PUCRS and in the
Laboratory of Herpetology of MPEG. Previously
published data (Lema and Renner, 1998), not pre-
sented here, includes two types of forms, one with
qualitative data and the other with quantitative data.
e most important variation is commented, inclu-
ding detection of some morphs and rare anomalies.
A large sample of A. nigrolineata was obtained thanks
to the eorts of Otávio Rodrigues da Cunha, assisted
by Francisco Paiva do Nascimento, both retired bio-
logists of the MPEG now. ey travelled on several
roads of the state of Pará and adjacent Maranhão
recruiting collaborators, to whom they gave plastic
recipients of 50L with formalin 10% and collecting
instructions. Aer some time, they returned to
those places to pick up the specimens, who were
then prepared and permanently stored in large glass
cylinders with 70% ethanol Using this strategy, they
obtained the largest known sample of Elapomorphi-
ni. is sample documents the local abundance of
A. nigrolineata and the scarcity of A. quinquelineata.
ree specimens of Apostolepis nelsonjorgei Lema &
Renner 2004, which were erroneously determined as
A. quinquelineata and later re-determined by Felipe
Cúrcio (Cúrcio et al., 2011), were also re-examined.
Cunha and Nascimento (1978, 1993) consi-
dered all MPEG specimens as A. quinquelineata.
We determined two morphs, which we called alpha
and beta. e former corresponds to A. nigrolineata,
and the latter to A. quinquelineata. More specimens
from other institutions, viz. Instituto Butantan,
Museu de Ciências e Tecnologia, Naturhistorisches
Museum zu Wien, Universidade Federal do Ceará,
Zoologisches Museum zu Berlin (see Appendix I),
were also analyzed by us.
ree specimens found at the Universidade
Federal do Ceará (LAROF.1349, 1950, and 2067),
published as A. quinquelineata (Nascimento &
Lima-Verde, 1989), were re-determined by the
senior author as belonging to an unknown species
(Loebmann et al., unpub. data), which is endemic
to an enclave of the state of Ceará, Serra do Baturité.
Acronyms for institutions follow Sabaj-Pérez
(2014); except: CEPB, Centro de Estudos e Pesquisas
Biológicas, Universidade Católica de Goiás, Goiânia;
CS, Christine Strüssmann eld number, Cuiabá,
MT; IMTM, Instituto de Medicina Tropical, Man-
aus; INPA, Instituto Nacional Pesquisas Amazônia;
LAROF, Laboratório de Herpetologia, Universidade
Federal do Ceará, Fortaleza (= NUROF); LPH, Lin-
ha Pesquisa Herpetologia PUCRS (now in MCP);
MZUFV, Museu Universidade Federal Viçosa; NU-
ROF, Núcleo Regional de Oologia, Fortaleza, Ceará
(= LAROF); WWF, Wild Life Foundation, Manaus;
ZUFMS, Museu de Zoologia da Universidade Fe-
deral de Mato Grosso do Sul, Campo Grande, Mato
Grosso do Sul.
Results
General observations
(a) Specimens with ve stripes are usually juveniles,
whereas adults usually have three stripes. (b) In the
sample from Maranhão, the paravertebral stripes
with dark margins are evident in the adults, die-
rent from the majority of specimens from the state
of Pará. (c) e stripes are blackish brown. (d) e
paravertebral stripes have dotted margins and fade
during development. (e) A comparison with other
striped species of Apostolepis revealed that a reduc-
tion in the paravertebral stripes is frequent during
the development of large specimens (Tables 1 and
2). (f) Females are larger than males (Tables 2 and
3). (g). All species of the nigrolineata group present
a total or partial white nuchal collar, and in most of
them it becomes only vestigial in adults. is fact
suggests a collared ancestor.
Features of the holotype of Elapomorphus ni-
grolineatus Peters 1869 agree with the holotype of
Apostolepis pymi Boulenger 1903 in many aspects.
erefore, both were synonymyzed with A. nigro-
lineata (Lema, 1997). e observed dierences are
due to individual variation, and several characters
described by dierent authors, are common to many
species of the tribe, and some are common to the
genus. e high number of ventrals on the type-

3
Cuad. herpetol. 31 (2): 00-00 (2017)
A. nigrolineata A. niceforoi A. sp. A. nigroterminata A. quinquelineata A. rondoni
Distribution Amazonas
Basin
SE
Colombia
Enclave Ceará E Peru/W
Amazonas
N Amazonas/
Guyana
W Amazonas/MT
Nucho-cervi-
cal collars
vestigial vestigial present in
juvenile
present absent absent
Tail blotch present present present present absent resent
Stripes 7/5/3 7 5/3/vestigial 5 5 5
Stripes
width
medium medium wide/lineal wide/medium wide wide
Paraventral
zone
whitish/darkish darkish whitish darkish white white
Vertebral
zone
brown/reddish yellowish
brown
yellowish/
reddish
bright red yellowish reddish orange
Supralabial
blotch
variable/oval variable variable/small small trapezoid very small small oval
Snout blotch white/dark dark dark white yellowish yellowish & dark
Table 1: Comparison of the Amazonian species of Apostolepis with major characters.
Table 2: CComparison of the species from nigrolineata group, including the new species. Abbreviations: A, adult; AC, anterior chin-
shields; BRA, Brazil; CE, Ceará State, BRA; COL, Colombia; GUY, Guyanas, IL, infralabial shield; N, neonate; PER, Peru; R1 = SC/VE;
R2 = TAL/TOL; R3 = TAL/SVL; SA, sub-adult; SC, subcaudal scale; SL, supralabial; SVL, snout-vent length; TAL, tail length; TOL,
total length; VE, ventral scale; x, average; Y, juvenile.
Characters A. nigrolineata A. a. nigrolineata A. niceforoi A. nigroterminata
Habitat Amazonian Forest: BRA,
GUY.
Relictual forests: BRA (CE) Amazonia: COL Amazonia: PER,
BRA(AC)
Snout color Large dark (A);
immaculate (Y),
Darkish (A); white (Y) Darkish White
Supralabial blotch Small oval (A), few long
as trapeze (Y); variable (N)
2 narrow large (A), three
small (Y),white (N)
Several, small, narrow
and vertical
Reduced, oblique
White nape collar Absent (rare); pair of
circular white blotches out
(A); vestigial (Y)
Absent (A); complete
(Y); vertical at side (SA),
Absent (A)
Absent Present long as 2 DO
Black cervical
collar
Absent Present, reduced (A) Absent Vestigial to narrow
Head ventral side Whitish, small irregu-
lar blotches on anterior
shields
Immaculate Whitish, small irregular
blotches on anterior
shields
Immaculate
Background color Brown (A), reddish brown
(Y)
Cinnamon (A), reddish
brown (Y)
Yellowish (xed) Brilliant red
Ventral color Yellow Yellow (A), white (Y) Whitish immaculate
(xed)
Immaculate white
Subcaudal color Blotched last SC Blotched last SC Median series of dots,
and last SC blotched
Immaculate or last
SC blotched
Tail blotch Short, dorsal - Long, fully Short, fully (A), dorsal (Y) ? Short, only dorsal or
small SC
Terminal shield Black up- Blackish brown Black (A), white (Y) ? White
Tail tip Conical – Rounded
(sexual dierence?)
Rounded (A), conical (Y) ? White

4
Lema et al.  Apostolepis nigrolineata variation
specimen (Peters, 1869) is very rare, which as noted
by Lema and Renner (1998), who found up to 246
VE, in a very long body.
Another species, Apostolepis niceforoi Amaral
1935, described for Colombia, is the same as A.
nigrolineata, at least based on the holotype, which
was destroyed in the re in Instituto Butantan. e
original description is laconic and lacks some data,
thus making this species invalid, and another synon-
ym of A. nigrolineata.
Specic observations
Head dorsal side: e pileon is blackish brown, limi-
ted anteriorly, by the snout blotch, and posteriorly
forming the nuchal ring with variable projections
never reaching the gular region (Fig. 1c).
Snout light blotch: A. nigrolineata presents a
characteristic light blotch on the snout, from PF to
RO, which is outlined by blackish brown, forming a
polygonal gure (Fig. 2d). It is white in newborns,
darkening gradually with age, becoming fully blac-
kish in large specimens (Figs. 2e, 3b, 3c). e same
happens in juveniles of A. nigroterminata Boulenger
1896 (Lema et al., in litteris). One variation is the
presence of a small black blotch on RO, or the RO
fully black, in which case the blotch is reduced to
the PF.
Supralabial blotch: is is the most variable
aspect of species coloration (Fig. 1a). In neonates and
juveniles there is more than one blotch, or the blotch
discontinuous, and it may coalesce with the snout
blotch. We observed that the blotch can be very
long in the early stages, shrinking gradually during
development, and becoming only small, oval, white
blotch under the eye. In juveniles, a long trapezoidal
blotch is present (Figs. 1a, 2c), becoming shorter in
large adults (Figs. 1a, 3b, 3c). For this reason, we
characterize the species using only adults (Lema
and Renner, 1998).
Head lower side: No variation was observed,
with the basic whitish cream coloration becoming
gradually yellow towards the VE. Exception occurs
in neonates, which present small black blotches on
the infralabial margins (Fig. 1d).
Nuchal white collar: e adult presents a single
pair of nuchal white oval blotches, which disappear
in giant adults (Figs. 3b, 3c). In neonates, and very
Number of stripes 5 (Y, A) 3(A) or 7 5 (Y), 3 (A) 7 7 or black
Temporal Present Present /absent Present Absent
VE average Ÿ214.5 – 233.9 211 - 207
VE average Ž228.4 – 233.8 - 248 -
SC average Ÿ33 – 36.3 35.3 - 26
SC average Ž26.3 – 34.5 - 23 -
R1 Ÿ0.154 – 0.170 0.167 - 0.126
R1 Ž0.115 – 0.148 0.103 0.102 -
Average (R1, R2) 0.135 – 0.159 0.103 - -
IL x AC 1-4 (1-5) 1-4 (A), 1-3 (Y) 1-4 1-4
Hemipenis Calyculate, mainly fringed,
basis spinulate
Calyculate, few basal
spines
? ?
Total
sample
Males Females
Variation in
total length 189.5 - 747 221 - 537 189.5 - 747
x (n) 434.2 (75) 420.1 (33) 448.2 (42)
Variation in
tail length 18-71 35-71 18 - 57
x (n) 46.4 (75) 50.4 (33) 42.4 (42)
R = TAL/SVL 0.66 - 0.189 0.097 - 0.189 0.066 - 0.141
x (n) 0.120 (75) 0.141 (33) 0.099 (42)
Variation of
VE 203 - 257 203 - 237 220 - 257
x (n) 218.9 (77) 213.2 (37) 224.6 (40)
Variation of
SC 21 - 40 32 - 40 21 -34
x (n) 38.5 (74) 37.1 (35) 29.9 (39)
R = SC/VE 0.111 - 0.202 0.145 - 0.202 0.111 - 0.149
x (n) 0.153 (114) 0.173 (70) 0.132 (44)
Table 3: Statistics of measurements and number of ventral
and subcaudal scales of a sample of Apostolepis nigrolineata.
Measurements in millimeters; abbreviations: n, number of
specimens; SVL, snout-vent length; TAL, tail length; x, avera-
ge, SC, subcaudal scales; VE, ventral scales (From Lema and
Renner, 1998, part)

5
Cuad. herpetol. 31 (2): 00-00 (2017)
early juveniles, the blotches are large and large and
vertical, on the sides of neck (Fig. 1a); during deve-
lopment they become reduced, sometimes breaking
down into two on each side; some specimens do not
present light blotches on the neck (Figs. 3b, 3c).
Vertebral zone: e background coloration
varies during the ontogeny, from yellowish (Fig.
2c) to brown (Figs. 2d, 2e), becoming reddish in
latter stages the end (Fig. 3c), sometimes even dark
(Fig. 3d).
Vertebral stripe: is is the narrowest and dar-
kest stripe, as in most striped species of the genus. It
reaches the median vertebral row of DO, and may
reach the adjacent angles of the seventh rows of DO.
Light intermediary stripes: Most striped spe-
cies of Apostolepis, have a linear light stripe between
the paravertebral and pleural stripes, occupying one
half of each row of DO. is are more evident in the
early stages (Fig. 2c), darkening during development,
and disappearing in the adult (Figs. 3c, 3d).
Paravertebral stripes: More evident in the early
stages (Figs. 2c, 2d), fading during development,
usually disappearing in the adult (Figs. 3b, 3d).
Pleural stripes: e widest stripe is darker on
the upper margin than on the lower (Figs. 2c, 2d).
ey become more evident due to a light upper stripe
that contrasts with the blackish margin of the pleural.
In larger specimens, this stripe becomes is reduced
to a linear stripe (Fig. 3c).
Lower pleural zones: Usually the zones under
the pleural stripes are dark, sometimes blackish dark
(Fig. 1a). In several specimens, the second row of
DO is colored on the median line forms a stripe (Fig.
1). is is the case of the holotype of A. niceforoi,
which may be a synonym of A. nigrolineata. Most
specimens from eastern Maranhão are more colored
in this area, apparently conguring a morph.
Ventral side: All observed have the venter im-
maculate, with the white basic coloration (Fig. 2c)
replaced by bright yellow (Figs. 2d, 2e).
Tail blotch: is is another strongly variable
feature (polymorphism) that is not subject to onto-
genetic variation varies from a complete blotch (DO
and SC) to one reduced to the dorsal side (DO), in
length. It varies from long to short (Figs. 1b, 3a).
Terminal: e TE is stocky, with conic minute
tip, without spine, varying from fully white to white
tip only (Figs. 1b, 3a).
Conclusions
Apostolepis nigrolineata is frequent in the Amazon
Forest Domain as shown by the MPEG collection, at
least, in the Pará state (Fig. 1d). e great variation
in the features of this species suggests that it became
established in the area a long time ago. ere are two
species occurring in neighboring areas, A. nigroter-
minata (Fig. 5c) and A. niceforoi. Both are very simi-
lar to A. nigrolineata, belonging to the same group
nigrolineata Lema 2003. Apostolepis nigroterminata
is diagnosed by having nucho-cervical collars, which
are absent in other species of the group, and having
the polygonal snout gure (Fig. 2e). Apostolepis.
niceforoi is not well known and is almost indistinct
from A. nigrolineata. Its original description is short
and the drawing of it is insucient for reliable iden-
tication (Amaral, 1935). It is known only from the
holotype, which was burned during a re at Instituto
Butantan. Other specimens were found and are being
studied at the Universidade Federal do Acre, who
prepared a communication about it (in litteris). e
type-locality of A. niceforoi is La Pedrera, Colombia,
a b
c d
Figure 1: a. Variation of supralabial blotch, in order of develop-
ment. b. Variation of tail blotch. c. Dorsal aspect of head pattern.
d. Ventral aspect of newborn (drawings: L. A. Martins).

6
Lema et al.  Apostolepis nigrolineata variation
at the border with the state of Amazonas, Brazil,
where the Amazon Forest biome also occurs. e
specimen erroneously reported from Duke Reserve
in Manaus (Amazonas) by Martins and Oliveira
(1998) belongs to A. nigrolineata. Several references
to Apostolepis pymi, and most to A. quinquelineata
(Fig. 5a), are references to A. nigrolineata, according
to examination of gures and/or published data.
Species of the nigrolineata group are distinctive
by the stocky body in adults, the non protruding
snout, the rounded head , the stocky and wide tail
with a conic tip, and the polygonal gure on snout
(Fig. 2b). e ancestor may have been widespread in
the old Hylaea and, aer the last glaciations, became
isolated in small elevations in Ceará, where relictual
forest existed. e Amazonian Forest is continuous
from Brazil to Colombia and Peru, and A. nigroli-
neata disperse to the West, reaching southeastern
Colombia (A. niceforoi), and to the Southwest rea-
ching Rondônia and adjacent lands. We believe A.
nigrolineata occurs in the whole Amazon Basin, but
there are few samples from most of the area, and it is
very extensive and sometimes impenetrable in many
densely forested areas.
a b
c
d e
Figure 2: a. Live newborn of A. nigrolineata. To notice the presence of white nuchal collar almost complete (Anonymous). b. Juvenile
specimen from Montagne de Kaw, in Roura, French Guiana. c. Fixed sub-adult (MCP.9193) from Madeira Riverbank, Rondônia. To
notice the dominant brown coloration (M. Di Bernado). d. Fixed sub-adult (MCP.9193) showing the characteristic white polygon on
the snout, the total reduction of the supralabial blotch, and a pair of white blotches aer the head, which are remnants of the white
nuchal collar (Marcos Di Bernardo). e. Sub-adult from Parque Nacional do Trairão, Pará. To notice the snout becoming darker (Te-
lêmaco Jason Mendes Pinto).

7
Cuad. herpetol. 31 (2): 00-00 (2017)
e quinquelineata group is represented by
A. quinquelineata (Fig. 5a) and A. rondoni (Fig.
5b) which are very small species, with ve black
permanent stripes and, light background color,
sometimes yellowish or reddish orange. ey are
distributed in very distant populations, the former
in northern Amazonia, and the latter in western
Amazonia (Fig. 4).
Artificial key to determine the species of the
Amazon Forest
1a. Vertebral color yellowish, ve black stripes du-
ring all development; paraventral zones always im-
maculate whitish .........................................................2
b. Vertebral color brown, red to blackish, ve stripes
usually reduced to three in adults; paraventral zones
immaculate whitish in early stages, later acquiring
dots and/or dark stripes ..............................................3
2a. Tail blotch absent ...................... A. quinquelineata
b. Tail blotch present .......................... A. rondoni rev.
3a. Vertebral color brown in early stage of develop-
ment, becoming bright red in adults ........................
......................................................... A. nigroterminata
b. Vertebral color brown in early stage, becoming
reddish brown to darkish in adult ................................
................................................................. A. nigrolineata
Acknowledgments
We are grateful to collections managers, and
colleagues who sent images; and to Oswaldo R.
Cunha and Francisco P. Nascimento, for their
attention and care at the MPEG and heir hospitality.
to colleagues Marcos Di Bernardo (in memoriam),
Christine Strüssmann, Paulo Bernarde, Breno
Almeida, Fancisco P. Nascimento, Omar M.
Entiauspe Neto, Telêmaco Jason, for photos or
live specimens. To Patrick Campbell, from The
Natural Museum of London, for the photos of the
holotypes of A. pymi and A. quinquelineata. To
Piter Keoma Bol by improvement of the english.
Literature cited
Amaral, A. 1935. Estudos sobre ophídios neotrópicos. XXXIII.
a b
c
d
Figure 3: a. Live nascent adult from Guaporé Riverbank, Rondônia. b. Adult live specimen from, Belem, Pará. To noticed the dark snout
(Breno Almeida). c. Adult specimen from Ilha do Outeiro, Pará. To notice the absence of paravertebral stripes (Marcos Di Bernardo).
d. Live specimen of Apostolepís quinquelineata. To notice the absence of tail blotch (Omar Machado Entiauspe Neto).

8
Lema et al.  Apostolepis nigrolineata variation
Novas espécies de ophídios da Colômbia. Memorias do
Instituto Butantan 9: 219-223.
Cunha, O.R. & Nascimento, F.P. 1978. Ofídios da Amazônia
X. As cobras da região Leste do Pará. Publicacoes Avulsas
Museum Paranaense Emílio Goeldi 31: 1-218.
Cunha, O.R. & Nascimento, F.P. 1993. Ofídios da Amazônia, X.
As cobras da região Leste do Pará. 2nd ed. Boletin do Museo
Paranaense Emílio Goeldi, Zoología 9: 1-191.
Cúrcio, F.F.; Nunes, P.M.S.; Harvey, M.B. & Rodrigues,
M.T. 2011. Redescription of Apostolepis longicaudata
(Serpentes: Xenodontinae) with comments on its hemipenial
morphology and natural history. Herpetologica 67: 318-331.
Ferrarezzi, H. 1993. Sistemática logenética de Elapomorphus,
Ph al ot ris e Aposto le pi s (S erpe ntes: Colubrida e:
Xenodontinae). Master Dissert., USP, São Paulo.
Lema, T. 1997b. A redescription of the tropical Brazilian
serpent Apostolepis nigrolineata (Peters, 1869) (Colubridae:
Elapomorphinae), synonymous with A. pymi Boulenger,
1903. Studies in Neotropical Fauna and Environment 32:
193-199.
Lema, T. & Renner, M.F. 1998. O status de Apostolepis
quinquelineata Boulenger, 1896, A. pymi B oulenger,
1903 e A. rondoni Amaral, 1925 (Serpentes, Colubridae,
Elapomorphini). Biociências 6: 99-121.
Martins, M. & Oliveira, M.E. 1998. Natural history of snakes
in forests in the Manaus region, Central Amazonas, Brazil.
Herpetological Natural History 6: 78-150.
Nascimento, F.P. & Lima-Verde, J.S. 1989. Ocorrência de ofídios
de ambientes orestais em enclaves de matas úmidas do
Ceará (Ophidia: Colubridae). Boletin do Museo Paranaense
Emílio Goeldi, Zoologia 5: 95-100.
Peters, W. 1869. Über neue oder weniger bekannte Amphibien
des Berliner Zoologischen Museums. Monatsb. Akad. Wiss.
Berlin 1869: 217-224.
Sabaj-Pérez, M.H. (editor). 2014. Standard symbolic codes
for institutional resource collections in herpetology and
ichthyology: an online reference. Version 5 (22 Sept 2014).
American Society of Ichthyologists and Herpetologists,
Washington, D.C. Available at: <http://www.asih.org/ Last
accessed in 10 June 2015.
Appendix I
Voucher Specimens
Apostolepis niceforoi --- COLOMBIA: Amazonas: La Pedrera,
Bajo Caquetá (IBSP.9197, holotype, lost).
Apostolepis nigrolineata --- (NNL.9218; ZMB.6447, holotype;
ZMB.10739, Rohde Co., not Paraguay; NMW.21992, F.
Steindachner col.). BRAZIL: (BMNH.1946.1.9.82, holotype
A. pymi). Amapá: Macapá (IBSP.25514, ac. Ferrarezzi, 1993).
Amazonas: (AMNH.101954, AMNH.101955); Manaus: INPA-
WWF Reserve (INPA.1166, ‘Apostolepis sp.’, Martins & Oliveira,
1998); IMTM.1335, IMTM.1537, IMTM.1577, MZUSP.8423,
MZUSP.8424, MZUSP.8657; AMNH.140772 (may be the same
“A. avotorquata lineata” ac. Ferrarezzi, 1993). Maranhão:
Nova Vida: BR-316, 25 Km Gurupá River (MPEG.10199, 10202,
10204, 11136, 12274, 12286, 12295, 12663-12672, 13697, 13698,
13700-13702, 14409, 14780, 14781, 15004-15006, 15290-15292,
15758-15763, 16225-16229). Paruá: BR-316 [Pará/Maranhão]
(MPEG.10835, 13641, 14352). Mato Grosso: Guaporé (CS.296).
Pontes e Lacerda (NW Cuiabá): Triângulo Farm, near Guaporé x
Madeira Rivers (CS.2500). Pará: (KU.127256, 127257, 128094).
Acará Road: Pirajauara River (MPEG.10939). Apeú: Boa Vista
(MPEG.586, 587, 696, 1174, 1476, 1479, 2657, 2666, 3331, 3332,
3334, 3335, 5718, 6916, 6919, 6943, 9459). Augusto Correa:
Cacoal (MPEG.3905, 3954, 5399, 6712, 6713, 6721, 6724, 6737,
8999, 9937, 10764, 12450, 13074). Belém (IBSP.3033, 3034);
Ananindeua, Maguari (KU.140153, 140154); Ilha de Mosqueiro
(MPEG.12769-12771; IBSP.54152); IPEAN, 5 Km E Belém
(KU.127256); Belém, Ilha do Outeiro (MCP.10718). Utinga, 5
Km Belém (KU.128094). Benevides (ZSM.137/11). Bragança:
Bom Jesus (MPEG.1699, 1700, 1957-1959, 2216, 2217, 2237,
2238, 2973, 3046, 3047, 3050, 3670-3675, 3946-3948, 4361, 4364,
4384, 5029, 5030, 5037, 5110, 5116, 5119, 5125, 5127, 6322, 6332,
6334, 6352, 7929, 7930, 7932, 7934, 7935, 7937, 7942, 7947,
7954, 7959, 8239, 8240, 8245, 8249, 8251, 8268, 8270, 8273,
8295, 8563, 9951-9953, 9970, 12375, 13007-13009. Castanhal:
Macapazinho (MPEG.5878, 7163, 7173, 10912, 10913,
11794, 12603). Colônia Nova: near Gurupí River, in BR-316
(MPEG.2174, 2970, 5160, 7821, 7827, 9546, 9558, 9818, 9829,
11486, 11488, 11933, 11937, 12882, 12883, 15060, 15063, 15863).
Curuçá: Marauá (MPEG.4057, 4063, 4878, 4881, 4882, 4885,
4886, 5898, 5903, 5913, 7130, 7131, 7132, 7135, 7140, 7626).
Curuá-Uma (MZUSP.8011). Fordlândia (IBSP.5126). Gurupá
(MPEG.16324). Igarapé-Açu (MPEG.868-871, 910, 912, 913,
924, 925). Inhamgabi: Arraial do Carmo (MPEG.1464, 1568,
1571). Mangabeira (IBSP.48502). Marabá: Carajás, Serra Norte
(MPEG.17304). Maracanã Road: Km 23 (MPEG.1596, 1600-
1605, 1891-1897, 2101, 2422, 2423, 2560, 2822, 2826, 2864-2866,
3386, 3387, 3389, 3390, 3448, 3949-3951, 4086, 4094, 4801, 4802,
4807, 4808, 4811, 4813-4817, 4828, 4858, 8187. Osório: Limão
Grande (MPEG.1658, 3945, 6150, 6187, 6197). Ourém: Limão
Grande, Puraquequara (MPEG.4224, 5004, 5005, 5012, 7016,
7019). Pareci Novo (not Parci) (ZSBS[ZSM] w/n). Pratinha:
Genipauba Road (MPEG.7570, 8399, 8615, 8631, 12571, 14285,
1546); Santa Bárbara (MPEG.1855, 2608, 3952). BR-316 [PA/
MA] Km 74 (MPEG.1084, 3581, 8192, 10851). Santarém Novo:
Trombetinha (MPEG.1841, 1977, 3251, 4154, 4796, 7081). Santo
Antônio do Tauá (MPEG.1000, 1453, 1872, 1873, 1879, 2375,
Figure 4: Schematic distribution of regions where specimens
belonging to the Apostolepis nigrolineata group were found.
Key: Apostolepis niceforoi (black circle), Apostolepis nigrolineata
(circles), Apostolepis nigroterminata (black triangles), Apostolepis
quinquelineata (squares), Apostolepis rondoni (triangles); triangle
outlined is the occurrence of Apostolepis nigroterminata in Brazil.

9
Cuad. herpetol. 31 (2): 00-00 (2017)
© 2017 por los autores, licencia otorgada a la Asociación Herpetológica Argenti-
na. Este artículo es de acceso abierto y distribuido bajo los términos y condiciones
de una licencia Atribución-No Comercial 2.5 Argentina de Creative Commons.
Para ver una copia de esta licencia, visite http://creativecommons.org/licenses/
by-nc/2.5/ar/
a b
c
Figure 5: a. Apostolepis rondoni from Rondônia. To notice the presence of the tail blotch, which is dierent from that of A. quinque-
lineata (Paulo Bernarde). b. Adult of Apostolepis nigroterminata Boulenger 1896, from Acre, Brazil (Danyella Paiva da Silva). c. Sub-
adult of Apostolepis sp. endemic from Serra do Baturité, Ceará. To notice the vestige of the nucho-cervical collars (Daniel Loebmann).
2376, 2643, 3306, 3940, 4718, 4720, 4721, 4723, 4730, 6958,
7557). Santa Rosa: Vigia Road (MPEG.3941-3944, 4614, 4615,
4617, 4620, 4642, 5656, 5665, 5666, 5683, 5685, 5686, 5690, 6774,
6792, 6799, 6802, 6887, 6984, 6988, 7487, 7497, 7537, 7542, 8490,
8514, 8517, 8551-8553, 8583, 9255, 9256, 9349, 10593, 10597-
10599, 11835, 11836, 12590). Serra dos Carajás (MZUFV.1071).
Uruá: Parque Nacional da Amazônia (IBSP.7285), near Tapajós
River (MZUSP.7287). Viseu: Bela Vista (MPEG.1735, 2292,
2293, 3714, 5239, 5249, 7291, 7325, 7338, 7701, 8959, 11267,
11268, 15126, 15127); Curupati (MPEG.10010, 10884, 10886,
10887, 13260). Fazenda Real (MPEG.1787, 2323, 2324, 2349,
3142, 3143, 3953, 4458, 5320, 5321, 5324, 5325, 5327, 5329,
6633, 17279). Rondônia: Porto Velho (ZUEC, w. n.). Samuel:
le Jamari Riverbank (CEPB.2851, 2852, 3060, 3111, 3162, 3227,
3321; MPEG.17817, MPEG.17879, MPEG.17880, MPEG.17982
MPEG.17983); Nova Colina (MZUSP.8513). GUYANA:
(ZMB.6447, holotype A. nigrolineata); Georgetown: Wismar,
Demerara River (FMNH.26665, re-det.); Upper Demerara,
Berbice (KU.26665). SURINAME: Kaisenberg Camp, Zuid
River (FMNH.121828, re-det., not A. avotorquata acc. Van
Wallach, 10/1995). )