Serpentes - FRANÇA2006

South American Journal of Herpetology, 1(1), 2006, 25-36
© 2006 Brazilian Society of Herpetology
THE CONSERVATION STATUS OF SNAKES IN CENTRAL BRAZIL
FREDERICO G. R. FRANÇA1,3 AND ALEXANDRE F. B. ARAÚJO2
1
Programa de pós-graduação em Ecologia, Departamento de Ecologia,
Universidade de Brasília, 70910-900, Brasília, Brasil. E-mail: [email protected]
2
Departamento de Biologia Animal, Universidade Federal Rural do Rio de Janeiro, 23890-000,
Seropédica, Rio de Janeiro, Brasil. E-mail: [email protected]
3
Corresponding author.
ABSTRACT: We assessed the conservation status of 61 species from a central Brazilian snake assemblage by ranking species according
to their vulnerability to ten threat factors that are thought to influence the survival of snake populations. The anomalepidid snake
Liotyphlops ternetzii whereas the species with the lowest risk and the colubrid Drymoluber brazili was the most threatened. Less
than 15% of the Distrito Federal snake fauna was considered free from any threat. The natural-history of the species, its geographic
distribution, and human attitudes were important factors in determining the levels of threat for central Brazilian snakes. Principal
Component and Cluster analyses were used to classify species into vulnerability groups that were based on sharing similar threat
factors. Thirteen groups were identified which classified species in categories ranging from no risk to threatened. Within Brazil,
status assessments of additional snake assemblages in other biomes would be useful in generating a comprehensive conservation
plan for the country.
KEY WORDS: Snakes, Central Brazil, Distrito Federal, Conservation Status, Cerrado.
INTRODUCTION
Snakes have recently been propelled into a new position as ‘model organisms’ in ecological research, as
evidenced by the increasing number of publications
on snake ecology (Shine and Bonnet 2000). However,
research related to snake conservation is still lacking
and the few existing studies have dealt primarily with
species that are rare or habitat specialists (Seigel, 1986;
Webb and Shine, 1997; Daltry et al., 2001). Brazil has
one of the highest diversities of snake species in the
world, but snake conservation efforts have been restricted to insular species (Duarte et al., 1995; Marques
et al., 2002) and to controlling exotic species (Eterovic and Duarte, 2002). Snake conservation efforts are
primarily hindered by the lack of basic natural history
information for most species, which is essential if one
is to assess species-specific threats (Dodd, 2001a).
Methods for developing management strategies for
snake conservation are scarce. Dodd (2001a) proposed
that the conservation status of snakes should be based
on factors that threaten population viability, and a combined score of these factors should be used to identify
candidate taxa and set priorities for further research
and management. However, few studies have been able
to test the vulnerability of snake species to threat factors (Fillipi and Luiselli, 2000; Reed and Shine, 2002).
Snake population declines can be related to lifehistory characteristics such as body size, reproductive
potential, aggregation tendency and foraging; or can
be related to distribution factors such as habitat occupation or use of altered habitats. Thus, not all species
are influenced equally by certain factors (Dodd, 2001a;
Fillipi and Luiselli, 2000).
Herein, we use the method proposed by Fillipi and
Luiselli (2000) along with data on natural history, distribution, and other factors to evaluate the conservation status of a snake assemblage in Distrito Federal,
Brazil. The Distrito Federal represents an important
core region of Cerrado in central Brazil (Werthein
et al., 2000). The Cerrado covers approximately onequarter of Brazil’s land surface and because of intense
habitat alteration and the accelerated pace of destruction, it has recently been listed as one of the most threatened regions of the world (Oliveira and Marquis, 2002;
Myers et al., 2000).
MATERIALS AND METHODS
Study Area
The Distrito Federal of Brazil covers approximately
5,814 km2 of Cerrado. The region is a mosaic of vegetation types with habitats ranging from interfluvial
open areas (campos and cerrados) to forest formations
(gallery forests). Other typical Cerrado formations
found in the study area include humid grasslands and
veredas (Eiten, 1994). The region consists of three
26
Conservation of snakes in Central Brazil
major hydrogeographic basins: the Paraná River, the
San Francisco River, and the Tocantins River basins
(Pinto, 1994). The climate is type Aw in the Köppen
classification, receiving annually 1500-2000 mm of a
highly predictable and strongly seasonal precipitation,
almost entirely restricted to the period from October
to April (Nimer, 1989).
Threat Factors
Ten factors known to influence survival of snake
populations in Distrito Federal were chosen. Some
categories are the same as those used by Fillipi and
Luiselli (2000). For each species, the factors were
classified into four categories ranging from 0 (least
risk) to 3 (highest risk). Factors can be divided into
two groups: 1) factors directly related to natural-history of the species (factors 1 to 5) and 2) factors not
directly related to natural-history of the species, but
related to geographic distribution and human attitudes (factors 6 to 10). Category scores for threat
factors for each snake species were based on published average conditions for snakes in the wild, or
on unpublished data and personal experience of the
authors (For review see França, 2003; França and
Araújo, in press). Threat factors and categories were
as follows:
1. Body size (BS): Smaller species are less vulnerable
to the direct threats of removal or death from humans;
0 = < 50 cm length; 1 = 51-100 cm length;
2 = 101-150 cm length; 3 = > 150 cm length.
2. Litter size (LS): Eggs or younglings; 0 = > 15;
1 = 15-11; 2 = 10-5; 3 = < 5.
3. Dietary breadth (DT): Based on taxonomic order
level of prey taken and percentage of main prey in the
diet; 0 = generalist, main prey item < 30% of diet; 1 =
low specialization, main prey 31-50% of diet; 2 = moderate specialization, main prey 51-70% of diet; 3 =
highly specialized, main prey > 70% of diet.
4. Habitat breadth (HB): Based on occurrence in four
Cerrado habitat types: campo, cerrado, mata, and water (river, pond and/or vereda); 0 = species found in
all four habitats; 1 = species found in three habitats;
2 = species found in two habitats; 3 = species found in
only one habitat.
5. Habits (HT): Based on the type of general habits
exhibited by the snakes in the wild; 0 = fossorial; 1 =
cryptozoic or aquatic; 2 = arboreal or semi-arboreal;
3 = terrestrial.
6. Distribution breadth in Distrito Federal (DB): 0 =
present in > 80% of the region; 1 = present in 51-80%;
2 = present in 21-50%; 3 = present in < 20% of the
region.
7. Adaptability to altered habitats (AH): 0 = extremely adaptable species (found even in urban centers); 1 =
adaptable species (found also in suburbia if small native patches are available); 2 = scarcely adaptable species (found at best in moderately sized natural habitats); 3 = inadaptable species (found only in large areas of natural habitat).
8. Rarity in Distrito Federal (RR): Based on the percentage of specimens found in DF; 0 = > 10% of total
specimens; 1 = 6-10%; 2 = 2-6%; 3 = < 2%.
9. Species color (CL): 0 = only one solid color, other
than red; 1 = with stripes or dots, but not like pitvipers
or Micrurus species; 2 = blotched pattern like pitvipers; 3 = coral snake triads or red-colored snakes. Species with ontogenetic color variation in life (Boiruna
or Clelia species) or more than one color pattern (Waglerophis) were ranked with lesser score.
10. Road mortality (RM): 0 = never found dead on
roads in Distrito Federal; 1 = < 10% of total species
found dead on roads; 2 = 10-20%; 3 = > 20%.
Statistical Analysis
Mean scores for the 10 factors were used to determine threat levels for every snake species in the Distrito Federal as proposed by Filippi and Luiselli (2000).
Mean scores < 1.2 indicate species with low risk, mean
scores between 1.3 and 1.9 indicate a species vulnerable to decline, and mean scores > 1.9 indicate a seriously threatened species.
We used a t test to determine if factors related to
the natural-history of species and factors related to geographic distribution and human attitudes differed in
importance. Differences in vulnerability, based on
mean scores, among phylogenetic groups of snake species were analyzed using a Kruskal Wallis test (Zar,
França, F. G. R. and Araújo, A. F. B.
RESULTS
Analysis of scores for the threatening factors
Category scores and mean scores for the 10 threat
factors for the 61 snake species in Distrito Federal are
presented in Table 1. The summary of those data are
presented in Table 2. Based on the classification of
mean scores, nine snake species (14.8%) are at low
risk of decline, 34 species (55.7%) are vulnerable to
decline, and 18 species (29.5%) are threatened (Table 1).
Mean scores for species ranged from 0.5 for Liotyphlops ternetzii (less vulnerable) to 2.3 for Drymoluber brazili (more threatened). For the phylogenetic
groups, the mean score was highest in Colubrinae
(x = 1.83 ± 0.31) and lowest in Scolecophidia (Anomalepididae + Leptotyphlopidae) (x = 1.00 ± 0.71).
However, there were no significant differences among
means of phylogenetic groups (Kruskal-Wallis ANOVA: H = 9.41; d.f. = 6; p = 0.15).
Mean scores for the 10 threat factors were highest
for the dietary breadth (2.26) and snake habits (2.03),
and lowest for road mortality (0.90) and species color
(1.20). Nevertheless, there was no significant difference between mean scores of factors related to natural-history of the species and factors related to geographic distribution and humans attitudes (t test = 1.6;
d.f. = 8; p = 0.14).
Principal Component and Cluster Analyses
The model proposed by Filippi and Luiselli (2000)
applying PCA to a data matrix allows classification
of species into threat groups. All these groups were
not easily recognized by PCA biplot graph (Fig. 1).
Additionally, we used a Cluster analyses to detect the
following 13 groups of snakes in Distrito Federal
(Fig. 2):
1: Snakes with small body size, black coloration, with
wide distribution in DF and adapted to altered habitats (low vulnerability). Liotyphlops ternetzii.
2: False-coral snakes with small body size, wide distribution in DF, fossorial habits and diet specialists
(low vulnerability). Apostolepis assimilis, Tantilla melanocephala.
3: False-coral snakes, terrestrial and nocturnal, with
medium to high litter size, wide distribution in DF and
high mortality on the roads of DF (vulnerable). Oxyrhopus guibei, Oxyrhopus rhombifer, Oxyrhopus
trigeminus.
2
55
20
23
1
44
1
44
0
41
24
58
11
52
42
4
18
48
-1
9
49
21
25
35
22
12 40
43
59
31
13
30
5750
16
56 60
17543051 37
36
1032
45
53
2
29
8
2734
33
61
26
19
39
Factor 2
1999). Principal Component Analysis and Cluster
Analysis were used to classify snake species in terms
of their relative similarity to particular threats. The
PCA was run using the factor analysis model with
Varimax orthogonal rotation (Tabachnik and Fidell,
2001). The Cluster Analysis was run using the UPGMA cluster method and Pearson correlation coefficient
(Valentin, 2000). All analyses were performed in SPSS
10.0, with a set at 5%.
27
46
47
3
14
7
-2
15
6
28
5
-3
-2
-1
0
1
2
Factor 1
Figure 1: Plot of factor scores from principal components for snake
species of Distrito Federal, showing some clearly threatned groups.
The species are: 1) Liotyphlops ternetzii; 2) Leptotyphlops koppesi;
3) Boa constrictor; 4) Epicrates cenchria; 5) Eunectes murinus;
6) Bothrops moojeni; 7) B. neuwiedi; 8) B. itapetiningae; 9) Crotalus durissus; 10) Chironius exoletus; 11) C. flavolineatus;
12) C. quadricarinatus; 14) Drymarchon corais; 13) Drymoluber
brazili; 15) Mastigodryas bifossatus; 16) Oxybelis aeneus; 17) Simophis rhinostoma; 18) Spilotes pullatus; 19) Tantilla melanocephala; 20) Atractus pantostictus; 21) Leptodeira annulata;
22) Sibynomorphus mikanii; 23) Apostolepis assimilis;
24) A. albicolaris; 25) A. flavotorquata; 26) A. gr. taenuis;
27) Boiruna maculata; 28) Clelia plumbea; 29) C. quimi;
30) Erythrolamprus aesculapii; 31) Gomesophis brasiliensis;
32) Helicops angulatus; 33) H. leopardinus; 34) H. modestus;
35) Liophis almadensis; 36) L. maryellenae; 37) L. meridionalis;
38) L. paucidens; 39) L. poecilogyrus; 40) L. reginae; 41) Lystrophis nattereri; 42) Oxyrhopus guibei; 43) O. trigeminus;
44) O. rhombifer; 45) Phalotris nasutus; 46) Philodryas aestiva;
47) P. olfersii; 48) P. nattereri; 49) P. patagoniensis;
50) P. psammophideus; 51) Phimophis guerini; 52) Pseudablabes
agassizii; 53) Pseudoboa nigra; 54) Rhachidelus brazili;
55) Echinanthera occipitalis; 56) Thamnodynastes hypoconia;
57) Thamnodynastes rutilus; 58) Waglerophis merremii; 59) Xenopholis undulatus; 60) Micrurus frontalis; 61) M. lemniscatus.
28
Conservation of snakes in Central Brazil
Table 1: Scores and threat categories for 10 factors affecting survival of the 61 Central Brazil snakes. Abbreviations are BS: Body size, LS:
Litter size, DT: Dietary breadth, HB: Habitat breadth, HT: Habits, DB: Distribution breadth in DF, AH: Adaptability to altered habitats, RR:
Rarity in DF, CL: Species color, RM: Road Mortality.
Species and Threat categories
Threatened (> 1.9)
Drymoluber brazili
Philodryas psamophidea
Apostolepis flavotorquata
Chironius exoletus
Helicops angulatus
Lystrophis nattereri
Oxybelis aeneus
Rhachidelus brazili
Simophis rhinostoma
Thamnodynastes rutilus
Apostolepis gr. taenuis
Gomesophis brasiliensis
Liophis almadensis
Liophis paucidens
Oxyrhopus trigeminus
Phimophis guerini
Pseudoboa nigra
Xenopholis undulatus
Vulnerable (1,3-1,9)
Erythrolamprus aesculapii
Leptodeira annulata
Phalotris nasutus
Chironius flavolineatus
Clelia plumbea
Drymarchon corais
Liophis maryellenae
Liophis meridionalis
Micrurus lemniscatus
Thamnodynastes hypoconia
Boiruna maculata
Clelia quimi
Helicops leopardinus
Apostolepis albicolaris
Bothrops itapetiningae
Echinanthera occipitalis
Epicrates cenchria
Micrurus frontalis
Oxyrhopus rhombifer
Tantilla melanocephala
Crotalus durissus
Eunectes murinus
Helicops modestus
Leptotyphlops koppesi
Mastigodryas bifossatus
Oxyrhopus guibei
Philodryas aestiva
Spilotes pullatus
Boa constrictor
Bothrops moojeni
Chironius quadricarinatus
Atractus pantostictus
Pseudablabes agassizii
Sibynomorphus mikanii
BS
LS
DT
HB
HT
DB
AH
RR
CL
RM
Mean
2
1
1
2
1
0
2
3
1
1
0
0
1
1
2
1
2
0
3
2
3
2
2
3
3
2
2
2
3
3
2
1
2
2
2
3
3
3
3
3
3
3
2
3
3
3
3
3
3
3
2
3
2
3
3
3
3
3
3
2
3
2
2
3
3
3
3
3
2
3
2
3
3
3
0
2
1
3
2
3
1
3
0
1
3
3
3
1
3
1
3
3
3
3
3
2
3
3
2
3
3
3
2
3
1
3
2
3
3
3
2
3
3
3
2
2
3
3
2
3
2
2
1
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
2
3
1
3
3
3
0
1
3
0
2
2
0
0
3
0
3
1
1
1
3
0
0
1
0
0
0
0
0
0
1
0
1
0
0
0
1
0
3
1
1
0
2.3
2.2
2.1
2.1
2.1
2.1
2.1
2.1
2.1
2.1
2.0
2.0
2.0
2.0
2.0
2.0
2.0
2.0
1
1
1
2
3
3
1
1
2
1
2
2
0
0
1
1
2
2
1
0
3
3
1
0
3
2
2
3
3
3
2
0
1
0
2
3
2
2
0
1
2
2
1
2
1
2
0
3
2
3
1
1
2
3
0
0
1
1
0
2
0
2
0
0
2
3
1
2
3
3
3
3
0
0
3
2
3
3
1
0
3
3
1
3
2
3
2
3
2
0
3
3
0
2
2
1
2
0
3
3
3
3
2
2
2
2
3
2
3
2
3
2
2
1
3
2
2
0
2
1
1
2
1
3
3
3
2
0
1
1
0
2
1
2
3
1
3
2
0
2
3
3
1
3
1
3
3
3
1
0
3
3
3
1
3
0
3
1
1
0
3
3
3
2
3
3
2
0
2
2
1
2
2
1
3
2
2
2
1
1
2
2
3
2
1
1
0
1
1
0
0
2
1
3
1
0
2
0
0
0
0
2
1
0
2
2
3
2
3
3
3
2
2
3
2
3
3
1
3
1
2
2
0
2
1
3
3
2
2
0
2
2
2
2
2
1
1
1
1
2
2
2
3
3
3
2
2
1
3
3
3
2
1
1
1
1
0
1
0
2
2
3
1
0
2
2
1
0
1
2
1
0
3
2
3
1
0
1
0
1
3
2
0
0
1
3
2
1
1
3
3
3
2
1
0
0
2
3
0
1
1
2
0
0
0
2
1
0
1
1
0
0
0
1
0
0
1
1
0
0
0
2
2
1
3
2
3
0
0
0
1
3
1
1
2
2
1
0
0
2
1.9
1.9
1.9
1.8
1.8
1.8
1.8
1.8
1.8
1.8
1.7
1.7
1.7
1.6
1.6
1.6
1.6
1.6
1.6
1.6
1.5
1.5
1.5
1.5
1.5
1.5
1.5
1.5
1.4
1.4
1.4
1.3
1.3
1.3
França, F. G. R. and Araújo, A. F. B.
29
Table 1: Continued.
Species and Threat categories
no risk (< 1,3)
Bothrops neuwiedi
Liophis reginae
Philodryas nattereri
Apostolepis assimilis
Philodryas olfersii
Waglerophis merremii
Liophis poecilogyrus
Philodryas patagoniensis
Liotyphlops ternetzii
BS
LS
DT
HB
HT
DB
AH
RR
CL
RM
Mean
1
1
3
0
2
2
1
2
0
1.41
0
2
1
3
1
0
2
0
1
1.66
0
2
1
3
1
3
2
1
3
2.26
2
2
1
1
2
0
0
1
0
1.97
3
3
3
0
2
3
3
2
0
2.03
0
0
0
0
0
0
0
0
0
1.48
2
1
0
0
1
0
0
1
0
1.95
0
1
0
0
0
0
0
0
0
1.74
2
0
0
3
0
0
0
0
0
1.20
2
0
3
1
2
3
1
2
1
0.90
1.2
1.2
1.2
1.1
1.1
1.1
0.9
0.9
0.5
1.66
4: Snakes with small to medium body size, terrestrial
and diurnal, habitat generalists, and found in almost
all DF (vulnerable). Liophis poecilogyrus, Echinathera
occipitalis.
5: Snakes with medium to large body size, terrestrial
or semi-arboreal, with high litter size and wide distribution in DF (low vulnerability). Boa constrictor, Crotalus durissus, Epicrates cenchria, Philodryas nattereri, Philodryas olfersii, Philodryas patagoniensis, Spilotes pullatus, Waglerophis merremii.
6: Snakes with blotched patterns like pitvipers, terrestrial, with high litter size and wide distribution in DF
(low vulnerability). Bothrops moojeni, Bothrops neuwiedi, Mastigodryas bifossatus.
7: Snakes that are diet specialists, and have medium
litter size (vulnerable). Chironius flavolineatus, Chironius quadricarinatus, Liophis almadensis, Liophis
reginae, Pseudablabes agassizii, Sibynomorphus mikanii.
8: Snakes with medium body size, terrestrial habits,
and habitat and diet specialists (vulnerable). Bothrops
itapetiningae, Erythrolamprus aesculapii, Thamnodynastes hypoconia.
9: Snakes with uniform color, terrestrial or semi-arboreal habits, reduced range and rare in DF, and inadaptable to altered habitats (vulnerable to threatened). Chironius exoletus, Drymoluber brazili, Liophis meridionalis, Liophis paucidens, Oxybelis aeneus, Philodryas aestiva, Philodryas psamophideus, Rhachidelus
brazili, Thamnodynastes rutilus.
10: Black snakes, terrestrial and nocturnal, with reduced range and rare in DF (vulnerable to threatened).
Boiruna maculata, Clelia quimi, Pseudoboa nigra.
11: Snakes with big body size, with high litter size,
reduced range and rare in DF (vulnerable). Eunectes
murinus, Clelia plumbea, Drymarchon corais.
12: Snakes with coral-snake patter of coloration, fossorial or cryptozoic habits, diet and habitat specialists, and rare in DF (vulnerable to threatened). Apostolepis albicollaris, Apostolepis flavotorquata, Apostolepis sp., Micrurus frontalis, Micrurus lemniscatus,
Phalotris nasutus, Simophis rhinostoma.
13: Snakes that are diet and habitat specialists, rare in
DF and inadaptable to altered habitats (threatened).
Atractus pantostictus, Gomesophis brasiliensis, Helicops angulatus, Helicops leopardinus, Helicops
modestus, Leptodeira annulata, Leptotyphlops koppesi, Liophis maryellenae, Lystrophis nattereri, Phimophis guerini, Xenopholis undulatus.
In the principal component analysis, two axes explained 65% of the variation in the data (Table 3).
The first axis (43% of the variation) was positively
correlated to rarity and distribution breadth in Distrito Federal and negatively to road mortality. This
axis is thus associated with factors related to geographic distribution and humans attitudes. The second axis (22% of the variation) was positively correlated to dietary breadth and litter size, and negatively to body size. The second axis is associated to
factors related to natural-history of the snake species.
30
Conservation of snakes in Central Brazil
C A S E
Label
Gomesophis brasiliensis
Xenopholis undulatus
Helicops angulatus
Leptotyphlops koppesi
Phimophis guerini
Liophis maryellenae
Helicops leopardinus
Helicops modestus
Atractus pantostictus
Leptodeira annulata
Lystrophis nattereri
Apostolepis flavotorquata
Apostolepis gr. taenuis
Apostolepis albicollaris
Simophis rhinostoma
Phalotris nasutus
Micrurus leminiscatus
Micrurus frontalis
Drymarchon corais
Clelia plumbea
Eunectes murinus
Boiruna maculata
Pseudoboa nigra
Clelia quimi
Chironius exoletus
Drymoluber brazili
Philodryas psammophidea
Thamnodynastes rutilus
Liophis paucidens
Rhachidelus brazili
Liophis meridionalis
Oxybelis aeneus
Philodryas aestiva
Erythrolamprus aesculapii
Thamnodynastes hypoconia
Bothrops itapetiningae
Chironius flavolinaetus
Chironius quadricarinatus
Sibynomorphus mikanii
Liophis almadensis
Pseudablabes agassizii
Liophis reginae
Bothrops moojeni
Mastigodryas bifossatus
Bothrops neuwiedi
Philodryas nattereni
Philodryas patagoniensis
Philodryas olfersii
Epicrates cenchria
Boa constrictor
Crotalus durissus
Waglerophis merremi
Spilotes pullatus
Liophis poecilogyrus
Echinantera occipitalis
Oxyrhopus trigeminus
Ocyrhopus rhombiter
Oxyrhopus gribei
Tantilla melanocephala
Apostolepis assimilis
Liotyphlops ternetzii
Group
0
5
10
15
20
25
+---------+---------+---------+---------+---------+
13
13
13
13
13
13
13
13
13
13
13
12
12
12
12
12
12
12
11
11
11
10
10
10
09
09
09
09
09
09
09
09
09
08
08
08
07
07
07
07
07
07
06
06
06
05
05
05
05
05
05
05
05
04
04
03
03
03
02
02
01
Figure 2: Cluster diagram showing the similarity groups for threatening factors among sixty species of Central Brazil snakes. Diamond
indicates point in clustergram where significance is achieved. Numbers to the right of species indicate the significant groups.
FAMILY
SUBFAMILY
Tribe
Species
ANOMALEPIDIDAE
Liotyphlops ternetzii
LEPTOTYPHLOPIDAE
Leptotyphlops koppesi
BOIDAE
Boa constrictor
Epicrates cenchria
VIPERIDAE
Bothrops itapetiningae
Bothrops moojeni
Bothrops neuwiedi
Crotalus durissus
ELAPIDAE
Micrurus frontalis
Micrurus lemniscatus
COLUBRIDAE
Colubrinae
Chironius exoletus
Chironius flavolineatus
Chironius quadricarinatus
Drymarchon corais
Drymoluber brazili
Mastigodryas bifossatus
Oxybelis aeneus
Simophis rhinostoma
Spilotes pullatus
Tantilla melanocephala
Dipsadinae
Dipsadini
Atractus pantostictus
Sibynomorphus mikanii
Leptoderini
Leptodeira annulata
*Incerta sedis
Echinanthera occipitalis
Xenopholis undulatus
Xenodontinae
Elapomorphini
Apostolepis assimilis
Habits
Fossorial
Fossorial
Terrestrial, semi-arb
Terrestrial, semi-arb
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Cryptozoic
Cryptozoic
Arboreal, Terrestrial
Arboreal, Terrestrial
Arboreal, Terrestrial
Terrestrial, semi-arb
Terrestrial
Terrestrial
Arboreal, semi-arb
Terrestrial
Arboreal, semi-arb
Fossorial, criptozoic
Cryptozoic
Terrestrial, semi-arb
Arboreal, semi-arb
Terrestrial
Cryptozoic
Fossorial
N
30
1
14
21
13
45
26
50
17
8
4
13
15
16
4
11
3
11
9
15
10
36
5
12
8
10
CE, CA, gf
CE, CA, gf
GF
GF, VE
GF, ce
VE, GF, ce
GF
GF, ve, ce
CE, ca
CE, gf
CE
CE, GF, CA
CE
CE, CA
GF, ve, ce
CA, CE
CE, CA, gf
GF
CA, ce
GF, ve, ce
CA, ce
CE, CA, gf
GF, ce
CE, ca
CA, CE
CA, CE, GF
Habitats
Nocturnal-Diurnal
Diurnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Nocturnal-Diurnal
Nocturnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Activity Patterns
Abn
Li, Amp
Amp
Amp
Ann
Gás
Amp, li, bi, mam
Amp, li, bi, mam
Amp, li, bi, mam
Mam, amp, li, bi, sn, abn
Li
Mam, amp, li, bi, sn, abn
Amp, li, bi, mam
Amp
Bi, mam
Chi
Sn, abn
Sn
Mam, li, amp, bi, mil, chi
Mam, li, amp, bi, sn, mil, chi
Mam, li, amp, bi, sn, mil, chi
Mam, bi
Mam., bi
Mam., bi, li
Ins
Ins
Diet
228.30
323.00
268.38
477.60
268.60
269.97
806.50
675.08
599.40
1248.50
493.29
1017.00
749.33
448.73
1299.33
228.33
650.24
603.00
304.00
618.45
412.85
755.25
598.86
520.86
165.00
239.41
SVL
71.92
69.18
66.17
101.28
95.00
108.09
96.42
119.46
80.90
297.05
187.99
382.89
47.82
105.20
297.87
61.73
234.45
311.57
116.78
320.07
145.08
262.63
267.53
260.71
17.00
60.99
23.00
107.25
47.88
167.20
30.50
61.67
468.75
440.54
360.40
304.44
128.67
392.91
468.67
116.00
432.00
73.27
42.18
42.50
39.23
101.00
59.85
68.57
77.77
67.29
4.29
TL
12.12
24.63
12.11
28.26
10.56
25.74
50.80
90.50
57.43
84.96
49.12
138.48
31.94
27.22
113.72
21.51
14.35
19.96
12.81
48.49
20.81
32.08
39.67
34.53
1.07
Table 2: Summary of the information of Natural History and body measurements (MEAN ± SE in mm) of the snakes in Distrito Federal. Abbreviations are: CA = Campo, CE = Cerrado, GF =
Gallery Forest, VE = Vereda, semi-arb = semi-arboreal, abn = amphisbaenian, amp = amphibian, ann = annelids, arn = aranae, bi = birds, chi = chilopoda, cro = crocodylians, fi = fish, gas =
gastropode, ins = insecta, li = lizards, mam = mammals, mil = millipede, sn = snakes, N = Sample sizes, SVL = snout-vent length, TL = tail length. Capital letter means principal habitats.
França, F. G. R. and Araújo, A. F. B.
31
FAMILY
SUBFAMILY
Tribe
Species
Apostolepis gr. tenuis
Apostolepis albicolaris
Apostolepis flavotorquata
Phalotris nasutus
Hydropsini
Helicops angulatus
Helicops leopardinus
Helicops modestus
Philodriadini
Philodryas aestiva
Philodryas nattereri
Philodryas olfersii
Philodryas patagoniensis
Philodryas psammophidea
Pseudablabes agassizii
Pseudoboini
Boiruna maculata
Clelia plumbea
Clelia quimi
Oxyrhopus guibei
Oxyrhopus rhombifer
Oxyrhopus trigeminus
Phimophis guerini
Pseudoboa nigra
Rhachidelus brazili
Tachymenini
Gomesophis brasiliensis
Thamnodynastes hypoconia
Thamnodynastes rutilus
Xenodontini
Erythrolamprus aesculapii
Liophis almadensis
Liophis maryellenae
Liophis meridionalis
Liophis paucidens
Liophis poecilogyrus
Liophis reginae
Lystrophis nattereri
Waglerophis merremii
Table 2: Continued
Habits
Fossorial
Fossorial
Fossorial
Cryptozoic, fossorial
Aquatic
Aquatic
Aquatic
Terrestrial
Terrestrial, semi-arb
Semi-arb, Terrestrial
Terrestrial, semi-arb
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Cryptozoic
Terrestrial
Terrestrial
Aquatic
Terrestrial, semi-arb
Terrestrial, semi-aqua
Terrestrial, cryptozoic
Terrestrial
Terrestrial, semi-aqua
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Terrestrial
Terrestrial
N
5
9
2
10
4
1
18
14
35
22
46
2
21
3
1
7
34
40
11
4
7
6
3
9
3
34
9
13
11
1
56
19
7
46
GF
CE, CA, gf
VE, gf
CE, CA, gf
CE
CE, CA, gf
GF
CA, ce
CE, GF
VE, gf
VE, gf
GF
CE
GF
GF, ce
GF, CE, CA
CA, CE, gf
CE, CA
CE, CA
CE
CE
CA, ce
CE, ca
GF, ce
CE, ca, ve
CE
CA, ce
GF, VE
GF
GF, VE
Habitats
CA
CE, CA
CE
CA, CE
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal-Nocturnal
Diurnal-Nocturnal
Diurnal
Diurnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Nocturnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Diurnal
Nocturnal
Nocturnal
Nocturnal
Activity Patterns
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Nocturnal-Diurnal
Sn, li
Amp
Fi
Amp, li
Li
Amp
Amp
Li (eggs)
Amp
Ann
Amp
Amp, fi
Sn, mam
Sn, li, mam
Sn, mam
Li, mam
Li, mam
Li, mam
Li
Li
Bi (eggs)
Mam, li
Mam, amp, li, bi
Mam, amp, li, bi
Mam, amp, li, bi
Li
Arn
Fi, Amp
Fi, Amp
Fi, Amp
Diet
Abn
Abn
Abn
Abn, Sn
426.29
285.11
304.92
443.91
369.00
369.05
417.16
245.00
560.74
289.00
323.44
275.00
458.00
1401.00
493.29
438.74
312.33
501.36
475.80
543.86
785.50
503.57
696.91
648.05
677.46
453.50
260.90
395.25
240.00
284.71
SVL
231.80
266.78
459.50
517.60
135.82
87.70
111.91
119.65
127.00
128.87
99.63
75.78
214.64
43.92
56.82
105.00
131.64
315.00
187.99
193.80
135.80
136.44
222.73
238.22
316.05
157.46
278.38
208.01
251.26
86.97
75.26
143.84
120.00
106.27
34.10
72.62
44.55
160.09
22.08
29.86
33.74
49.99
33.19
48.70
16.06
38.87
58.56
90.00
94.00
167.27
87.23
159.11
44.00
98.30
31.82
22.77
43.82
49.12
55.11
36.04
28.98
66.09
85.14
103.52
128.67
116.82
77.15
128.00
131.00
180.86
213.33
69.67
113.67
108.67
17.52
94.00
63.40
120.73
82.65
87.20
43.13
24.14
31.26
93.29
214.14
277.77
261.18
252.13
155.50
85.19
75.87
4.09
9.79
2.12
13.71
187.25
TL
27.20
29.56
41.50
57.70
32
Conservation of snakes in Central Brazil
França, F. G. R. and Araújo, A. F. B.
Table 3: Factor loadings of each variable on the first two principal
components and proportion of the variance explained by each component.
Variable
Body size
Litter size
Dietary breadth
Habitat breadth
Habits
Distribution breadth in DF
Adaptability to altered habitats
Rarity in DF
Species color
Road Mortality
Eigenvalue
Variance explained
Percent
Cumulative
Principal component
factor loadings
Factor I
Factor II
-0.157
-0.810
0.175
0.731
0.118
0.777
0.833
0.123
-0.143
-0.696
0.887
0.186
0.847
-0.112
0.932
0.124
-0.277
0.434
-0.814
-0.253
4.30
2.20
42.95
42.95
22.08
65.03
DISCUSSION
The lack of basic natural history information on
many snake species and data on the phylogenetic relationships among species complicate evaluations of the
factors that contribute to snake population declines
(Greene, 1994). Our intensive studies on the snake assemblage in Distrito Federal over the last several years
has generated a wealth of natural history data (França,
2003), which has permitted us to asses the conservation status for snakes in central Brazil. Filippi and
Luiselli (2000) pointed out that several Italian snakes
are more vulnerable to distribution-related attributes,
whereas species-specific life-history traits and trade
appear to be threats for a lower number of taxa. In
snakes from Distrito Federal, life-history factors and
distribution attributes affected the viability of snake
populations similarly. Moreover, phylogenetic groups
did not differ in their risk, as species in different clades
are present in groups with different degrees of risk.
Although the method proposed by Filippi and
Luiselli (2000) was designed for a snake assemblage
in the temperate zone, with less than one-third of the
species richness found in the tropical region of DF,
our results were similar. Filippi and Luiselli (2000)
found that of 19 snake species in Italy, only 10.5%
were not at risk, 52.6% were vulnerable, and 36.8%
were threatened. Our results on snakes in Distrito Federal, Brazil, placed 14.8%, 55.7%, and 29.5% of species in the same categories, respectively. Mean threat
scores for Italian snake species ranged from 0.7 to 2.4
33
(Filippi and Luiselli, 2000), whereas the mean threat
scores for Brazilian species ranged from 0.5 to 2.3.
Mean scores for each of the 10 factors used by Filippi
and Luiselli (2000) ranged from 0.4 to 2.3, whereas
mean scores ranged from 0.9 to 2.3 for Brazilian
snakes. Finally, multivariate analysis produced 5
groups with similar threat factors in the Italian snake
assemblage (Filippi and Luiselli, 2000), whereas we
delineated 13 groups. However, because of the higher
number of snake species in DF compared to Italy (61
versus 19), the number of groups is comparable. Our
results demonstrate that the method outlined by Filippi and Luiselli (2000) is consistent and applicable to
snake assemblages in other regions.
Of 13 groups formed by PCA and Cluster analyses, we consider one group with no risk, three with
low risk, and nine groups ranging from vulnerable to
threatened. Almost all of these assessments combine
life-history and distribution-related factors. Group 13,
which includes one leptotyphlopid and 10 colubrids,
had the highest threat values due to the combination
of specialized natural-history traits such as diet, habitat, the inadaptability to altered habitats, and rarity in
the region. Small snakes that are habitat generalist,
are found in altered environments in DF, and have a
wide distribution were at the lowest risk, for example,
Liotyphlops ternetzii (group1), and Apostolepis assimilis and Tantilla melanocephala (group 2).
Specific life-history traits increase risk for several
species and groups. Species that eat exclusively a single prey type, which can be seasonally abundant, are
more prone to risk during the season of lowest prey
abundance (Vitt, 1983). In Distrito Federal, some
snakes eat exclusively frogs (e.g., some Liophis, Thamnodynastes and Waglerophis merremii), or invertebrates (e.g., Liotyphlops ternetzii, Leptotyphlops koppesi, Gomesophis brasiliensis, Pseudablabes agassizii, and Tantilla melanocephala). The habits of snakes
can also influence the degree of threat. Terrestrial and
diurnal snakes are more vulnerable to predators, especially visually oriented predators such as birds (Greene,
1997; Dodd, 2001b). Finally, habitat specificity is one
of the most important factors determining risk in the
herpetofauna of central Brazil (Colli et al., 2002). The
Cerrado has been undergoing habitat alteration at an
accelerated pace (Alho and Martins, 1995) and a concomitant loss of biodiversity has occurred. Species with
specific habitat requirements such as the three species
of watersnake Helicops, Gomesophis brasiliensis, and
34
Conservation of snakes in Central Brazil
Liophis maryellenae, forest snakes as Chironius exoletus, and snakes restricted to open areas such as Leptotyphlops koppesi and Drymoluber brazili, are more
sensitive to habitat modification.
Factors related to geographic distribution of species are known to be threats to snakes in all regions of
the world. Since 1954, the Distrito Federal has lost
more than 55% of its original vegetation and this loss
continues at a rapid pace (Werthein et al., 2000). This
loss is an especially serious problem for species with
limited distributions in the region, such as Apostolepis flavotorquata, Chironius exoletus and Philodryas
psamophidea. The first two species are found in a dry
forest area that is not under any conservation protection, and the latter species was found in an area that
has been entirely urbanized and has not been encountered again since the 1970s. These species also do not
adapt well to altered environments, which places them
at higher risk.
Human attitudes also create serious threats to
snakes. The traditional Judeo-Christian view of snakes
is exceedingly antagonist, and the fear and lack of
knowledge results in high mortality at the hands of
humans (Greene, 1997; Shine and Bonnet, 2000). In
central Brazil, all coral-snakes have triad patterns with
red, black and white colors. All snakes with these colors are considered venomous and are killed indiscriminately, even though some species are non-venomous
coral snake mimics. In Distrito Federal, we found two
groups of snakes with coral-snake patterns; one group
included species of Oxyrhopus, and the other group
included Apostolepis, Micrurus, Phalotris and Simophis. All species are considered under threat because
of their aposematic coloration, but the species of Oxyrhopus are considered less vulnerable than the other
groups because they are widely distributed and have a
more generalist ecology.
Road mortality is a serious source of mortality for
many wild animals in the world (Trombulak and Frissel, 2000). The elongated bodies and relatively slow
movement of snakes, make them susceptible to vehicular mortality. Also, snakes that disperse from their
birth area, make seasonal movements to and from hibernacula, track changing prey resource abundances,
search for mates, or use roads for thermoregulation
sites are at increased risk of being run over (Bonnet
et al., 1999; Dodd, 2001b). High numbers of dead
snakes have been reported on roads in several places
(Dodd et al., 1989; Bush et al., 1991; Enge and Wood,
2002). On four roads in Distrito Federal, totaling
42,5 km, a one year study on road mortality found 575
dead reptiles, of which 362 were snakes (Rodrigues
et al., 2002). The colubrids Oxyrhopus guibei, Philodryas nattereri, and Waglerophis merremii were the
most frequently killed snakes on roads in DF, all of
which are terrestrial.
Conservation of snakes can be accomplished by a
variety of methods. If the goal of a conservation program is to ensure the long-term survival of a snake
species, its habitat needs to be conserved (Dodd,
2001b). Habitats may be protected by the implementation of parks, reserves, or conservation easements
with private landowners (Sutherland, 2001). The Distrito Federal has three conservation units encompassing 50,000 ha that are integral in the protection of
Cerrado flora and fauna (Werthein et al., 2000). Although these three areas represent less than 25% of
the total area of the DF region, they are important to
the maintenance of the local avifauna, protecting about
81% of all bird species (Braz and Cavalcanti, 2001).
However, as stated previously, other important areas
inside DF, such as the north dry forest, are still in need
of protection. Additionally, the construction of tunnels
or culverts under highways, or wildlife barriers might
be useful in deterring snakes from crossing roads and
minimize road mortality (Dodd, 2001b). Other potential snake conservation methods may include translocation or repatriation (Dodd and Seigel, 1991; Dodd,
2001b), although the impacts of these managements
on individual snakes are not completely known. Some
studies report that translocated snakes can move larger distances and show different habitat preferences to
resident snakes, concluding that this practice influences
individual snakes (Butler et al., 2005). Finally, educational programs can be a powerful conservation tool
to aid in the protection of snake species and assemblages. In DF, educational programs and materials can
be presented at universities, schools, or local Zoos in
an attempt to alleviate fear, correct misinformation and
myths, and to teach the importance of snakes in nature.
Assessing the conservation status of snake species
in a specific region is an important first step in changing attitudes and generating interest in preserving snake
diversity (Dodd, 2001a). However, conservation efforts are limited by the constraints imposed by the species’ natural history. Basic biological data are lacking
for most snake species and this is problematic in as-
França, F. G. R. and Araújo, A. F. B.
sessing the conservation status of snakes in most regions of the world. The method proposed by Fillipi
and Luiselli (2000) worked well for assessing the conservation status of snakes in central Brazil and further
ecological studies on Brazilian snake assemblages
should be done to test the applicability of the method
to other regions. Ultimately, assessing the conservation status of snake species in different areas will allow comparisons among regions and will generate a
better status assessment that will aid in the conservation of Brazilian snakes.
RESUMO
Nós avaliamos o status de conservação de 61 espécies de uma comunidade de serpentes do Brasil central pelo ranqueamento das espécies de acordo com
suas vulnerabilidades a dez fatores de ameaça que influenciam a sobrevivência de populações de serpentes.
A serpente anomalepidide Liotyphlops ternetzii foi a
espécie com menor risco e o colubrídeo Drymoluber
brazili foi a mais ameaçada. Menos de 15% da fauna
de serpentes do Distrito Federal foi considerada livre
de qualquer ameaça. A história natural das espécies,
suas distribuições geográficas e atitudes humanas foram importantes fatores determinando os níveis de
ameaça para as serpentes do Brasil central. Análise de
Componentes Principais e Análise de Agrupamento
foram usadas para classificar as espécies em grupos
de vulnerabilidade. Treze grupos foram identificados
variando de nenhum risco a grupos ameaçados. No
Brasil, a avaliação do status de conservação para outras comunidades de serpentes em outros biomas pode
ser útil para gerar um plano de conservação efetivo
para o país.
ACKNOWLEDGEMENTS
We are grateful to D. Shepard, M. Mira, R. Constantino and
V. Braz for helpful critical comments on previous version of the
manuscript and for help in English and to Guarino Colli, Francisco Franco and Ronaldo Fernandes for permission to examine
specimens on CHUNB, IB and MNRJ. This work was supported
by a master’s fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq to FGRF.
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Submitted 12 January 2006
Accepted 15 March 2006