Skip to main content

Full text of "Breviora"

See other formats


Nl m s e ui m oi ^©mparaitive Zoology 

US ISSN 0006-9698 

Cambridge, Mass. 17 October 2011 Number 526 





Javier Sunyer, 1 Josiah H. Townsend, 2 David B. Wake, 3 Scott L. Travers, 4 - 6 
Sergio C. Gonzalez, 4 Lenin A. Obando, 1 and Ardiel Z. Quint ana 5 

Abstract. We describe a new species of Oedipina (subgenus Oedipina) from premontane elevations of three isolated 
mountains in northern Nicaragua. The new cryptic species differs in molecular characters from its closest relatives: 
Oedipina cyclocauda (an Atlantic lowland species with a distributional range from central Panama to extreme 
southeastern Nicaragua) and Oedipina pseudouniformis. We regard all Nicaraguan specimens previously referred to as O. 
pseudouniformis to be conspecific with the new species herein described and restrict O. pseudouniformis as a Costa Rican 
endemic species. We also record the fourth known locality (and southernmost) of the Nicaraguan endemic O. nica and 
discuss additional species of Oedipina that are likely to be found in Nicaragua as field research continues in the country. 

Resumen. Describimos una nueva especie de Oedipina (subgenera Oedipina) de alturas premontanas de tres 
montanas aisladas del norte de Nicaragua. La nueva especie criptica difiere en caracteres moleculares de sus parientes 
mas cercanos: Oedipina cyclocauda (una especie de las tierras bajas del Atlantico entre el centro de Panama y el 

1 Museo Herpetologico de la UNAN-Leon (MHU"L), Departamento de Biologia, Facultad de Ciencias y Tecnologia, 

Universidad Nacional Autonoma de Nicaragua-Leon, Leon, Nicaragua; e-mail:; 

2 School of Natural Resources and Environment, University of Florida, Gainesville, Florida 32611, U.S.A., and 

Centro Zamorano de Biodiversidad, Escuela Agricola Panamericana Zamorano, Departamento de Francisco 

Morazan, Honduras; e-mail: 

3 Museum of Vertebrate Zoology and Department of Integrative Biology, 3101 VLSB, University of California 
Berkeley, California 94720-3160, U.S.A.; e-mail: 

4 Department of Wildlife Ecology and Conservation, and Florida Museum of Natural History, University of Florida, 
Gainesville, Florida 32611, U.S.A.; e-mail:; 

5 Hebron 3, 35018 Las Palmas de Gran Canarias, Islas Canarias, Spain; e-mail: 

6 Present Address: Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 
19085, U.S.A. 

® The President and Fellows of Harvard College 2011. 


No. 526 

extreme sureste de Nicaragua) y O. pseudouniformis. Consideramos a todos los especimenes nicaraguenses 
previamente referidos como Oedipina pseudouniformis representantes de la nueva especie aqui descrita y a O. 
pseudouniformis una especie endemica de Costa Rica. Tambien registramos la cuarta localidad conocida (y mas al 
sur) de la salamandra endemica O. nica y discutimos acerca de especies adicionales de Oedipina candidatas a ser 
encontradas en Nicaragua a medida que se continue investigando en el pais. 

Key words: 16S; cyt b; mtDNA; environmental modeling; Oedipina koehleri sp. nov.; Oedipina nica; Parque 
Nacional Cerro Saslava; Reserva Natural Cerro Musun 

Despite their remarkably conserved 
external morphology. Neotropical worm 
salamanders (Caudata: Plethodontidae: 
Oedipina) have been shown in recent 
phylogenetic studies to exhibit a surprising 
degree of evolutionary diversity (Garcia- 
Paris and Wake, 2000; McCranie et al, 
2008). Most recently, Sunyer et al. (2010) 
described a new species of Oedipina of the 
cryptic subgenus Oeditriton (O. nica) from 
three isolated highlands in north-central 
Nicaragua. The description of O. nica 
marked the first in a series of papers dealing 
with the systematics of various unresolved 
populations of Oedipina from around the 
country. The present contribution is the 
second of these papers and addresses the 
systematic status of three additional isolated 
populations of Oedipina (two of which had 
previously been assigned to Oedipina pseu- 
douniformis) from northern Nicaragua. 

The taxon O. pseudouniformis has been 
reported in Nicaragua from two isolated 
premontane localities (Brame, 1968; Kohler 
et al., 2004). In his seminal revision of the 
genus, Brame (1968) included eight para- 
types of O. pseudouniformis based on a series 
collected in July 1957 from "Hacienda La 
Cumplida, 1 .5 km north of Matagalpa, 73 1 m 
elevation," Dept. Matagalpa, Nicaragua. 
Premontane elevations in this area have 
undergone severe human alteration in the 
last five decades, and cattle and agriculture 
(mostly coffee plantations) have isolated the 
few remaining forest patches to extreme 
upper portions of the surrounding mountain 
peaks. Kohler et al. (2004) additionally 

reported two specimens referred to O. 
pseudouniformis from pristine forest between 
approximately 600 and 945 m elevation in 
Parque Nacional Cerro Saslaya, Region 
Autonoma Atlantico Norte, Nicaragua. 

Although we have so far failed to secure 
fresh samples of Oedipina from premontane 
elevations in the surroundings of Hacienda 
La Cumplida in Matagalpa, we recently 
collected an additional specimen from pre- 
montane elevations at Parque Nacional 
Cerro Saslaya, as well as two specimens of 
Oedipina from Reserva Natural Cerro Mu- 
sun, Dept. Matagalpa, Nicaragua. Although 
external morphology has been unhelpful in 
elucidating taxonomic assignments for these 
populations, phylogenetic analysis of data 
from two mitochondrial genes (cytochrome b 
[cyt b] and 16S) demonstrates that the 
Saslaya and Musun populations represent a 
single undescribed species in the subgenus 
Oedipina, a sister of a clade of Costa Rican 
taxa Oedipina cyclocauda and O. pseudouni- 
formis. We herein provide a taxonomic 
description of this new species, evaluate its 
phylogenetic relationships within the genus 
Oedipina, and further comment on our 
understanding of Nicaraguan populations 
of Oedipina. 


Taxon Sampling. We formulated a new 
phylogenetic hypothesis for the genus Oedi- 
pina, and included representatives of both 
the Saslaya and Musun populations of the 
new species, as well as all congeners available 



Table 1 . Locality, voucher, and Genbank accession numbers for taxa and samples used in 

phylogenetic analyses. 






Nototriton barbouri 
Oedipina alleni 
Oedipina carablanca 
Oedipina collaris 
Oedipina complex 
Oedipina cyclocauda 

Oedipina elongata 
Oedipina gephyra 
Oedipina gracilis 
Oedipina grandis 
Oedipina ignea 
Oedipina kasios 

Oedipina koehleri 

sp. nov. 
Oedipina leptopoda 
Oedipina maritima 
Oedipina nica 

Oedipina pacificensis 
Oedipina petiola 
Oedipina poelzi 


Oedipina quadra 
Oedipina savagei 
Oedipina sp. 1 
Oedipina stenopodia 
Oedipina taylori 
Oedipina tomasi 
Oedipina uniformis 

Honduras: Atlantida 
Costa Rica: Puntarenas 
Costa Rica: Limon 
Panama: Code 
Panama: Colon 
Costa Rica: Heredia 

Guatemala: Izabal 
Honduras: Yoro 
Costa Rica: Heredia 
Costa Rica: Puntarenas 
Honduras: Ocotepeque 
Honduras: Olancho 
Honduras: Francisco Morazan 
Nicaragua: Atlantico Norte 
Nicaragua: Matagalpa 
Honduras: Yoro 
Panama: Bocas del Toro 
Nicaragua: Matagalpa 
Nicaragua: Jinotega 

Costa Rica: Puntarenas 
Honduras: Atlantida 
Costa Rica: Alajuela 

Costa Rica: Cartago 

Honduras: Gracias a Dios 
Costa Rica: Puntarenas 
Nicaragua: Jinotega 
Guatemala: San Marcos 
Guatemala: Zacapa 
Honduras: Cortes 
Costa Rica: Cartago 

UF 156538 
MVZ 190857 
No voucher 
SIUC H 8896 
MVZ 236255 
MVZ 138916 
MVZ 203747 
UTA A-51906 
UF [JHT2443] 
MVZ 210398 
MVZ 225904 
USNM 530586 
MVZ 232825 
UF 156500 
UF 156456 
SMF 90079 
MVZ 167772 
MVZ 219997 
MHUL 003 
MVZ 263774 
UF 156447 
UF 156453 
UCR 12063 
USNM 343462 
MVZ 181235 
MVZ 206398 
MVZ 203749 
MVZ 181229 
MVZ 190852 
MCZ 232824 
UCR 14587 
SMF 78738 
MVZ 163649 
USAC 1134 
UF 150066 
MVZ 203751 

AF 199207 
FJ 196862 
FJ 196863 
JN 190930 
AF 199219 
FJ 196864 
AF 199231 
FJ 196866 
HM 113477 
JN 190926 

JN 190928 
HM 11 3474 
HM 11 3475 
AF 199222 

AF 199223 
AF 199227 

AF 199209 
AF 199228 
JN 190929 
AF 199230 



FJ 196869 

FJ 196870 






HM 113484 
JN 190934 


HM 113482 

HM 113483 








FJ 196871 


JN 190935 

on GenBank (; 
species, locality, and voucher information 
for these taxa are summarized in Table 1. 
Acronyms for museum collections follow 
those of Leviton et al. (1985), except MHUL 
(Museo Herpetologico de la UNAN-Leon, 
Universidad Nacional Autonoma de Nicara- 
gua-Leon, Leon, Nicaragua), N field num- 
bers, which correspond to specimens col- 
lected in Nicaragua between 2007 and 2008 

by University of Florida field teams in 
collaboration with the UNAN-Leon, and 
JHT (field series of the second author), 
which is used for a specimen of Oedipina 
gephyra donated to the University of Florida 
(UF) in May 2009 that remains uncataloged. 
Nototriton barbouri, a member of the sister 
genus to Oedipina (Garcia-Paris and Wake, 
2000; Wiens et al, 2007), was used as an 


No. 526 

Morphological Examinations. Measure- 
ments follow those used in McCranie et al. 
(2008). All measurements are in millimeters 
(mm) and made to the nearest 0.1 mm with 
dial calipers and a dissecting microscope 
with ocular micrometer. SL is the distance 
from the tip of the snout to the posterior 
angle of the vent. Males were determined by 
the presence of mental glands behind the tip 
of the mandible and small papillae in the 
anterior part of the vent and females by the 
presence of folded vent margins and absence 
of mental glands and vent papillae. Maxil- 
lary and vomerine tooth counts are totals of 
the paired bones. Limb interval equals the 
number of costal interspaces between ad- 
pressed limbs. We provide a list of the 
Nicaraguan comparative specimens exam- 
ined in the Appendix. 

DNA Extraction and Sequencing. Template 
DNA was extracted from tissue with a 
Qiagen PureGene DNA Isolation Kit (Qia- 
gen, Valencia, California) following manu- 
facturer's instructions. Fragments of two 
mitochondrial genes were targeted for ampli- 
fication: a 516-bp fragment of the 16S large 
subunit rRNA (16S) was amplified using 
primers 16Sar-L and 16Sbr-H (Palumbi et 
al, 1991), and a 692-bp fragment of cyt b was 
amplified using primers MVZ15 and MVZ16 
(Moritz et al, 1992). Conditions for PCR did 
not differ between genes, with initial dena- 
turation at 94°C for 3 min, 35 amplification 
cycles of 45 s denaturation at 94°C, 45 s 
annealing at 50°C, 45 s extension at 72°C, 
and a final extension of 5 min at 72°C. 
Samples were cleansed of unincorporated 
dNTPs through application of USB Exo- 
SAP-IT before following standard sequenc- 
ing protocol on an ABI 3130x1 automated 
sequencer (Applied Biosystems, Foster City, 
California) at the University of Florida 
WEC/SFRC Molecular Ecology Lab. 

Phylogenetic Analyses. Cytochrome b se- 
quences were trimmed to 385 bp to match 

available sequences in GenBank from other 
studies (Garcia-Paris et al, 2000; McCranie 
et al, 2008; Sunyer et al, 2010), and 
sequence alignment was estimated using 
MAFFT (Katoh et al, 2002). Bayesian 
phylogenetic analysis was performed in 
MrBayes v3.1.2 (Huelsenbeck and Ronquist, 
2001), with sequence data partitioned by 
gene for 16S and by codon position for cyt b. 
Using the Akaike Information Criterion 
in MrModeltest2.2 (Nylander, 2004), we se- 
lected the nucleotide substitution model 
GTR+I+r for 16S, and GTR+I+r, GTR+r, 
and HKY+r for first, second, and third 
codon position of cyt b, respectively. Bayes- 
ian analysis consisted of two parallel runs of 
four chains, run for 20 X 10 6 generations and 
sampled every 1,000 generations, with the 
first 4,000 samples discarded as burn-in. The 
remaining 16,001 post-burn-in trees from 
both runs were used to generate a 50% 
majority rule consensus tree. Cumulative and 
sliding window plots of split frequencies and 
the correlation of split frequencies in first 
versus second runs were visualized in Gen- 
eious v4.8 (Drummond et al, 2009) to assess 
convergence around posterior quantities. 
Maximum likelihood (ML) phylogenetic 
analysis was conducted in RAxML v7.2.6 
(Stamatakis, 2006) using the same data 
partitions as the Bayesian analysis and the 
GTR+r model for each partition; 1,000 
bootstrap replicates were performed using 
the rapid bootstrapping algorithm. 

Macroecological Modeling. We created an 
environmental niche model based on the 
localities of Oedipina koehleri using the 
maximum entropy method (Phillips et al, 
2006) as implemented in the program Max- 
Ent, to determine whether a resulting distri- 
bution model would predict occurrence of O. 
koehleri at Hacienda La Cumplida, Dept. 
Matagalpa, the locality given for eight 
paratypes of O. pseudouniformis (Brame, 
1968). Using presence-only data (i.e., local- 



ities of occurrence), MaxEnt uses the princi- 
ple of maximum entropy density estimation 
to generate a probability distribution (Phil- 
lips et al, 2006; Phillips and Dudik, 2008). It 
has been shown to produce more accurate 
models with lower sample sizes than other 
niche-modeling methods (Elith et al, 2006; 
Hernandez et al, 2006). We used the 19 
WorldClim Current BioClim climate layers, 
which have a resolution of 30 arc-seconds 
(about 1 km 2 ). These layers are based on 
data from 1950 to 2000 and include variables 
reflecting annual, as well as seasonal, climat- 
ic trends and extremes of precipitation and 
temperature (Hijmans et al, 2005). We did 
not make any assumptions of correlation 
among these variables and thus chose to use 
the entire set of environmental layers. We 
clipped the WorldClim layers in ESRI 
ArcGIS 9.3 to our working extent before 
using them in MaxEnt. A model representing 
the probability of occurrence of O. koehleri 
was produced in MaxEnt using a cross- 
validation approach for our specimen local- 
ities. The cross-validation function splits the 
data set into n samples of one case that are 
individually tested against all remaining 
samples, which become the training set of 
localities during each run (Araujo et al, 
2005). This eliminated the need to partition a 
data set into large training and testing sets. 
In this case, this approach was necessary 
because splitting the data would have result- 
ed in a training set of insufficient size. The 
final mean logistic output of the model runs 
was used to assess our results. The area 
under the curve (AUC) of the receiver 
operating characteristic plot was used to 
evaluate model performance. 

Systematic Account 

Oedipina koehleri sp. nov. 

Figure 1 

Oedipina pseudouniformis (Brame, 1968) in 
part: Brame (1968:25-28, fig. 20). Paratypes 

UMMZ 119523(1-8) from "Hacienda La 
Cumplida, 1.5 km N of Matagalpa, elevation 
731 m (2,400 ft), Dept. Matagalpa, Nicara- 
gua"; Villa (1972:51-54); Villa (1983:21); 
Villa et al (1988:7-8); Kohler (1999:11); 
Kohler (2001:23); Ruiz and Buitrago 
(2003:36-37); Kohler et al (2004:18); Sunyer 
and Kohler (2010:500); Kohler (2011:86). 

Holotype. UF 156456, an adult male, from 
Parque Nacional Cerro Saslaya (along the 
trail from "Las Guardiolas" to "El Reve- 
nido"), 13°42.8'N, 85°01.9'W, 724 m above 
sea level (a.s.l.), Region Autonoma Atlantico 
Norte, Nicaragua, collected 1 August 2008 
by Scott L. Travers, Stephen Doucette-Riise, 
Sergio C. Gonzalez, Atanasio Baldonado, 
and Ignacio Cruz (original field num- 
ber N614). 

Paratypes. Four; SMF 82225, an adult 
male, from the southern slope of Parque 
Nacional Cerro Saslaya (along the trail from 
Campamento "Las Pavas" [13°44.5'N, 
85°01.5'W] to Campamento "Los Monos" 
[13°45.1'N, 85°02.2'W]), 945 m a.s.l., Region 
Autonoma Atlantico Norte, Nicaragua; 
SMF 82874, an unsexed juvenile, from the 
southern slope of Parque Nacional Cerro 
Saslaya (along the trail from Campamento 
"El Carao" [13°42.8'N, 84°58.7'W] to 
Campamento "Las Pavas" [13°44.5'N, 
85°01.5'W]), 400-600 m a.s.l., Region 
Autonoma Atlantico Norte, Nicaragua; 
SMF 90078-79, both adult females, from 
the southern slope of Reserva Natural Cerro 
Musun (FUNDENIC Cabins [12°57.3'N, 
85°13.9'W]), 628 m a.s.l., Dept. Matagalpa, 

Referred Specimens. Eight; UMMZ 
119523, four adult males and four adult 
females, all from Hacienda La Cumplida, 
1.5 km N of Matagalpa, 731 m a.s.l., Dept. 
Matagalpa, Nicaragua. 

Diagnosis. A slender species of moderate 
size (largest referred specimen 50.4 mm SL) 
and robustness assigned to the genus Oedi- 


No. 526 

Figure 1 . Adult female paratypes of Oedipina koehleri (a) SMF 90078 and (b) SMF 90079 from Reserva Natural 
Cerro Musiin; and (c) juvenile paratype of O. koehleri (SMF 82874) from Parque Nacional Cerro Saslaya. 

pitta based on the presence of more than 13 
costal grooves between the short limbs, and 
tail much longer than head plus body. This 
species is a member of the subgenus Oedipina 
(based on molecular data; Fig. 2) and is 
distinguished from its closest relatives, O. 

pseudouniformis, in having fewer maxillary 
teeth (mean 38 vs. 49.8 in males; 39.8 vs. 45 
in females) and vomerine teeth (mean 20.5 
vs. 25.9 in males; 22.2 vs. 25.7 in females), 
and O. cyclocauda in having a more rounded 
snout, a broader head, and somewhat longer 



O. pseudouniformis (MVZ 181229) 
O. pseudouniformis (Mvz 190852) 
O. pseudouniformis (mvz 203749) 

100/1,0 | O. CydocaudO (MVZ 203747) 

*• 0. cyclocouda (mvz 138916) 

O. koehleri sp. nov. (Cerro Saslaya; Holotype, UF 156456) 
'. koehleri Sp. nov. (Cerro Musiin; Paratype, SMF 90079) 

————— 0. leptopoda (mvz 167772) 


■ O. COlloris (SIUC H-8896) 


— O. grond/s (mvz 219593) 

• 0. poe/z/ (MVZ 206398) 

61/0.88 I 

O. uniformis (mvz 203751) 

O. pacificensis{\JCR 12063) 
— — 0. gracilis (mvz 203753) 

•Oedipina sp. 1 (SMF 78738) 

— 0. stenopodia (mvz 163649) 

— ^— ^— O. /'gneo (usnm 530586) 

— — ^— — — — ^^— — O. toy/or/ (USCG 1134) 

— O. gephyra (UF [JHT2443]) 

— — — O. petiola (USNM 343462) 

— — — — ^— — 0. tomasi (UF 150066) 



• 0. elongata (uta a-51906) 
^^— — — — O. carablanca 
— O. savagei (ucr 14587) 

8 2/0.97 r 

'0. o//en/ (MVZ 190857) 

- O. maritima (mvz 219997) 

— — — -^^— ^— 0. complex (MVZ 236255) 

■ 0. parvipes (mvz 210404) 

95/1.0 I 


0. nica (UF 156447) 

0. n/CO(MHUL003) 

0. n/CO (UF 156453) 

O. nica (MVZ 263774) 

O. fa7S/OS (MVZ 232826) 

kaSIOS (UF 156500) 

0. quadra (mvz 232824) 


■ Nototriton barbouri (UF 156538) 

Figure 2. Maximum likelihood (ML) phylogram (InL = -5,504.696063) of the genus Oedipina, showing 
placement of Oedipina koehleri (shown in bold) within the Oedipina subgenus. Bootstrap support values from ML 
analysis (scaled 0-100) and Bayesian posterior probabilities (scaled 0-1.0) are shown above the branches; ML 
bootstrap values omitted when less than 50, posterior probabilities omitted when less than 0.65. 

legs. Further distinguished from its closest 
geographic congener, O. (Oeditriton) nica, in 
having pale brown pigmentation on the 
proximal limb surfaces, in being slightly 
more robust, in having fewer maxillary teeth, 
and in having shorter limbs (hind limb length 
has mean value of 7.28 times SL in males, 
7.36 in females, averaging 11.3 costal folds 

uncovered by adpressed limbs (limb interval) 
vs. hind limbs more than 8 times SL and limb 
interval more than 13 in O. nica). The only 
other Nicaraguan species of the genus, 
Oedipina collaris, is much larger and has a 
long pointed snout and large limbs, manus, 
and pes. The new species differs from other 
members of its clade as follows: it is more 


No. 526 

robust and has longer limbs than Oedipina 
pacificensis, imiformis, leptopoda, and graci- 
lis: it is much smaller and lacks a dorsal band 
of brownish color dorsally that characterizes 
Oedipina poelzi and Oedipina altura; it is 
much smaller than O. grandis; it has more 
maxillary teeth than O. paucicarinatus and O. 
alfaroi; it is less elongate with more maxillary 
teeth than O. taylori; it has longer legs with 
broader manus and pes than Oedipina 
stenopodia; it has fewer maxillary teeth than 
Oedipina ignea; and it is smaller than 
Oedipina stuarti. It differs also by its 
combination of having distinct, rounded 
but syndactylous digits, moderately broad 
manus and pes, and predominantly black 
coloration, with some brown pigmentation 
on the dorsal surfaces of the proximal 
segments of the limbs and dispersed whitish 
to bluish speckling over the body and tail. 

Description of the Holotype. An adult 
male, as judged by having an inconspicuous 
mental gland behind the tip of the mandible 
and small papillae in the anterior portion of 
the vent. This species is a moderate-sized 
member of the genus (SL = 40.4 mm) with a 
moderately broad head (head width 10.9% of 
SL), slender habitus (trunk width at midbody 
12.1% of SL), and long tail (tail length 1.82 
times SL) with no apparent basal constric- 
tion; nares small, snout broadly rounded, 
and nasolabial protuberances not well devel- 
oped; maxillary teeth 17 on left side and 20 
on right side (37 total maxillary teeth), single 
premaxillary tooth set relatively far forward 
of interior margin of upper lip; vomerine 
teeth arranged in two arches with seven teeth 
on left arch and five teeth on right arch 
(12 total vomerine teeth); costal grooves 
number 19 and are relatively shallow, but 
well demarcated by unpigmented line at 
deepest point of groove; limbs short, 13 
costal grooves visible between adpressed 
limbs; front and hind feet with rounded, 
differentiated toe tips, toes well-defined but 

fused and essentially syndactylous; relative 
length of digits is I < IV < II < III on hands 
and I < V < II < IV < III on feet. 

Measurements (in mm) of Holotype. Snout 
to posterior angle of vent (SL) 40.4; tail 
width 4.9; head length 6.7; head width 4.4; 
tail length 73.6; trunk width 4.9; hind limb 
length 6.2; front limb length 5.2; hind foot 
width 1.2; eyelid length 1.7; eyelid width 0.9; 
interorbital distance 1.6; anterior rim of orbit 
to snout 1.6; distance separating internal 
nares 1.0; distance separating external nares 
1.8; snout projection beyond mandible 0.3; 
distance from axilla to groin 28.9; tail depth 
at base 3.4; tail width at base 3.4. 

Coloration of the Holotype in Alcohol. 
Ground color of dorsal, lateral, and ventral 
surfaces of head, body, and tail black; dorsal 
surface of head and ventral surfaces of body 
and tail, and tip of tail, slightly paler. Chin 
and throat markedly paler than dorsal 
surfaces of head and body, with an unpig- 
mented band along the leading edge of the 
gular fold. The proximal portions of the limbs 
are also paler than the dorsal and lateral 
ground color, and the surface of the body 
around the point of articulation for each limb 
is pale to unpigmented. Under magnification, 
all dorsal surfaces are profusely spotted with 
brown chromatophores, which become more 
numerous ventrally and are most abundant in 
the midventral portion of the posterior half of 
the body. The midlateral portions of the body 
are paler and the ventral surfaces are mostly 
unpigmented, with some scattered silvery 
spots present on the throat and anterior 
portions of the ventral surface. Pale chro- 
matophores so profuse on chin that ground 
color is not apparent, giving the chin an 
overall pale appearance. The upper lip and 
nasolabial protuberances are unpigmented. 
The center of each costal groove is unpig- 
mented, making the grooves appear more 
pronounced than would be evident from their 
actual physical depth. 



Variation. Variation in external morphol- 
ogy among the four adult specimens in the 
type series is minimal. The adult male 
paratype (SMF 82225) is larger than the 
male holotype (UF 156456) and proportion- 
ally has the longest tail, measuring 48.0 mm 
SL with a tail length 2.4 times that of SL; 
it has 39 (18/21) maxillary teeth, a single 
premaxillary tooth, and 19 (9/10) vomerine 
teeth. Compared with the holotype, SMF 
82225 has a slightly broader head (head 
width/SL = 0.116 vs. 0.109), shorter fore- 
limbs (right forelimb length/SL = 0.116 vs. 
0.121) and hind limbs (right hind limb 
length/SL = 0.137 vs. 0.153), and wider hind 
feet (right hind foot width/SL = 0.035 vs. 
0.030). Two adult female paratypes (SMF 
90078-79) are larger than the holotype; SMF 
90078 is the longest bodied type specimen of 
O. koehleri (49.2 mm SL, tail length 1.74 
times SL), and has 40 (19/21) maxillary, four 
premaxillary, and 19 (10/9) vomerine teeth; 
SMF 90079 measures 44.6 mm SL with a tail 
length 1.62 times that of SL. Compared with 
the holotype, the two female paratypes have 
slightly narrower heads (head width/SL = 
0.104-0.105 vs. 0.109), shorter forelimbs 
(right forelimb length/SL = 0.096-0.101 vs. 
0.121), and shorter hind limbs (right hind 
limb length/SL = 0.120-0.126 vs. 0.153). 

The referred specimens (UMMZ 119523; 
eight specimens) also show little variation 
from the type series. One specimen, a female, 
is the largest representative of O. koehleri, 
measuring 50.4 mm SL with a tail that is 1.8 
times that of the SL. The remaining seven 
specimens in this series range from 39.3 to 
42.9 mm SL in males (with tails 1.5-1.7 times 
SL) and 40.7 to 44.6 mm SL in females (with 
tails 1.6-1.7 times SL). Compared with the 
type series, the UMMZ series has a similar 
number of maxillary teeth (36-39 in four 
males, 36-44 in females) and a slightly higher 
count of vomerine teeth (20-22 in four males, 
23-26 in females) but otherwise agrees with 

the morphological proportions of the type 

Phylogenetic Relationships. Our analyses 
support assignment of the populations at 
Saslaya and Musun to a single taxon, O. 
koehleri (Fig. 2, ML bootstrap value = 100, 
posterior probability = 1.0), and also sup- 
port a sister relationship between O. koehleri 
and the more southerly O. cy do caudal O. 
pseudouniformis clade (Fig. 2, ML bootstrap 
value = 99, posterior probability = 1.0) 
within the subgenus Oedipina. Deeper rela- 
tionships within the subgenus Oedipina are 
generally poorly resolved, with four clades: 
an O. collarislO. grandislO. poelzi clade, an 
O. gracilis/O. pacificensisl O. uniformis clade, 
an O. ignealO. stenopodial O. taylori clade, 
and the aforementioned O. cy do caudal O. 
pseudouniformis I O. koehleri clade. Addition- 
ally, the relationships of two taxa with 
respect to the rest of the subgenus Oedipina 
are unresolved, O. leptopoda and Oedipina 
sp. 1 (see comments in Sunyer et al. [2010] 
regarding Oedipina sp. 1). Monophyly of the 
subgenus Oedipina is supported (84/0.99), as 
is the sister taxon relationship between the 
subgenera Oedipina and Oedopinola (100/ 

Natural History. This is a secretive and 
fossorial species known to occur from 
approximately 600 to 945 m elevation at 
three isolated localities in northern Nicara- 
gua (Fig. 3). Two of these localities (Cerro 
Saslaya and Cerro Musun) correspond to the 
Premontane Wet Forest formation and the 
remaining locality (near Matagalpa) to the 
Premontane Moist Forest formation (Hol- 
dridge, 1967). The holotype was collected in 
undisturbed, primary broadleaf rainforest 
with a dense canopy structure and a rela- 
tively open understory. It was found under a 
fallen log during a late-morning hike while 
ascending the southern slopes of Cerro El 
Toro, a sister peak approximately 5 km 
southwest of Cerro Saslaya that lies within 



No. 526 

Figure 3. Map of Nicaragua showing the localities of members of the genus Oedipina (see Appendix): O. koehleri 
(stars), O. nica (circles), O. collaris (square), and O. cyclocauda (triangle). Open symbols represents each species' type 
locality, if it appears on map. If situated very close to one other, we combined distribution points to yield a single 
point on our map. Water surfaces are shaded pale gray. Areas above 600 m are shaded gray. Areas above 1 ,200 m are 
shaded dark gray. 

the confines of the park boundaries. The 
adult male paratype from Parque Nacional 
Cerro Saslaya (SMF 82225) was collected 
around 1400 h in pristine forest under a 
decaying log alongside a forest trail on a 
moderately steep hill slope. It suddenly 
jumped downslope by body flipping. The 
juvenile paratype (SMF 82874) from Parque 
Nacional Cerro Saslaya was collected 
around 0900 h in pristine forest under a 
large rock at the edge of a shady stream 
bank. It was found buried in a wet mixture of 
mud-rich sand and debris. The paratypes 
from Reserva Natural Cerro Musun (SMF 
90078-79) were collected in the garden of an 
isolated tourist cabin, which, although sur- 

rounded by pastureland, is relatively close to 
the reserve's forest edge. They were both 
found during diurnal surveys involving close 
inspection of large piles of a humid mixture 
of mostly cut grass with some leaf litter and 
other groundskeeping debris from the gar- 
den, characterized by a few large trees that 
gave partial shade to the grass and orna- 
mental bushes. A third specimen escaped by 
quickly burrowing itself into the dense 

Macroecological Modeling. Our environ- 
mental niche model appeared to track the 
niche requirements and distribution of O. 
koehleri accurately because the resulting 
mean AUC value of our test runs was 0.984 




Figure 4. Habitat of Oedipina koehleri from (a) Reserva Natural Cerro Musun and (b) Parque Nacional 
Cerro Saslaya. 

(SD = 0.011), where a value of 1 is optimal 
and 0.5 is as good as random. This interpre- 
tation of our AUC value is consistent with 
the literature for other taxa (Fielding and 
Bell, 1997; Osborne and Suarez-Seone, 2002; 
Hernandez et al, 2006; Rodder et al, 2010). 
On comparing the model's predictions with 
the Hacienda La Cumplida locality (Fig. 4), 
we see that our environmental niche model- 
ing predicts a high probability of occurrence 
for O. koehleri at and around that locality, as 
well as throughout the premontane areas of 
northern Nicaragua. Thus, the locality Ha- 
cienda La Cumplida resides within an area 
where the environmental conditions are 
nearly optimal for the presence of O. 
koehleri, further supporting inclusion of the 
Nicaraguan paratypes of O. pseudouniformis 
under the new taxon. 

Etymology. The specific name koehleri is a 
patronym for our friend and colleague 
Gunther Kohler, in recognition of his many 
important contributions to the herpetology 
of Central America in general and Nicaragua 
in particular. 

Conservation Status. Using the criteria 
established by IUCN for evaluating threat- 
ened species, O. koehleri should be classified 
as Endangered (EN B2ab[iii]) because of its 

limited distribution (known only from three 
isolated mountainous forest areas with a 
total extent of less than 500 km 2 ) and the 
continued loss of habitat at these localities. 
Despite repeated searches, representatives of 
this species in the vicinity of Brame's (1968) 
Matagalpa locality have not been collected 
since 1957, and the locality is almost 
completely converted to agriculture, cattle 
ranching, or otherwise degraded, as is the 
majority of intervening territory for the two 
localities of the type specimens. 


Members of the subgenus Oedipina are 
noted for their lack of morphological differ- 
entiation (Taylor, 1952; Brame, 1968; Good 
and Wake, 1997; Garcia-Paris and Wake, 
2000), which has led to a somewhat confus- 
ing taxonomic history for some populations. 
Phylogenetic analysis of two mitochondrial 
loci indicate that O. koehleri is the sister 
species to the clade containing O. pseudouni- 
formis and O. cyclocauda (Fig. 2), two 
morphologically unremarkable species de- 
scribed on the basis of Costa Rican material. 
Good and Wake (1997) commented on the 
difficulty of distinguishing O. pseudounifor- 
mis and O. cyclocauda from one another on 



No. 526 

morphological grounds, and the same is true 
for O. koehleri. However, all three species are 
genetically well differentiated (Fig. 2) and 
are not known to occur in sympatry, 
supporting the validity of each taxon (Sav- 
age, 2002). 

The type locality of O. pseudouniformis is 
near Turrialba, Prov. Cartago, Costa Rica, 
and the original description of this species 
included 182 paratypes (Brame, 1968). All of 
these paratypes were collected in the low- 
lands and premontane elevations of Costa 
Rica, with the exception of eight specimens 
collected at premontane elevations in Dept. 
Matagalpa, Nicaragua (Brame, 1968). Para- 
types from Nicaragua average fewer maxil- 
lary teeth than Costa Rican O. pseudouni- 
formis but otherwise are indistinguishable 
from the Costa Rican specimens (Brame, 
1968). Counts of maxillary teeth can be 
useful in discriminating species of Oedipina 
(Brame, 1968). Some species lack teeth 
entirely, whereas those of O. pseudouniformis 
and O. koehleri are moderately high in 
number and not very useful for diagnostic 
purposes. Savage (2002:156) did not include 
Nicaragua in the distribution of O. pseudou- 
niformis and only briefly mentioned the 
Nicaraguan population assigned to that 
species (Savage, 2002:150). Given that the 
Matagalpan and Costa Rican populations 
are isolated by the Nicaraguan Depression, 
one of the major biogeographic boundaries 
in Central America (Savage, 2002), and that 
most species of the genus Oedipina, other 
than a few lowland species, have relatively 
restricted distributions (AmphibiaWeb, 
2011), we think it likely this Matagalpan 
population represents a different taxon than 
O. pseudouniformis. Although we lack fresh 
tissue samples for molecular analysis from 
the Matagalpan population, we refer the 
Nicaraguan paratypes of O. pseudouniformis 
to O. koehleri (as referred specimens) on the 
basis of evidence from morphological char- 

acteristics and macroecological modeling 
(see Fig. 5). Therefore, O. pseudouniformis 
is no longer considered to occur in Nicara- 
gua, and its distribution is restricted to Costa 

The predicted distribution of O. koehleri 
corresponds to the premontane slopes of the 
southern terminus of the nuclear Central 
American highlands, along the humid At- 
lantic versant (Fig. 5). This area is relatively 
poorly known in terms of its herpetological 
diversity and includes a relatively vast 
portion of land extending from Departa- 
mento Chontales in central Nicaragua to the 
northern border of the country, and poten- 
tially extending peripherally into southeast- 
ern Honduras. Unfortunately, premontane 
elevations within this area are highly dis- 
turbed and have largely been converted to 
agriculture or other anthropogenic uses, 
with few exceptions. Intact premontane 
habitat within the predicted distribution of 
O. koehleri appears to be limited to the few 
mountains present in the large Reserva de la 
Biosfera Bosawas and a series of relatively 
small protected areas, which include both 
localities of the type specimens as well as 
the following Reservas Naturales: Cerro 
Apante, Cerro Banacruz, Cerro Cola 
Blanca, Cerro Cumaica-Cerro Alegre, Cerro 
Datanli-El Diablo, Cerro Guabule, Cerro 
Kilambe, Cerro Kuskawas, Cerro Momba- 
chito-La Vieja, Fila Cerro Frio-La Cum- 
plida, Fila Masigiie, Macizo de Penas 
Blancas, Sierra Amerrisque, Sierra Quirra- 
gua, and Cerro El Arenal. Recent field trips 
to the highlands of the vicinity of Reserva 
Natural Cerro El Arenal (in Finca Mon- 
imbo, the property adjacent to Hacienda La 
Cumplida, where the Nicaraguan paratypes 
of O. pseudouniformis were collected) result- 
ed in the addition of a single specimen of O. 
nica (MHUL 003), which corresponds to the 
fourth known population and southernmost 
distribution record of this Nicaraguan en- 




Figure 5. Environmental niche modeling showing the potential distribution of Oedipina koehleri in 
northern Nicaragua. 

demic species (see Figs. 2 and 3, Table 1, 
and Appendix). 

Oedipina koehleri is the fourth species of 
worm salamander recorded in Nicaragua 
(see Fig. 3), and more species of this genus 
are likely to be encountered as systematic 
investigation continues in the country. 
Aside from known Nicaraguan specimens 
with ambiguous taxonomic assignments (see 
Sunyer et al, 2010), at least three more 
species of Oedipina have been recorded 
from relatively near the political border in 
neighboring Honduras and Costa Rica and 
are likely to be found in Nicaragua as field 
research continues in the country: O. 
quadra is known from the lowland Carib- 
bean slope of northern and eastern Hon- 
duras approximately 5 km from the border 

between Honduras and Nicaragua (McCra- 
nie et al, 2008) in habitat continuous with 
that of adjacent Nicaragua and likely 
occurs in broadleaf rainforests in the 
northeastern part of the country; O. taylori 
occurs at low and moderate elevations on 
the Pacific versant from southeastern Gua- 
temala to southern Honduras (McCranie 
and Wilson, 2002) in similar habitat as that 
in northwestern Nicaragua and could occur 
in premontane forests in that area; and O. 
gracilis is known from the humid Atlantic 
lowlands between extreme northwestern 
Panama and northeastern Costa Rica (Sav- 
age, 2002) in habitat continuous with that 
in nearby southeastern Nicaragua and 
could occur in the Rio San Juan rain- 



No. 526 


Collecting and exportation permits were 
provided by B. Quintero-Guatemala, C. 
Rivas-Leclair, M. G. Camacho-Bonilla, E. 
Duarte, C. R. Mejia, F. Gadea-Castillo, F. 
Rivera, R. Salvador-Castellon, A. Choza- 
Lopez, R. Gutierrez, F. Vanegas, A. Lorio, 
and Y. Palacios, Ministerio del Ambiente y 
los Recursos Naturales (MARENA), Mana- 
gua, Nicaragua. Special thanks go to D. E. 
Manzanarez, S. Doucette-Riise, A. Baldo- 
nado, I. Cruz, P. Lopez, and the indigenous 
volunteer forest rangers of Bosawas for their 
assistance in the field. We thank C. Bermudez 
(FUNDENIC), R. Dilger (GTZ), C. Land- 
ero, and personnel from MARENA-SETAB 
for logistic support. We are very thankful to 
D. J. Marenco for his kind invitation to do 
herpetological research on his property (Finca 
Monimbo) and his warm hospitality. For the 
loan of specimens under their care, we thank 
G. Kohler, Senckenberg Forschungsinstitut 
und Naturmuseum (SMF), Frankfurt am 
Main, Germany, and R. Nussbaum and G. 
Schneider, University of Michigan Museum 
of Zoology (UMMZ), Ann Arbor, Michigan. 
We also thank T. Papenfuss and S. Rovito for 
helpful discussions that improved this manu- 
script, and S. Rovito for providing 16S 
sequence data for MHUL 003. Genetics work 
was carried out in the University of Florida 
WEC/SFRC Molecular Ecology Laboratory 
under the supervision of J. Austin, whom we 
thank along with J. Hargrove, N. Johnson, 
and E. Saarinen for support and many fruitful 
discussions in the lab. This research was 
carried out thanks to the "Memorandum of 
agreement between the UNAN-Leon and the 
MVZ" and was supported in part by the 
Deutscher Akademischer Austausch Dienst 
(DAAD), the German Reconstruction Credit 
Institute, the Critical Ecosystem Partnership 
Fund, and the St. Louis Zoo (SLZ UFF-8165- 


Specimens Examined 

Oedipina collaris. Nicaragua: Atldntico 
Sur. Topaz Mine, 90 miles NW of Bluefields 
and 50 miles back in direct line from the 
coast, 120 m: USNM 37350. 

Oedipina cyclocauda. Nicaragua: Rio San 
Juan: Finca El Tamagas, approximately 
1.5 km south of El Castillo: KU 173532. 

Oedipina nica. Nicaragua: Jinotega: El 
Gobiado, Reserva Natural Cerro Datanli-El 
Diablo, 13°09'N, 85°52'W, 1,420 m: MVZ 
263774; Reserva Natural Macizos de Pehas 
Blancas, 13°17'N, 85°43'W, 1,515 m: UF 
156453-55; Reserva Natural Cerro Kilambe, 
13°34'N, 85°42'W, 1,625 m: UF 156443^5; 
Reserva Natural Cerro Kilambe, 13°35'N, 
85°43'W, 1,660 m: UF 156446-50; Camp El 
Hielo, Reserva Natural Cerro Kilambe, 
1,490 m: SMF 78736; Camp 2, Reserva 
Natural Cerro Kilambe, 13°35.25'N, 
85°41.50'W, 1,360 m: SMF 78737, 78739- 
40; Matagalpa: Finca Monimbo, 13.03173°N, 
85.88682°W, 1,360 m: MHUL 003. 


AmphibiaWeb: information on amphibian biology and 
conservation [Web application]. 2011. Berkeley. 
California: University of California, Berkeley [cited 
2011 Jun 17]. Available from: http://amphibiaweb. 

Araujo, M. B., R. G. Pearson, W. Thuiller, and M. 
Erhard. 2005. Validation of species-climate impact 
models under climate change. Global Change 
Biology 11: 1504-1513. 

Brame, A. H., Jr. 1968. Systematics and evolution of the 
Mesoamerican salamander genus Oedipina. Journal 
of Herpetology 2: 1-64. 

Drummond, A. J., B. Ashton, M. Cheung, J. Heled. M. 
Kearse, R. Moir, S. Stones-Havas, T. Thierer, 
and A. Wilson. 2009. Geneious v4.8 [cited 2011 
Dec 1]. Auckland, New Zealand: Biomatters Ltd. 
Available from: 

Elith, J., C. H. Graham, R. P. Anderson, M. Dudik, S. 
Ferrier, A. Guisan, R. J. Humans, F. Huettmann. 
J. R. Leathwick, A. Lehmann, J. Li. L. G. 




Lohmann, B. A. Loiselle, G. Manion, C. Moritz, 
M. Nakamura, Y. Nakazawa, J. McC, M. Over- 
ton, A. T. Peterson, S. J. Phillips, K. S. 
Richardson, R. Scachetti-Pereira, R. E. Scha- 
pire, J. Soberon, S. Williams, M. S. Wisz, and 
N. E. Zimmermann. 2006. Novel methods improve 
prediction of species' distributions from occurrence 
data. Ecography 29: 129-151. 

Fielding, A. H., and J. F. Bell. 1997. A review of 
methods for the assessment of prediction errors in 
conservation presence/absence models. Environmen- 
tal Conservation 24: 38^-9. 

Garcia-Paris, M., D. A. Good, G. Parra-Olea, and 
D. B. Wake. 2000. Biodiversity of Costa 
Rican salamanders: implications of high levels of 
genetic differentiation and phylogeographic struc- 
ture for species formation. Proceedings of the 
National Academy of Sciences of the U.S.A. 97: 

Garoa-ParIs, M., and D. B. Wake. 2000. Molecular 
phylogenetic analysis of relationships of the tropical 
salamander genera Oedipina and Nototriton, with 
descriptions of a new genus and three new species. 
Copeia 2000: 42-70. 

Good, D. A., and D. B. Wake. 1997. Phylogenetic and 
taxonomic implications of protein variation in the 
Mesoamerican salamander genus Oedipina (Cau- 
data: Plethodontidae). Revista de Biologia Tropical 
45: 1185-1208. 

Hernandez, P. A., C. H. Graham, L. L. Master, and 
D. L. Albert. 2006. The effect of sample size and 
species characteristics on performance of different 
species distribution models. Ecography 29: 773— 

Humans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, 
and A. Jarvis. 2005. Very high resolution interpo- 
lated climate surfaces for global land areas. 
International Journal of Climatology 25: 1965-1978. 

Holdridge, L. R. 1967. Life Zone Ecology. San Jose, 
Costa Rica: Tropical Science Center. 


MRBAYES: Bayesian inference of phylogenetic 
trees. Bioinformatics (Oxford) 17: 754-755. 

Katoh, K., K. Misawa, K. Kuma, and T. Miyata. 2002. 
MAFFT: a novel method for rapid multiple 
sequence alignment based on fast Fourier trans- 
form. Nucleic Acids Research 30: 3059-3066. 

Kohler, G. 1999. The amphibians and reptiles of 
Nicaragua — a distributional checklist with keys. 
Courier Forschungsinstut Senckenberg 213: 1-212. 

Kohler, G. 2001. Anfibios y Reptiles de Nicaragua. 
Offenbach, Hessen: Germany: Herpeton. 

Kohler, G. 2011. Amphibians of Central America. 
Offenbach, Hessen: Germany: Herpeton. 

Kohler, G., A. Z. Quintana, F. Buitrago, and H. 
Diethert. 2004. New and noteworthy records of 
amphibians and reptiles from Nicaragua. Salaman- 
dra 40: 15-24. 

Leviton, A. E., R. H. Gibbs, Jr., E. Heal, and C. E. 
Dawson. 1985. Standards in herpetology and 
ichthyology. Part I. Standard symbolic codes for 
institutional resource collections in herpetology and 
ichthyology. Copeia 1985: 802-832. 

McCranie, J. R., D. R. Vieites, and D. B. Wake. 2008. 
Description of a new divergent lineage and three 
new species of Honduran salamanders of the genus 
Oedipina (Caudata, Plethodontidae). Zootaxa 1930: 

McCranie, J. R., and L. D. Wilson. 2002. The Amphi- 
bians of Honduras. Ithaca, New York, U.S.A.: 
Society for the Study of Amphibians and Reptiles. 

Moritz, C, C. J. Schneider, and D. B. Wake. 1992. 
Evolutionary relationships within the Ensatina 
eschscholtzii complex confirm the ring species 
interpretation. Systematic Biology 41: 273-291. 

Nylander, J. A. A. 2004. MrModeltest v2. Program 
distributed by the author. Uppsala University, 
Sweden: Evolutionary Biology Centre. 

Osborne, P. E., and S. Suarez-Seoane. 2002. Should 
data be partitioned spatially before building large- 
scale distribution models? Ecological Modelling 157: 

Palumbi, S. R., A. Martin, S. Romano, W. O. 
McMillan, L. Stice, and G. Grabowski. 1991. 
The Simple Fool's Guide to PCR, Version 2.0, 
privately published document compiled by S. 
Palumbi. Honolulu, Hawaii, U.S.A.: Deptartment 
of Zoology, University of Hawaii. 

Phillips, S. J., R. P. Anderson, and R. E. Schapire. 
2006. Maximum entropy modeling of species 
geographic distributions. Ecological Modelling 190: 

Phillips, S. J., and M. Dudik. 2008. Modelling of 
species distributions in Maxent: new extensions and 
a comprehensive evaluation. Ecography 31: 161-175. 

Rodder, D., F. Weinsheimer, and S. Lotters. 2010. 
Molecules meet macroecology — combining species 
distribution models and phylogeographic studies. 
Zootaxa 2426: 54-60. 

Ruiz, G. A., and F. Buitrago. 2003. Guia ilustrada de la 
herpetofauna de Nicaragua. Managua, Nicaragua: 

Savage, J. M. 2002. The Amphibians and Reptiles of 
Costa Rica: A Herpetofauna between Two Conti- 
nents, between Two Seas. Chicago, Illinois, U.S.A.: 
The University of Chicago Press. 

Stamatakis, A. 2006. RAxML-VI-HPC: Maximum 
likelihood-based phylogenetic analyses with thou- 



No. 526 

sands of taxa and mixed models. Bioinformatics 22: 

Sunyer, J., and G. Kohler. 2010. Conservation status 
of the herpetofauna of Nicaragua, pp. 488-509. In 
L. D. Wilson, J. H. Townsend, and J. D. Johnson 
eds. Conservation of Mesoamerican Amphibians and 
Reptiles. Utah, U.S.A.: Eagle Mountain Publishing. 

Sunyer, J., D. B. Wake, J. H. Townsend, S. L. Travers, 
S. M. Rovito, T. J. Papenfuss, L. A. Obando, and 
G. Kohler. 2010. A new species of worm salaman- 
der (Caudata: Plethodontidae: Oedipina) in the 
subgenus Oeditriton from the highlands of northern 
Nicaragua. Zootaxa 2613: 29-39. 

Taylor, E. H. 1952. The salamanders and caecilians of 
Costa Rica. University of Kansas Science Bulletin 

Villa, J. D. 1972. Anfibios de Nicaragua: Introduccion a 
su sistemdtica, vida y costumbres. Managua, Nica- 
ragua: Instituto Geografico Nacional & Banco 
Central de Nicaragua. 

Villa, J. D. 1983. Nicaraguan Fishes, Amphibians and 
Reptiles: Checklist and Bibliography. Managua, 
Nicaragua: Universidad Centroamericana. 

Villa, J. D., L. D. Wilson, and J. D. Johnson. 1988. 
Middle American Herpetology, a Bibliographic 
Checklist. Columbia, U.S.A.: University of Mis- 
souri Press. 

Wiens, J. J., G. Parra-Olea, M. Garcia-Paris, and D. 
B. Wake. 2007. Phylogenetic history underlies 
elevational biodiversity in tropical salamanders. 
Proceedings of the Royal Society London (Ser. Bj 
21 A: 919-928.