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Description of a new species of the Bolitoglossa subpalmata group

(Caudata: Plethodontidae) from Costa Rica

Article  in  Herpetological Journal · January 2008

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 HERPETOLOGICAL JOURNAL 18: 23–31, 2008

Description of a new species of the Bolitoglossa

subpalmata group (Caudata: Plethodontidae)
from Costa Rica
Mario García-París1, Gabriela Parra-Olea2 & David B. Wake3
1
Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain
2
Departamento de Zoología, Instituto de Biología, UNAM, Mexico
3
Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, USA

The Costa Rican plethodontid salamander long known as Bolitoglossa subpalmata is a species complex that includes
B. subpalmata of the Cordillera Central and adjoining areas, B. pesrubra of the Cordillera de Talamanca, B. bramei and
B. gomezi from the Pacific slopes of the Panama–Costa Rica border region and a species from the extreme northern
portions of the Cordillera de Talamanca and the Cerros de Escazú described here as Bolitoglossa tica. The new species
is a gracile, semi-arboreal species that has a prominent head well delimited from the neck. It differs from the parapatrically
distributed B. pesrubra in coloration, and it occupies lower elevations. Allozymes and mitochondrial DNA sequences
distinguish it from other species in the complex.
Key words: biogeography, Central America, salamander, taxonomy

INTRODUCTION ous groups of populations have been recorded, and the

existence of unnamed taxa noted (García-París et al.,
T he Bolitoglossa subpalmata clade in the subgenus
Eladinea (Parra-Olea et al., 2004) comprises several
closely related species from the uplands of Costa Rica
2000a).
Analyses of allozyme and mtDNA data led to a new
phylogenetic hypothesis, that there are four well-sup-
and extreme western Panama: B. subpalmata, B. ported clades within the B. subpalmata clade
pesrubra, B. gracilis, B. bramei and B. gomezi and some (García-París et al., 2000a). A northern clade includes
additional undescribed species from the Costa Rica– populations in the volcanic Cordillera Central and adja-
Panama border region (García-París et al., 2000a; Wake, cent ranges and bears the name B. subpalmata. Two
2005). The enigmatic B. diminuta may be a member of this clades are distributed parapatrically along the Cerro de la
group as well (Robinson, 1976). The subpalmata clade is Muerte region in the Cordillera de Talamanca. The most
sister to a morphologically heterogeneous clade that in- widely distributed species of high elevations in the region
cludes B. cerroensis, B. marmorea, B. epimela, B. known as Cerro de la Muerte and extending at least as far
sooyorum and B. minutula, all occurring in mountainous as Cerro Chirripó is B. pesrubra, and the other, described
central and eastern Costa Rica and western Panama. below (Bolitoglossa species B of García-París et al.,
Bolitoglossa pesrubra is by far the most studied of the 2000a), has a more restricted distribution in mid-eleva-
roughly 230 species that comprise the neotropical tions along the northern slopes of the Cordillera de
plethodontid salamander fauna, although literature refer- Talamanca and to the northwest in the neighbouring
ences almost exclusively use the name B. subpalmata; the Cerros de Escazú. The fourth clade includes B. bramei
independent status of these two species was established and B. gomezi (which together correspond to B. species C
by García-París et al. (2000a). The former abundance of B. of García-París et al., 2000a) from parts of the Talamancan
pesrubra in the uplands of the Cordillera de Talamanca in uplands along the border between Costa Rica and north-
Costa Rica and its relative ease of maintenance under ern Panama and in the Cordillera de la Costa along the
controlled laboratory conditions made possible studies Pacific versant, and undescribed species (Wake et al.,
of its ecology (Vial, 1968), reproduction (Houck, 1982), 2007).
development (Collazo, 1996; Wake & Hanken, 1996) and Here we describe a new species that is distinctive in
genetics (Sessions & Kezer, 1991; Hanken & Wake, 1982). molecular traits and morphology.
The B. subpalmata clade includes a diverse array of geo-
graphically delimited units located at high elevations
MATERIALS AND METHODS
(from 1500 to more than 3000 m) over most of the Costa
Rican Cordillera Central and Cordillera de Talamanca and Measurements were made using digital or dial callipers or
some minor upland areas. Extreme local polymorphism in a dissecting microscope fitted with an ocular micrometer;
body shape and coloration patterns has made it difficult standard length (SL) was measured from the anterior tip of
to characterize these local units, but genetic differentia- the snout to the posterior angle of the vent. Limb interval
tion is remarkable. Large genetic distances in both equals the number of costal interspaces between the tips
allozymes and mtDNA between geographically contigu- of appressed fore- and hind limbs, measured in one-half

Correspondence: Gabriela Parra-Olea, Instituto de Biología, UNAM, AP 70-153 Ciudad Universitaria, Mexico, D.F. CP 04510.
E-mail: gparra@ibiologia.unam.mx

23
M. García-París et al.

Table 1. Localities, voucher information and GenBank accession numbers for the sequences and specimens used
in this study. Numbers in brackets correspond to sequences used in previous studies: (1) Jackman et al., 1997; (2)
García-París & Wake, 2000; (3) García-París et al., 2000a; (4) García-París et al., 2000b; (5) Parra-Olea et al., 2002;
(6) Parra-Olea et al., 2004. Abbreviations: DBW: D. B. Wake field number; MVZ: Museum of Vertebrate Zoology
collection (USA); UCR: Universidad de Costa Rica collection (Costa Rica).

Name Locality Voucher Cytb 16S

1 B. (E.) gracilis Costa Rica: Cartago: Reserva Tapantí MVZ229170 AF212067 (3) AY526121 (6)
2 B. (E.) gracilis Costa Rica: Cartago: Reserva Tapantí MVZ229171 AF212068 (3) AY526122 (6)
3 B. (E.) pesrubra Costa Rica: Cartago: Salsipuedes, 19 km S
of El Empalme UCR12068 AF212069 (3) AY526132 (6)
4 B. (E.) pesrubra Costa Rica: Cartago: 22.7 Km SE of
El Empalme, 2760 m MVZ190923 AF212074 (3) EU448104
5 B. (E.) pesrubra Costa Rica: Cartago: Cerro Asunción,
37.1 km S of El Empalme, 3230 m MVZ210361 AF212080 (3) –
6 B. (E.) pesrubra Costa Rica: Cartago: Cerro Asunción,
37.1 km S of El Empalme, 3230 m MVZ210360 – EU448105
7 B. (E.) tica Costa Rica: Cartago: Macho Gaff UCR12066 AF212088 (3) AY526137 (6)
8 B. (E.) tica Costa Rica: Cartago: 1.1 Km S of El
Empalme, 2400 m MVZ194858 AF212086 (3) EU448106
9 B. (E.) subpalmata Costa Rica: Alajuela: Cerro Pata de Gallo,
8 km S of San Ramón MVZ194828 AF212091 (3) EU448107
10 B. (E.) subpalmata Costa Rica: Puntarenas: Monteverde
Cloud Forest Preserve MVZ229172 AF212094 (3) AF416697 (5)
11 B. (E.) cerroensis Costa Rica: San José: Cuericí, 5 km E
of Villa Mills DBW5123 AF199195 (2) AF199233 (2)
12 B. (E.) sooyorum Costa Rica: San José: 22.9 km SE
of El Empalme MVZ 190847 – EU448108
13 B. (E.) marmorea Panama: Chiriquí MVZ 210286 U89631 (1) AF218493 (4)
14 B. (E.) epimela Costa Rica: Cartago: Turrialba MVZ 181260 AF212097 (3) AY526120 (6)
15 B. (E.) minutula Costa Rica: Puntarenas: Las Tablas,
Cerro Pando MVZ 225870 AF212098 (3) AY526124 (6)
16 B. (E.) adspersa Colombia: Cundinamarca MVZ 158485 AF212984 (4) AF218492 (4)
17 B. (E.) robusta Costa Rica: Alajuela: Salto El Angel MVZ190830 EU448110 EU448109
18 B. (B.) mexicana Belize: Toledo: Blue Creek MVZ 191635 AF212099 (3) AF177588 (4)

increments. Tooth counts are based on direct counts of mexicana as an outgroup. Treatments of data follow
clearly ankylosed teeth. Numbers of maxillary and vomer- Parra-Olea et al. (2004).
ine teeth are summed for right and left sides. Institutional
abbreviations are as listed in Leviton et al. (1985), except Description of new species
for UCR (Universidad de Costa Rica). Bolitoglossa tica, new species
Sequences of 16S (548 bp) were obtained for six speci- Tico salamander, salamandra tica
mens representing the following taxa: Bolitoglossa
(Eladinea) pesrubra, B. (E.) subpalmata, B. (E.) tica sp. Holotype. MVZ 203684, an adult male from 0.8–0.9 km
nov., B. (E.) sooyorum and B. (E.) robusta. An additional SSW El Empalme junction on InterAmerican Highway 2,
short fragment of cyt b (376 bp) was obtained for one Prov. Cartago and San José, Costa Rica; 9.7137, –83.9507;
specimen of B. (E.) robusta. These sequences were com- 2360–2370 m elevation; collected by D.C. Cannatella, D.B.
piled together with previously analysed sequences from Wake, M.H. Wake and T.A. Wake, 7 July 1986.
the B. subpalmata group (Table 1) to reconstruct a Paratypes. MVZ 114121, 5.1 km N of El Empalme, Prov.
phylogenetic hypothesis of relationships for B. tica sp. Cartago, Costa Rica; MVZ 138895–98, 143836, 173377–78,
nov. Extraction, amplification, sequencing and alignment 190918–19, 190921, 194858–59, all from vicinity of type lo-
of the gene products was performed as in Parra-Olea et al. cality, 2200–2400 m elevation; MVZ 203685, 203687,
(2004). Phylogenetic analyses were performed using the 203690, 203692, same data as holotype; MVZ 225894,
combined data set, which included 17 samples of UCR11771–72, 4.5 km NNE of Cañón, below La Damita ,
Bolitoglossa subgenus Eladinea, plus B. (Bolitoglossa) Prov. Cartago, Costa Rica, 2380 m elevation; MVZ 221313,

24
 New Bolitoglossa from Costa Rica

Table 2. Comparison of measurements of three species of Bolitoglossa from Costa Rica. Ranges; means in
parentheses.
Size (SL; mm) Limb interval SL/HW Maxillary teeth Vomerine teeth Foot width (mm)
Males
B. pesrubra 42.2–52.8 (46.1) 0–1 (0.5) 6.1–6.8 (6.4) 33–53 (42) 19–22 (20.1) 4.4–5.4 (5.0)
B. subpalmata 45.1–54.4 (48.2) 1–2.5 (1.6) 6.2–7.6 (6.6) 51–60 (48.0) 15–24 (19.8) 4.8–5.8 (5.2)
B. tica 37.7–59.7 (45.1) 0–1.5 (0.8) 6.3–7.1 (6.7) 39–59 (45.8) 19–34 (24,2) 3.6–5.5 (4.6)
Females
B. pesrubra 41.7–57.8 (51.4) 2–3 (2.3) 6.7–7.5 (7.0) 44–57 (49.2) 17–28 (22.2) 4.4–5.6 (5.1)
B. subpalmata 52.0–58.1 (54.6) 2.5 (2.5) 6.5–7.3 (6.8) 37–65 (53.8) 18–21 (19.5) 5.4–5.8 (5.6)
B. tica 41.3–53.9 (46.8) 1–2.5 (1.9) 6.1–6.7 (6.4) 38–61 (46.0) 22–46 (28.9) 4.3–5.5 (4.8)

along branch of Río Agrés, Cerros de Escazú, approxi- allozymes and mtDNA haplotypes, and by having a par-
mately 5.5 km S of San Antonio de Escazú, Prov. San José, ticularly well-defined head; in addition, distinguished
Costa Rica, 1745 m elevation; UCR 6544–45, Pico Blanco, from B. subpalmata by having fewer maxillary and more
Escazú, Prov. San José, Costa Rica; UCR 12065–66, vomerine teeth, and from B. pesrubra by having more
9.6861, –83.8944 near Macho Gaff, 2440 m elevation, Prov. vomerine teeth (Table 2). It has smaller hands and feet
Cartago, Costa Rica. than either B. pesrubra or B. subpalmata. It differs from B.
Diagnosis. A member of the B. subpalmata clade distin- gracilis in having a generally shorter but still long tail, in
guished from all other members by differences in achieving larger size and in having much darker colora-
tion. It is much larger than B. diminuta. It differs from all
of these species in having prominent whitish spots on the
venter, especially in the vicinity of the tail base.
Description. This is a salamander of moderate size that
has long limbs. SL ranges from 37.7 to 59.7 mm (mean 45.1)
in ten males, and from 41.3 to 53.9 (mean 46.8) in seven fe-
males. Tails are long and generally slender, usually
exceeding standard length; SL divided by tail length
ranges from 0.76 to 1.1 (mean 0.96) in males and from 0.88
to 1.0 (mean 0.97) in females. The head is moderately broad
(Brame & Wake, 1972); SL divided by head width is 6.3–
7.1 (mean 6.7) in males and 6.1–6.7 (mean 6.4) in females.
The snout is truncate to bluntly rounded. Nostrils are
small, and nasolabial protuberances are modest to well-
developed (in sexually mature males). Eyes are moderate
in size and relatively protuberant; they protrude slightly
beyond the lateral margins of the head in ventral view.
Teeth are moderate in number. There are 2–5 (mean 3.4)
premaxillary teeth in males and 3–5 (mean 3.7) in females.
In sexually mature males the teeth are long and anteriorly
placed, lying outside the mouth where they protrude from
the upper lip. Maxillary teeth of moderate size range from
39 to 59 (mean 45.8) in males, and from 38 to 61 (mean 46.0)
in females. Vomerine teeth range from 19 to 34 (mean 24.2)
in males, and from 22 to 46 (mean 28.9) in females. The
trunk is relatively slender; distance across the shoulders
is 3.9–5.2 mm (mean 4.6) in males, and 4.1–5.5 mm (mean
5.2) in females. Limbs are relatively long; limb interval
ranges from 0 to 1.5 (mean 0.8) in males, and from 1 to 2.5
(mean 1.9) in females. Hands and feet are relatively large
and broad (3.6–5.5 mm, mean 4.6 in males, 4.3–5.5 mm,
mean 4.8 in females); digits are moderately webbed (Wake
& Brame, 1969), with two or more phalanges of the longest
digits free of webbing. Digits are bluntly tipped, and all
Fig. 1. Habitus in life of Bolitoglossa tica. Top: holotype digits can bear subterminal pads that are especially well
from 0.8–0.9 km SSW of El Empalme. Centre: adult developed on the longest digits. Fingers, in order of de-
male active at night, photographed in situ, from near creasing length, are 3-4-2-1; toes are 3-4-2-5-1. Postiliac
Macho Gaff (UCR 12065). Bottom right and left: two glands are generally obscure. Mental glands (indicating
juvenile specimens showing diversity of coloration sexual maturity) are present in males larger than 47.4 mm
patterns from 4.5 km NNE of Cañón, below La Damita. (absent in 4 paratypes between 43.1–47.3 mm); they are

25
M. García-París et al.

Fig. 2. Geographic distribution of Bolitoglossa tica. Numbers indicate the following: 1) Type locality: 0.8–0.9 km
SSWof El Empalme junction on InterAmerican Highway 2, Prov. Cartago, 2360–2370 m; 2) Génesis II, 4.5 km NNE
of Cañón, below La Damita; elevation 2360 m, Prov. Cartago; 3) near Hotel Tapantí; 4) along branch of Río Agres,
Cerros de Escazú, approximately 5.5 km S of San Antonio de Escazú; elevation 1745 m, Prov. San José, Costa Rica.

large and oval, with dimensions of 2.3–3.3 mm (mean 2.7) appeared about midbody. A brownish red mid-dorsal
wide and 1.9–3.5 mm (mean 2.5) long. stripe appeared at about the shoulder level and gradually
broadened, only to teminate abruptly at the tail constric-
Measurements of the holotype (in mm) and tooth counts.
tion. The tail was very dark. The tip of the snout and the
Head width 7.8; snout to gular fold (head length) 12.5;
area in front of the eyes was pale tan, and the iris was a
head depth at posterior angle of jaw 4.0; eyelid width 1.3;
bright gold-grey. Ventrally the ground colour was dark
eyelid length 3.2; anterior rim of orbit to tip of snout 3.2;
shiny black, with speckles of bright white concentrated in
horizontal orbit diameter 2.2; interorbital distance be-
the pelvic region. The throat was a bit lighter than the rest
tween angle of eyes 3.8; interorbital distance between
of the ventral surface. Three of the largest specimens
eyelids 2.2; length of groove extending posteriorly from
were relatively dark and one was almost solid black
eye 2.6; distance between nuchal groove and gular fold
dorsally; the others had reddish brown highlights and
4.2; snout to forelimb 15.4; distance separating external
partial stripes. All were darker ventrally and all had whit-
nares 2.7; distance separating internal nares 2.1; snout
ish speckles or lichen-like patches, all smaller than the
projection beyond mandible 1.1; snout to posterior angle
eye, on the venter with the heaviest concentration near
of vent (standard length) 52.5; snout to anterior angle of
the cloaca and on the tail and pre-pelvic region, as well as
vent 48.1; axilla to groin 27.6; shoulder width 4.7; number
the gular area. The iris was grey-gold.
of costal interspaces between appressed limbs 0.5; tail
There may be some geographic variation (see Fig. 1 for
length 48.2; tail width at base 2.7; tail depth at base 3.5;
a view of overall diversity within the species). A juvenile
forelimb length (to tip of longest finger) 12.1; hind limb
(approximately 32 mm SL) from the Cerros de Escazú area
length 13.4; hand width 4.5; foot width 5.5; length of fifth
was very dark reddish brown, nearly black on the flanks,
toe 1.0; length of third toe 1.9; distance between vomerine
and was streaked with black dorsally. A dorsolateral red-
teeth and parasphenoid tooth patch 0.4; width of mental
dish brown stripe or band started at the eye and extended
gland 3.3; length of mental gland 2.8. Number of teeth:
over the shoulder along the back and on to the tail. The
premaxillary 5; maxillary 22–25; vomerine 8–11.
stripe contained a line of whitish speckles with brassy
Coloration (in life). Notes for 14 specimens collected at highlights. The tail was mottled dark reddish brown and
the type locality on 7 July 1986 indicate that the general black with brassy highlights. The venter was very dark
colour was a flat reddish brown dorsally with a darker tail, brown-speckled and flecked with very fine brassy pig-
especially the tail venter. The largest specimen had an ment and much less numerous coarser guanophores,
obscure reddish brown stripe over each shoulder that dis- which made a few bright white spots. The tail venter was

26
 New Bolitoglossa from Costa Rica

100/100/100 B. (E.) gracilis 1

B. (E.) gracilis 2
76
64/53
100/100/100 B. (E.) tica 7
B. (E.) tica 8
72
74/64
100/100/100
B. (E.) subpalmata 9
96/100/100 B. (E.) subpalmata 10
100
100/100 B. (E.) pesrubra 3
80/--/91
B. (E.) pesrubra 4
100/100/100
B. (E.) pesrubra 5+6

B. (E.) cerroensis 11
100/--/98
B. (E.) marmorea 13
67/--/50 B. (E.) epimela 14
72/--/-- B. (E.) minutula 15
B. (E.) sooyorum 12

98/86/66 B. (E.) adspersa 16

B. (E.) robusta 17

B. (B.) mexicana
0.01 substitutions/site

Fig. 3. Phylogenetic relationships of Bolitoglossa tica based on Cytb and 16S mtDNA sequence data. One of the two
trees obtained using ML (–lnL = 4656.1324), which differ in the internal structure of the B. epimela clade. Numbers
on branches correspond to non-parametric bootstrap pseudoreplicates (ML: 100, MP: 1000, ME: 1000). See Table
1 for locality information.

nearly black but had more whitish spots than the trunk limbs are a little lighter than the body, and the hands and
venter. Tips of the nasolabial protuberances were cream feet are lighter still, pale grey mottled with darker grey.
in colour. An adult female from Cañón, below La Damita, The limbs are mottled with some yellowish spots. The tail
observed on 31 May 1994, had a broad reddish brown dor- is uniformly dark grey-black, dorsally and ventrally. The
sal band mottled with darker brown. Numerous tiny venter of the trunk is also grey-black, just a little lighter
punctate to semireticulate cream-coloured guanophores than the flanks, and the gular region is pale grey. The
were present on the lateral and ventral surfaces, and much mental gland is large and prominent, and is nearly devoid
larger, bright white spots or patches were present. The of pigment.
facial area was mottled reddish brown, cream and black. Habitat and geographic range. This species is known
The tail venter was dark brown with a streak of bright from the northern slopes of the Cordillera de Talamanca
white. between 2200 and 2500 m, as well as from the Cerros de
Coloration (in alcohol). The holotype is dark grey-black Escazú, isolated to the northwest, which form the south-
dorsally with a narrow tan stripe that extends from the ern boundary of the Meseta Central (Fig. 2). In the Cerros
nape of the neck to the end of the body, abruptly terminat- de Escazú the species descends to at least 1745 m. The
ing at the base of the tail. A pair of similarly coloured habitat of B. tica was discussed by García-París et al.
broad stripes occurs in the shoulder region, lateral to the (2000b; as Bolitoglossa sp. B). The vegetation in the El
main stripe. The stripe is irregularly bordered and inter- Empalme area corresponds to the transition between the
rupted in places by the encroaching ground colour. The lower montane and montane rainforest of Tosi (1969), and
head is somewhat lighter than the trunk, and is dark grey- between the subtropical montane rainforest and subtropi-
brown, becoming pale grey at the end of the snout and on cal cloud forest of Gómez (1986). The mean annual
the relatively pronounced nasolabial protuberances. The temperature is 12–15 ºC and between 1825 and 2300 mm of

27
M. García-París et al.

rain falls each year, with a moderate seasonal deficit be- western Panama. Based on general morphology, this
tween January and April. clade (as the B. subpalmata group) was placed in the al-
The species is relatively arboreal in its habits. It has pha section of Bolitoglossa by Wake & Lynch (1976). It
frequently been found in bromeliads, and has been ob- is one of four main clade groups in the subgenus
served at night climbing on ferns (Lycopodiaceae) and Eladinea (Parra-Olea et al., 2004), and is a sister-taxon of
other vegetation from 15 cm to 3 m above the ground. the B. epimela clade, which includes co-occurring species
However, it has also been taken under surface litter, under in the Cordillera de Talamanca (B. epimela, B. cerroensis,
the bark of logs and on road banks at night. In July 1986, B. compacta, B. marmorea, B. minutula and B.
14 individuals were observed in one day at the type local- sooyorum). Photographs of B. subpalmata, B. gracilis, B.
ity, a disturbed oak forest with abundant arboreal diminuta, B. pesrubra, B. epimela, B.cerroensis, B.
bromeliads. Of these, eight were obtained from inside minutula and B. sooyorum are published in Savage
bromeliads, one from under a fallen bromeliad, one under (2002), and can be compared with our pictures of B. tica.
the bark of a stump, one in a rotten log and the remainder In the past, salamanders of the subpalmata clade were
in leaf litter or under surface debris. Field observations abundant. These were long included in a single taxon, B.
compared specimens of the new species with B. subpalmata (e.g. Dunn, 1926). Taylor (1952) recognized
subpalmata and B. pesrubra, and noted that they look some of the diversity within the complex and described
and act differently. Members of this species are generally two species, B. pesrubra and B. torresi, from the high
quick and lively, and they appear large-headed and slen- central region of the Cordillera de Talamanca (Cerro de la
der. Muerte). Subsequently Vial (1966) reduced these two to
Etymology. This species is named in honour of the Costa the synonymy of B. subpalmata, based on the lack of
Rican people, who refer to themselves as “ticos”, in rec- morphological differentiation. The first genetic studies
ognition of their leadership in habitat preservation and reported high levels of differentiation in allozymes
conservation. (Hanken & Wake, 1982). More extensive studies includ-
ing both allozymes and mtDNA sequences led to the
Comparisons. Coloration is subject to substantial varia-
conclusion that several species-level taxa were repre-
tion in this species, with patterns that range from nearly
sented, and the name B. pesrubra was resurrected for the
solid dark brownish black to light grey or ochre with vari-
high Talamancan populations (García-París et al., 2000a).
ous dorsal highlights of brighter yellowish, orange or
In the meantime, another member of the complex, B. graci-
reddish colour. Some individuals have a reddish dorsal
lis, was described by Bolaños et al. (1987) from lower
band that is highly irregular and much interrupted by en-
elevations (approximately 1280–1500 m) in the Tapantí
croachment of the darker ground colour. The ground
valley of the Río Reventazón, which drains the northern
colour of the venter is dark blackish, especially the tail.
Talamancan region. This species appears to be truly rare,
Most individuals have irregular spots or lichen-like
because it has been encountered infrequently despite in-
patches of whitish pigmentation on the venter, especially
tensive sampling in the Tapantí region. A third species,
in the vicinity of the hind limb insertions and tail base.
the even rarer, tiny B. diminuta, is known from only two
Neither of the two commonest colour patterns character-
adult specimens (as well as two clutches of eggs, one
istic of B. pesrubra are found. These are the “pesrubra”
partly hatched). It also occurs in the Tapantí region, be-
pattern, consisting of a dark brown dorsum variously
tween 1300 and 1650 m elevation. Although this species
mottled or streaked with lighter and darker tan, brown or
was tentatively placed in the B. epimela group by Parra-
black and having reddish to red-orange limb insertions, or
Olea et al. (2004), molecular data are scanty and its
entire limbs including hands and feet, and the “torresi”
relationships are uncertain.
pattern, consisting of a black ground colour and a more
García-París et al. (2000a) studied 19 proteins from five
superficial overlay or “frosting” of silvery, silvery-grey or
populations of B. subpalmata, one population of B. tica,
whitish coloration arranged in patches of varying size and
one population of B. gracilis, one population of B.
shape (Taylor, 1952).
bramei and seven populations of B. pesrubra. In addi-
tion, a single specimen of B. diminuta was used. We
DISCUSSION
reexamine these data for the first three species and
The Bolitoglossa subpalmata clade inhabits moderate to present information that could not be presented because
high elevations (above 1500 m) in humid cloud forests of the condensed nature of their publication. Population
and more upland forests and paramo-like habitats (to over sizes for B. subpalmata were: Volcán Turrialba 3, Volcán
3300 m) in the mountains of Costa Rica and western Irazú (Las Nubes) 1, Volcán Barva (Braulio Carillo) 10,
Panama. This distribution encompasses two disjunct Volcán Poás 4, Cordillera de Aguacate (Cerro Pata de
geographic units. The northern unit includes populations Gallo) 10; for B. tica 7, and for B. gracilis 1. Values of DN
from Volcán Cacao to Volcán Turrialba along the (Nei, 1972) were 0.28–0.45 between B. tica and nearby
Cordillera de Guanacaste, Cordillera de Tilarán and populations of B. pesrubra (the smallest geographic dis-
Cordillera Central, as well as in the small and isolated tance between samples is to a population approximately
Cordillera de Aguacate. All of these populations are as- 20 km southeast of the B. tica type locality). The lowest
signable to B. subpalmata (sensu stricto). The second genetic distance from B. tica to any other species is to B.
unit includes all populations located in the Cordillera de gracilis (DN=0.16), but the latter is a sample of only one so
Talamanca from the isolated northwestern Cerros de the metric is suspect. There is one “fixed” difference (i.e.
Escazú to the mountains east of Volcán Barú in Chiriquí, no alleles shared between taxa for one protein) between

28
 New Bolitoglossa from Costa Rica

these two taxa, which are closely parapatric. Genetic dis- these three species (100 bs). The sister group to the
tances from B. tica to B. subpalmata range from 0.21 (to subpalmata group as a whole is the epimela group (80, 91
Volcán Irazú, also a sample of only one) to 0.43 (Volcán bs) (B. cerroensis, B. epimela, B. marmorea, B. minutula
Turrialba); these are slightly less than the distances to B. and B. sooyorum. The epimela group is well supported
pesrubra. While B. tica was long included in B. pesrubra (100, 98 bs) except for the inclusion of B. sooyorum in MP
(both as B. subpalmata) (Vial, 1968), the species are well analyses (a problem of lack of cytb data for this species),
differentiated in allozymes (DN=0.28–0.45; García-París et but largely unresolved.
al., 2000a). Differentiation within both B. pesrubra and B. It is not surprising that the species of this group are so
subpalmata is great (see García-París et al., 2000a, Fig. 5). similar in general morphology, given their close relation-
The Pata de Gallo population of B. subpalmata is more ships. However, there are differences in coloration,
similar to B. tica (DN=0.243) than to other populations of ecology, behaviour and altitudinal distribution. The only
B. subpalmata (DN=0.33–0.47 to the three volcano known sympatry is between B. gracilis and B. diminuta,
populations). There are three “fixed” differences between but B. tica might overlap with both (at present there is an
Pata de Gallo and B. tica, and from two to three fixed differ- altitudinal gap of more than 500 m separating them). We
ences between Pata de Gallo and the volcano populations expect B. tica and B. pesrubra will be found in sympatry,
(suggesting that the Pata de Gallo population should be because they are separated by only a few kilometres and
considered a candidate for species status). There are by about 100 m in altitude. Closely related species of
from one to three “fixed” differences between volcano plethodontid salamanders often hybridize when they
populations of B. subpalmata and B. tica. Multidimen- come into contact, but if any hybridization occurs it can-
sional scaling of genetic distances shows B. tica (referred not be very much, because B. tica and B. pesrubra are not
as “Emp” in Fig. 5 in García-París et al., 2000a) somewhat clearly sister taxa and they approach each other closely in
closer to B. subpalmata than to B. pesrubra. distribution without showing any signs of genetic inter-
The genetic distances between B. gracilis and B. change. There are two to three “fixed” genetic differences
subpalmata range from 0.23–0.35, with two to four “fixed” between B. tica and any given population of B. pesrubra
differences. Data are available for a single specimen of B. (although only one of 19 loci shows a difference between
diminuta, which differs by DN=0.29 (four “fixed” differ- all samples of the two species), and there are no
ences) from B. tica, DN=0.24 (five “fixed” differences) from haplotypes shared by the two species for the cytochrome
B. gracilis, and DN=0.27–0.40 from B. subpalmata. b gene, sampled in nine populations of B. pesrubra and
An earlier allozyme study (Hanken & Wake, 1982) in- four of B. tica. These haplotypes differ by a minimum of
cluding B. tica (n=11) and a population of B. subpalmata 6.6% (K2P).
(Volcán Poás, n=7) recorded DN=0.33, nearly the same The northern Cordillera de Talamanca has an unusu-
(DN=0.34) as in the newer study using different specimens ally large salamander fauna (Wake, 1987, 2005;
and some different proteins. The ranges of B. tica and B. García-París et al., 2000a; Hanken et al., 2005; Wake et al.,
subpalmata are discontinuous, with the latter generally 2007). What is unusual about the local assemblages of
distributed on the north side of the Meseta Central (which salamanders in this area is that they include clusters of
is about 1000 m high). closely related species that are sympatric or narrowly
A phylogenetic hypothesis (maximum parsimony) parapatric, suggesting that this region has been an active
based on sequences of the mitochondrial cytochrome b centre of species formation. Endemism is high in the area.
gene showed support (99 bootstrap, bs) for the clade as a In the immediate vicinity of the type locality of B. tica, two
whole (García-París et al., 2000a), and for the monophyly other species occur, Oedipina altura and Oedipina
of B. pesrubra (nine samples), B. subpalmata (five sam- paucidentata. The former is known from the type series
ples) and B. tica (four samples) (99–100 bs). (collected in 1959; Brame, 1968) and a couple of additional
Relationships among the species that were studied (B. specimens, while the latter is known only from the type
subpalmata, B. pesrubra, B. gracilis, B. tica and B. series (also collected in 1959; Brame, 1968) (DBW, unpub-
bramei, the last two identified as species B and C, respec- lished data). In the Tapantí region, immediately
tively) were unresolved. However, B. subpalmata and B. downslope (to an altitude of 1200 m) to the north and east
tica may be sister taxa (decay index of two but no of the El Empalme sites, other endemic species occur: B.
bootstrap support). A more extensive study of cyto- gracilis, B. diminuta, B. obscura, Nototriton tapanti and
chrome b and 16S RNA sequences found strong support N. picadoi. Also at Tapantí is the rare B. epimela. Just
for the clade but relationships among B. subpalmata, B. upslope from the El Empalme area occur the endemic spe-
pesrubra, B. tica (identified as Bolitoglossa sp. 4) and B. cies B. cerroensis and B. sooyorum. A rare species that
gracilis were unresolved (Parra-Olea et al., 2004). occurs from the Cerros de Escazú to the Cerro de la
We have added some new 16S mtDNA data for Muerte area is B. nigrescens. The only relatively wide-
Bolitoglossa tica, B. pesrubra, B. subpalmata and B. spread species in the region are the formerly abundant B.
sooyorum. The analyses (ML, MP, ME) of these data to- pesrubra, which is a high elevation endemic, Oedipina
gether with previously published sequences for the B. uniformis, which is present in the Cerros de Escazú and
subpalmata group provide support for a B. subpalmata Tapantí region, and B. robusta, which is widespread at
clade as previously reported (Parra-Olea et al., 2004) (Fig. elevations generally below 1500 m to the northwest, north
3). We find B. tica and B. subpalmata to be sister taxa (72, and southeast (Savage, 2002).
74, 64, 71 bs). In turn, they form a sister group to B. graci- Taxonomic work on Costa Rican Bolitoglossa is not
lis (76, 64, 53 bs), and B. pesrubra is the sister taxon to completed. Savage (2002) drew attention to populations

29
M. García-París et al.

assigned to B. subpalmata from Cerro Cacao and the Gómez, L.D. (1986). Vegetación de Costa Rica. Apuntes
Cordillera de Tilarán, suggesting that they might repre- para una Biogeografía Costarricense. Vegetación y
sent undescribed species. A population at Monteverde, Clima de Costa Rica Vol. 1. San José, Costa Rica:
in the Cordillera de Tilarán, studied by García-París et al. Editorial Universidad Estatal a Distancia.
(2000a), clusters with other samples of B. subpalmata Hanken, J. & Wake, D.B. (1982). Genetic differentiation
with high support (bs 99), but it is sister to the remaining among plethodontid salamanders (genus Bolitoglossa) in
samples. The divergence is relatively low (K2P distances Central and South America: implications for the South
range from 0.023 to 0.033 to the other samples). Accord- American invasion. Herpetologica 38, 272–287.
ingly, we assign the Cordillera de Tilarán populations to Hanken, J., Wake, D.B. & Savage, J.M. (2005). A solution to
B. subpalmata. Members of this complex that occur in the the large black salamander problem (genus Bolitoglossa)
Cordillera de Guanacaste (one adult from Volcán Cacao in in Costa Rica and Panama. Copeia 2005, 227–245.
MVZ, one juvenile from Volcán Rincón de la Vieja in UCR) Houck, L.D. (1982). Growth rates and age at maturity for
lack tissue samples. The MVZ specimen is a long-tailed, the plethodontid salamander Bolitoglossa subpalmata.
slender, arboreal animal. We tentatively assign these Copeia 1982, 474–478.
specimens to B. subpalmata. Leviton, A.E., Gibbs, R.H., Jr., Heal, E. & Dawson, C.E.
(1985). Standards in herpetology and ichthyology: Part
ACKNOWLEDGEMENTS I. Standard symbolic codes for institutional resource
Federico Bolaños, Eberhard Meyer, Marvalee Wake, Tom collections in herpetology and ichthyology. Copeia
Wake, James Hanken and David Cannatella helped col- 1985, 802–832.
lect specimens in the field, David Cannatella provided the Nei, M. (1972). Genetic distance between populations.
photograph of the holotype, and David Good performed American Naturalist 106, 283–292.
the allozyme study. Juan Carlos Windfield-Pérez prepared Parra-Olea, G., García-París, M. & Wake, D.B. (2004).
the map. Research support was provided by NSF (current Molecular diversification of salamanders of the tropical
grant EF-0334939) to DBW, Ministerio de Educación y American genus Bolitoglossa (Caudata: Plethodontidae)
Ciencia of Spain (current grant CGL2007-64621) to MG-P, and its evolutionary and biogeographical implications.
and UC-MEXUS 022043 to GP-O. Costa Rican collecting Biological Journal of the Linnean Society 81, 325–346.
permits were provided by Dirección General de Vida Robinson, D.C. (1976). A new dwarf salamander of the
Silvestre. genus Bolitoglossa (Plethodontidae) from Costa Rica.
Proceedings of the Biological Society of Washington 89,
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