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Herpetologists' League

Reproduction in a Neotropical Salamander, Bolitoglossa adspersa (Peters)


Author(s): Darío Valdivieso and J. R. Tamsitt
Reviewed work(s):
Source: Herpetologica, Vol. 21, No. 3 (Sep. 24, 1965), pp. 228-236
Published by: Herpetologists' League
Stable URL: http://www.jstor.org/stable/3891110 .
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228 HERPETOLOGICA Vol. 21, No. 3

Science Departmentof the Fort WorthChildren'sMuseumavailable


for study, and Dr. Howard K. Gloyd for reading the manuscript.

LITERATURE CITED

GLOYD, HowAlw K. 1955. A review of the massasaugas, Sistruruscatenatus,


of the southwestern United States (Serpentes: Crotalidae). Bull. Chicago
Acad. Sci., 10(6):83-98.
KLAUBER,LAWRENCEM. 1956. Rattlesnakes, their habits,life histories,and
influence on mankind. Univ. Calif. Press, Berkeley, Vol. I, pp. 1-708.
KNOPF,GARY N., AND DONALDW. TINKLE. 1961. The distribution and habits
of Sistrurus catenatus in northwest Texas. Herpetologica (17)2:126-131.
WERLER, JOHN E. 1963. Poisonous snakes of Texas and first aid treatment for
their bites. Texas Game and Fish Comm., Austin, Bull. 31, pp. 1-31.
WOODIN, WILLIAM H. 1953. Notes on some reptiles from the Huachuca area
of southeastern Arizona. Bull. Chicago Acad. Sci., 9(15):285-296.
WRIGHT, ALBERT H., AND ANNA A. WRIGHT. Handbook of snakes. Comstock
Pub. Co., Ithaca, Vol. II.
ZEHm, DAVID R. 1962. Stages in the normal developement of the common
garter snake, Thamnophis s. sirtalis. Copeia, 1962(2):322-329.

Pi Kappa Alpha Box, S. U. Station, Georgetown, and 4332 Calmont


Avenue, Fort Worth, Texas.

REPRODUCTIONIN A NEOTIROPICALSALAMANDER,
BOLITOGLOSSAADSPERSA (PETERS)

AND J. R. TAMSITT
DARIOVALDIVIESO

INTRODUCTION
Salamanders of the genus Bolitoglossa which inhabit the high
Andean regions of Colombia have been considered to be ovovivip-
arous by some herpetologists (Peters, 1863; Posada, 1909; Noble,
1931). In reference to Bolitoglossa adspersa (Peters), the common
salamander of the eastern Colombian Andes, Ruthven (1922)
simply stated that, "this species is a viviparous species," basing his
conclusion only on the presence of eggs in the ovary and, as such,
having no direct evidence. Dunn (1944) referred to Neotropical
plethodontid salamanders and stated that, "some are oviparous,
whereas others, especially in the mountainous regions of Colombia,
are thought to be viviparous. However, it is not definitely known
if this is the case, and any information concerning the mode of
reproduction of these salamanders would be interesting." This
question remained unanswered until Niceforo Marla (19,60) pre-
sented evidence to show that B. aclspiersa was oviparous and not
viviparous as believed by earlier workers. He removed six eggs of
this species from beneath a rock at Dintel (2,700 m.) in the Eastern
1965 REPRODUCTION IN A SALAMANDER 229

Andes and later obtained newly hatched salamanders from the eggs.
During 1961-1962, the authors obtained additional data on the
life history and reproductive organs of this oviparous salamander
which supplement the original note of Niceforo Marla. Collections
were made in January, July, August, September, October, and
November, 1961, and in March, April, and May, 1962, near Bogota
(40 35' N, 740 04' W, 2,599 m.), Dept. of Cundinamarca, Colombia.
The salamanders, which are active throughout the year, were taken
from beneath rocks or rusted sheets of tin in wooded areas on
mountain slopes above this city.
The Bogot'a region is found in the lower montane dry forest
formation according to the classification of Holdridge (1947).
Rain, however, falls in every month, and at Bogot'a in 1961 most rain
fell in April, June, July, October, and November, the yearly average
being 925 mm. Temperatures may reach extremes, and the 1961
minimum was -1.1? C. and the maximum 23.0? C.; the annual
temperature mean was 13.40 C. The annual mean relative humidity
for 1961 at Bogot'a was 79 per cent (Empresa de Acueducto y
Alcantarillado de Bogot'a, 1961), and the total annual variation in
day length at latitude 40 N in Colombia is approximately 24 minutes
(Miller, 1959).

MATERIALS, METHODS,AND ACKNOWLEDGMENTS


A series of 136 specimens was collected and examined. The
animals were killed in formol, and snout-vent lengths were
determined by measuring from the tip of the snout to the
posterior margin of the vent. Ovaries of females were examined to
determine the number of immature and mature eggs. If mature
eggs were present in an ovary, the diameter of the largest egg was
measured. In males the lobes of the multiple testes were counted
and measured. To study the microanatomy of the testes, sections
were serially cut at five and 10 micra and stained with eosin-
hematoxylin technique.
The assistance of Adolfo Valdivieso for aid in collecting and for
preparing stained sections of the gonads is gratefully acknowledged.
Charles M. Bogert and Richard G. Zweifel kindly allowed us to ex-
amine specimens of Bolitoglossa adspersa in the American Museum
of Natural History. We are grateful to Dr. Zweifel for his sugges-
tions and for critically reading the manuscript. This work was
supported by the University of the Andes, Bogot'a, and the Penrose
Fund of the American Philosophical Society.

IDENTIFICATION OF SEX
Sexual dimorphism in body size occurs in this species, and the
adult female is considerably larger (snout-vent length 45-66 mm.)
than the adult male (snout-vent length no greater than 50-55 mm.).
230 HERPETOLOGICA Vol. 21, No. 3

TABLE 1.-Numbers of female Bolitoglossa adspersa of different snout-vent


lengths containing yolked and unyolked eggs.
Snout-vent Number Number of unyolked eggs Number of yolked eggs
length in of
mm. indi- Right Left
viduals Right ovary Left ovary ovary ovary
Mean Range Mean Range Mean Range Mean Range

25-29 11 51 30-100 45 26-100 - - - -


30-34 1 42 - 23 - - - - -
35-39 4 59 20-100 60 20-100 - - - -
40-44 4 62 51-74 55 39-81 - - - -
45-49 18 44 21-80 47 20-100 4 1-9 5 1-10
50-55 18 36 8-76 37 13-59 7 5-9 6 1-11
56-60 5 59 33-100 58 33-88 1 - 2 -
61-66 6 47 18-64 45 36-57 7 7-7 8 7-9

Adult males can be recognized easily by the presence of a rounded


mental gland and the swollen snout in the region of the nostrils.
The cirrus at the termination of the nasolabial groove is fairly prom-
inent and branched in males, whereas in females it is unbranched
and inconspicuous. In males three or four premaxillary teeth per-
forate the edge of the upper lip, whereas in females the lip is not
pierced. Numerous villi of the cloacal glands line the wall of the
cloaca in males, and the cloacal lining is pleated and without villi in
females. In young individuals less than 35 mm. snout-vent length,
however, these characters are of limited use for recognition of sex.
Females.-Sixty-seven females representing all age groups were
examined to obtain data on reproductive condition. The ovaries of
adult individuals contained from one to 11 opaque white, maturing
yolked eggs without evidence of inner capsules, the largest per
ovary varying in size from 1.0 to 4.5 mm. and from eight to 100
unyolked, nucleated eggs less than 1 mm. in diameter (Table 1).
The ovaries of mature individuals were elongate, but the closeness of
the eggs to each other gave the ovary a compact appearance.
Larger females (snout-vent length 61-65 mm.) tended to have
more yolked and fewer unyolked eggs than smaller adult females,
but there was no direct correlation between the size of the female
and the total number of yolked eggs. The mean yolked egg number
in 43 adult females was 4.8 in the right ovary and 5.3 in the left
ovary, with a mean of 10.0 eggs for both ovaries. The number of
eggs per individual varied from two to 19. Some females, however,
may have deposited shortly before capture, and the low number of
eggs recorded in some individuals may represent only a small pro-
portion of the total. In mature females the oviduct was invariably
enlarged, but no oviducal eggs were found. Apparently passage of
the eggs from the ovary to the outside is rapid.
The ovaries of salamanders of the smaller size class (Table 1)
1965 REPRODUCTION IN A SALAMANDER 231

were less compact and ribbonlike in appearance, with considerable


interovular space. The ova in these females (snout-vent length
25-44 mm.) were unyolked and nucleated and less than 1 mm. in
diameter. The number of unyolked eggs varied from 20 to over
100 per ovary, with an average number of 53.5 for the right ovary
and 45.8 for the left ovary in 21 individuals. In the smallest in-
dividuals (snout-vent length 25-29 mm.), the elongate ovaries
were less than 1 mm. in width and could hardly be seen with the
naked eye. In all females less than 44 mm. in snout-vent length,
the oviduct was small and almost invisible.
A series of B. adspersa in the American Museum of Natural
History (Nos. 20382-20408) from "mountains"near Muzo, 3,041 m.,
Dept. of Boyaca and 100 km. north of Bogot'a, was examined to
supplement the Bogot'a data. In this series were 17 females, six of
which were immature (snout-vent length 31-46 mm.) without yolked
eggs, the smallest identifiable females measuring 31 and 34 mm. in
snout-vent length. Eleven females (snout-vent length 44-58 mm.),
however, contained yolked eggs. The number of yolked eggs, all 2-3
mm. in diameter, varied from two to eight with a mean of 4.6 in the
right ovary and from three to seven with a mean of 5.3 in the left
ovary. The number of eggs per female varied from five to 11, with
an average of 9.8 for both ovaries. Although individual variation
was great, the extent of geographic variation in size and the number
of ovarian yolked eggs in populations from Bogot'a and Muzo is
negligible.
Stebbins and Hendrickson (1959) reported on a small collection
of B. adspersa from Bogota and found a number of females
with large, heavily yolked eggs but none with embryos. Likewise
Brame and Wake (1963) did not find evidence of development in
the oviducts of females of this species. We have not encountered
females with embryos, but on three occasions females heavy with
eggs subsequently oviposited under small tiles when placed in a
terrarium. On September 10, 1961, a cluster of 10 eggs was found,
and on October 31, 1961, another cluster of the same number was
found. On March 2, 1962, 11 eggs were found under a tile. Both
a male and a female were found in company with these eggs, the
female having curved her body around them. The female remained
with the eggs until March 7, when they became covered with a
growth of fungus. All these eggs, which measured 6-8 mm. in
diameter, were laid directly on the ground as an oblong adhering
mass and not a short distance from each other as found by Niceforo
Marla (1960). Oviparity appears to be the normal reproductive
condition in the genus Bolitoglossa. Ovoviviparity in Central and
South American plethodontid salamanders has never been proven,
and all species for which there is reliable information have been
found to be oviparous (Brame and Wake, 1963).
232 HERPETOLOGICA Vol. 21, No. 3

Adult females with heavily yolked eggs and ready to breed have
been found in every month of the year except February, June, and
December, for which no data are available. Egg clutches have been
found in March, September, and October, and the clutch described
by Niceforo Marla (op. cit.) was encountered in November. Al-
though more observations would be desirable, even from these data
it can be seen that reproduction in B. adsp.ersa shows no seasonal
pattern and is apparently acyclic. There is no single egg-laying
season, and fecund females can be found in most months of the
year. Climatic conditions in the collecting area are relatively uni-
form, and a constant food supply is available to sustain continuous
reproduction. Under such conditions Neotropical salamander re-
productive patterns should be expected to be altered from the
seasonal cycles of North American temperate zone plethodontids
(see Organ, 1961; Highton, 1962; Martof, 1962).
Males.-Sixty-nine males of all ages, collected during 6 months
in 1961 and during 3 months in 1962, were examined to obtain the
following data. The testes of the smallest individuals possessed only
one lobe, the largest single-lobed testis measuring 8 mm. in in-
dividuals less than 40 mm. in snout-vent length. As the salamander
grows, the testes become elongate and clearly divided into two or
three lobes of unequal length. In some adult males, however, only
a single large lobe persisted, the largest single-lobed testis in the
sample measuring 13 mm. in an individual 42 mm. in snout-vent
length. In their sample Stebbins and Hendrickson (1959) found
that the smallest breeding male was 41.0 mm. in snout-vent length,
and we have found that males smaller than 39 mm. in snout-vent
length have small mental glands, slender sperm ducts and small,
single-lobed testes less than 8 mm. in length. In these males
spermatogenesis is only beginning, and they are not capable of
reproducing. Males less than 20 mm. in snout-vent length are
difficult to distinguish from females. In these the testes are
membranous and spermatogenesis has not begun. In all males
greater than 39 mm. in snout-vent length, the mental gland was
clearly seen, the central longitudinal duct was filled with sperm, and
the testes were single or bilobed. Only in one sexually mature male
(snout-vent length 47 mm.) was a small, posterior third lobe of the
testes present.
Histological examination of the testes of sexually mature males
indicates that structure and the spermatic cycle are very much as
those described by Humphrey (1922) for other urodeles. The
lobules of the elongated testes empty directly by very short ducts
into a central longitudinal duct. This duct receives mature sperm,
which are then transported through efferent tubules to the Wolffian
duct. There is no second longitudinal duct near the mesonephros as
has been found in other amphibia (Noble, 1931).
1965 REPRODUCTION IN A SALAMANDER 233

Each lobe of the testis contains numerous lobules, and the


reproductive cells of each lobule are in the same developmental
stage. Lobules of a given region of the testes likewise tend to be in
the same stage of spermatogenesis, with the developmental sequence
from anterior to posterior. The anterior end of a lobe contains lobules
in very early stages of spermatogenesis. i.e., containing spermato-
gonia or some primary spermatocytes and Sertoli cells. Posteriorly
the lobules are progressively in later stages of spermatogenesis,
and toward the middle of a lobe spermatids and mature sperm are
being produced by the lobules. At the posterior end of the lobe, the
lobules have vacuated their sperm and contain only some Sertoli
cells and spermatogonia.
Humphrey (1922) and Organ (1961) have established the
relationship between age of males and the number of lobes of the
testes in cyclic reproducing species of the plethodontid genus
Desmognathus. The smaller, younger males have one lobe per
testis and the larger, older males have two to five lobes, with a direct
relationship between the number of lobes per testis and the size
of the male. They were also able to assign a time interval between
the formation of successive lobes of the testis in species of this genus,
the males with the largest number of lobes having experienced the
greatest number of seasons of sexual activity. As B. adspersa is
apparently an acyclic species which breeds continuously, we could
not determine the time intervals between the formation of successive
lobes but were able to correlate the number of lobes per testis
with the size of males and the number of breeding seasons they had
experienced. As Humphrey (op. cit.) and Organ (op. cit.)
found in Desmognathus, we also found considerable variation in the
development and size of the lobes in males of B. adspersa, and all
lobes, whether small or large, were counted equally to avoid the
need for classifying the various sizes of lobes in males. The relation-
ship of the lobes of the testis to the size distribution of 58 males
of B. adspersa, which were collected in April and May, 1962, is given
in Figure 1. The size-frequency category based on one lobe per
testis is trimodal, suggesting that there are three age classes present:
yearlings or juvenile males, young adult sexually immature males,
and young adult sexually mature males. The size-frequency
category based on two lobes per testis is bimodal, suggesting that
there are two age classes, males in their second and third breeding
season. Males in the three-lobe category would be in at least their
fourth breeding season. It is not known if the same relationship
occurs in collections of males in the other months of the year
for which data are available, since sample size was too small for
analysis. However, as females are capable of laying eggs during
most months of the year, it would be expected that at least some
234 HERPETOLOGICA Vol. 21, No. 3

3-
JflI] 3 LOBES

5
:D
0 3
2 LOBES

Z 7-

5- LOBE
o1

20 25 30 35 40 45 50 55

SNOUT-VENT LENGTH (mm)


FIG. 1.-Relationship of snout-vent length and number of lobes of the
testis.

males are capable of breeding and others are preparing to breed at


any given time, irrespective of age and breeding season.
In studies of North American plethodontid salamanders, the age
and size of males at sexual maturity have been found to be somewhat
variable. Organ (1961) found the maturing age to be 3.5 years in
five species of the genus Desmognathus, but the maturing size
varies from 25 mm. snout-vent length in D. wrightii to 55 mm.
snout-vent length in D. quadramaculatus. In Leurognathus mar-
moratus males reach sexual maturity at 50 mm. snout-vent length
and at least at 2 years of age (Martof, 1962), and in Plethodon
welleri Thurow (1963) found that males mature at 30 mm. snout-
vent length at 3 years of age. In his study of geographic variation in
the life history of Plethodon glutinosus, Highton (1962) found that
the growth rate at northern latitudes was slower than in the south
because of hibernation and the subsequent decrease in activity
periods. Salamanders of northern populations mature at a larger
size (snout-vent length 53 mm.) and do not breed until 5 years
old, whereas those of southern populations breed at the age of 3 and
at a smaller size (snout-vent length 40 mm.). In Colombia B.
adspersa reaches sexual maturity at 39 mm. snout-vent length. If
growth rate is correlated with the length of the growing season, as
suggested by Highton (op. cit.), it would be expected that tropical
species would have rapid growth rates and accelerated reproductive
cycles. The age at which B. adspersa matures is not known, nor is it
known if males of this species reach sexual maturity and breed
immediately or if there is a gap between maturity and breeding.
It is likewise not known if breeding is continuous or seasonal in these
1965 REPRODUCTION IN A SALAMANDER 235

males. It would be expected, however, that individual breeding


periods, if such exist, would telescope and not be synchronous in
continually active salamanders, and that there would be an overlap
of age groups in the population at any given time. Additional
studies must be made at regular time intervals to answer these
questions.

SUMMARY
Field and laboratory studies of the plethodontid salamander
Bolitoglossa adspersa (Peters) at Bogota, Colombia, during 1961-
1962 present evidence that this species is oviparous and that re-
production is apparently acyclic. Fecund females and mature males
were found in 9 nonconsecutive months of the year. There is no
single egg-laying season, and females oviposited from 10-11 eggs
in March, September, October, and November, months for which
data were available.
All females larger than 45 mm. in snout-vent length were sexually
mature, irrespective of the month of capture, and there was no
correlation between the size of the female and the number of yolked
eggs, which averaged 10 in number in 44 adults of snout-vent length
45-66 mm.
Males larger than 39 mm. in snout-vent length were sexually
mature, and the number of lobes per testis varied from one to three.
A sample of 58 males collected in April and May, 1962, consisted of
six age groups as determined by the size of the male and the
number of lobes per testis, the oldest males being at least in their
fourth breeding season.
The acyclic reproductive pattern of B. adspersa is discussed in
relation to the cyclic behavior of temperate zone species.

LITERATURE CITED
BRAME, A. H., JR., AND D. B. WAKE. 1963. The salamanders of South
America. Los Angeles Co. Mus. Contr. in Sci., 69:5-72.
DUNN, E. R. 1944. Herpetology of the Bogota area. Rev. de la Acad.
Colomb. de Cien. Exact., Fisic. y Nat., 6:68-81.
EMPRESA DE ACUEDUCTO Y ALCANTARILLADO DE BOGOTA. 1961. Boletin
informativo, 1961:1-114.
HIGHTON, R. 1962. Geographic variation in the life history of the slimy
salamander. Copeia, 1962:597-613.
HOLDRIDGE, L. R. 1947. Determination of world plant formations from simple
climatic data. Science, 105:367-368.
HUMPHREY, R. R. 1922. The multiple testis in urodels. Biol. Bull., 43:45-67.
MARTOF, B. S. 1962. Some aspects of the life history and ecology of the
salamander Leurognathus. Amer. Mid. Nat., 67:1-35.
MILLER, A. H. 1959. Reproductive cycles in an equatorial sparrow. Proc.
Nat. Acad. Sci., 45:1095-1100.
NIc'FORO MARIA, HNO. 1960. Salamandras de la Familia Plethodontidae:
Hallazgo de los huevos de Bolitoglossa adspersa (Peters). Caldasia,
8:337-339.
236 HERPETOLOGICA Vol. 21, No. 3

NOBLE, G. K. 1931. The biology of the Amphibia. McGraw-Hill Book Co.,


Inc., New York. 577 pp.
ORGAN,J. A. 1961. Studies of the local distribution, life history and
population dynamics of the salamander genus Desmognathus in Virginia.
Ecol. Monogr., 31:189-220.
PETERS, W. 1863. Femere Mittheilungen fiber neue Batrachier. Monats.
Konig. Preuss Akad. Wissenschaft., Berlin, 1863:445-570.
POSADA, A. 1909. Estudios cientificos del Doctor Andres Posada con algunos
otros escritos suyos sobre diversos temas y con ilustraciones o grabados.
Medellin, Colombia. iii + 432 pp.
RuTHvEN, A. G. 1922. The amphibians and reptiles of the Sierra Nevada
de Santa Marta, Colombia. Univ. Mich. Mus. Zool. Misc. Publ., 8:1-69.
STEBBINS,R. C., AND J. R. HENDRICKSON. 1959. Field studies of amphibians
in Colombia, South America. Univ. Calif. Publ. in Zool., 56:497-540.
THUROW, G. R. 1963. Taxonomic and ecological notes on the salamander,
Plethodon welleri. Univ. Kans. Sci. Bull., 44:87-108.
Dept. of Biology, Yale University, New, Haven, Conn., and
University of the Andes, Bogotd, Colombia.