Society for the Study of Amphibians and Reptiles

Reproductive Activity, Diet, and Microhabitat Use in Bolitoglossa nicefori (Caudata:

Plethodontidae)
Author(s): Jesús E. Ortega, John Maury Monares-Riaño and Martha Patricia Ramírez-Pinilla
Source: Journal of Herpetology, Vol. 43, No. 1 (Mar., 2009), pp. 1-10
Published by: Society for the Study of Amphibians and Reptiles
Stable URL: http://www.jstor.org/stable/25599180
Accessed: 03-11-2015 01:37 UTC

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JournalofHerpetology,Vol. 43,No. 1, pp. 1-10, 2009
Copyright 2009 Society for the Study ofAmphibians and Reptiles

Reproductive Activity, Diet, and Microhabitat Use in

Bolitoglossa nicefori (Caudata: Plethodontidae)

E. Ortega,1 and Martha

Jesus John Maury Monares-Riano, Patricia RamIrez-Pinilla2

Laboratorio de Biologia Reproductiva de Vertebrados, Coleccion Herpetologica, Escuela de Biologia,

Universidad Industrial de Santander, Bucaramanga, Colombia

a terrestrial salamander only known

Abstract.?Bolitoglossa nicefori is from its original description. We

report the discovery of two populations of this species; analyze annual reproductive activity, diet, and
microhabitat use of one population; and compare this information with that known for other species of

Bolitoglossa. Sexually mature males ranged between 29 and 50 mm standard length and females between 39
and 75 mm.Histological analyses of testes and ducts revealed the presence of sperm through the year,

indicating continuous reproductive activity for males. Adult females were captured year-round; however,
reproductive females were observed only during the driest months of the year (November to February),
indicating that females have a seasonal reproductive activity. The contents of 89 stomachs were analyzed,
and perch height, type of vegetation, and substrate type were registered. The diet of this population consists
of 13 items, with ants and coleopterans accounting for 87% of food ingested by the different age and sex
classes. Ants represent 58% of the diet, reflecting their greater availability in this microhabitat. Intra- and
intersexual differences in diet were not found. Bolitoglossa nicefori exhibited both terrestrial and arboreal
behaviors related to temperature and humidity conditions during the daily cycle. Mature nonreproductive
females, males, and juveniles were found perching from 0-60 cm above the ground on Araceae bushes that

predominate in the study area, whereas reproductive females were always found within the leaf litter. Life

history features of B. nicefori are determined by environmental conditions; however, they follow common
trends shared with other species of Bolitoglossa.

The Neotropical genus Bolitoglossa (Pletho Bolitoglossa males undergo continual spermato
dontidae) contains nearly 95 species (Frost, genesis, and most
species possess continually
2007) and is the largest and most widely developed secondary sexual characteristics (Vi
distributed genus of salamanders (Garcia-Paris al, 1968; Houck, 1977a, 1982; Chan, 2003).
et al, 2000; Parra-Olea et al, 2004). In most However, are influenced
patterns
reproductive
Bolitoglossa (Plethodontidae), females reproduce by local factors assuch
particular climatic

seasonally (Bolitoglossa engelhardti, Bolitoglossa conditions, type of microhabitat, and the rich

franklini,Bolitoglossa occidentalis,Bolitoglossa lin ness and the abundance of resources (Wake and
colni,Houck, 1977a; Bolitoglossa rostrata,Houck, Lynch, 1976; Houck, 1982; Wake, 1987; Chan,
1977b). However, Bolitoglossa adspersa (Valdi 2003).
vieso and Tamsitt, 1965), Bolitoglossa colonnea Diet and microhabitat preferences have been
(Bruce, 1997), and Bolitoglossa subpalmata (Vial, studied in fewer
species (e.g., B. subpalmata Vial,
1966, 1968; Houck, 1982) have continuous 1968; Bolitoglossapersubraand Bolitoglossa cerroen
reproduction
in females and males. For seasonal sisMead and Boback, 2002, in Costa Rica; and
species, clutch sizes (ranging from 20-50 eggs) Bolitoglossa mexicana and
Bolitoglossa rufescens
are positively correlated with female body size Anderson and Mathis, 1999, in Mexico). For
(Houck, 1977a). Adult females are significantly these populations, the dominant prey category
than adult males in large
larger species (e.g., B. was Formicidae, followed by Coleoptera and
subpalmataVial, 1968; B. rostrataHouck, 1977b; Collembola. Also, in B. mexicana and B. rufescens
a significant positive
relationship was found
Chan, 2003), whereas in small males
species,
and females have similar body sizes (e.g., B. between body size and the size and volume of
adspersa, Valdivieso and Tamsitt, 1965; Houck, the consumed prey (Anderson and Mathis,
1977b). Unlike temperate plethodontids, which 1999). Individuals of these populations were
have markedly seasonal active when collected on the surface of
reproductive cycles, leaves,
stems, on the forest floor, and on tree
plants
1
Present address: de Ecofisiologia
trunks.Vial (1968) also collected individuals in
Grupo del
Universidad de los bromeliads and under rocks. Detailed informa
Comportamiento y Herpetologia,
tion about microhabitat is also available formany
Andes,
2 Bogota, Colombia.
Author. E-mail: Guatemalan and Honduran (Wake
Corresponding mpramir@uis. Bolitoglossa
edu.co and mpramir@gmail.com and Lynch, 1976;McCranie and Wilson, 2002).

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 2 J.E. ORTEGA ET AL.

20 160
Bolitoglossa (Eladinea) nicefori is a moderate -|-j-
sized from the northern part of the " 140
species t-**-\
Colombian Cordillera Oriental. Itwas grouped
in the Bolitoglossa (Eladinea) adspersa group by
Parra-Olea et al. (2004). The is known
species
from
tion based
the data
on
registered
a population
in its
original
from San Gil
descrip I'8 / ...^^ \ """I
and some observations of micro
municipality I
?-17 - * y \ co
-A' \.-?---"-\.t"i \ 60 -
(Wake and Lynch, 1976); no other
habitat use E /

of its natural are known.

aspects history
16- *
However, its conservation status was
recently
listed as Least Concern because, its r20
although wet
1 1
dry wet
22
dry
extent of occurrence is less than
probably 15 I I I I I I I I I I I I I0
20,000 km2, it is common with a Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
presumed
(Ramirez-Pinilla et al., 2004). Month
large population
We report the discovery of two relatively large Fig. 1. Monthly mean rainfall and temperature of
of this some
populations species, provide the study area. Data correspond to the monthly mean
details of its natural history (reproductive (solid line, in millimeters) and temper
precipitation
activity, diet composition, and microhabitat ature (broken line, in ?C) over the last 20 yr. Data
use), and compare this information with reports recorded from the nearest IDEAM climatological
on other of the genus. station.
species

Materials and Methods vegetation, and substrate type (fern, moss,

forest floor, leaf litter, and Salamanders
During 2003, we found two neighboring
leaves).
were immediately euthanized with 10% ethanol
populations of Bolitoglossa nicefori in the San and fixed in 10% formalin for 15 days to
tander area on the west flank of the Cordillera
Oriental of theColombian Andes. One is located interrupt the digestive processes and prey
were transferred to
in the Hacienda el Roble, Piedecuesta and Mesa decomposition. Specimens
de los Santos Municipalities and 70% ethanol and deposited in theherpetological
(06?53'N
collection of the Museo de Historia Natural,
73?3'W, 1,500-1,700 m elevation), inhabiting
of
Universidad Industrial de Santander (UIS-A).
agroecosytems (large plantation organic
The to the
Leaf litter arthropods were collected during
coffee). other, which corresponds
and seasons with an insect net and a
studied population, is located in Vereda Las rainy dry
Microcuenca La Venta, Berlesse funnel at the study location to quantify
Amarillas, Municipality
food resource and richness.
of Piedecuesta, Santander, Colombia, South availability
In the laboratory, salamanders were dissected
America (06?58'10.6"N and 73?1'17.5"W, 1,400
tracts were for
2,000 m altitude). The habitat is a highly and their reproductive removed

disturbed tropical dry forest (bs - T) according analysis of sexual maturity

and reproductive
In males, we recorded the and
to the Holdridge et al. (1971) system. Mean activity. longest
annual rainfall is 1,160 mm, and mean annual shortest diameters (to calculate testicular vol

is 17.36?C. The rainfall is ume

using the formula for an ovoid spheroid,
temperature regime
bimodal, with one peak inApril and May and a Caldwell and Vitt, 1999) and the number of
second in October. December toMarch are lobes of the testes. To for reproductive
peak inspect
the driest months, and July to August are activity and document the SL range for onset of
months with reduced rains (IDEAM [Instituto sexual the left testis was extracted,
maturity,
de Hidrologia, Meteorologia y Estudios Am fixed in 70% ethanol, embedded in paraffin,
bientales de Colombia], 2004; Fig. 1). sectioned at 6 um, and stained with hematoxy
The individuals used in this study were lin-eosin. The stage of spermatogenesis
was

visual encounters two determined following Chan's (2003) classifica

captured by during
nights of surveys (1900-0100 h) each month
tion: stage 1, primary spermatocytes; stage 2,
between and December 2004, spermatocytes and stage 3, sperma
January covering secondary
different areas of the forest. The was tozoa.
sampling
standardized as two persons for six hours each Female sexual and
maturity reproductive
night. The specimens were collected by hand
was confirmed the presence of
activity by
and placed into individually labeled bags. We yolked follicles, oviductal eggs, and enlarged
recorded standard length (SL) and mouth width convoluted oviducts; we recorded ovarian

(MW) according to Bovero et al. (2003). The volume and diameter of the yolked follicles or
following variables were recorded for each oviductal eggs. Reproductive activity data for
collected individual: perch height, type of each animal were used to establish the percent

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 REPRODUCTION, DIET, AND MICROHABITAT OF BOLITOGLOSSA NICEFORI 3

8 r-.-.-.-.-.-.-.-.-.-.-.-.-.-,-.-r*

6 -
9
0

8 8
1 8 ?
* ft
|
=
o?
8 t
-i * *
8
x
a
A ?
i a ?
,: 8 ?
2
! i i ;
1
Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov
Wet1
Dry1 22
Wet
Dry
Season

Fig. 2. Distributions of age (SL, cm) and sex of the individuals collected from the population of Bolitoglossa
nicefori. Reproductive adult males (filled triangles), nonreproductive males (open triangles), nonreproductive
adult females (open circles), adult reproductive females (filled circles), juvenile males (gray rhombuses), juvenile
females (open squares), sex (rhombuses). The arrows indicate the minimum size at
juveniles of undetermined
sexual maturity for each sex.

age of males and females in each measured with the Shannon-Wiener

reproductive diversity
each month and season the index. The number,
stage throughout percentage, frequency,
year. Ovarian egg data were used to estimate mass, and prey length
and width were record
mean clutch size. Number of ovarian eggs was ed. We tested correlations between salamander
correlated with female body size (SL). To detect SL and MW and prey size and volume (using
significant
intra- and intersex variation in the ovoid spheroid formula) to see whether
over time, we size on salamander size. Mann
reproductive stages employed prey depended
tests or G-tests. We calculated linear U-tests were used to see whether
Chi-square Whitney
between volume and SL of differences existed between sexes
regressions gonad significant
each individual. Reproductive data of each for all diet variables. tests were used
Chi-square
month were into three-month intervals to whether statistical
grouped investigate significant
(that corresponds to the four rainfall periods differences existed in the use of microhabitat
that occur
during the year, see
Fig. 1). Statistical and perch heights.
differences in among
reproductive activity
seasons were assessed of covari
using analysis
Results
ance (ANCOVA) on the gonad volumetric data
with body size (SL) as a covariate. The possible ReproductiveActivity and Size atMaturity.?We
effects of climatic factors on
reproductive
collected 123 individuals: 39 adult males, 31
were tested with linear regres adult females, and 53 juveniles. The number of
activity multiple
sions between themonthly scores of rainfall (in collected males, females, and immatures was

millimeters) and temperature (?C) and gonadal not significantly different (X2[2;3]= 2.901 P >
=
volume. 0.5, N 123) showing equal capture for both
tracts of every individual were sexes and all seasons. Mature
Digestive juveniles during
=
removed and their contents in 70% males occurred the year
preserved throughout (X2[3]
ethanol. Taxonomic determinations of prey 4.27 P > 0.20, N = 39), whereas the occurrence
were made Borror et al. (1989). An index of reproductive mature females varied
using signifi
=
of relative importance
was calculated to evalu cantly among months (X2[3] 22.99 P < 0.001,N
=
ate the contribution of each category to this 31,
Fig. Sexually 2). ranged
mature males

population's diet (following Pinkas et al., 1971). from 29-50 mm SL (mean ? SD, X = 39.7 ?
=
The relationship of the prey items and their 0.59 mm, N 39); mature females ranged be
contribution to the diversity of the diet was tween 39 and 75 mm SL (X = 51.99 ? 0.84 mm,

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 4 J.E. ORTEGA ET AL.

25
-|

? 20-1
~
1

Jl I I I I I n
12-17,0 18-23 24-29 30-35
Jill
36-41 42-47 48-53 54-59 60-65 66

SL range (mm)
Fig. 3. Distribution for sizes (SL) of the individuals in the different categories considered in the population.
Notice themore restricted size distribution in adult males compared to the wide range of sizes and much larger
SLs attained by females. Juveniles of undetermined sex, gray bars; juvenile males, vertical lines bars; juvenile
females, horizontal lines bars; adult males, black bars; adult females, white bars.

N = 31, Fig. 2). This population exhibits strong = > 2.5 mm, and
678.86, N 13; follicle diameter
sexual dimorphism in body size (SL, f[68]= between 25 and 40 yolked follicles,mean = 34).
= was a
-7.13, P 0.0001, There correlation between
Fig. 3). positive body
Testes were
unpigmented and consisted of size and fecundity (number of yolked follicles, r
=
one or two lobes; largemales (up to 40 mm SL) 0.76, P < 0.05). By December,
maximum
had two lobes per testis. The ovarian size was attained. The first postrepro
usually spermato
genesis
was observed
polarized
in each lobe: ductive females (with distended oviducts) were
only primary spermatocytes
were
present in the found in February, and between March and
anterior of the testis; and sperma October, females had ovaries of small volumes
portion only
= 12.42 ? <
tozoa were found in the posterior portion. The (mean 2.4; follicle diameter
occurrence ofmales with testes in stage 3 (with 1.0mm, and groups of 10-14 follicles of similar
spermatozoa) did not show significant differ
=
size). Therefore, ovulation and oviposition
ences over time (G10 15.8, P > 0.10). There occurs between the end of the driest season
was a significant relationship between SL and and thebeginning of the firstrainy season of the
= = =
testicular volume (r2 0.30, F[1/37] 16.12, P year (January to April; Fig. 5B). We found
= clutches between April and June; they were
0.0002, N 39). Testicular volume of mature
males did not differ significantly among seasons found among the leaf litter,inwet organic soils
= = and in the holes formed by banana roots. Two
(ANCOVA F [1/3] 1.07, P 0.378, Fig. 4A).
However, when testis volume is females were observed close to two
compared attending
months, it is to observe a of eggs. Hatchlings and neonates were
among possible groups
dramatic increase in December when females not found; however, a neonate (9.7 mm SL) was
have the largest follicular sizes and are preovu born in the lab. The results of multiple
latory; testisvolume fell from January toMarch regressions indicate that only ovarian volume
when most of the females oviposited (Fig. 5A). is positively associated with rainfall; inmales,
Almost all males (36 males, 92%) producing variation in rainfall and temperature
seem not

sperm had visible mental glands; large males to significantly affect testicular volume (see
had more developed mental glands. Eight Table 1).
percent of the adult males had sperm in their Diet.?Eighty-four stomachs (39males and 45
testes and no discernible mental gland. females) were dissected, revealing 516 prey
Reproductive females were collected only
items identified to order and grouped into 13
between the months of November and Febru categories (Table 2). The diet was composed of
was a be insects and other such as
ary. There significant relationship arthropods spiders
= and mites. there was some
tween SL and ovarian volume (r2 0.507, Although plant
F[i_29]
= = =
29.85, P 0.0001, N 31). There were material, itwas not considered part of the diet
significant differences in ovarian volume among because it was found in only three of 84
=
seasons (ANCOVA, 6.44, P = 0.002, stomachs. According to the Index of Relative
Fu_3]
Fig. 4B). Between November and February, Importance (IRI), the most important food
females had yolked follicles and the ovaries category was Formicidae (all genera 58%; with
had their largest volumes (mean = 215.89 ? Atta spp. the most represented), followed by

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 REPRODUCTION, DIET, AND MICROHABITAT OF BOLITOGLOSSA NICEFORI 5

a Mean ?SE H~ ?SD

* A
\

40

E* L
n It
3 I [ I I
\A O \ T
J_
co 20 r~i

I
10 T H\ V 5 I

Dry1 Wet1 Dry 2 Wet 2

-
6001- -.-1
MeanQ ?SE ZH ?SD
Q
D
500 r

400
c^

3
| 300 M
I]
o
c 200 U
.2
>
O 100I

T
-
-100 I-- -1-1
Dry1 Wet1 Dry2 Wet 2
Season
Fig. 4. Seasonal in gonadal volume in males and females of Bolitoglossa nicefori. (A) Testis volume
changes
did not vary significantly among seasons; (B) ovarian volume varied significantly among seasons.

Coleoptera (19.2%), and larval Diptera (7%). correlation between SL and prey size (r = 0.28;
The high percentage of ants in the diet was P = 0.015; N = 75), SL and prey volume (r =
related to thehigh availability of this resource in = = =
0.24; P 0.039; N 75),MW and prey size (r
the study area (Table 3). P = N = and MW and
0.27; 0.02; 75), prey
Prey composition of males and females did volume (r = 0.24; P = 0.021; N = 75).
not differ significantly (U1/13= 592; P = 0.31). Microhabitat.?Eighty five percent of the
There also were no differences were collected on herbaceous
significant specimens plants.
between the sexes in the numeric importance However, preovulatory (individuals with large
= =
(^1,13 70, P 0.78), frequency in stomachs yolked follicles), gravid, and clutch attendant
= P = females were collected exclusively within the
(Ui/13 80.5; 0.83), and volume of ingested
= =
prey (U1/13 84, P 0.98), or in the index of leaf litterbetween January and March of 2004.
relative importance (Ulfl3 = 80; P = 0.82). There was no significant difference between
Adult B. nicefori showed significant positive sexes inperch use = >
(X2[4] 9.41; P 0.05). There
correlations between SL and MW, and size and was a difference in substrate use
significant
of a =
volume consumed prey, with (ferns, floor, moss, leaves, and leaf litter, X2[4]
significant

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 6 J.E. ORTEGA ET AL.

160 45
r-1-.-.-j

A 40 f
140 . /

120 r \ / 35
/ \ A / <C
/ -* \\ / \ / 30 ??<
E, 100 / y^-^V c \
* / K V 25I
*i
80 / /\A> 2? ?
/ / \ ^\ y\
60 / /\ / H
\
10
40: ^^-^-^ V ^
20 I- - - - - - - - - - -1 5
Jan Feb Mar Apr May Jun Jul Sep Oct Nov Dec

Months

160 r- - - - -1 400

350
140 ' / R
A/
y/ \ -300
120 \ A
/
^ t / \ /\ *?/
/ 250 |
10? \ \y^^ 200
JL
? / j\ |?
\ / 80 /\ 150
| \ / / \ c
\/ / \ 10?>
60 ' X ?
I \ '50
' * "-"""
//1 \
40 ^- *^^m^^ \

I- 20 - - - - -1 -50
Jan Feb Mar Apr May Jun Jul Sep Oct Nov Dec

Months

Fig. 5. in mean volume in males and females of Bolitoglossa

Monthly changes gonadal nicefori and its
relationship with mean rainfall values. Gonadal volume (solid lines), rainfall values (gray lines).

= N = 39, females N = 45). Perch height used

147.1; P < 0.001; N 89), with leaves being
themost used substrate (73% of the individu was significantly different = <
= (X2[4] 55.63; P
als). The type of leaf used also exhibited 0.001; N 89), with most of the individuals
= >
significant differences (X2[4] 9.405; P
=
0.05; encountered in the 0-29. 9 cm and 30^59. 9 cm
N 89), with leaves of araceous (see 6); there were no
plants ranges Fig. significant
being most frequently used (53% of the indi differences in perch height between the sexes
= =
viduals); there were no differenc 3.06; P > 0.50; males N 39, females
significant (X2[4]
es between sexes
(X2[4j
=
2.46; P ^ 0.05; males N = 45).

Table 1. Multiple regression results for possible effects of temperature and rainfall on gonadal volume in a

population of Bolitoglossa nicefori. P-values in boldface are

significant.

Beta temperature (?C) Beta rainfall (mm) FP r2

Ovarian volume 0.302 -0.70 0.5414 = 0.007

F2/28 5,80
Testicular volume 0.134 -0.36 0.2879 = 1.62 0.210
F2,36

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 REPRODUCTION, DIET, AND MICROHABITAT OF BOLITOGLOSSA NICEFORI 7

Table 2. Diet
composition in a population of Bolitoglossa nicefori. Numerical (number of prey
importance
items in relation to the total number of items found in the species),
frequency (percentage of prey item number
in relation to total number of items found in the species), prey volume (total volume of prey category in all
= % FO
individuals examined), and percentage of relative importance (IR) (% V + % N); FO, percentage of
stomachs containing a specific item; V, volumetric importance; and N, numerical importance.

Diet /Prey
Numerical importance Frequency %IRI
Prey volume
Acarinae
20 8 30.75 93.95
299
Formicidae 61 1,610.12 15,109.77
99
Coleoptera 49 1,005.35 5,497.08
Collembola
19 13 166.59 260.13
Diptera (larvae) 36 23 378.56 1,018.22
Diptera (adult) 7 32.898
5.22
18Araneida 10 181.14 268.97
Hymenoptera 8 7 91.25 73.76
Blattaria 1 1 0.73 0.85
Pseudoescorpionida 3 5.44 3
5.94
Dermaptera 1 1 4.36 1.22
Hemiptera 1 1 9.42 2.82
Orthoptera 3 3 10.19 8.63
516 Total 84 3,499.67 10,551.65

Discussion cease. takes

abruptly Oviposition place during
the dry season, and egg occurs
and Size at development
Reproductive Activity Maturity.?
at the dry season and season
the first rainy
Females of B. nicefori mature larger body sizes during
of the year. in female
and have larger maximal sizes than males. Seasonality reproductive
seems to be common in
Sexual in
body size is common in activity Neotropical
dimorphism
and salamanders. In fact, it has been
Neotropical bolitoglossines tends to be plethodontid
more
pronounced in
larger species (Houck, suggested that in subtropical and Neotropical
1977a,b) and may be associated with reproduc
plethodontid species living in areas of pro
tion: in females nounced seasonality, is
larger body size may allow wet-dry oviposition
concentrated in the dry season and
clutch sizes. In B. as in some hatching
greater nicefori
occurs the wet season and
other species of Bolitoglossa, female fecundity during (McDiarmid
For B. rostrata and other
increases with increasing body size (Vial, 1968; Worthington, 1970).
Guatemalan species, Houck (1977a,b) found
Houck, 1977a;Wake and Dickie, 1998).
The reproductive activity of B. nicefori is that eggs are laid and brooded during the dry
season, and emerge the
seasonal, related to rainfall Ovarian hatchlings during
regime.
of the rainy season when moisture
follicles begin vitellogenesis at the end of the beginning
wet months and reach their maximal diameter
is favorable to growth and dispersal. By
December, the month when the rains
by
25
-j

Table 3. Richness of arthropods in the study site. -

20 I
Ants were the most abundant prey in the litter and in
the higher sites during the rainy and
perch
dry months. 1'- I
In
PreyLeaf litter Perch

Formicidae 43.86 50.61

Atta spp. 5.26 39.61
Other genera 38.6 11
Acarinae 31.58 0
3.51 8.54
IIH^
Coleoptera
Araneida
Blattaria 0 11.59
7.02
5.49
ill 0-29.9 30-59.9 60-89.9
Perch height range (cm)
90-119-9 120-150

Orthoptera 0 9.76
Fig. 6. Perch used sexes
Colembolla 3.51
7.32 height by both of
Bolitoglossa nicefori. Males, black bars; females, white
Diptera (larvae) 10.53
0
bars. Intersexually differences in perch height range
Diptera (adults) 0 6.7
are presumed to be associated with behavior of
Total 100
100
reproductive females.

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 8 J.E. ORTEGA ET AL.

females are continuous breeders in testicular volume was observed

contrast, by December
from less seasonal habitats (B. when the females are and testis
species tropical periovulatory,
adspersa, Valdivieso and Tamsitt, 1965; B. sub volume fell during the following months per
palmata, Vial, B. colonnea, Bruce,
1968; and 1997). haps in response to the increased mating
the reproductive season of B. nicefori, because occur around
During opportunities matings
adult nonreproductive females were not found, the time of egg-laying. Because there was no

suggesting thatallmature females produce only correlation between precipitation

and tempera
one clutch annually. By contrast,Houck (1977b) ture and testis volume, the observed in
changes
found that in a of B. rostrata two testis volume are more related to
population probably
groups of females occur the than to climatic factors.
during reproduc mating activity
tive season a biennial Diet and Microhabitat.?Bolitoglossa
suggesting reproduction nicefori
for this species. Biennial was also feeds on it eats a wide
reproduction mainly ants; however,
suggested for B. subpalmata (Vial, 1968) and B. spectrum of items. Ants were the most abun
rufescens(Anderson and Mathis, 1999),whereas dant dietary
resource the whole year in the
Bruce (1997) suggested that B. colonnea inhabit area, that prey
study suggesting consumption
ing a less seasonal wet forestmight produce may be related to prey availability. This species
more than one clutch it has been
annually. Also, inhabits both arboreal and terrestrialsiteswhere
suggested that seasonally reproductive bolito ants are the most abundant resource. However,
have and more variable clutch a broader is also
glossines larger generalist diet suggested
sizes than continuous breeders (Bruce, 1997). it ingests items. In
because several other prey
Clutch sizes are larger and correlated with
fact, the diet of B. niceforisuggests two foraging
female body sizes in seasonal breeders (B.
modes; active foraging (feeding on mites and
rostrata seven of Neo
larvae) and sit-and-wait foraging (feeding on
Houck, 1977b; species
tropical salamanders Houck, 1997a; B. nicefori ants and coleopterans).
whereas in continuous breeders
present study), Diet studies forother Bolitoglossa species have
like B. B. colonnea, and B.
adspersa, rufescens shown variable results. Some have low
are species
clutch sizes small and not correlated with
indices in consumed prey
diversity species,
female body size (Valdivieso and Tamsitt, 1965;
suggesting that only a few prey types are
Bruce, 1997; Anderson and Mathis, 1999). consumed or at least that the greatest number
Although females of B. nicefori reproduce of individuals belong to a single prey category.
the presence of developed second
seasonally, Anderson and Mathis (1999) and McCranie et
ary sexual characters (mental gland) and the al. (1996) found that ants were the most
histological observation of the testes and vas item for B. mexicana and B.
a important prey
deferens showed that there is continuous = 1.58 and H" =
and rufescens (H" 1.16, Table 4) in
spermiogenesis spermiation, suggesting Veracruz, Mexico and B. dofleini in Guatemala,
that males of this are of
population capable
and the year. respectively. This low diversity index and high
courtship mating throughout of ants is similar to that found for B.
Continuous and percentage
mating activity spermatoge =
netic have been for Dendrotriton nicefori (H" 0.98, Table 4) in our study. In
cycle reported B. cerroensis and B. pesrubra feed on a
and contrast,
bromeliacia Pseudoeurycea goebeli (Chan,
wider of with no taxon
2003) and other species of Bolitoglossa, including variety prey, single prey
= 2.11 and H"
both seasonal and aseasonal breeders ad being dominant in theirdiets (H"
(B. = and Boback, 2002). For these
Valdivieso and Tamsitt, 1965; B. 1.97, Mead
spersa subpal
and
mata Vial, 1968; B. rostrataHouck, 1977b; B. species, Coleoptera, Diptera, Collembola,
Acarina were the most prey.
colonnea Bruce, 1997; B. rufescens Anderson and important
B. occidentalis, B. rostrata Chan,
Vial (1968),Wake (1987), Garcia-Paris et al.
Mathis, 1999;
2003). Houck (1977a) suggested that continual (2000), and Walton (2005) suggested that exter
an evolution nal factors (seasonal prey abundances and
spermatogenesis may represent
or absence and intrinsic
arily stable strategy for salamanders if the cost presence of predators)

ofmaintaining and producing mature sperm is factors (ecological and morphological tolerance)
low. However, detailed ex related to body size influenced the selection of
using histological
amination of the testis,Chan (2003) identified as well as microhabitats used for foraging.
prey,
subtle levels of variation and cryptic temporal These also were reported
in the
relationships
patterns in testis activity not detectable by
of B. mexicana and B.
populations rufescens
external appearance
or the presence of second (Anderson and Mathis, 1999) and for B. cerroen

ary sexual characteristics. Although

testis vol sis and B. pesrubra (Mead and Boback, 2002),
ume did not change sea that in salamanders, as in other
significantly among showing
sons, it was possible
to detect this same
amphibians, the type and size of prey is
variation in testis activity of B. niceforiobserving explained by morphological constraints and by
the monthly behavior of testis volume. Maximal variation in the spectrum of prey types available

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 REPRODUCTION, DIET, AND MICROHABITAT OF BOLITOGLOSSA NICEFORI 9

Table 4. Shannon-Wiener index and relative contributions of richness and evenness to the diet of Bolitoglossa

nicefori. Data for Bolitoglossa cerroensis and Bolitoglossa pesrubra from Mead and Boback (2002); for Bolitoglossa
mexicana and Bolitoglossa rufuscens from Anderson and Mathis (1999). Abbreviations are S = number of prey
= = evenness. of only few types of
taxa, H" diversity index, and E Low-diversity indices show the consumption
and/or of in the same prey category (in the case of B.
prey overconsumption specimens nicefori, corresponding
to the abundance of ants and coleopterans in their diets.

E SH" ln(S) ln(E)

12
B. cerroensis 2.11 0.687 2.48 -0.37
B. 10
pesrubra 1.97 0.717 2.30 -0.33
B. 14
mexicana 1.58 0.346 2.63 -1.05
B. 17
rufuscens 1.16 0.187 2.83 -1.67
B. 13 0.98 0.21 2.56 -1.56
nicefori

(Vial, 1968; Harper and Guynn, 1999; Lima and conditions. Bolitoglossa nicefori showed signifi
Magnusson, 2000;Walton, 2005). cant differences in the use of specific types of
Bolitoglossa nicefori exhibits both terrestrial leaves and plants in this study. This selection
and arboreal behaviors that are related to appeared to be related to the abundance of
temperature and humidity conditions during resources in the area
(type and abundance of
the daily cycle. At night, the salamanders perch plants). Thus, as in other salamanders, particu
on leaves with thick and stems, lar microhabitat features determine variation in
strong especial
ly on plants of the familyAraceae. This offers preferences of populations in different areas
them an easier climb up to the leaf surface (Wake and Lynch, 1976; Mead and Boback,
where there is ample room for free movement 2002; Walton, 2005). The use of prey items and
related to It also a microhabitat resources in B. is deter
prey capture. provides nicefori
substrate for mating the mined by their availability and by reproductive
during reproductive
season us on condition in the case of females.
(as observed by three occasions).
The prevalence of this family of plants in the The comparison of the natural-history fea
area has increased because of its constant tures of B. niceforiand those of other species of
study
sowing. During the day, the salamanders hide Bolitoglossa shows that life-history traits and
within the leaf litteror deep within the axils of patterns of reproduction are strongly influenced
the leaves. Wake and Lynch (1976) categorized by ecological In fact, these fea
relationships.
B. as "intermediate" in microhabitat use tures vary related to climatic and local
nicefori regional
(offthe ground but either under thebark of logs ecological conditions; however, it is possible to
or on observe common trends in
sometimes but not in bromeliads life-history strategies
plants,
or of these Neotropical salamanders.
arboreal mosses). They based thiscategori
zation on the field notes of A. H. Brame, who
collected a series of B. nicefori in the rolled bases Acknowledgments.?We thank the Laboratorio

of palm tree de Biologia Reproductiva de Vertebrados of the

by day.
was no Universidad Industrial de Santander for finan
There relationship between perch
cial and use of reagents and
height and body size in B. nicefori.Mead and support laboratory
Boback (2002) also found no significant differ equipment, to Varta de Colombia for donation
ences in the between mass or SL
of batteries for the lights used during the
relationship
and for B. cerroensis and B. fieldwork, to Corporation Regional para la
perch height pesrubra
in Costa
Defensa de laMeseta de Bucaramanga (CDMB)
Rica. However, there were differences
for the collection and research and D.
in microhabitat use females of permits,
by reproductive F. Caceres, I. Barrero,
Rincon, L. Gutierrez and
B. niceforiduring January toMarch, when they
R. Caicedo, Escuela de Biologia; UIS, forhelping
were found exclusively buried in the leaf litter.
in the of the salamanders. We also
This behavior seems to be related to their capture
thank L. Gutierrez and B. Bock for their
inability to ascend perches caused by the
comments on the and
increase in their body mass while gravid, egg important manuscript
for theirhelp reviewing the English. We thank
attendance, and to the search for and
humidity two reviewers and the editors for
conditions for the and anonymous
temperature clutch,
theirhelpful suggestions on themanuscript.
also to predator avoidance.
possibly
Vial (1968) and Houck (1977b) suggested that
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All use subject to JSTOR Terms and Conditions
 10 J.E. ORTEGA ET AL.

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