Zoosyst. Evol. 98 (1) 2022, 129-136 | DOI 10.3897/zse.98.80418

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Clarifying the type locality of Liotyphlops wilderi (Garman, 1883)
(Serpentes, Anomalepididae), with comments on other reptiles from

Sao Cyriaco, Minas Gerais

Henrique C. Costa!

1 Programa de Pos-graduacdo em Biologia Animal, Universidade Federal de Vigosa, 36570-900, Vigosa, MG, Brazil

2 Current address: Universidade Federal de Juiz de Fora. Instituto de Ciéncias Bioldgicas, Departamento de Zoologia. 36036-900, Juiz de

Fora, MG, Brazil
http://zoobank.org/8 D9 1 BODE-A626-4452-8A5E-35CDDB63F5B2

Corresponding author: Henrique C. Costa (ccostah@gmail.com)

Academic editor: Pedro Taucce @ Received 11 January 2022 # Accepted 13 April 2022 Published 5 May 2022

Abstract

The snake species Zyphlops wilderi (today Liotyphlops wilderi) was described in 1883 based on specimens from Sao Cyriaco, in
Minas Gerais, Brazil. The name of this type locality has been cited in different ways in the literature, making its geographic location
confusing. Solving this question is an important issue for future taxonomy and systematic studies. After searching for information on
the collector of the type series of L. wilderi (John Casper Branner) using the Google Scholar database, I found that SAo Cyriaco was
a gold mining company located in the current municipality of Alvorada de Minas. Besides elucidating the type locality of L. wilderi,
I searched for reptile specimens collected by Branner, deposited in collections registered at the VertNet Portal and SpeciesLink, and

personally examined the extant material from Minas Gerais.

Key Words

Amphisbaenia, lizards, Natural History Museum, snakes, Squamata, taxonomy

Introduction

In zoological nomenclature, the type locality of a species
or subspecies is the geographical (and, sometimes, strati-
graphical) place of capture, collection, or observation of
the name-bearing type (holotype, lectotype, neotype, or
syntypes), “the objective standard of reference whereby
the application of the name of a nominal taxon can be
determined” (International Commission on Zoological
Nomenclature 1999). It is not uncommon, however, that
taxa have an uncertain or somewhat vague (e.g., “Brazil’’)
type locality, especially those described more than a cen-
tury ago (e.g., Frost 2021; Uetz et al. 2021). A well-de-
fined type locality is of great importance to taxonomy and
systematics. If populations attributed to a single species
are found to diverge sufficiently (morphologically and/or
genetically, for example) to be considered two or more

subspecies or species, the population most closely relat-
ed to the name-bearing type will retain the taxon name
(e.g., Sturaro et al. 2018; Ascenso et al. 2019; Perez and
Borges-Martins 2019). In the current “genomic era”,
many historical herpetological type specimens, usually
formalin-fixed, lack genetic samples, and extracting and
sequencing DNA from them is still complex (Bell et al.
2020). In such cases, samples from topotypes, 1.e., new
specimens from (or close to) the type locality, can be a
valuable contribution to systematics (Fouquet et al. 2016;
Bell et al. 2020; Mangia et al. 2020). But if the type local-
ity is uncertain or too vague, it becomes difficult to assign
proper names to clades (Cacciali et al. 2018).

The snake species Liotyphlops wilderi (Garman, 1883)
(originally 7yphlops wilderi) is known from a few speci-
mens from Bahia, Minas Gerais and Rio de Janeiro states,
Brazil (Nogueira et al. 2019) and there is confusing

Copyright Costa HC. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribu-

tion, and reproduction in any medium, provided the original author and source are credited.

130

information regarding its type locality. Specimens used in
the original description were said to have been collected
at “Sao Cyriaco, Brazil” (Garman 1883). Later, the local-
ity name was cited as “Cyriaco, near Serra Providencia,
Minas Geraes, Brazil” (Hammar 1908), “Sao Cypriao,
Minas Geraes, Brazil” (Barbour and Loveridge 1929;
Marx 1958; Gans 1966; Dixon and Kofron 1983), “Cipri-
ano, Minas Gerais State, SE Brazil, 19°45'S, 43°57'W, el-
evation 850 m” (a location within the city of Vespasiano)
(Wallach et al. 2014), and “Sao Cyriaco, near the village
of Santo Anténio do Rio do Peixe. Currently, Alvorada de
Minas” (Nogueira et al. 2019).

Besides being the type locality of Zyphlops wilderi,
Sao Cyriaco 1s the locality of the collection of a wormliz-
ard specimen assigned to Amphisbaena prunicolor (Cope
1885) (Gans 1966) a species mostly distributed in south-
ern Brazil, Paraguay, and Argentina (Perez et al. 2012).
This raises questions regarding the identity of the spec-
imen (whether it was misidentified) and the geographic
location of Sao Cyriaco (if it could somehow be in south-
ern, instead of southeastern Brazil).

The wormlizard specimen and the type series of
Liotyphlops wilderi were collected by the geologist John
Casper Branner (1 850—1922). Born in New Market, U.S.A.,
from a distinguished family, Branner entered Cornell
University in 1870, where he met the geologist Charles
Hartt, who invited him for a trip to Brazil in 1874 (Penrose
1925). This expedition set the stage for the Comissao
Geologica do Império do Brasil (Geological Commission
of the Brazilian Empire), with Hartt as its director and
Branner as his assistant from 1875 to 1877 (Penrose
1925). Following the termination of the commission, in
1879 and 1880 Branner became assistant of the mining
engineer James E. Mills, who was superintendent of a U.S.
mining company in the state of Minas Gerais (Branner
1902). He returned to his home country in 1880, but a
few months later came back to Brazil, employed by the
inventor Thomas A. Edison to search for a vegetable fiber
to strengthen incandescent lights (Penrose 1925). In 1882,
working for the U.S. Department of Agriculture, Branner
traveled to study the insects affecting cotton and sugar
cane cultures in Brazil (Penrose 1925; Oliveira 2014).

In 1899, as a professor at Stanford University, Branner
returned to Brazil with collaborators for the ‘Branner-
Agassiz Expedition’, funded by Alexander Agassiz (son
of Louis Agassiz), to study the geology of ocean reefs,
atolls, and volcanic islands, besides zoology (particularly
ichthyology) traveling along the coast of Rio Grande do
Norte and Bahia states (northeastern Brazil) and visiting
islands such as the Fernando de Noronha archipelago
(Penrose 1925; Oliveira 2014). Another visit occurred
in 1907 to study the black diamonds districts of Bahia
and the geology of Alagoas and Sergipe states, also in
northeastern Brazil (Penrose 1925). In 1911, Branner
led the ‘Stanford Expedition to Brazil’ (or ‘Hopkins-
Branner Expedition’ (Schmidt and Inger 1951)), intended
to explore the Brazilian coast from the northeast to the
mouth of the Amazon river, in the north (Oliveira 2014).

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Costa, H.C.: The type locality of the snake Liotyphlops wilderi

The original objectives were not accomplished, but the
team made geological and zoological collections in the
states of Rio Grande do Norte, Ceara, Para, Amazonas,
and Rond6onia, as well as Bolivia (Oliveira 2014, 2018).
Despite being a geologist, Branner was trained as a nat-
uralist, making observations, and collecting material other
than of geological interest, even before his interdisciplin-
ary expeditions as a professor at Stanford. This led to the
publication, for example, of an account of the identifica-
tion of the supposedly deadly peanut-headed lantern fly
(Fulgora lanternaria) (Branner 1885) and of notes on the
fauna of Fernando de Noronha (Branner 1888). He also
collected specimens that would later become the types of
new species, like the treefrog Dendropsophus branneri
(Cochran, 1948) and the aforementioned snake Lioty-
Phlops wilderi. To find the correct name and current lo-
cation of Sao Cyriaco, type locality of L. wilderi, I decid-
ed to investigate in more detail the life and work of J. C.
Branner. Additionally, I aimed to examine the specimen
identified as Amphisbaena prunicolor collected by Bran-
ner at Sao Cyriaco, as well as other reptile specimens from
the same locality housed in natural history collections.

Methods

With the intention of finding published records that could
shed light on the geographic location and the current
name of the type locality of Liotyphlops wilderi, in ear-
ly 2019 I used the Google Scholar database to search for
the following keywords: “S&o0 Cyriaco” AND Branner;
“Sao Cyprido” AND Branner; “Cypriao” AND Branner;
“Cypriano” AND Branner. I also searched at the VertNet
Portal (http://portal.vertnet.org) and SpeciesLink (https://
specieslink.net) for reptile specimens collected by J. C.
Branner, deposited in collections registered in those data-
bases, and in April 2019 I personally examined the extant
specimens, all deposited in U.S. museums. To ensure a
proper identification of these specimens, I compared their
external morphology (mainly scale counts, but also the
color pattern and measurements when necessary) with the
original descriptions or updated taxonomic studies (Gans
1966; Roze 1967; Peters and Donoso-Barros 1970; Peters
and Orejas-Miranda 1970; Dixon and Kofron 1983; Dixon
1989; Etheridge and Williams 1991; Silva and Sites 1999;
Vanzolini 2002; Campbell and Lamar 2004; Rodrigues et
al. 2006; Centeno et al. 2010; Perez et al. 2012; Costa
et al. 2015, 2019; Breitman et al. 2018; Santos and Reis
2018). I took measurements; snout-vent length (SVL) and
tail length (TL), with a ruler to the nearest millimeter and
photographs in dorsal view of all but one of the specimens
(one syntype of L. wilderi), for the purpose of illustration.

Results and discussion

The search for the correct name and location of the type
locality of Liotyphlops wilderi was successful. As stated

Zoosyst. Evol. 98 (1) 2022, 129-136

131

r-3 Alvorada de Minas
CC) States
— Rivers

Elevation (meters)
MH 0-349

MM 350-699
[9 700-1049
| | @— 1050-1399
| | Ml 1400-1749
| | Ml 1750-2099
MH 2100-2449
MM 2450-2799
MH 2800-3149
MH 3150-3499
MH 3500-3849
MH 3850-4200
[J > 4200

Figure 1. Map of the municipality of Alvorada de Minas, state of Minas Gerais, Brazil, type locality of Liotyphlops wilderi, where
the SAo0 Cyriaco Gold Mining Company was established in the 19" century. The star is placed over the city of Alvorada de Minas.

in the original description (Garman 1883) Sao Cyriaco is
the correct name. The S40 Cyriaco Gold Mining Compa-
ny of Boston received authorization from the Brazilian
Empire for operation at Minas Gerais in 1878 (Senado
Federal 1878). The mining was established close to the
village of Santo Antdnio do Rio do Peixe, an area said to
contain fertile soil, many fields, hills, and forests (Mills
1878). John Casper Branner worked in Sao Cyriaco in
1879 and 1880 as an interpreter and assistant engineer to
superintendent James E. Mills (Branner 1902). The vil-
lage of Santo Anténio do Rio do Peixe later became a dis-
trict of the municipality of Serro, and in 1962 became a
separate municipality named Alvorada de Minas (Carval-
ho 2018; Neves and SimG6es 2021) (18.72°S, 43.37°W)
(Fig. 1). This information is briefly cited, without details,
by Nogueira et al. (2019). Hammar (1908) cites “Cyriaco,
near Serra Providencia’”. The mines of SAo Cyriaco were
located in the Espinhago Mountain range (Gontijo 2008),
but I did not find any reference to a ‘serra’ (mountain)
named Providéncia in the region. It may be possible that
its name has changed.

Only 18 squamate reptiles collected by John C. Bran-
ner in Minas Gerais are registered at VertNet and six are
registered at SpeciesLink (all of the latter are at VertNet).
Those specimens were deposited at the collections of the
Field Museum (FMNH) (one specimen), the Museum
of Comparative Zoology (MCZ) (six specimens), and
the Cornell University Museum of Vertebrates (CUMV)
(11 specimens). The specimens were collected by Bran-
ner before he became a professor at Stanford University,
when he was working at SAo Cyriaco Gold Mining Com-
pany. He sent the specimens to his alma mater, Cornell
University, whence some were later exchanged with the

MCZ. One syntype of L. wilderi was sent from MCZ to
the FMNH, according to the collections’ catalogues. Un-
fortunately, one specimen from MCZ and all but three
specimens from CUMV are missing (Charles M. Dardia,
in litt., 2019). Therefore, to the best of my knowledge,
only nine specimens of reptiles collected by J. C. Branner
in Minas Gerais remain in museum collections. Below, I
provide information on those specimens, all personally
examined, and discuss reidentifications when needed.

ANOMALEPIDIDAE

Liotyphlops wilderi (Garman, 1883). Two specimens.
MCZ R-5126 (syntype) (Fig. 2A). Minas Gerais, Sao
Cyriaco. Sex unknown; SVL 163 mm; TL 5 mm. FMNH
73387 (syntype). Minas Gerais, SAo Cyriaco. Sex un-
known; SVL 156 mm; TL 4.6 mm.

ELAPIDAE

Micrurus corallinus (Merrem, 1820). Two specimens.
CUMV 1925 (Fig. 2B). Minas Gerais, Sao Cyriaco. Male.
SVL 415 mm; TL 66 mm. MCZ R-5568 (Fig. 2C). Minas
Gerais, Sao Cyriaco. Male; SVL 350 mm; TL 61 mm.
Micrurus frontalis (Duméril, Bibron & Dumeril,
1854). One specimen. CUMV 1928 (Fig. 2D). Minas
Gerais, Sao Cyriaco. Sex unknown; SVL ~300 mm; TL
21 mm. The specimen is desiccated, making the SVL
measurement less precise. It was originally identified as
M. lemniscatus Linnaeus, 1758. Despite its poor condi-
tion, a pattern of black triads is visible at some parts of the

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Figure 2. Reptiles collected by John Casper Branner in Minas Gerais between 1878 and 1879. A. Liotyphlops wilderi (MCZ
R-5126, syntype); B. Micrurus corallinus (CUMV 1925); C. Micrurus corallinus (MCZ R-5568); D. Micrurus frontalis (CUMV
1928); E. Erythrolamprus maryellenae (CUMV 1930); F. Amphisbaena metallurga (MCZ R-5124); G. Enyalius bilineatus (MCZ
R-5567); H. Urostrophus vautieri (MCZ R-5566). Scale bars: 10 mm.

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Zoosyst. Evol. 98 (1) 2022, 129-136

body. Among the Micrurus species known for the region,
only M. frontalis and M. carvalhoi Roze, 1967 (formerly
M. lemniscatus carvalhoi) show a triad pattern (Campbell
and Lamar 2004; Nogueira et al. 2019), and can be distin-
guished from each other mainly by the presence of a light
band on the snout of M. carvalhoi, absent in M. frontalis.

DIPSADIDAE

Erythrolamprus maryellenae (Dixon, 1985). One speci-
men. CUMV 1930 (Fig. 2E). Minas Gerais, So Cyriaco.
Sex unknown; SVL 280 mm; TL 90 mm. The specimen
was identified as Liophis merremii (= Erythrolamprus
miliaris merremii (Wied, 1821)). I reidentified it as
E. maryellenae by its having 19-19-17 dorsal scale rows
without apical pits, 152 ventrals, a divided cloacal shield,
66 paired subcaudals, eight supralabials (fourth and fifth
contacting the eye), and 10 infralabials (Dixon 1989).

AMPHISBAENIDAE

Amphisbaena metallurga Costa, Resende, Teixeira Jr.,
Dal Vechio & Clemente, 2015. One specimen. MCZ
R-5124 (Fig. 2F). Minas Gerais, Sao Cyriaco. Sex un-
known; SVL 123 mm; TL 14 mm. Garman (1883) cited
three specimens (with no collection catalogue informa-
tion) of Amphisbaena darwinii Dumeéril & Bibron, 1839,
one of which may be MCZ R-5124 (the other two may
be lost and I did not find any additional record of them).
Gans (1966) examined MCZ R-5124 and identified it as
A. prunicolor (Cope, 1885). Specimens of Amphisbaena
prunicolor have a dark purplish-brown color that fades to
pale brown in preservative. The color pattern 1s still clear-
ly visible in the holotype (Academy of Natural Sciences,
Philadelphia; ANSP 12969), collected in late 19" century
(Perez et al. 2012). In contrast, MCZ R-5124 presents a
uniform cream color pattern. Furthermore, 4. prunicolor
exhibits a row of postmalar scales (Gans 1966; Perez et
al. 2012), absent in MCZ R-5124. Gans (1966) noted this,
as can be seen in the document with the character data
for each specimen he examined (Document Number 8998
in the Library of Congress, Washington, D.C., U.S.A.).
There, Gans noted “2+4[8]” for the “chin segments”
of MCZ R-5124. The brackets indicate a row of scales
posterior to the mouth commissure, which should not be
counted as a postmalar row but rather as the first body an-
nulus, as can be seen in his annotations of A. albocingula-
ta Boettger, 1885. The color pattern and the morphology
of MCZ R-5124 (205 body annuli, three lateral annuli, 19
caudal annuli, autotomic site at 8" caudal annulus, lateral
sulcus present, dorsal and ventral sulci absent, 12 dorsal
and 14 ventral segments at a midbody annulus, four pre-
cloacal pores sequentially arranged, three supralabials,
three infralabials, two scales on first postgenial row, four
scales on second postgenial row, and no postmalars) best

133

fit the diagnosis of Amphisbaena metallurga, whose type
locality is Conceicaéo do Mato Dentro, a neighboring mu-
nicipality south of Alvorada de Minas (Costa et al. 2015,
2019). MCZ R-5124 increases the range of body annuli
of A. metallurga from 185-199 to 185-205 and the range
of caudal annuli from 23—25 to 19-25. Therefore, the re-
cord of Amphisbaena prunicolor for Sao Cyriaco, Minas
Gerais, is here invalidated.

LEIOSAURIDAE

Enyalius bilineatus Duméril & Bibron, 1837. One speci-
men. MCZ R-5567 (Fig. 2G). Minas Gerais, unknown lo-
cality. Sex unknown; SVL 77 mm; TL 168 mm (tip broken).
Urostrophus vautieri Duméril & Bibron, 1837. One
specimen. MCZ R-5566 (Fig. 2H). Minas Gerais, un-
known locality. Sex unknown; SVL 76 mm; TL 95 mm.

According to the collection catalogues, the nine miss-
ing specimens were: 1) CUMV 1926, Minas Gerais,
Sao Cyriaco — recorded as Erythrolamprus aesculapii
monozona (Jan, 1863) (Serpentes: Dipsadidae); the tax-
onomy of E. aesculapii needs clarification (Curcio et al.
2015), but the name EF. a. venustissimus (Wied, 1821) has
been used for non-Amazonian populations, including for
morphs with fused black rings (Costa and Bérnils 2018).
2) CUMV 1924, Minas Gerais, Sao Cyriaco — recorded as
Elapomorphus quinquelineatus (Raddi, 1820) (Serpentes:
Dipsadidae). 3-4) CUMV 1927 and 1939, Minas Gerais,
Sao Cyriaco — recorded as Oxyrhopus trigeminus Duméril,
Bibron & Dumeril, 1854 (Serpentes: Dipsadidae), possibly
correct, but we cannot dismiss Oxyrhopus guibei Hoge &
Romano, 1978, described almost a century after the speci-
men’s collection, quite similar to O. trigeminus (Zaher and
Caramaschi 1992) and also expected to occur 1n the region
(Nogueira et al. 2019). 5) CUMV 1931, Minas Gerais, Sao
Cyriaco — recorded as Liophis reginae (Linnaeus, 1758)
(= Erythrolamprus reginae;, Serpentes: Dipsadidae), most
probably Erythrolamprus macrosoma (Amaral, 1935),
formerly a subspecies of FE. reginae that recently received
full species status and is expected to occur in the region,
contrary to E. reginae sensu stricto (Ascenso et al. 2019).
6-7) CUMV 1933 and 1935, Minas Gerais, SAo0 Cyriaco —
recorded as Liophis cobella (Linnaeus, 1758), (= Erythrol-
amprus cobella;, Serpentes: Dipsadidae) today restricted to
northern South America (Nogueira et al. 2019); no species
of the E. cobella group is expected to occur in the region
(Fernandes et al. 2002) and possibly the referred specimens
are E. poecilogyrus poecilogyrus (Wied, 1824), a common
species in southeastern Brazil (Nogueira et al. 2019). 8)
CUMV 1936, Minas Gerais, S40 Cyriaco — one syntype of
Typhlops wilderi Garman, 1883 (Serpentes: Anomalepidi-
dae). 9) MCZ R-144556, Minas Gerais, unknown locality
— Enyalius bilineatus (Iguania: Leiosauridae).

Minas Gerais has one of the richest reptile fauna
among Brazilian states (Costa et al. 2022), probably

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134

related to its large area and presence of varied ecoregions
(Drummond et al. 2005). During the 19" century, Minas
Gerais was visited by naturalists who traveled mainly
along the mining districts of the Espinhaco mountain
range (Papavero 1971). John C. Branner was a geologist
but collected reptile specimens while working for the
Sao Cyriaco Gold Mining Company, in the Espinhaco
range. Unfortunately, half of the 18 specimens collect-
ed by him in Minas Gerais that had been catalogued in
museums are lost. But the remaining material includes
valuable specimens such as two syntypes of Liotyphlops
wilderi and a wormlizard reidentified here as Amphis-
baena metallurga, a recently named taxon. Sao Cyriaco
(now Alvorada de Minas) is the fifth locality from which
A. metallurga is known to occur (Costa et al. 2015, 2019;
Dal Vechio et al. 2018), and all but one (Morro do Pilar)
previous records of this species are in areas impacted by
mining activities.

In the so called ‘century of extinctions’, when biodi-
versity is facing a crisis by human activities (Ceballos
et al. 2015), taxonomy is crucial for conservation biol-
ogy (Dubois 2003; Hortal et al. 2015). In this regard,
reviewing and updating information on doubtful type
localities is important to overcome some problems that
hamper advances in taxonomy and systematics (Bell
et al. 2020). Liotyphlops wilderi has a relatively broad
geographic range (Nogueira et al. 2019), although being
known from few specimens (Centeno et al. 2010; San-
tos and Reis 2018). The two remaining syntypes are dis-
colored, dissected, and lack genetic samples. Knowing
the exact type locality will allow the future collection
of topotypes. Such new specimens would be useful for a
morphological reanalysis of the species and its inclusion
in molecular phylogenies. If future research finds that
specimens assigned to L. wilderi belong to more than
one species, specimens from its type locality will be
very important.

Acknowledgments

I am grateful to Alan Resetar and Joshua Mata
(FMNH), Charles M. Dardia (CUMV), James Hanken
and Jose Rosado (MCZ) for allowing access to speci-
mens under their care; to Eva Lynn Gans and the Gans
Collections and Charitable Fund, for making available
to me the document of Carl Gans deposited in the L1-
brary of Congress. To Pedro Taucce (subject editor),
Angele Martins, Rodrigo C. Gonzalez, and Thais B.
Guedes for valuable comments on a previous version
of this article that greatly improved the final text. To
Ross D. MacCulloch for his English review. This work
was funded by a visiting scholarship from the Field
Museum (2019), and a postdoctoral fellowship by
Programa Nacional de Pés-Doutorado, Coordenacao
de Aperfeigoamento de Pessoal de Nivel Superior
(PNPD/CAPES) at Universidade Federal de Vicosa
(2018-2019).

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Costa, H.C.: The type locality of the snake Liotyphlops wilderi

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