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Reproduction in the Yellow-spotted night lizard, Lepidophyma flavimaculatum (Squamata, Xantusiidae), from Costa Rica

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The yellow-spotted night lizard Lepidophyma flavimaculatum from Costa Rica is histologically examined to explore their reproductive behavior. A total of 60 Lepidophyma flavimaculatum including 26 adult females, six adult males, and 15 neonates were analyzed from the herpetology collection of the Natural History Museum of Los Angeles County between 1961 and 1992. The left testis was removed from males and the left ovary was removed from females for histological analysis. An unpaired t-test was employed to compare Lepidophyma flavimaculatum male and female mean body sizes, while chi-square test was used to compare ratios of males versus females. The sex ratio of six adult males and 26 adult females was comprehensively different from the expected 50:50 ratio, suggesting that some of the Lepidophyma flavimaculatum females from Costa Rica are parthenogenetic. Lepidophyma flavimaculatum may comprise sexually and parthenogenetic populations, mating in late summer, with females producing in spring or over the year.
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Phyllomedusa
- 8(1), July 2009
59
Reproduction in the Yellow-spotted night lizard,
Lepidophyma flavimaculatum (Squamata,
Xantusiidae), from Costa Rica
Stephen R. Goldberg
Department of Biology, Whittier College, PO Box 634, Whittier, California 90608, USA - E-mail: sgoldberg@whittier.edu.
Received 7 April 2009.
Accepted 15 May 2009.
Distributed July 2009.
Phyllomedusa 8(1):59-62, 2009
© 2009 Departamento de Ciências Biológicas - ESALQ - USP
ISSN 1519-1397
Lepidophyma flavimaculatum Duméril, 1851
is a secretive inhabitant of undisturbed moist
and wet forests, typically found under fallen
logs in the humid lowlands from Oaxaca and
southern Veracruz, Mexico to central Panama
(Savage 2002). Like other xantusiids L.
flavimaculatum is viviparous (Goin et al. 1978).
Telford and Campbell (1970) reported that L.
flavimaculatum populations from central
Panama were all-female, however, Bezy (1989)
concluded that L. flavimaculatum populations
from Honduras and northward included 41%
(30/73) males and were probably bisexual. The
purpose of this note is to add information on
reproduction of L. flavimaculatum from a
histological examination of gonadal material
from museum specimens from five Provinces of
Costa Rica. The first information on the
testicular cycle is presented. Minimum sizes for
reproduction of males and females are given.
Keywords: Squamata, Xantusiidae, Lepidophyma flavimaculatum, reproduction, Costa
Rica.
Palavras-chave: Squamata, Xantusiidae, Lepidophyma flavimaculatum, reprodução, Costa Rica.
A total of 60 L. flavimaculatum from Costa
Rica including 26 adult females (mean snout
vent length, SVL = 85.0 mm ± 6.6 SD,
range = 73-96; six adult males, mean
SVL = 87.5 mm ± 7.4 SD, range = 77-98 mm;
13 juveniles, mean SVL = 63.5 ± 4.0 SD. range
= 58-71 mm and 15 neonates, mean SVL = 36.3
mm ± 3.0 SD, range = 30-39 mm) were
examined from the herpetology collection of the
Natural History Museum of Los Angeles County
(LACM), Los Angeles, California (Appendix I).
Lizards were collected 1961 to 1992.
The left testis was removed from males and
the left ovary was removed from females for
histological examination. Enlarged follicles
(> 4 mm length) were counted. Tissues were
embedded in paraffin and cut into sections of
5 μm. Slides were stained with Harris
hematoxylin followed by eosin counterstain
(Presnell and Schreibman 1997). Slides of testes
were examined to determine the stage of the
spermatogenic cycle. Slides of ovaries were
examined for the presence of yolk deposition or
corpora lutea. Histology slides were deposited
in LACM. An unpaired t-test was used to
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60
compare L. flavimaculatum male and female
mean body sizes and chi-square test was used
to compare ratios of males versus females
(Instat, vers. 3.0b, Graphpad Software, San
Diego, CA).
No significant size difference was detected
between L. flavimaculatum males and females
(unpaired t-test, t = 0.82, df = 30, P = 0.42). Two
stages were present in the testicular cycle of L.
flavimaculatum (Table 1). (1) Recrudescence:
occurs prior to the onset of spermiogenesis
(sperm formation). Secondary spermatocytes
and spermatocytes are the predominant cells; (2)
Spermiogenesis in which the seminiferous
tubules are lined by clusters of spermatozoa
and/or metamorphosing spermatids. The
smallest reproductively active male (in
recrudescence) measured 77 mm SVL (LACM
131097) and was from August. My samples are
too small to completely elucidate the seasonal
testicular cycle of L. flavimaculatum as one
each spermiogenic male came from Limón and
Heredia Provinces, nevertheless these
preliminary data indicated a late-summer to
autumn period of sperm formation. This appears
similar to the timing of the testicular cycles of
other species of Lepidophyma: L. gaigae
(Goldberg and Camarillo-Rangel 2003), L.
sylvaticum (Ramírez-Hernández 2003, Ramírez-
Bautista et al. 2008) and L. pajapanensis
(Méndez-de La Cruz et al. 1999) in which
males are reproductively active in summer to
autumn. It thus appears from my results and
other studies on congeneric species that
Lepidophyma males undergo a late-summer to
autumn period of sperm formation This timing
differs from males of the xantusiid lizards,
Xantusia vigilis (Zweifel and Lowe 1966) a
desert species, and Xantusia riversiana
(Goldberg and Bezy 1974), an island species in
which mating occurs in spring.
Yolk deposition in L. flavimaculatum
commences in spring and continues into late
summer (Table 2) when males are producing
sperm. Twelve of the August females in Table
2 were from the same locality, Hacienda
Tapezco, 29 km W Tortugero in Límon
Province. Seven of these exhibited quiescent
ovaries with no yolk deposition. Five were in
early yolk deposition. One female (LACM
159177) from Heredia Province collected in
January contained 4 enlarged follicles > 5 mm
diameter suggesting young would have been
produced late that spring. This is the only clutch
I can report. Lepidophyma flavimaculatum from
Panama produce 4-8 young that measure 35-38
mm SVL (Telford and Campbell 1970, Alvarez
del Toro 1982). This is in agreement with
Telford and Campbell (1970) who reported L.
flavimaculatum in Panama are born in late
April-early June around the start of the wet
season and June or July in Chiapas, Mexico
(Alvarez del Toro 1982). This occurs in other
species of Lepidophyma which also produce
young in spring (L. tuxtlae Castillo-Cerón and
López-González, 1990; L. lowei Camarillo R.,
1999; L. sylvaticum Ramírez-Hernández, 2003;
L. gaigae Goldberg and Camarillo-Rangel,
2003). The smallest reproductively active
females of L. flavimaculatum (both in early yolk
deposition) measured 79 mm SVL (LACM
128547, 131092) and were from September and
August, respectively. In Costa Rica, lizards of
neonate size were collected in May to
September.
The sex ratio of six adult males and 26 adult
females was significantly different from the
expected 50:50 ratio (chi squared = 12.5, df =
1, P = 0.0004). This may suggest that at least
some of the L. flavimaculatum females from
Costa Rica are parthenogenetic. My findings of
Goldberg
Table 1 - Monthly stages in the testicular cycle of six
Lepidophyma flavimaculatum from Costa Rica.
Month nRecrudescent Spermiogenesis
June 1 1 0
July 1 1 0
August 3 2 1
October 1 0 1
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61
a reduced frequency of males in Costa Rica
suggests either a patchwork of parthenogenetic
and sexual populations or replacement of sexual
populations by parthenogentic populations.
Similar sex ratio bias toward females has been
reported for L. flavimaculatum in Panama
(Telford and Campbell 1970), L. reticulatum
(Bezy 1989) and L. tuxtlae from Veracruz,
Mexico (Castillo-Cerón and López González
1990).
The presence of 15/23 (65%) non-
reproductive females (no yolk deposition) of
adult size (May-September) during which time
other L. flavimaculatum females are depositing
yolk indicates only a portion of the female
population reproduces each year. This was
also reported in X. riversiana (Goldberg and
Bezy 1974) and also occurs in Xenosaurus
grandis in Mexico (Ballinger et al. 2000),
but is more typical of lizards living in very
harsh environments (Cree and Guillette Jr.
1995, Boretto and Ibargüengoytía 2006,
Ibargüengoytia and Casalins 2007).
Utilization of museum specimens to gather
reproductive data is becoming increasingly
important as it is very difficult to obtain
permission to collect monthly samples of native
populations from the same locality. This is
particularly true for secretive species like L.
flavimaculatum, collection of which, results in
habitat destruction. Also, localized variations in
the reproductive cycle will likely not be
Table 2 - Monthly stages in the ovarian cycle of 26 Lepidophyma flavimaculatum from Costa Rica.
Month nNo yolk deposition Early yolk deposition Follicles > 4 mm
January 2 1 0 1
March 1 1 0 0
April 1 1 0 0
May 4 3 1 0
July-August 1 0 1 0
August 12 7 5 0
September 5 4 1 0
detected from examination of museum
specimens since the investigator must work with
available materials.
In summary, L. flavimaculatum in Costa
Rica may consist of a mixture of sexually
reproducing and parthenogenetic populations
(based on female-biased sex ratios), mating
occurs in late summer, females produce live
young in late spring at the beginning of the wet
season, and only a portion of females produce
offspring in a given year. This reproductive
cycle is similar to that in other tropical
xantusiids.
Acknowledgements
I thank Christine Thacker (LACM) for
permission to examine specimens. Some L.
flavimaculatum are part of the CRE (= Costa
Rica Expeditions) collection donated to LACM
by Jay M. Savage in 1998.
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Appendix I Lepidophyma flavimaculatum from Costa Rica (by province) examined from
the herpetology collection of LACM.
Alajuela: 114858, Guanacaste: 137449,
159156, Heredia: 128538, 128539, 128541,
128547, 128549, 128555, 128556, 128558,
159146, 159150, 159152, 159155, 159158,
159159, 159168, 159177, 159179-159181,
Limón: 131086-131088, 131092-131102,
131104, 131108-131111, 132392, 159153,
159161, 159163, 159164, Puntarenas:
72323, 76161-76169, 106794, 159140-
159142.
Goldberg
... It appears that the basal branch in the Xantusiidae is comprised of the smallest species, the Cuba Night Lizard (Cricosaura typica, maximum SVL 38.9 mm, Fong et al. 1999), which has been reported to lay a single egg (Moreno 1987). The closest relative of Xantusia is Lepidophyma (tropical night lizards) with most species having a large body and litter sizes (Méndez-de la Cruz et al. 1999, Bezy and Camarillo 2002, Goldberg 2009). Within Xantusia, studies of DNA sequences (Sinclair et al. 2004;Noonan et al. 2013) differ somewhat regarding the phylogenetic placement of the giant Island Night Lizard (Figs. 2, 4). ...
... We then measured snout-vent length (SVL) with a digital caliper (± 0.01 mm) and sexed them by the hemipenal eversion technique (Harlow, 1996). For laboratory tests, we only included adult individuals: L. flavimaculatum (77 mm; Goldberg, 2009); L. gaigeae (49 mm; Goldberg and Camarillo-Rangel, 2003); L. pajapanense (66 mm; Méndez-de la Cruz et al., 1999); L. sylvaticum (55 mm; Ramírez-Bautista et al., 2008); L. tuxtlae (50 mm; Greene, 1970). As there are no available data on the reproductive biology for L. smithii, we considered for this lizard the average size to sexual maturity for the other species studied (59.4 mm SVL). ...
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