Diet and Microhabitat Use of Bolitoglossa cf.

pandi (Caudata: Plethodontidae)

from the Cordillera Oriental of Colombia
Author(s): Jennifer S. Del Río-García , Víctor H. Serrano-Cardozo , Martha P. Ramírez-Pinilla
Source: South American Journal of Herpetology, 9(1):52-61. 2014.
Published By: Brazilian Society of Herpetology
DOI: http://dx.doi.org/10.2994/SAJH-D-13-00031.1
URL: http://www.bioone.org/doi/full/10.2994/SAJH-D-13-00031.1

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South American Journal of Herpetology, 9(1), 2014, 52–61
© 2014 Brazilian Society of Herpetology

Diet and Microhabitat Use of Bolitoglossa cf. pandi

(Caudata: Plethodontidae) from the Cordillera
Oriental of Colombia
Jennifer S. Del Río-García1, Víctor H. Serrano-Cardozo2, Martha P. Ramírez-Pinilla3,*

1 Facultad de Ciencias, Universidad Distrital Francisco José de Caldas, Colombia. Email: biojenniferdrg@yahoo.com.co

2 Laboratorio de Ecología, Grupo de Estudios en Biodiversidad, Escuela de Biología, Universidad Industrial de Santander, Bucaramanga, Colombia.
Email: vserrano@uis.edu.co
3
Colección Herpetológica y Laboratorio de Biología Reproductiva de Vertebrados, Grupo de Estudios en Biodiversidad, Escuela de Biología,
Universidad Industrial de Santander, Bucaramanga, Colombia.
* Corresponding author. Email: mpramir@uis.edu.co

Abstract. Bolitoglossa cf. pandi is a terrestrial salamander that inhabits a fragment of secondary forest located in the Cordillera Oriental of
the Colombian Andes. Few aspects of its biology are known. Here we studied its diet, microhabitat use, population structure, and arthropod
richness at the study site during rainy and dry seasons. We also recorded perch height, substrate type, and time of capture. Encounter rate
for Bolitoglossa cf. pandi was very high during rainy months and low during dry season. Juveniles were more abundant than adults. To obtain
consumed items we used the stomach-flushing technique; the contents of 87 stomachs were analyzed and 1324 prey items were identified
and grouped in 20 prey categories. Diet was represented by a great variety of arthropods and the most important prey categories, according
to the index of relative importance (IRI), were Acari, Coleoptera, and Formicidae. No differences were found in diet between sexes; however,
ontogenetic variation was found: there was a shift in consumption of ants and mites related to ontogeny. Volume of coleopterans and ants in
stomachs increased with body size, whereas occurrence of mites varied inversely with body size. Only Acari consumption changed between
dry and wet seasons. Bolitoglossa cf. pandi forages on the ground, as well as on herbaceous vegetation; larger individuals were found in the
highest perches, usually on leaves. Diet and microhabitat use of this salamander is similar to other species of Bolitoglossa and are affected by
local environmental factors, such as prey availability and climate regime, and endogenous factors, such as body size.

Keywords. Acari; Coleoptera; Foraging; Formicidae; Salamander; Stomach-flushing.

Resumen. Bolitoglossa cf. pandi es una salamandra terrestre habitante de un relicto de bosque secundario ubicado en la Cordillera Oriental
de los Andes colombianos. Se conocen pocos aspectos sobre su biología. Estudiamos su dieta, uso del microhábitat, estructura poblacional y
la disponibilidad de alimento en el ambiente, durante la época seca y de lluvias. También registramos la altura de la percha, tipo de sustrato
y hora de captura. La tasa de encuentros de Bolitoglossa cf. pandi fue muy alta durante los meses lluviosos y baja durante la época seca. Los
individuos juveniles fueron más abundantes que los adultos. Se empleó la técnica de lavado estomacal para describir y analizar la dieta de la
población, y se analizaron 1324 presas correspondientes a 87 contenidos estomacales. La dieta de esta especie estuvo representada por una
gran variedad de artrópodos, correspondientes a 20 categorías de presas principalmente. Las categorías de presa más importantes según
el índice de importancia relativa (IRI) fueron Acari, Formicidae y Coleoptera. No se encontraron diferencias en el consumo de presas entre
sexos. Sin embargo se encontró un cambio ontogénico con respecto al consumo de hormigas y ácaros. El volumen consumido de coleópteros
y de hormigas incrementó con el tamaño corporal, mientras el de ácaros presentó una variación inversamente proporcional. Solamente el
consumo de Acari cambió durante las estaciones. Bolitoglossa cf. pandi se alimenta tanto en la hojarasca del suelo como en la vegetación ar-
bustiva; los individuos de mayor tamaño fueron encontrados en las perchas más altas, generalmente sobre la superficie de las hojas. La dieta
y uso del microhábitat de esta salamandra es similar a la de otras especies del género Bolitoglossa y son afectadas por factores ambientales,
disponibilidad de alimento, régimen climático y otros factores como el tamaño corporal.

INTRODUCTION in the diets of all of studied species, followed by Coleop-

Bolitoglossa is a genus of terrestrial Neotropical
plethodontid salamanders that contains around 121 spe-
cies (Frost, 2014) and is the largest and most widely dis-
tributed genus of salamanders (García-Paris et al., 2000;
Parra-Olea et  al., 2004). Despite such high diversity,
there are few studies about the trophic ecology of these
salamanders (e.g., B.  subpalmata, Vial, 1968; B.  pesrubra
and B. cerroensis in Costa Rica, Mead and Boback, 2002;
B.  mexicana and B.  rufescens in Mexico, Anderson and
Mathis, 1999; and B. nicefori in Colombia, Ortega et al.,
2009). Formicidae was the most representative prey item
tera, suggesting that these are important resources for
salamanders of this genus. All of these studies were done
using abdominal dissection of preserved specimens; how-
ever, non-lethal methods are preferable when studying
diets of vulnerable wild populations.
Most species of Bolitoglossa have generalized terres-
trial habits and are ground wanderers that live under cover
provided by leaf litter (e.g., B. morio, B. rostrata, B. flavimem-
bris, Houck, 1977; B. mombachoensis, Jansen and Köhler,
2001; B. equatoriana, Cisneros-Heredia, 2006; B. guaneae,
Acosta-Galvis and Gutiérrez-Lamus, 2012). These spe-
cies usually forage in the leaf litter and climb to perch on

Submitted: 25 September 2013 Handling Editor: Ricardo Sawaya

Accepted: 03 April 2014 doi: 10.2994/SAJH-D-13-00031.1
South American Journal of Herpetology, 9(1), 2014, 52–61
leaves of herbaceous vegetation or low bushes < 2 m above
the ground at night. Ground surface activity is mainly re-
lated to seasonal rainfall: when the ground becomes dry,
salamanders retreat to subterranean refugia. However, in
Central America, several species of Bolitoglossa are cloud
forest specialists, and the epiphytic component of these
forests offer salamanders two classes of arboreal micro-
habitats (bromeliads and moss mats; e.g., B.  engelhardti,
B.  franklini, Houck, 1977; B.  alvaradoi, B.  arborescandens,
B. diminuta, Wake, 1987). Arboreal and terrestrial micro-
habitats are related to morphological features and body
size. Thus, arboreal salamanders typically have smaller
bodies than ground surface salamanders and possess lon-
ger and prehensile tails (Wake, 1987). These differences in
microhabitat use might also result in differences in diet.
Our main goal was to determine and describe the
diet of a population of Bolitoglossa cf. pandi located in a
cloud forest fragment of the Cordillera Oriental of the
Colombian Andes using the stomach-flushing technique.
We compared diet between age categories and sexes and
related it to body size. We also studied microhabitat use,
population structure, and availability of arthropods at the
study site during rainy and dry seasons, and we compared
our results with those of previous studies of Bolitoglossa.
MATERIALS AND METHODS
Species identity
In 2007 a previously unknown population of Bolito-
glossa was discovered in a forest fragment on the western
slopes of the Cordillera Oriental of the Colombian An-
des (G. Chaves-Portilla, pers.  comm.). It was initially as-
signed to B. pandi Brame and Wake, 1963 because of its
geographic location (near the municipality of Pandi, the
type locality of B.  pandi) and morphological similarity
(Acosta-Galvis and Gutiérrez-Lamus, 2012). Bolitoglossa
pandi is considered to be “Endangered because its extent
of occurrence is less than 5000 km2, all individuals are in
fewer than five locations, and there is continuing decline
in the extent and quality of its habitat” (Ramírez-Pinilla
et al., 2004). Only one specimen was used for the species
description, limiting our knowledge of the variability in
this species. In addition, the holotype is poorly preserved,
preventing evaluation of diagnostic characters and the
future allocation of specimens to this species. Therefore,
the most prudent position in this paper is to consider the
population as B. cf. pandi.
Study area
The studied population is located in the Vereda San
Marcos, Supatá Municipality, Department of Cundina-
Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla
marca, Colombia (05°01’51.13”N, 74°15.30’99”W), at
1800–2000  m above sea level. The study area is a pro-
tected, small (< 2 ha) remnant of cloud forest under in-
tense anthropogenic pressure, mainly deforestation for
cattle farming and agriculture. It is also the habitat of the
Supatá golden poison frog (Andinobates sp.), and several
conservation programs are being developed there (e.g., G.
Chaves-Portilla, pers. comm.). Annual rainfall is 2000 mm
and average annual temperature is 18–24°C. The rainfall
regime is bimodal with the first peak of rains from March–
May and the second from September–November. The ma-
jor dry season occurs from June–August and there is a
less pronounced dry season around December–February.
Salamander sampling
We captured individuals through visual encoun-
ter surveys (VES; Crump and Scott, 1994; Angulo et al.,
2006) two nights per month from February–July 2011,
covering different areas of the study site. Two collectors
conducted sampling for 6  h each night. For each indi-
vidual, we recorded perch height, substrate type (leaf,
trunk, leaf litter, under rotten logs), and time of capture.
Salamanders were captured by hand and taken to a safe
place inside individual plastic bags for examination and
stomach-flushing. We marked the spot where each sala-
mander was found with flagging tape and returned them
to the same site. Based on the presumption of a sedentary
nature, as observed in other Bolitoglossa species, and in
order to minimize recapture probability, we did not search
for other individuals at those marked sites. We measured
snout–vent length (SVL) and mouth width (MW) using a
Vernier caliper (± 0.2 mm) and body mass using a portable
scale (± 0.1 g). We classified individuals according to SVL
as follows: neonates (≤ 23  mm), juveniles (24–43  mm,
without developed mental glands), and adults (≥ 44 mm).
Adults were sexed using secondary sexual characters:
males showed evident and well developed mental glands
and females showed presence of abdominal eggs.
Stomach-flushing
The stomach-flushing technique that we used dif-
fered slightly from previously reported methods (Legler
and Sullivan, 1979; Solé, 2005) because we substituted
intravenous catheters for a stainless steel needle usu-
ally employed to feed birds. Additionally, we did not use
mechanical devices to open the mouths of the salaman-
ders. Stomachs were not flushed into a square of gauze;
instead, we used a small Petri dish and a soft brush to pick
up prey items, and we used spring water for flushing. Af-
ter the procedure, salamanders were observed overnight
and returned to their home habitat the next day.
53
South American Journal of Herpetology, 9(1), 2014, 52–61
Arthropod sampling
We collected arthropods of the study area during
rainy and dry seasons using an entomological net, pitfall
traps, and Winkler traps in order to determine the avail-
ability of prey and arthropod richness. To capture aerial
insects, we actively searched the vegetation with an ento-
mological net to the highest perch in which we observed
salamanders; one person conducted sampling efforts dur-
ing 3 hours for two nights in every season. In order to
capture ground-dwelling arthropods, we made two per-
pendicular lineal transects and installed 50 pitfall traps in
each one. Each trap consisted of a 250 ml plastic container
containing 70% ethanol buried that was in the leaf litter
10 m from the closest trap; we left traps open for three
days each season. Winkler traps were used to capture soil
and litter arthropods; we randomly made four quadrats
(1 m2) each season and sieved the leaf litter and topsoil
through a wire sieve with a mesh width of about 10 mm.
We fixed the samples in 70% ethanol.
Laboratory analyses
All prey items were preserved in 70% ethanol, la-
beled, and stored. Prey items were counted, identified to
the lowest taxonomic category possible (most of them to
family, and some ants to genera), and then we measured
length and width to 0.01 mm with a caliper. Prey volume
was estimated in two ways, (1) with the spheroid formula:
V = 4/3 π (length/2) (width/2)2; and (2) we measured vol-
ume by volumetric displacement using a graded plastic
cylinder (0.1–100  μl) and adding water with a micropi-
pette. The first method has been criticized by Magnus-
son (2003), and we agree with those criticisms; however,
we used both methods because although volume can be
measured directly by fluid displacement for most arthro-
pods, the process is tedious and difficult to perform for
very small arthropods, (e.g., ants, springtails, and mites).
Data analyses
We constructed an accumulation curve of prey cat-
egories (identified to family level) versus stomach content
using Estimates 8.2 with 1000 random additions (Colwell,
2009) to determine the minimum number of stomach
samples required for precise estimation of species diet.
In order to describe the importance of each prey category
consumed (t), we calculated the index of relative impor-
tance (Pinkas et  al., 1971) as: IRIt  =  %Ot (%Nt  +  %Vt),
where %Ot is the occurrence percentage (i.e., the number
of guts containing each t category), %Nt is the percentage
of the number of t items in all guts, and %Vt is the per-
centage of the volume of t items in all guts.
Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
54
We tested correlations between SVL and MW of in-
dividuals and prey content (in volume and number) using
Spearman Rank Correlation to see if prey size depends on
salamander SVL or MW. The same analysis was employed
to see the correlation between SVL and body mass with
perch height, and the relationship between body mass
and prey content (volume and number). In addition, we
performed an analysis of variance (ANOVA) to determine
if SVL is significantly different between sexes. Statistical
differences in prey volume between sexes and age cate-
gories were calculated through an analysis of covariance
(ANCOVA), employing SVL as a covariate. We performed
the same analyses only for adults to determine if signifi-
cant differences existed between males and females. We
analyzed the variation of number and volume of prey for
sexes and age categories (separately) and between seasons
employing a two-way ANOVA.
We tested the statistical differences in the consump-
tion of the most important prey categories between sea-
sons with an ANCOVA using SVL as covariate. Also, we
performed an ANOVA to detect significant differences
among most important preys categories and sampling
months. We used Tukey’s test a posteriori to detect months
that differed. Finally, to detect statistical differences be-
tween sex and type of microhabitat used we performed
Chi-square tests. For the application of parametric analy-
ses, we evaluated normality using a Kolmogorov-Smirnov
test, and homoscedasticity using the Levene test. To at-
tain the assumptions we log10 transformed some of the
data. If after the transformation, data were still non-nor-
mal or with unequal variances, we used nonparametric
tests. All statistical procedures were conducted using the
STATISTICA 7 software package (StatSoft Inc., 2004).
RESULTS
Population structure
During the six months of sampling we captured
204 salamanders: 157 juveniles, 33 adult females, and 14
adult males (Table 1). Only 143 individuals were stomach-
flushed; however, accumulation curves reached an as-
ymptote with 17 stomachs for juveniles and 10 stomachs
for female and male adults. Therefore, we only considered
87 stomach contents for diet analyses (12 adult females,
12 adult males, 57 juveniles of indeterminate sex, and 6
neonates), indicating that sample size was sufficient to
describe the diet of this population. Altogether the total
mortality in our experiments was less than 1% while the
salamanders were under our direct observation.
Owing to the fact that we captured a high number
of salamanders in February and March, we decided to col-
lect only 20 individuals per month for the next sampling
months. However, in June, with the same capture effort,
Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla
South American Journal of Herpetology, 9(1), 2014, 52–61

Table 1. Summary of Bolitoglossa cf. pandi sampling.

No. individuals No. individuals subjected No. individuals No. individuals included Days of Capture effort
Month
captured to stomach flushing with prey items in diet analysis sampling (person hours)
February 77 77 76* 21 2 22
March 71 20 20 20 2 18
April 21 21 21 21 1 4
May 30 20 20 20 1 7½
June 5 5 5 5 2 12
July 0 0 0 0 3 30
Total 204 143 142 87 11 93

* One individual with an empty stomach died during stomach-flushing procedure.

Table 2. Diet composition of Bolitoglossa cf. pandi. Percentages are given in relation to total number of prey items. n: number of prey items from a given
taxon; F: frequency of prey item; V: total volume of prey item; Index of Relative Importance IRI [%IRI= % F (% V+ %n)]; N.N: unidentified specimen.

Prey type n %n F %F V (mm3) %V IRI

Total Acari 587 44.34 80 7.46 241.01 12.02 93.05
Oribatidae 353 26.66 59 5.50 176.00 8.78 49.80
Euphthiricaridae 3 0.23 2 0.19 0.90 0.04 0.01
Galumnidae 56 4.23 26 2.43 70.00 3.49 8.57
Phthricaridae 1 0.08 1 0.09 0.05 0.00 0.00
Uropodidae 91 6.87 33 3.08 22.69 1.13 3.70
N.N 202 15.26 80 7.46 82.36 4.11 31.80
Total non-Oribatidae 234 17.67 50 4.66 65.00 3.24 15.95
Total Hymenoptera 394 29.76 73 6.81 328.90 16.41 113.77
Total Formicidae 349 26.36 50 4.66 299.17 14.36 68.20
Total Myrmicinae 200 15.11 33 3.08 133.75 6.67 21.01
Solenopsis spp. 62 4.68 16 1.49 29.65 1.48 2.28
Pheidole spp. 95 7.18 19 1.77 49.07 2.45 4.47
Acromyrmex spp. 1 0.08 1 0.09 10.00 0.50 0.05
Cyphomyrmex spp. 30 2.27 12 1.12 39.60 1.98 2.24
Strumigenys spp. 5 0.38 1 0.09 1.72 0.09 0.01
N.N 6 0.45 2 0.19 4.04 0.20 0.04
Total Dolichoderinae 24 1.81 5 0.47 37.80 1.89 0.89
Linephitema spp. 24 1.81 5 0.47 37.80 1.89 0.89
Total Ecitoninae 17 1.28 2 0.19 23.34 1.16 0.22
Labidus spp. 15 1.13 1 0.09 22.50 1.12 0.11
N.N 2 0.15 1 0.09 0.84 0.04 0.00
Total Formicinae 20 1.51 7 0.65 9.46 0.47 0.32
Brachymyrmex spp. 20 1.51 6 0.56 9.46 0.47 0.27
Total Hetereponerinae 1 0.08 1 0.09 1.00 0.05 0.00
N.N 1 0.08 1 0.09 1.00 0.05 0.00
Total Ponerinae 25 1.89 6 0.56 60.39 3.01 1.70
cf. Simopelta spp. 20 1.51 2 0.19 36.89 1.84 0.35
cf. Pachycondyla spp. 1 0.08 1 0.09 10.00 0.50 0.05
N.N 4 0.30 3 0.28 13.50 0.67 0.19
Total Proceratiinae 1 0.08 1 0.09 1.00 0.05 0.00
N.N 1 0.08 1 0.09 1.00 0.05 0.00
Total non-Formicidae 45 3.4 37 3.45 41.11 2.05 7.20
Evaniidae 2 0.15 2 0.19 4.00 0.20 0.04
Tiphiidae/Thynninae 1 0.08 1 0.09 2.00 0.10 0.01
cf. Chalcididae 2 0.15 2 0.19 1.00 0.05 0.01
cf. Diapriidae 2 0.15 2 0.19 4.00 0.20 0.04
cf. Figitidae 3 0.23 2 0.19 6.00 0.30 0.06
N.N 35 2.64 22 2.05 24.11 1.20 2.52
Total Collembola 95 7.18 43 4.01 18.92 0.94 4.07
Sminthuridae 39 2.95 24 2.24 3.51 0.18 0.46

Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla 55
South American Journal of Herpetology, 9(1), 2014, 52–61

Prey type n %n F %F V (mm3) %V IRI

Entomobryidae 11 0.83 6 0.56 11.12 0.55 0.32
Poduridae 3 0.23 1 0.09 0.45 0.02 0.00
N.N 42 3.17 17 1.59 3.84 0.19 0.35
Total Coleoptera 94 7.10 51 4.76 386.91 19.30 92.18
Curculionidae 13 0.98 9 0.84 130.00 6.49 5.45
Staphylinidae 11 0.83 7 0.65 14.41 0.72 0.47
Scydmaeninae 8 0.60 5 0.47 5.94 0.30 0.14
Chrysomelidae 2 0.15 2 0.19 3.43 0.17 0.03
Carabidae 1 0.08 1 0.09 10.00 0.50 0.05
Coccinellidae 1 0.08 1 0.09 1.41 0.07 0.01
N.N 66 4.98 40 3.73 221.72 11.06 41.46
Total Diptera 33 2.49 25 2.33 41.11 2.05 4.84
Chironomidae 2 0.15 2 0.19 0.71 0.04 0.01
Tipulidae 1 0.08 1 0.09 0.00 0.00 0.00
Sciaridae 1 0.08 1 0.09 0.00 0.00 0.00
Choloropidae 1 0.08 1 0.09 0.30 0.01 0.00
cf. Tanydaridae 1 0.08 1 0.09 0.25 0.01 0.00
N.N 27 2.04 21 1.96 39.85 1.99 3.93
Total Araneae 20 1.51 13 1.21 156.60 7.81 9.49
Tetragnathidae 1 0.08 2 0.19 4.00 0.20 0.04
Araneidae 2 0.15 2 0.19 25.00 1.25 0.23
Gasteracantha spp. 1 0.08 1 0.09 20.00 1.00 0.09
N.N 16 1.21 12 1.12 107.60 5.37 6.02
Total Isopoda 16 1.21 11 1.03 173.00 8.63 8.87
Oniscidae 8 0.60 6 0.56 80.00 3.99 2.24
N.N 8 0.60 5 0.47 93.00 4.64 2.17
Total Polydesmida 16 1.21 12 1.12 300.00 14.97 16.77
Pseudoscorpionida 12 0.91 11 1.03 9.40 0.47 0.49
Total Hemiptera 10 0.76 10 0.93 33.00 1.65 1.54
Aphidae 1 0.08 1 0.09 2.00 0.10 0.01
Cicadellidae 1 0.08 1 0.09 4.00 0.20 0.02
Aradidae 1 0.08 1 0.09 3.00 0.15 0.01
Coccoidea 1 0.08 1 0.09 0.50 0.02 0.00
N.N 6 0.45 6 0.56 23.50 1.17 0.66
Total Orthoptera 9 0.68 9 0.84 36.00 1.80 1.51
Gryllidae 1 0.08 1 0.09 4.00 0.20 0.02
N.N 8 0.60 8 0.75 35.00 1.75 1.31
Total Dermaptera 6 0.45 3 0.28 60.00 2.99 0.84
Forficulidae 6 0.45 3 0.28 60.00 2.99 0.84
Total Geophilomorpha 5 0.38 5 0.47 25.00 1.25 0.58
Total Lepidoptera 5 0.38 5 0.47 91.00 4.54 2.12
Geometridae 2 0.15 2 0.19 73.00 3.64 0.68
N.N 3 0.23 3 0.28 18.00 0.90 0.25
Total Pulmonata 4 0.30 4 0.37 6.15 0.31 0.12
Radiodiscus spp. 4 0.30 4 0.37 6.15 0.31 0.12
Total Opiliones 4 0.30 4 0.37 40.50 2.02 0.76
Laniatorina 2 0.15 2 0.19 20.00 1.00 0.19
Palpatorina 1 0.08 1 0.09 0.50 0.02 0.00
N.N 1 0.08 1 0.09 20.00 1.00 0.09
Total Thysanoptera 4 0.30 3 0.28 1.75 0.09 0.03
Phlaeothripidae 2 0.15 1 0.09 1.25 0.06 0.01
N.N 2 0.15 2 0.19 0.50 0.02 0.00
Blattodea 4 0.30 4 0.37 55.00 2.74 1.03
Blattidae 1 0.08 1 0.09 7.30 0.36 0.03
Neuroptera 1 0.08 1 0.09 0.00 0.00 0.00
Hemerobiidae 1 0.08 1 0.09 0.00 0.00 0.00
Nusalala 1 0.08 1 0.09 0.00 0.00 0.00
TOTAL 1324 99.62 1072 100. 2004.3 100.0 10099.9

Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
56 Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla
South American Journal of Herpetology, 9(1), 2014, 52–61

we only found 5 individuals, and in July, the last month of from ground surface to 120 cm. Therefore, there was a sig-
sampling, we did not find any individuals, even though we nificant difference in substrate use (Chi-Square = 404.16,
increased the time spent on surveys (Table 1). df = 6, p < 0.0001). We did not find significant differences in
microhabitat use between sexes (Chi-Square = 2.2, df = 6,
p  =  0.53) or among age categories (Chi-Square  =  0.33,
Diet analysis df = 12, p = 0.5). However, perch height was related to SVL
and body mass (rs = 0.29, p = 0.007, n = 87 and rs = 0.32,
All but one of the examined salamanders of Bolito- p = 0.002, n = 87, respectively, Fig. 2).
glossa cf. pandi contained at least one complete prey item in
their stomachs. The diet of Bolitoglossa cf. pandi was com-
posed mainly of arthropods: 1324 prey items were iden-
tified and grouped into 20 categories (Table 2). Acari and
Formicidae were the most numerically dominant taxa. Ac-
cording to the IRI, the most important food category was
Acari (Oribatids the most represented), followed by Cole-
optera and Formicidae (Myrmicinae the most represented).
We found significant positive correlations between
volume of consumed prey and SVL (rs = 0.413, p = 0.001,
n = 87) and body mass (rs = 0.45, p = 0.001, n = 87). We
did not find a significant relationship between number of
consumed prey and SVL (rs = 0.003, p = 0.97, n = 87), body
mass (rs = -0.04, p = 0.69, n = 87), MW (rs = -0.06, p = 0.58,
n = 87), and perch height (rs = 0.032, p = 0.77, n = 87). This
population of Bolitglossa cf. pandi exhibits strong sexual di-
morphism in body size (F(1, 45) = 49.17, p = 0.0001) with fe-
males having significantly larger SVLs. However, when we
adjusted prey volume to SVL, males and females they did
not differ significantly (ANCOVA F(1, 21) = 0.13, p = 0.71).
Prey volume was significantly greater during rainy
rather than dry months (F(1, 81) = 4.78, p = 0.03), but prey
numbers did not significantly change between seasons
(F(1,  81)  =  2.34, p  =  0.13). There were significant positive
relationships between the volume of the most dominant
prey taxa and salamander SVL: Coleoptera (rs  =  0.33,
p = 0.001), and Formicidae (rs = 0.43, p = 0.001, n = 87),
whereas there was a significant negative relationship be-
tween the volume of Acari and SVL (rs = -0.24, p = 0.027,
n = 87; Fig. 1).
There were significant differences in the volume of
consumed Acari between seasons, with an increase ob-
served during the rainy season (F(1,  84)  =  5.20, p  =  0.02).
There was no significant change in the adjusted vol-
ume of ants and coleopterans between seasons when
all individuals were considered (F(1,  84)  =  2.14, p  =  0.14,
F(1, 84) = 1.92, p = 0.16). However, adults consumed a sig-
nificantly greater volume of ants during the dry season
(F(2, 81) = 4.76, p = 0.02), whereas neonates and juveniles
consumed a greater volume of ants during the rainy season
(F(2, 81) = 4.76, p = 0.02, F(2, 81) = 4.76, p = 0.04, respectively).

Microhabitat

Salamanders were found mainly perching on the up- Figure 1. Relationship between snout–vent length (mm) of Bolitoglossa
per side of leaves (90% of individuals) at heights ranging cf. pandi and volume (mm3) of most important prey items.

Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla 57
South American Journal of Herpetology, 9(1), 2014, 52–61
Arthropod availability
In the study area, arthropod fauna was composed
mainly of Coleoptera, Acari, Diptera, Formicidae, and
other Hymenoptera; most of them were collected in the
leaf litter. During the dry season, Coleoptera was the most
represented (22.84%), followed by Orthoptera (21.68%),
and Formicidae (16.08%). During the rainy months, Cole-
optera was again the most abundant (30.61%), followed
by Acari (22.27%), and Orthoptera (20.67%). Coleoptera
was collected both in the leaf litter and on the vegetation,
whereas Acari and Formicidae were most commonly col-
lected in the leaf litter (Table 3).
DISCUSSION
Capture of Bolitoglossa cf. pandi was high during the
rainy season. However, although February is typically a
dry month, there were strong rains during most of the
month and also on the sampling days. This fact may have
contributed to the high rate of capture in this month,
whereas during June and July, months of the second dry
season of the year, the extreme dryness might have re-
sulted in the minimal capture rate. We searched inten-
sively during the driest months but the salamanders
seemed to have disappeared. They could be concealed
in wet microhabitats, such as inside deep axils of some
plants, under the leaf litter, and even buried in the soil,
reducing their activity. García-Vasquez et  al. (2006) ob-
served that terrestrial plethodonthids might be hidden
in wet sites during the dry season. In other Bolitoglossa
species, a strong seasonal impact has been observed in
population density and total number of individuals re-
lated to the weather, being greater when rains increased
(e.g., B.  subpalmata, Vial, 1968; B.  altamazonica, Gutiér-
rez-Lamus et al., 2011).
Figure 2. Relationship between snout–vent length (mm), body mass (g),
and perch height (cm) in Bolitoglossa cf. pandi.
Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
58
Population structure
Juveniles were the most abundant individuals dur-
ing the six months of sampling, which suggests that rate
of growth is very slow, as has been observed in individu-
als of Bolitoglossa subpalmata, which took about 18 years
to reach sexual maturity (Vial, 1968). However, greater
abundance of juveniles than adults is not uncommon in
amphibians and might be related to more than just slow
growth rates; several other factors, such as high fecundity
or high mortality rates also regulate population structure.
It is important to conduct demographic analyses for this
population and other Bolitoglossa species to test if life his-
tory features of B. subpalmata are shared or similar to that
of other species of the genus.
In several species of Bolitoglossa with continuous
male reproductive activity, all adult males exhibit con-
spicuous mental glands (e.g., B.  nicefori, González-León
and Ramírez-Pinilla, 2009); the mental gland has been
described as a prominent male secondary sexual feature
related to hormonal control. In Bolitoglossa species with
strongly seasonal reproductive cycles, adult males with-
out a well-developed mental gland have been observed
during the non-reproductive season (Houck, 1977); addi-
tionally, males start sexual maturity at smaller body sizes
than females. Therefore, if the males of B. cf. pandi have a
seasonal reproduction cycle, it is possible that some adult
males might have been included in the juvenile category.
Further studies are necessary to better understand the re-
productive biology of this population.
Diet
Bolitoglossa cf. pandi feeds mainly on mites, ants,
and coleopterans; however, other arthropods such as col-
lembolans, dipterans, and hymenopterans also composed
its diet, suggesting two foraging modes: active foraging
(feeding on mites, springtails and larvae) and sit-and-
wait foraging (feeding on ants and coleopterans). Rove
beetles, springtails, and mites are typical leaf litter ar-
thropods, suggesting that salamanders feed in leaf litter
microhabitats. Other prey items, such as dipterans and
some hymenopterans, are found mainly on leaves, there-
fore salamanders feed in both microhabitats. Results of
other studies in Bolitoglossa species show similar tenden-
cies (Mead and Boback, 2002; Ortega et  al., 2009) and,
although diversity of dietary items varies among species,
values are within similar ranges (Table 4). Our population
of Bolitoglossa presented a diversity index (H’ = 1.72) simi-
lar to B. mexicana (H’ = 1.58) and B. pesrubra (H’ = 1.97).
In Bolitoglossa nicefori, Formicidae, Coleoptera, and
Diptera (larvae) were the most important prey items
(Ortega et al., 2009). Anderson and Mathis (1999) found
that Formicidae was the most important prey in the diet
Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla
South American Journal of Herpetology, 9(1), 2014, 52–61

Table 3. Arthropod availability in leaf litter and on Bolitoglossa cf. pandi perches during the rainy and dry seasons.

Dry season Rainy season

Taxonomic groups Subtotal Subtotal Total
Leaf litter Perch Leaf litter Perch
Coleoptera 85 13 98 202 0 202 300
Diptera 27 25 52 41 0 41 93
Hymenoptera 15 8 23 22 0 22 45
Formicidae 69 0 69 48 0 48 117
Blattodea 0 1 1 10 0 10 11
Dermaptera 2 0 2 5 0 5 7
Hemiptera 2 2 4 4 0 4 8
Neuroptera 1 0 1 0 0 0 1
Phasmatodea* 1 0 1 0 0 0 1
Plecoptera* 0 0 0 2 0 2 2
Psocoptera* 0 2 2 0 0 0 2
Thysanoptera 14 1 15 3 0 3 18
Orthoptera inm. 86 7 93 136 0 136 229
Coleoptera inm. 2 1 3 19 0 19 22
Lepidoptera inm. 7 2 9 5 0 5 14
Araneae 25 25 50 33 0 33 83
Opiliones 0 1 1 2 0 2 3
Pseudoscorpions 12 0 12 15 0 15 27
Geophilomorpha 1 0 1 1 0 1 2
Scolopendromorpha* 0 0 0 1 0 1 1
Polidesmida 0 0 0 20 0 20 20
Glomerida* 0 0 0 1 0 1 1
Glomeridesmida* 0 0 0 5 0 5 5
Julida* 1 0 1 0 0 0 1
Isopoda 1 0 1 7 0 7 8
Collembola 10 3 13 9 0 9 22
Acari 18 1 19 147 0 158 166

* These arthropods were not observed in Bolitoglossa cf. pandi stomach contents.

of B. mexicana and B. rufescens, whereas B. cerroensis and
B.  pesrubra consumed a wide spectrum of prey without
any particular taxon being predominant (Mead and Bo-
back, 2003). In this study, we found that Acari was the
most important prey category in the diet of B.  cf.  pandi
and an important resource for all age categories and body
sizes. However, due to their reduced size, the contribu-
tion of mites to the total stomach content volume was not
most significant. Nevertheless, the volume of mites was
inversely related to body size, so mites are an important
resource for the smallest salamanders.
The second most important prey type of our Bolito-
glossa population was Coleoptera, consumption of which
was related to increased salamander body size. Guix
(1993) suggested that larger individuals must consume
larger prey items to satisfy their energy requirements.
There was no significant difference in volume of coleop-
terans between seasons, although coleopterans availabil-
ity was greater in rainy months. Coleoptera is the largest
order of species in the animal kingdom (Costa, 2000);
they appear in almost every kind of habitat in the world.
Staphylinidae, was important in the diet of Bolitoglossa cf.
pandi and the most collected family at the study site.
Ants were also important in the diet of Bolitoglossa
cf. pandi. Parmelee (1999) suggested that ants are easy
to catch because they are slow and live in colonies. Myr-
micinae ants were the most abundant, both in volume
and absolute numbers: Pheidole  spp., followed by Sole-
nopsis spp., were the most representative Myrmicinae in
the diet of B. cf. pandi. Myrmicinae is the most abundant
and complex subfamily of Formicidae, and Pheidole and
Solenopsis are its most common genera in the Neotropics
(Fernandez and Sharkey, 2006). In fact, Pheidole was the
most abundant dietary resource in the study area, sug-
gesting that the high consumption of these ants was due
to their availability (Table 3). An important ontogenetic
shift in the diet of Bolitoglossa cf. pandi was found in this
study. Ant consumption significantly increased in adults.
Wheeler et  al. (2007) found similar results in Plethodon
elongatus and suggested that differences between age cat-
egories could be attributed to the inability of juveniles to
consume larger prey, due in part to gape limitations.
In some other amphibians, mites and ants are im-
portant dietary sources of alkaloids sequestered for chem-
ical defense (Saporito et  al., 2012; Hantak et  al., 2013).
We observed that individuals of our population secreted a

Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla 59
South American Journal of Herpetology, 9(1), 2014, 52–61
Table 4. Shannon-Wiener index and relative contributions of richness
and evenness to the diet of Bolitoglossa cf. pandi (modified from Mead
and Boback, 2002). Data for Bolitoglossa cerroensis and B. pesrubra from
Mead and Boback (2002), for B. mexicana and B. rufuscens from Anderson
and Mathis (1999), and for B. nicefori from Ortega et al. (2009). Low-
diversity indices show the consumption of only few types of prey and/
or overconsumption of specimens in the same prey category (in the case
of Bolitoglossa cf. pandi, corresponding to the abundance of mites and
ants in their diets). S = number of prey taxa; H’ = diversity index; E =
evenness.
S H’ E ln(S) ln(E)
B. cerroensis 12 2.11 0.687 2.48 -0.37
B. pesrubra 10 1.97 0.717 2.30 -0.33
B. mexicana 14 1.58 0.346 2.63 -1.05
B. rufuscens 17 1.16 0.187 2.83 -1,67
B. nicefori 13 0.98 0.21 2.56 -1.56
Bolitoglossa cf. pandi 20 1.72 0.28 3.00 -1.27
semi-viscous, sticky, transparent substance from the skin
when handled, possibly as an antipredator response (cf.
Brodie and Ducey, 1991). These secretions and the promi-
nence of mites and ants in the diet of B. cf. pandi lead us
to speculate that this species and other species of Bolito-
glossa might also sequester alkaloids for chemical defense.
Analysis of the chemical composition of B. cf. pandi skin
secretions is required to test this hypothesis.
Bolitoglossa cf. pandi consumed a significantly great-
er volume of prey during the rainy months. It has been
shown that the richness, abundance, and diversity of ar-
thropods are greater during the rainy season (López-Gó-
mez et al., 2009; Blanco-Becerril et al., 2010). Prey items
most abundant in the environment in both dry and rainy
season were Coleoptera and Orthoptera; however, these
two categories were not the most consumed by B. cf. pan-
di. Flies and spiders were also abundant in the environ-
ment; although these prey categories were consumed by
B. cf. pandi, they were not significant components in its
diet. Mites were consumed significantly more in the rainy
season and were more abundant in the study area during
rains; therefore, the availability of mites as prey in this
period might have influenced their greater consumption.
The availability of these prey items in the environment,
their small size, and the predominance of juveniles in this
population account for the importance of mites in the
diet of this population. Formicidae presented its greatest
abundance in the environment and as dietary items dur-
ing the dry season; therefore, it is possible that this pref-
erence by Bolitoglossa cf. pandi has been influenced in part
by the high availability of ants, and in part by their easy
capture because of their size.
A relationship between diet and prey availability has
not been included in many studies of amphibian diets.
Nevertheless, in a study of Bolitoglossa nicefori (Ortega
et al., 2009), Formicidae found to be the most abundant
prey item both in the diet and in the study area, suggest-
ing that this species exploits the food availability offered
Diet and Microhabitat Use of Bolitoglossa cf. pandi (Caudata: Plethodontidae) from the Cordillera Oriental of Colombia
60
by its environment. Considering that B. nicefori is larger
than B. cf. pandi, we suggest that the size of the predator
is indeed a limiting factor, one that prevents the exploita-
tion of the prey provided by the environment.
We employed for first time the stomach-flushing
technique to study the diet of a species of Bolitoglossa;
we did not use any anesthetic and we obtained success-
ful results, showing that this method works very well if
correctly applied, causing a low mortality to the individu-
als. Stomach-flushing has also been used successfully in
amphibians (in anurans, Solé et al., 2005; in larval sala-
manders, Cecala et al., 2007; and in terrestrial salaman-
ders, Crovetto et  al., 2012). Therefore, for endemic or
protected amphibian populations, we recommend this
procedure.
Microhabitat use
Bolitoglossa cf. pandi exhibited both terrestrial and
arboreal habits, like other Bolitoglossa species do (e.g.,
B.  mombachoensis, Jansen and Köhler, 2001; B.  equato-
riana, Cisneros-Heredia, 2006; B.  nicefori, Ortega et  al.,
2009). At night, salamanders were observed on shrubs
and perched on leaves where they foraged; during daylight
hours, they hid in the leaf litter and in the axils of bro-
meliads. There was a positive relationship between perch
height and body size and mass (Fig. 2). Neonates and ju-
veniles were usually perched on lower plants like ferns,
while adults perched on taller plants. This relationship
was not observed in other species of Bolitoglossa (B. cer-
roensis and B. pesrubra, Mead and Boback, 2002; B. nice-
fori, Ortega et al., 2009; B. paraensis, Neckel-Oliveira et al.,
2011).
The occurrence of individuals of Bolitoglossa cf.
pandi was strongly related to environmental humidity
conditions, being most abundant in rainy months. The
juvenile age category was by far the most prevalent. Al-
though there are many common features in the life-his-
tory strategies of the Neotropical salamanders studied to
date, the diet and life history traits of the Bolitoglossa cf.
pandi studied here are strongly influenced by ecological
factors.
ACKNOWLEDGMENTS
We thank the Fundación Ecodiversidad Colombia for
their financial support during fieldwork, the Laboratorio
de Zoología y Ecología Acuática of the Universidad de los
Andes for allowing us to use their laboratory equipment;
O. Sanabria of the Laboratorio de Entomología, Universi-
dad Industrial de Santander, for his aid in the taxonomi-
cal identification of arthropods. We also thank D. Dombro
for help in reviewing the English writing.
Jennifer S. Del Río-García, Víctor H. Serrano-Cardozo, Martha P. Ramírez-Pinilla
South American Journal of Herpetology, 9(1), 2014, 52–61
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