Notes on the ecology of the colubrid snake Leptodeira annulata in the Pantanal, Brazil

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278 Herpetological Review 38(3), 2007
its comparative cephalic anatomy and phylogenetic position in rela-
tion to Viperinae and Crotalinae. Field. Zool. 59:64–126.
MCDOWELL, S. B. 1987. Systematics. In R. A. Seigel, J. T. Collins, and S.
S. Novak. (eds.), Snakes: Ecology and Evolutionary Biology, pp. 3–
50. Macmillan, New York.
NIXON, K. C., J. M. CARPENTER, and D. W. STEVENSON. 2003. The PhyloCode
is fatally flawed, and the “Linnaean” system can easily be fixed. Botan.
Rev. 69:111–120.
OPPEL, M. 1811. Die Ordnungen, Familien, und Gattungen der Reptilien,
also Prodrom einer Naturgeschichte dersaelben. J. Lindauer, Munich.
POUGH, F. H., R. M. ANDREWS, J. E. CADLE, M. L. CRUMP, A. H. SAVITSKY,
AND K. D. WELLS. 2004. Herpetology. Pearson Prentice Hall, Upper
Saddle River, New Jersey.
ROMER, A. S. 1956. Osteology of the Reptiles. Univ. Chicago Press, Chi-
cago.
SMITH, M. A. 1939. A revision of the Acrochordinae (Snakes). Ann. Mag.
Natur. Hist. (London)(11)3:393–395.
STEBBINS, R. C. 2003. A Field Guide to Western Reptiles and Amphibians,
3rd ed. Houghton Mifflin Co., Boston.
ZAHER, H. 1999. Hemipenial morphology of the South American
xenodontine snakes, with a proposal for a monophyletic Xenodontinae
and a reappraisal of colubroid hemipenes. Bull. Am. Mus. Nat. Hist.
240:1–168.
ZUG, G. R., L. J. VITT, and J. P. CALDWELL. 2001. Herpetology: An Intro-
ductory Biology of Amphibians and Reptiles. Academic Press, New
York.
ARTICLES
Herpetological Review, 2007, 38(3), 278–280.
© 2007 by Society for the Study of Amphibians and Reptiles
Notes on the Ecology of the Colubrid Snake
Leptodeira annulata in the Pantanal, Brazil
ROBSON W. ÁVILA
Programa de Pós-Graduação em Biologia Geral e Aplicada
Departamento de Parasitologia, Instituto de Biociências, UNESP
Distrito de Rubião Jr., s/nº, CEP 18618-000, Botucatu, SP, Brazil
e-mail: robsonavila@gmail.com
and
DRAUSIO H. MORAIS
Programa de Pós-graduação em Ecologia e Conservação da Biodiversidade
Universidade Federal do Mato Grosso, Cuiabá, MT, Brazil
The ecology of many Neotropical snakes, especially Brazilian
species, is poorly known (Cadle and Greene 1993; Vitt 1996).
Moreover, published studies are often based on examination of
preserved specimens (Marques 1996) and therefore deal mainly
with diet and reproduction of particular species (e.g., Bizerra et al.
2005), whereas activity patterns, habitat use and thermal ecology
are infrequently reported (e.g., Oliveira and Martins 2001).
The Brazilian Pantanal is a low-lying floodplain covering an
area of some 140,000 km2, consisting of a mosaic of lakes, perma-
nent swamps and seasonally inundated grassy fields with elevated
patches bearing forest or cerrado vegetation (Ratter et al. 1988).
The Pantanal is located in the Western region of Brazil and east-
ern Bolivia and is characterized by mean annual temperature of
25ºC, and annual precipitation of 1100-1200 mm (Brasil 1997).
The Pantanal has low species richness relative to the Cerrado and
Amazon, but has some locally abundant snake species, thus facili-
tating studies of snake ecology (Strüssmann and Sazima 1993).
In spite of being one of the most abundant species in the Pantanal,
little is known about the biology of the cat-eyed snake Leptodeira
annulata in Brazil (Brasil 1997). Moreover, available data on L.
annulata are largely from the Amazon (Vitt 1996) and Chaco
(Lavilla and Scrocchi 1996) biomes. Here we present data on the
activity, thermal ecology and habitat use of Leptodeira annulata
in the Nhecolândia region, Pantanal, collected over five months.
MATERIALS AND METHODS
Study Site.—The study was conducted from February–May and
July 2005 in the vicinity of human habitation at the Nhumirim
Ranch (18º98'814"S; 56º61'900"W), Corumbá municipality, Mato
Grosso do Sul state, western Brazil. The region has an elevation
of around 100 m and consists of a mosaic of lakes, grassland, sa-
vanna (“cerrado” vegetation) and semideciduous forest (Ratter et
al. 1988).
One-hour searches were conducted on seven days each month,
between 1800 h and 2400 h, with two observers searching for
snakes in all accessible microhabitats. Each observed snake was
considered an activity record; thus, each individual could have
been observed more than once during the study. However, no snake
was counted more than one time in a day.
We marked all trees (N = 32) at the 4 ha study site and recorded
tree height (m) and diameter at breast height (mm). For each snake
observed we recorded the microhabitat (tree, ground, building).
When possible we caught the snake by hand and took the body,
substrate, and air temperature with a cloacal thermometer (Miller
and Weber Inc.). We considered snakes as active if they were
moving or otherwise observed outside of tree holes.
In the laboratory, we measured snout–vent length (SVL) to the
nearest cm using a measuring tape, tail length (TL) and head length
(HL) to the nearest mm with a digital caliper (Mitutoyo Corp.),
and mass to the nearest g using a Pesola scale. The snakes were
sexed by probing. We then marked the individuals with ventral
scale clips and released them at the site of capture.
To evaluate sexual size dimorphism we used analysis of covari-
ance (ANCOVA) on tail length, head length, head width, and body
mass with SVL as covariate and sex as a factor. Differences in
SVL between sexes were tested by t-test. We also performed a
Pearson’s correlation between body vs. air and substrate tempera-
ture.
RESULTS
We marked 19 (10F: 9M) Leptodeira annulata. Female SVL
(481.60 ± 54.41 mm) was not significantly different from male
SVL (528.44 ± 99 mm; t = 1.277, P = 0.218). Females also had
significantly head width and were heavier than males (ANCOVA
F = 7.097, P = 0.017, r2 = 0.358; F = 12.434, P = 0.003, r2 = 0.470;
Table 1).
Observed activity of L. annulata (N = 81) occurred mainly be-
tween 1830 h and 2330 h, with a peak from 1930 h to 2230 h (Fig.
1). Around 1830 h snakes were observed emerging from tree holes.
We found snakes in Acuri palms (Attalea phalerata) most often

Herpetological Review 38(3), 2007 279
(63 %), followed by fig trees (Ficus calyptroceras; 23 %) and an
unidentified tree species of Leguminosae (6%; Fig. 2). Only 3%
of detections were of snakes on the ground. Trees where snakes
were located averaged 0.80 ± 0.83 m diameter and snake height
on the tree averaged 1.65 ± 0.65 m.
Body temperature averaged 26.8 ± 2.9ºC (range 22.5–31.4ºC,
N = 20 including one recapture) and was positively correlated with
substrate (r = 0.92, P < 0.001) and air temperature (r = 0.88, P <
0.001). There was no difference in body temperature between sexes
(t = 0.46, P = 0.81).
DISCUSSION
Although we conducted our investigation in close proximity to
human habitations, we did observe several L. annulata in more
pristine environments, indicating that this species occurs in a va-
riety of habitats.
The observed activity of L. annulata, a primarily anuran-eating
snake (Lavilla and Scrocchi 1986) seems to coincide with am-
phibian activity, as suggested by Vitt (1996). At our study sites,
we observed Scinax acuminatus and Scinax nasicus during obser-
vations, including in the same tree with L. annulata. The activity
of these amphibians is, in general, restricted to 4–6 h after dark
(Cardoso and Martins 1987), which may explain the reduced ac-
tivity of L. annulata after 2230 h. Our sampling efforts however
ceased at 2400h so we cannot say anything about snake activity
after midnight.
Although snakes may regulate their body tempera-
ture both behaviorally and physiologically (Peterson
et al. 1993), the thermal environment (e.g., air and
substrate temperature) can influence activity patterns,
even in tropical nocturnal snakes (Shine and Madsen
1996). Thus, the observed low snake activity in late
evening could conceivably be due to the drop in am-
bient temperature (Shine and Madsen 1996), rather
than due to reduced prey availability as discussed
above.
In the Pantanal, L. annulata largely used arboreal
habitats, in contrast to previous findings (Vitt 1996;
Martins and Oliveira 1998). It is notable that the
Pantanal has more open habitats (even in forests) than the Ama-
zon, but even so, fewer snakes were found on the ground in the
Pantanal. Habitat openness or vegetation cover may affect vulner-
ability of reptiles to visual predators (Stuart-Fox and Ord 2004).
Thus, predation pressure may cause greater use of vegetation and
reduced use of open habitats (Watts 1991). Alternatively, taxo-
nomic differences may account for the observed differences, since
Vitt (1996) studied the biology of L. a. annulata, while we studied
the subspecies L. a. pulchriceps. It is also possible that our detec-
tion probability for terrestrial snakes was lower than for arboreal
snakes.
The use of Acuri palms by L. annulata may be due to either the
ready availability of crevices and holes in the trunk (provided also
by F. calyptroceras in the study area) or the abundance of this
tree, which represents 44% of individual trees on the study site. In
pristine areas of the Pantanal at Nhumirim Ranch, Acuri palms
are the most common tree species in forests (Ratter et al. 1988).
Due to the short duration of our study, further work is needed to
understand seasonal variation in body temperatures, activity and
habitat use. The Pantanal has a highly seasonal climate with rain-
fall restricted to November–March and a flood season from April-
August (Junk and Cunha 2005) and these cycles may affect snake
biology.
Although apparently abundant, Leptodeira annulata is vulner-
able to reductions in population size, due to indiscriminate killing
of individuals. During our study, two individuals were known to
have been killed by local inhabitants. Humans may have a natural
FIG. 1. Observed activity patterns (bars) and body temperatures (line)
of Leptodeira annulata in the Pantanal, Brazil. FIG. 2. Observed habitat use of Leptodeira annulata in the Pantanal,
Brazil, based on 81 observations of active snakes.
TABLE 1. Summary of statistics on sexual size dimorphism of Leptodeira annulata in
the Pantanal, Brazil. Test statistics for head length (HL), head width (HW), tail length
(TL) and body mass (MASS) are from ANCOVAs adjusting for SVL, and thus refer to
intersexual differences in size.
Males (N = 9) Females (N = 10) Statistical Results
SVL 528.44 ± 99.00 481.60 ± 54.41 t = 1.277, df = 1, P = 0.218
HL 14.12 ± 1.27 14.64 ± 1.69 F = 4.434, P = 0.054
HW 10.15 ± 1.77 11.15 ± 1.93 F = 7.097, P = 0.017
TL 140.11 ± 17.14 139.20 ± 18.56 F = 0.869, P = 0.365
MASS 29.91 ± 7.13 33.70 ± 8.11 F = 12.434, P = 0.003

280 Herpetological Review 38(3), 2007
fear of snakes (Greene 1997) and this species in particular is often
confused with a venomous snake (the pitviper Bothrops
mattogrossensis; Lavilla and Sccrochi 1986; pers. obs). Educa-
tional programs, especially for children, are necessary in the re-
gion to prevent indiscriminate killing of snakes.
Acknowledgments.—We thank Björn Lardner and one anonymous re-
viewer for comments on a previous version of this manuscript. We are
grateful to Christine Strüssmann and Vanda L. Ferreira for making this
work possible. We also thank Tami Mott for suggestions and corrections
on the English version of this manuscript.
LITERATURE CITED
BIZERRA, A., O. A. V. MARQUES, AND I. SAZIMA. 2005. Reproduction and
feeding of the colubrid snake Tomodon dorsatus from south-eastern
Brazil. Amphibia-Reptilia 26:33–38.
BRASIL (MINISTÉRIO DO MEIO AMBIENTE DOS RECURSOS HÍDRICOS E DA
AMAZÔNIA LEGAL). 1997. Plano de Conservação da Bacia do Alto
Paraguai – PCBAP. Diagnóstico dos meios fisicos e biótico. V.II, t.III.
Meio biótico. Brasília: MMA/PNMA, 433 pp.
CADLE, J. E., AND H. W. GREENE. 1993. Phylogenetic patterns, biogeogra-
phy, and the ecological structure of neotropical snake assemblages. In
R. E. Ricklefs and D. Schluter (eds.), Species Diversity in Ecological
Communities: Historical and Geographical Perspectives, pp. 281–293.
Univ. Chicago Press, Chicago.
CARDOSO, A. J., AND J. E. MARTINS. 1987. Diversidade de anuros durante o
turno de vocalizações, em comunidade neotropical. Pap. Avul. Zool.
36:279–285.
GREENE, H. W. 1997. Snakes: The Evolution of Mystery in Nature. Univ.
California Press, Berkeley.
JUNK, W. J., AND C. N. CUNHA. 2005. Pantanal: a large South American
wetland at a crossroads. Ecol. Engin. 24:391–401.
LAVILLA, E. O., AND G. J. SCROCCHI. 1986. Leptodeira annulata pulchriceps
Duellman. Rev. Franc. d’Aquar. 309:1–2.
MARTINS, M., AND M. E. OLIVEIRA. 1998. Natural history of snakes in for-
ests of the Manaus region, Central Amazonia, Brazil. Herp. Nat. Hist.
6:78–150.
MARQUES, O. A. V. 1996. Reproduction, seasonal activity and growth of
the coral snake, Micrurus corallinus (Elapidae), in the southeastern
Atlantic forest in Brazil. Amphibia-Reptilia 17:277–285.
OLIVEIRA, M. E., AND M. MARTINS. 2001. When and where to find a pitviper:
Activity patterns and habitat use of the lancehead, Bothrops atrox, in
Central Amazonia, Brazil. Herpetol. Nat. Hist. 8:101–109.
PETERSON, C. R., A. R. GIBSON, AND M. E. DORCAS. 1993. Snake thermal
ecology: the causes and consequences of body temperatures variation.
In R. A. Seigel and J. T. Collins (eds.), Snakes: Ecology & Behavior.
pp. 49–78. McGraw-Hill, New York.
RATTER, J. A., A. POTT, V. J. POTT, C. N. CUNHA, AND M. HARIDASSAN.
1988. Observations on woody vegetation types in the Pantanal and
around Corumbá. Notes Royal Bot. Garden Edinburgh 45:503–525.
SHINE, R. AND T. M ADSEN. 1996. Is thermoregulation unimportant for most
reptiles? An example using water pythons (Liasis fuscus) in tropical
Australia. Phys. Zool. 69:252–269.
STRÜSSMANN, C., AND I. SAZIMA. 1993. The snake assemblage of the Pantanal
at Poconé, Western Brazil: Faunal Composition and Ecological Sum-
mary. Studies on Neotropical Fauna and Environment 28:157–168.
STUART-FOX, D. M., AND T. J. ORD. 2004. Sexual selection, natural selec-
tion and the evolution of dimorphic coloration and ornamentation in
agamid lizards. Proc. Royal Soc. London 271:2249–2255.
VITT, L. J. 1996. Ecological observations on the tropical colubrid snake
Leptodeira annulata. Herpetol. Nat. Hist. 4:69–76.
WATTS, B. D. 1991. Effects of predation risk on distribution within and
between habitats in Savannah sparrows. Ecology 72:1515–1519.
Herpetological Review, 2007, 38(3), 280–282
© 2007 by Society for the Study of Amphibians and Reptiles
A Previously Undescribed Bone in the Snout of the
Brown Watersnake, Nerodia taxispilota
DOUGLAS A. ROSSMAN1
and
JEFF BOUNDY2
Museum of Natural Science, Louisiana State University
Baton Rouge, Louisiana 70803, USA
Current addresses:
1Department of Biology, Luther College
Decorah, Iowa 52101, USA
e-mail: rossmado@luther.edu
2Louisiana Department of Wildlife and Fisheries
P. O. Box 98000, Baton Rouge, Louisiana 70898-9000, USA
e-mail: jboundy@wlf.louisiana.gov
While examining more than 400 skulls of thamnophiine snakes
currently assigned to the genera Nerodia and Thamnophis, we
encountered a bone in the snout region of most of the specimens
of the Brown Watersnake, Nerodia taxispilota, that was not present
in any other species we examined—nor are we aware of a compa-
rable osseous element being described in any other snake species.
Here we describe and illustrate this neomorph and speculate about
its possible function.
The neomorph, which we propose to call the postnasal strut,
is present in ten of the 16 skulls (62.5%) of Nerodia taxispilota we
examined (LSUMZ 10569, 16849, 20555, 21062, 24363, 28213–
214, 34183, 43155, 43455). The skulls range in length from 22.5–
33.1 mm, and represent both sexes (5 females, 4 males, 1 undeter-
mined). Six specimens are from Florida, two from North Caro-
lina, and two from undetermined localities. The six skulls that lack
the postnasal strut (LSUMZ 12876, 16851, 16935, 391194, 43159,
43454) range in length from 19.3–35.5 mm, and also represent
both sexes (4 females, 2 males). Four are from Florida, two from
North Carolina.
The following description is based on the skull of LSUMZ
34183, a large (1029 mm snout–vent length, 33.1 mm skull length)
female from Lake Newnan, Alachua Co., Florida. The faintly
grooved dorsal surface of the narrow postnasal strut lies essen-
tially in the same horizontal plane as the dorsal laminae of the
nasal bones and the dorsal surface of the frontals, hence the strut
is readily apparent when the dorsal aspect of the snout region is
viewed (Fig. 1, upper). The strut is relatively long, its dorsal sur-
face being nearly 70% as long as the dorsal laminae of the nasals
(nearly 60% in LSUMZ 20555; 29.5 mm skull length). The
anterodorsal tip of the strut is inserted between the posteromedial
ends of the nasals. The posterodorsal tip of the strut is inserted
between the anteromedial ends of the frontals, which are deflected
laterally to accommodate it, but they are not deflected in snakes
lacking the strut (Fig. 1, lower).
In order to better determine the relationship of the strut to the
bones around it, we soaked the skull in water for several hours to
loosen the dried soft tissue that remained after the initial cleaning
by dermestid beetles. Further cleaning was then accomplished by
hand-picking tissue with a small needle-nosed forceps. Finally,
the entire nasal component was removed when it was discovered