patterns of space, time and trophic resource use by
TRANSCRIPT
27
Patterns of space time and trophic resource use by Tropidurus hispidus and T semitaeniatus in an area of Caatinga northeastern BrazilFabiacuteola Fonseca Almeida Gomes1 Francis Luiz Santos Caldas2 Rafael Alves dos Santos1 Bruno Duarte da Silva1 Daniel Oliveira Santana2 Steacutephanie Menezes Rocha2 Anthony Santana Ferreira1 amp Renato Gomes Faria1
1Programa de Poacutes-Graduaccedilatildeo em Ecologia e Conservaccedilatildeo Universidade Federal de Sergipe Cidade Universitaacuteria Prof Joseacute Aloiacutesio de Campos Av Marechal Rondon sn Jardim Rosa Elze
- CEP 49100-000 - Satildeo CristoacutevatildeoSE Brazil
2Programa de Poacutes-Graduaccedilatildeo em Ciecircncias Bioloacutegicas Universidade Federal da Paraiacuteba Cidade Universitaacuteria - CEP 58051-900 - Joatildeo Pessoa - PB - Brazil
Herpetological Journal FULL PAPER
Correspondence Fabiacuteola Fonseca Almeida Gomes (biola_gomeshotmailcom)
Volume 25 (January 2015) 27ndash39
Published by the British Herpetological Society
This study examines how two species of diurnal lizards (Tropidurus semitaeniatus and T hispidus Tropiduridae) use spatial trophic and temporal resources in the Conservation Unit of Monumento Natural Grota do Angico Poccedilo Redondo Sergipe (Brazil) Both species were mostly active during sunny days with a reduction in activity during the hottest hours and showed a preference for rocks using rock crevices as main shelter Tropidurus hispidus is the larger species as measured with SVL and the species did not markedly differ in overall body shape Both species mostly predated ants insect larvae and termites The head morphologies of T semitaeniatus and T hispidus are better adapted for the ingestion of larger and longer prey respectively Tropidurus semitaeniatus individuals modified their food intake during periods of higher rainfall possibly to avoid competition with T hispidus Despite the high overlap in the use of space time and diet the coexistence of the two species is facilitated through resources strategies that minimise the negative effects of competition
Key words dry forest ecology lizards resource partitioning sympatry
INTRODUCTION
Organisms coexist by sharing available resources (Toft 1985) and interspecific competition is one of
the main factors responsible for community structure (Milstead 1965 Janzen amp Schoener 1968 Schoener 1975 Huey amp Pianka 1977 Ribeiro amp Freire 2009 2011) Competition can result in competitive exclusion and habitat shifts (Hutchinson 1957 Schoener 1975) or may enable co-occurrence through character displacement (Pianka 1973) Lizards are considered to be excellent models for ecological studies about coexistence (Arauacutejo 1987 Rodrigues 1987 Colli et al 1992 Vitt amp Pianka 1994 Carvalho et al 2005) The presence of lizards in given environments is strongly connected with the availability of resources such as food shelter and sites for thermoregulation (Vitt 1991 1993 Bergallo amp Rocha 1993) The degree of resource sharing can be quantified using differences in morphology spatial resources and foraging modes (MrsquoCloskey amp Hecnar 1994 Vitt amp Zani 1998 Faria amp Araujo 2004) Morphology may be linked to structural characteristics of habitats (Ricklefs et al 1981 Losos 1990 Colli et al 1992) and head as well
as jaw size are associated to diet preferences (Vitt 1995 Silva amp Arauacutejo 2008)
Tropidurus hispidus (Spix 1825) and T semitaenitus (Spix 1825) are members of the torquatus and semitaeniatus groups within the family Tropiduridae respectively (Frost et al 2001 Beacuternils amp Costa 2012) Tropidurus hispidus is considered the largest species of the genus and occupies a wide distribution that extends into the Caatinga area (Rodrigues 1987) it is a habitat generalist which can often be observed on rocky substrates (Vitt et al 1996 1997 VanSluys et al 2004) Tropidurus semitaeniatus is exclusively saxicolous with a flattened head and body to allow the use of rocky crevices as shelters and is found throughout the Caatinga of northeastern Brazil (Rodrigues 2005 Freitas amp Silva 2007 Carvalho et al 2013) Species of the genus Tropidurus are characterised by phylogenetic inertia associated with foraging modes (VanSluys 1993 Faria amp Arauacutejo 2004 Cooper 1994 Pianka amp Vitt 2003) which should lead to intense competitive interactions (Webb et al 2002 Losos 2008) In this study we investigated how T hispidus and T semitaeniatus use and share spatial trophic and temporal resources
28
FFA Gomes et a l
MATERIALS AND METHODS
The Caatinga has an estimated area of 800000 km2 in northeastern Brazil extending from 2deg54rsquo to 17deg21rsquoS (Prado 2005) Shallow flagstones crystalline soils and irregular rainfall contribute to xeromorphic vegetation (Chiang amp Koutavas 2004 Krol et al 2001 Prado 2005) Annual precipitation ranges from 240ndash1500 mm (Sampaio 1995 Prado 2005) Despite high annual variation long periods of drought are common (Nimer 1972 Reis et al 2006) Populations of T hispidus and T semitaeniatus were studied in the State Conservation Unit of Monumento Natural Grota do Angico located in the semi-arid region of Sergipe state (Brazil 9deg41rsquoS and 38deg31rsquoW) between the municipalities of Poccedilo Redondo and Canindeacute de Satildeo Francisco (Fig 1) The Conservation Unit has an area of 2183 ha and its vegetation is typical of the Caatinga biome The average annual precipitation is 500 mm and the altitude ranges from 10 to 200 m (Ruiz-Esparza et al 2011)
Fig 1 Location of the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE (Image Sidney Feitosa Gouveia)
The study was undertaken between December 2008 and November 2009 Data collections were made on three consecutive days in each month between 0600 and 1730 hours each day Three flat areas measuring 450times20 m (27 ha) were demarcated with a 50-m tape measure in the bedrocks of dry streams Active searches were employed to achieve systematic surveys Lizards were captured with nylon ties attached to fishing rods (25 m) Observations were undertaken over one day in each area For each captured lizard we recorded time of capture substrate when located (1) and after (2) the approach of the observer (rock tree rock crevice litter bromeliad lair excreta and cactus) activity when located (1) and after (2) the approach of the observer (motionless walking running agonism foraging interacted with lace) sun exposure (sun shadow or mosaic) perch height and weather conditions (sunny cloudy drizzle or rainy) We measured snoutndashvent length (SVL) tail length body length and width head length width and height and length of both limbs (right side of the body) using a digital caliper with an accuracy of
001 mm (Faria amp Arauacutejo 2004) Mass was also recorded using a Pesolareg balance (accuracy 05 g) Captured lizards were marked with Corrector water-based white colour to prevent recapture After measurements animals were released at the site of capture
Five specimens of each species per month were sacrificed using a lidocaine solution for diet analysis Specimens were fixed in 10 formalin and preserved in 70 ethanol and deposited in the Coleccedilatildeo Herpetoloacutegica da Universidade Federal de Sergipe (CHUFS) Ingested items were identified to the lowest possible taxonomic level Whole specimens were counted and their length and width was measured with a digital caliper (accuracy 001 mm) Prey volume was estimated using the formula for an ellipsoid (volume=(πlengthwidthsup2)6 Magnusson et al 2003) or through measurement in a water column using a graduated cylinder (plant material) Prey availability was estimated using monthly collections Fifteen pitfall traps (250 ml plastic pots) were placed in each area at a minimum distance of 5 m from each other for three consecutive days Each trap contained a solution of water salt and detergent for conserving invertebrates until they were transferred to 70 ethanol
The data were analysed using Systat v120 and BioEstat v50 for Windows A 5 significance level was applied Normality of the samples was tested using a ShapirondashWilkrsquos test in order to determine whether parametric or nonparametric analysis should be used Before analysis all morphometric variables were log10-transformed in order to convert the sample to a normal distribution and reduce scale effects For animals with broken or regenerated tails the original length was estimated using a regression model (SVLxtail length Faria amp Arauacutejo 2004) Body size was defined as an isometric variable following the protocol of Somers (1986) by which the scores of an isometric vector initially set at plt05 were obtained by multiplication of the matrix n x p of the log10-transformed data where n is the number of observations and p the isometric eigenvector (Jolicoeur 1963 Somers 1986) The residuals of the regressions of each log10-transformed variable with body size was used A principal component analysis (PCA) of size-adjusted morphological variables served to examine possible differences in morphology between species To test if the differences in form between the species were significant we undertook a multivariate analysis of variance (MANOVA) on the first five factors of the PCA The body size and mass of the two species were also compared by variance analysis (ANOVA)
The numerical and volumetric compositions of the prey categories consumed by the two species were compared using a KolmogorovndashSmirnov test on a monthly basis The widths of food niches (number and volume of prey) spatial niches (substrates and perch height) and temporal niches (time of activity period in which the animal remains exposed) were calculated using the inverse of Simpsonrsquos (1949) diversity index
B= 1
sumi = 1
n
p i2
29
Interact ion of sympatr ic Tropidur idae
where p is the proportion of resource category (trophic spatial or temporal) used and n is the number of resource categories adopted B ranges between 1 (exclusive use of a resource type) and 0 (homogeneous use of all types of resources) The estimated availability (total and monthly) of food resources was also measured using this method
The overlap between the food spatial and temporal niches were calculated using the formula for symmetrical overlap (Pianka 1973)
sum sum
sum
= =
==n
i
n
iikij
nikij
jk
pp
pp
1 1
22
1φ
where j and k represent different species Values close to zero indicate no similarity in resource use and values close to one indicate the similar use of such resources This index was also adopted to compare prey categories ingested with those available in the environments A canonical correlation between two set of variables (maximum length and maximum width of prey versus length width and height of the head) was used to investigate the relationship between the prey dimensions and head measurements
RESULTSIn total 1760 observations were made (422 for T hispidus and 1338 for T semitaeniatus) Morphometric and diet analyses were performed using a total of 102 specimens comprising 51 T hispidus (9 males 9 females and 33 young) and 51 T semitaeniatus (12 males 9 females and 30 young)
No significant differences were observed between both species with respect to substrate use (G=93421 gl=7 p=0229 nT hispidus=421 nT semitaeniatus=1333) In total 8313 and 9317 of T hispidus and T semitaeniatus were found on rocks (Fig 2A) and niche space width (B) was 142 and 115 respectively Overlap in use of microhabitats was high ( φjk=099) The average perch height was 6322plusmn6607 cm (n=300) for T hispidus and 5636plusmn5130 cm (n=912) for T semitaeniatus (including animals found on the ground Fig 2B) without significant differences (MannndashWhitney U=4250 p=05708 n=1212) Niche widths (B) of perch height were 289 for T hispidus and 273 for T semitaeniatus with a high overlap between species ( φjk=099)
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931
Fig 2 Relative frequencies of (A) substrate use when located (B) perch height use (C) weather condition (D) sun exposure (E) activity levels across the day (F) behaviour when sighted (G) behaviour when escaping from the observer (H) substrate use after the approach of the observer of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE
30
FFA Gomes et a l
Tabl
e 1
Des
crip
tive
data
for
mor
phol
ogic
al c
hara
cter
istics
of r
epro
ducti
ve in
divi
dual
s of
T h
ispi
dus
and
T s
emita
enia
tus
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E L
inea
r mea
sure
men
ts a
re in
mill
imet
res
the
wei
ght i
s in
gra
ms
and
valu
es in
par
enth
eses
refe
r to
size-
adju
sted
var
iabl
es
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=9
)M
ales
(n=1
2)Fe
mal
es (n
=9)
Mal
es (n
=9)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
352
plusmn05
32
68ndash4
25
648
plusmn13
43
48ndash8
33
105
0plusmn2
197
81ndash1
358
155
5plusmn6
342
09ndash2
399
Mas
s6
99plusmn1
00
585
ndash90
014
69plusmn
391
800
ndash20
2523
48plusmn
553
165
0ndash31
00
312
2plusmn14
17
142
5ndash52
00
(00
52plusmn0
110
)(-0
068
ndash02
42)
(-00
94plusmn0
268
)(-0
846
ndash01
60)
(00
75plusmn0
127
)(-0
085
ndash03
27)
(00
04plusmn0
061
)(-0
100
ndash00
81)
SVL
651
6plusmn3
6759
69-
719
979
68plusmn
456
731
7ndash87
32
840
5plusmn7
9074
16-
961
195
54plusmn
136
471
19ndash
114
08(0
047
plusmn00
20)
(00
17ndash0
073
)(0
073
plusmn00
14)
(00
49ndash0
095
)(0
017
plusmn00
15)
(-00
10ndash0
043
)(-0
028
plusmn00
65)
(-01
25ndash0
110
)Bo
dy w
idth
202
5plusmn1
5417
61ndash
223
723
08plusmn
414
152
3ndash29
83
250
0plusmn2
0619
74-
282
124
82plusmn
404
164
2ndash31
06
(00
97plusmn0
030
)(0
043
ndash01
33)
(00
86plusmn0
061
)(-0
062
ndash01
76)
(00
46plusmn0
039
)(-0
015
ndash01
01)
(-00
62plusmn0
056
)(-0
148
ndash00
32)
Body
hei
ght
745
plusmn11
15
36ndash9
10
848
plusmn10
96
64ndash9
93
140
7plusmn1
4611
22ndash
163
915
64plusmn
439
439
ndash22
09(0
015
plusmn00
60)
(-01
00ndash0
097
)(-0
021
plusmn00
54)
(-01
67ndash0
048
)(0
077
plusmn00
55)
(-00
07ndash0
162
)(-0
055
plusmn01
01)
(-02
26ndash0
073
)He
ad w
idth
120
3plusmn0
7311
04ndash
135
015
61plusmn
172
112
5ndash18
00
171
9plusmn1
7115
21ndash
197
419
93plusmn
395
116
2ndash23
99
(00
11plusmn0
020
)(-0
017
ndash00
49)
(00
57plusmn0
037
)(-0
020
ndash01
02)
(00
16plusmn0
020
)(-0
018
ndash00
49)
(-00
32plusmn0
047
)(-0
109
ndash00
45)
Head
leng
th17
16plusmn
164
125
7ndash18
84
214
4plusmn1
8117
24ndash
248
023
64plusmn
239
208
5ndash26
86
326
1plusmn18
45
168
1ndash91
82
(00
08plusmn0
044
)(-0
112
ndash00
43)
(00
44plusmn0
019
)(0
014
ndash00
79)
(00
02plusmn0
013
)(-0
017
ndash00
33)
(-00
01plusmn0
177
)(-0
153
ndash05
62)
Head
hei
ght
580
plusmn03
74
97ndash6
37
717
plusmn07
65
44ndash8
40
103
1plusmn1
009
23ndash1
240
120
2plusmn3
304
18ndash1
777
(-00
26plusmn0
022
)(-0
067
ndash00
02)
(-00
10plusmn0
029
)(-0
069
ndash00
30)
(00
42plusmn0
025
)(0
002
ndash00
76)
(-00
42plusmn0
061
)(-0
127
ndash00
84)
Tail
leng
th98
60
plusmn67
589
72ndash
116
8713
155
plusmn12
5110
487
ndash149
18
122
44plusmn1
716
887
2ndash14
131
144
13plusmn1
902
111
62ndash1
713
6(-0
004
plusmn00
28)
(-00
36ndash0
070
)(0
078
plusmn00
42)
(-00
10ndash0
148
)(-0
111
plusmn00
56)
(-01
11ndash0
056
)(-0
014
plusmn00
55)
(-00
82ndash0
080
)Fo
rele
g le
ngth
326
6plusmn1
6429
99ndash
350
039
83plusmn
303
932
55ndash
444
340
41plusmn
256
361
3ndash43
83
460
5plusmn7
6233
27ndash
564
0(0
044
plusmn00
18)
(00
06ndash0
063
)(0
073
plusmn00
19)
(00
40ndash0
106
)(0
009
plusmn00
23)
(-00
42ndash0
042
)(-0
029
plusmn00
53)
(-01
14ndash0
074
)Hi
nd li
mb
leng
th45
25plusmn
262
402
1ndash48
89
570
5plusmn3
8249
61ndash
629
457
64plusmn
365
505
0ndash62
82
681
5plusmn9
7950
56ndash
807
2(0
022
plusmn00
20)
(-00
12ndash0
043
)(0
066
plusmn00
11)
(00
50ndash0
085
)(0
001
plusmn00
23)
(-00
42ndash0
034
)(-0
018
plusmn00
51)
(-00
97ndash0
090
)
31
Interact ion of sympatr ic Tropidur idae
nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to activity when sighted (G=04808 gl=4 p=09753 nT hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φ jk = 099) Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=1
3)M
ales
(n=1
7)Fe
mal
es (n
=15)
Mal
es (n
=18)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
100
plusmn04
90
25ndash2
01
295
plusmn16
00
75ndash6
17
388
plusmn17
81
37ndash6
84
395
plusmn17
11
15ndash6
44
Mas
s1
96plusmn0
88
075
ndash35
05
62plusmn3
84
110
ndash13
007
77plusmn3
78
200
ndash15
258
07plusmn3
38
250
ndash12
50(-0
009
plusmn00
63)
(-01
40ndash0
072
)(-0
015
plusmn00
74)
(-01
59ndash0
112
)(-0
029
plusmn01
11)
(-02
64ndash0
068
)(0
035
plusmn00
40)
(-00
24ndash0
104
)SV
L44
22plusmn
782
269
6ndash56
84
596
5plusmn10
67
416
7ndash72
76
574
2plusmn10
99
399
1ndash72
71
579
1plusmn8
7238
82ndash
693
6(-0
094
plusmn00
72)
(-02
76ndash-
000
8)(0
010
plusmn00
54)
(-00
98ndash0
075
)(-0
025
plusmn00
61)
(-01
67ndash0
031
)(-0
020
plusmn00
40)
(-01
35ndash0
022
)Bo
dy w
idth
117
2plusmn2
216
93ndash1
468
164
5plusmn3
7610
87ndash
226
615
38plusmn
330
112
6ndash21
02
154
4plusmn3
044
105
0ndash19
44
(-01
05plusmn0
086
)(-0
306
ndash-0
006)
(00
05plusmn0
073
)(-0
122
ndash00
92)
(-00
41plusmn0
060
)(-0
120
ndash00
45)
(-00
40plusmn0
058
)(-0
143
ndash00
35)
Body
hei
ght
465
plusmn11
53
37ndash7
69
626
plusmn14
803
51ndash8
73
889
plusmn21
65
38ndash1
230
897
plusmn23
25
57ndash1
219
(-01
13plusmn0
089
)(-0
256
ndash00
78)
(-00
53plusmn0
079
)(-0
224
ndash00
46)
(00
71plusmn0
068
)(-0
058
ndash01
43)
(00
72plusmn0
074
)(-0
036
ndash01
73)
Head
wid
th9
07plusmn1
80
606
ndash11
9411
91plusmn
243
762
ndash15
7212
05plusmn
171
933
ndash14
5012
28plusmn
180
920
ndash15
14(-0
082
plusmn00
74)
(-02
21ndash0
019
)(0
007
plusmn00
62)
(-01
34ndash0
075
)(-0
002
plusmn00
31)
(-00
57ndash0
053
)(0
004
plusmn00
34)
(-00
59ndash0
070
)He
ad le
ngth
129
6plusmn1
899
33ndash1
555
159
4plusmn3
129
45ndash2
022
175
7plusmn2
6013
14ndash
222
317
63plusmn
246
125
5ndash21
52
(-00
70plusmn0
057
)(-0
185
ndash00
10)
(-00
18plusmn0
075
)(-0
248
ndash00
47)
(00
10plusmn0
031
)(-0
062
ndash00
58)
(00
10plusmn0
033
)(-0
075
ndash00
53)
Head
hei
ght
402
plusmn05
52
99ndash4
97
562
plusmn09
83
99ndash7
20
744
plusmn10
95
71ndash8
73
773
plusmn12
25
69ndash9
55
(-01
20plusmn0
054
)(-0
224
ndash-0
049)
(-00
27plusmn0
044
)(-0
112
ndash00
30)
(00
72plusmn0
030
)(0
028
ndash01
32)
(00
86plusmn0
035
)(0
027
ndash01
61)
Tail
leng
th81
15plusmn
163
853
34ndash
102
4510
703
plusmn20
9876
87ndash
150
9097
02plusmn
118
475
06ndash
112
8797
32plusmn
119
269
96ndash
119
44(-0
072
plusmn00
89)
(-02
31ndash0
046
)(0
033
plusmn00
65)
(-00
73ndash0
144
)(-0
019
plusmn00
43)
(-00
91ndash0
056
)(-0
018
plusmn00
46)
(-01
18ndash0
058
)Fo
rele
g le
ngth
232
4plusmn4
2413
97ndash
293
730
57plusmn
572
194
6ndash37
79
294
0plusmn4
7721
03ndash
358
728
47plusmn
414
197
2ndash35
55
(-00
81plusmn0
077
)(-0
270
ndash00
13)
(00
15plusmn0
063
)(-0
135
ndash01
02)
(-00
17plusmn0
047
)(-0
112
ndash00
41)
(-00
31plusmn0
040
)(-0
136
ndash00
26)
Hind
lim
b le
ngth
343
7plusmn5
5522
80ndash
434
444
36plusmn
755
311
5ndash53
59
434
5plusmn5
9532
67ndash
503
843
08plusmn
635
310
8ndash52
01
(-00
75plusmn0
064
)(-0
224
ndash-0
008)
(00
12plusmn0
055
)(-0
097
ndash00
77)
(-00
11plusmn0
039
)(-0
087
ndash00
24)
(-00
16plusmn0
043
)(-0
105
ndash00
40)
Tabl
e 2
Des
crip
tive
data
for m
orph
olog
ical
cha
ract
eristi
cs o
f non
-rep
rodu
ctive
indi
vidu
als
of T
hisp
idus
and
T s
emita
enia
tus
in th
e Co
nser
vatio
n U
nit o
f the
Sta
te
Mon
umen
to N
atur
al G
rota
do
Angi
co P
occedilo
Redo
ndo
- SE
Lin
ear m
easu
rem
ents
are
in m
illim
etre
s th
e w
eigh
t is
in g
ram
s an
d va
lues
in p
aren
thes
es re
fer
to s
ize-
adju
sted
var
iabl
es
32
FFA Gomes et a l
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931 nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)
Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus
Taxon Availability Tropidurus semitaeniatus (n=60) Tropidurus hispidus (n=60)
n n F F n n V (mm3) V F F n n V (mm3) V
Acarina 268 074 2 333 2 014 039 000 4 667 14 049 71176 231
Araneae 523 145 20 3333 35 236 27219 227 16 2667 26 090 69893 226
Blattaria 272 076 1 007 5 833 5 017 9811 032
Chilopoda 8 002 1 167 1 007 122 010 1 167 1 003 57009 185
Coleoptera 3497 971 19 3167 32 216 13121 109 36 6000 98 341 148896 482
Dermaptera 3 001
Diplopoda 92 026 1 167 1 003 2925 009
Diplura 1 000
Diptera 5386 1495 15 2500 33 223 24458 204 10 1667 12 042 10033 033
Embioptera 1 000
Ephemeoptera 6 002
Gastropoda 24 007 2 333 4 027 3754 031 1 167 1 003 347 001
Hemiptera 20 006 2 333 2 007 30919 100
Homoptera 56 016 2 333 5 034 1739 014 3 500 10 035 2731 009
Hymenoptera 24908 6916 54 9000 989 6682 277634 2313 56 9333 2088 7265 867513 2811
Isopoda 9 002 1 167 1 003 2028 007
Isoptera 72 020 7 1167 39 264 4505 038 8 1333 412 1434 114157 370
Insect larvae 118 033 30 5000 309 2088 767065 6390 30 5000 175 609 1342030 4348
Lepidoptera 693 192 15 2500 21 142 32576 271 15 2500 22 077 39560 128
Mantodea 1 lt001
Organic material 5 833 055 00046 17 2833 1730 560
Mecoptera 1 lt001
Neuroptera 6 002
Odonata 3 001
Opilionidae 13 004
Orthoptera 4 667 4 027 45371 378 4 667 4 014 144351 468
Protura 2 001 000
Pseudoscorpionida 14 004 2 333 4 027 461 004 1 167 2 007 187 001
Pscoptera 1 lt001 000
Scorpionida 12 003 1 167 1 007 1299 011
Siphonoptera 1 lt001
Strepsitera 1 lt001
Thrichoptera 1 lt001
Thysanura 2 001
TOTAL 36015 100 1480 100 1200516 100 2874 100 3086566 100
B 202 296 206 226
Table 3 Summary of prey availability and diets of Tropidurus hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE n ndash number of prey n ndash percentage of prey F ndash frequency of prey V ndash volume V ndash percentage of volume
33
Interact ion of sympatr ic Tropidur idae
respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to
activity when sighted (G=04808 gl=4 p=09753 nT
hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT
semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φjk = 099)
Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
The first and second principal components of a PCA together explained 70 of the variation in morphology of the two species The first principal component was related to SVL anterior and posterior limb length and head width The two species did not significantly differ in shape (MANOVA Wilkrsquos Lambda=0893 p=0566) although T hispidus is slightly larger than T semitaeniatus with a larger and higher head longer limbs and a higher body
A total of 60 stomachs were analysed for T semitaeniatus and T hispidus each Eighteen prey categories were used by T hispidus and 15 were used by T semitaeniatus The most frequent prey categories for T hispidus were Hymenoptera Coleoptera insect larvae Araneae and Lepidoptera The corresponding groups for T semitaeniatus were Hymenoptera insect larvae Araneae Coleoptera Diptera and Lepidoptera The most abundant prey types were Hymenoptera and Isoptera for T hispidus and Hymenoptera and insect larvae for T semitaeniatus Highest prey volumes were represented by insect larvae and Hymenoptera for T hispidus and insect larvae and Hymenoptera for T semitaeniatus (Table 3) Formicidae represented 9995 of the Hymenoptera ingested by the two species (Table 3) Both species also consumed plant material (28 of T hispidus individuals representing 60 of the volume of food consumed and 833 of T semitaeniatus representing 00046 of food volume
The trophic niche widths estimated for T hispidus and T semitaeniatus were 206 and 202 for prey number and 226 and 296 for prey volume respectively Overlap
was higher with regards to prey number ( φjk=096 prey volume φ jk=097) but prey number and prey volume were significantly different from each other (prey number KolmogorovndashSmirnov Dmax=01584 plt001 prey volume KolmogorovndashSmirnov Dmax=01816 plt001 Table 3) A total of 36015 invertebrates distributed into 33 categories were used to estimate prey availability in the environment The distribution of available prey differed from the consumed prey for both species (T hispidus Dmax=02267 plt001 T semitaeniatus Dmax=02294 plt001)
The mean number of prey categories consumed for each species was seven (T semitaeniatus 5ndash11 T hispidus 4ndash11) Five categories comprised more than 10 in at least one monthly sample for T hispidus (Hymenoptera insect larvae Isoptera Coleoptera and Lepidoptera) and four of these also comprised more than 10 in at least one monthly sample for T semitaeniatus (all except Lepidoptera) The largest niche widths (B) were observed in February (254) June (248) April (245) and May (204) for T hispidus and in July (310) February (289) June (284) and May (221) for T semitaeniatus Diet overlap was high (Oslashgt050) in all months except April (011) and December (020) However significant differences between the diets were found in December February April May and August (Table 4)
The proportion of items most used in the diets was similar to available prey in January April September and October for T hispidus and in December January September and October for T semitaeniatus (Table 4) The prey availability occurred between December 2008 and March 2009 and between October and November 2009 (Table 4) The numbers of available prey categories ranged from eight (August) to 19 (February) The highest diversity of available prey was observed in May (378) (Table 4)
Focusing on the two most common food items Hymenoptera were most abundantly available in December 2008 and January 2009 and between September and November 2009 (Table 4) Tropidurus semitaeniatus largely consumed Hymenoptera (over 50 of diet) in the months of December 2008 January March and July to November 2009 whereas insect larvae were more consumed in February April May and June For T hispidus Hymenoptera comprised gt50 of the diet in all month except December and February (Table 4) Insect larvae never exceeded 50 of the number of prey consumed
A strong relationship was seen when comparing the morphology of the head of each species Tropidurus with the dimensions of prey actually consumed by them (Table 5) The first canonical variable for T semitaeniatus showed an inverse relationship in which animals with narrower heads were related to larger prey (Table 5) Already T hispidus for the first canonical variable was significantly positive for the relation between animals with large heads and longer prey (Table 5)
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
28
FFA Gomes et a l
MATERIALS AND METHODS
The Caatinga has an estimated area of 800000 km2 in northeastern Brazil extending from 2deg54rsquo to 17deg21rsquoS (Prado 2005) Shallow flagstones crystalline soils and irregular rainfall contribute to xeromorphic vegetation (Chiang amp Koutavas 2004 Krol et al 2001 Prado 2005) Annual precipitation ranges from 240ndash1500 mm (Sampaio 1995 Prado 2005) Despite high annual variation long periods of drought are common (Nimer 1972 Reis et al 2006) Populations of T hispidus and T semitaeniatus were studied in the State Conservation Unit of Monumento Natural Grota do Angico located in the semi-arid region of Sergipe state (Brazil 9deg41rsquoS and 38deg31rsquoW) between the municipalities of Poccedilo Redondo and Canindeacute de Satildeo Francisco (Fig 1) The Conservation Unit has an area of 2183 ha and its vegetation is typical of the Caatinga biome The average annual precipitation is 500 mm and the altitude ranges from 10 to 200 m (Ruiz-Esparza et al 2011)
Fig 1 Location of the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE (Image Sidney Feitosa Gouveia)
The study was undertaken between December 2008 and November 2009 Data collections were made on three consecutive days in each month between 0600 and 1730 hours each day Three flat areas measuring 450times20 m (27 ha) were demarcated with a 50-m tape measure in the bedrocks of dry streams Active searches were employed to achieve systematic surveys Lizards were captured with nylon ties attached to fishing rods (25 m) Observations were undertaken over one day in each area For each captured lizard we recorded time of capture substrate when located (1) and after (2) the approach of the observer (rock tree rock crevice litter bromeliad lair excreta and cactus) activity when located (1) and after (2) the approach of the observer (motionless walking running agonism foraging interacted with lace) sun exposure (sun shadow or mosaic) perch height and weather conditions (sunny cloudy drizzle or rainy) We measured snoutndashvent length (SVL) tail length body length and width head length width and height and length of both limbs (right side of the body) using a digital caliper with an accuracy of
001 mm (Faria amp Arauacutejo 2004) Mass was also recorded using a Pesolareg balance (accuracy 05 g) Captured lizards were marked with Corrector water-based white colour to prevent recapture After measurements animals were released at the site of capture
Five specimens of each species per month were sacrificed using a lidocaine solution for diet analysis Specimens were fixed in 10 formalin and preserved in 70 ethanol and deposited in the Coleccedilatildeo Herpetoloacutegica da Universidade Federal de Sergipe (CHUFS) Ingested items were identified to the lowest possible taxonomic level Whole specimens were counted and their length and width was measured with a digital caliper (accuracy 001 mm) Prey volume was estimated using the formula for an ellipsoid (volume=(πlengthwidthsup2)6 Magnusson et al 2003) or through measurement in a water column using a graduated cylinder (plant material) Prey availability was estimated using monthly collections Fifteen pitfall traps (250 ml plastic pots) were placed in each area at a minimum distance of 5 m from each other for three consecutive days Each trap contained a solution of water salt and detergent for conserving invertebrates until they were transferred to 70 ethanol
The data were analysed using Systat v120 and BioEstat v50 for Windows A 5 significance level was applied Normality of the samples was tested using a ShapirondashWilkrsquos test in order to determine whether parametric or nonparametric analysis should be used Before analysis all morphometric variables were log10-transformed in order to convert the sample to a normal distribution and reduce scale effects For animals with broken or regenerated tails the original length was estimated using a regression model (SVLxtail length Faria amp Arauacutejo 2004) Body size was defined as an isometric variable following the protocol of Somers (1986) by which the scores of an isometric vector initially set at plt05 were obtained by multiplication of the matrix n x p of the log10-transformed data where n is the number of observations and p the isometric eigenvector (Jolicoeur 1963 Somers 1986) The residuals of the regressions of each log10-transformed variable with body size was used A principal component analysis (PCA) of size-adjusted morphological variables served to examine possible differences in morphology between species To test if the differences in form between the species were significant we undertook a multivariate analysis of variance (MANOVA) on the first five factors of the PCA The body size and mass of the two species were also compared by variance analysis (ANOVA)
The numerical and volumetric compositions of the prey categories consumed by the two species were compared using a KolmogorovndashSmirnov test on a monthly basis The widths of food niches (number and volume of prey) spatial niches (substrates and perch height) and temporal niches (time of activity period in which the animal remains exposed) were calculated using the inverse of Simpsonrsquos (1949) diversity index
B= 1
sumi = 1
n
p i2
29
Interact ion of sympatr ic Tropidur idae
where p is the proportion of resource category (trophic spatial or temporal) used and n is the number of resource categories adopted B ranges between 1 (exclusive use of a resource type) and 0 (homogeneous use of all types of resources) The estimated availability (total and monthly) of food resources was also measured using this method
The overlap between the food spatial and temporal niches were calculated using the formula for symmetrical overlap (Pianka 1973)
sum sum
sum
= =
==n
i
n
iikij
nikij
jk
pp
pp
1 1
22
1φ
where j and k represent different species Values close to zero indicate no similarity in resource use and values close to one indicate the similar use of such resources This index was also adopted to compare prey categories ingested with those available in the environments A canonical correlation between two set of variables (maximum length and maximum width of prey versus length width and height of the head) was used to investigate the relationship between the prey dimensions and head measurements
RESULTSIn total 1760 observations were made (422 for T hispidus and 1338 for T semitaeniatus) Morphometric and diet analyses were performed using a total of 102 specimens comprising 51 T hispidus (9 males 9 females and 33 young) and 51 T semitaeniatus (12 males 9 females and 30 young)
No significant differences were observed between both species with respect to substrate use (G=93421 gl=7 p=0229 nT hispidus=421 nT semitaeniatus=1333) In total 8313 and 9317 of T hispidus and T semitaeniatus were found on rocks (Fig 2A) and niche space width (B) was 142 and 115 respectively Overlap in use of microhabitats was high ( φjk=099) The average perch height was 6322plusmn6607 cm (n=300) for T hispidus and 5636plusmn5130 cm (n=912) for T semitaeniatus (including animals found on the ground Fig 2B) without significant differences (MannndashWhitney U=4250 p=05708 n=1212) Niche widths (B) of perch height were 289 for T hispidus and 273 for T semitaeniatus with a high overlap between species ( φjk=099)
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931
Fig 2 Relative frequencies of (A) substrate use when located (B) perch height use (C) weather condition (D) sun exposure (E) activity levels across the day (F) behaviour when sighted (G) behaviour when escaping from the observer (H) substrate use after the approach of the observer of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE
30
FFA Gomes et a l
Tabl
e 1
Des
crip
tive
data
for
mor
phol
ogic
al c
hara
cter
istics
of r
epro
ducti
ve in
divi
dual
s of
T h
ispi
dus
and
T s
emita
enia
tus
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E L
inea
r mea
sure
men
ts a
re in
mill
imet
res
the
wei
ght i
s in
gra
ms
and
valu
es in
par
enth
eses
refe
r to
size-
adju
sted
var
iabl
es
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=9
)M
ales
(n=1
2)Fe
mal
es (n
=9)
Mal
es (n
=9)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
352
plusmn05
32
68ndash4
25
648
plusmn13
43
48ndash8
33
105
0plusmn2
197
81ndash1
358
155
5plusmn6
342
09ndash2
399
Mas
s6
99plusmn1
00
585
ndash90
014
69plusmn
391
800
ndash20
2523
48plusmn
553
165
0ndash31
00
312
2plusmn14
17
142
5ndash52
00
(00
52plusmn0
110
)(-0
068
ndash02
42)
(-00
94plusmn0
268
)(-0
846
ndash01
60)
(00
75plusmn0
127
)(-0
085
ndash03
27)
(00
04plusmn0
061
)(-0
100
ndash00
81)
SVL
651
6plusmn3
6759
69-
719
979
68plusmn
456
731
7ndash87
32
840
5plusmn7
9074
16-
961
195
54plusmn
136
471
19ndash
114
08(0
047
plusmn00
20)
(00
17ndash0
073
)(0
073
plusmn00
14)
(00
49ndash0
095
)(0
017
plusmn00
15)
(-00
10ndash0
043
)(-0
028
plusmn00
65)
(-01
25ndash0
110
)Bo
dy w
idth
202
5plusmn1
5417
61ndash
223
723
08plusmn
414
152
3ndash29
83
250
0plusmn2
0619
74-
282
124
82plusmn
404
164
2ndash31
06
(00
97plusmn0
030
)(0
043
ndash01
33)
(00
86plusmn0
061
)(-0
062
ndash01
76)
(00
46plusmn0
039
)(-0
015
ndash01
01)
(-00
62plusmn0
056
)(-0
148
ndash00
32)
Body
hei
ght
745
plusmn11
15
36ndash9
10
848
plusmn10
96
64ndash9
93
140
7plusmn1
4611
22ndash
163
915
64plusmn
439
439
ndash22
09(0
015
plusmn00
60)
(-01
00ndash0
097
)(-0
021
plusmn00
54)
(-01
67ndash0
048
)(0
077
plusmn00
55)
(-00
07ndash0
162
)(-0
055
plusmn01
01)
(-02
26ndash0
073
)He
ad w
idth
120
3plusmn0
7311
04ndash
135
015
61plusmn
172
112
5ndash18
00
171
9plusmn1
7115
21ndash
197
419
93plusmn
395
116
2ndash23
99
(00
11plusmn0
020
)(-0
017
ndash00
49)
(00
57plusmn0
037
)(-0
020
ndash01
02)
(00
16plusmn0
020
)(-0
018
ndash00
49)
(-00
32plusmn0
047
)(-0
109
ndash00
45)
Head
leng
th17
16plusmn
164
125
7ndash18
84
214
4plusmn1
8117
24ndash
248
023
64plusmn
239
208
5ndash26
86
326
1plusmn18
45
168
1ndash91
82
(00
08plusmn0
044
)(-0
112
ndash00
43)
(00
44plusmn0
019
)(0
014
ndash00
79)
(00
02plusmn0
013
)(-0
017
ndash00
33)
(-00
01plusmn0
177
)(-0
153
ndash05
62)
Head
hei
ght
580
plusmn03
74
97ndash6
37
717
plusmn07
65
44ndash8
40
103
1plusmn1
009
23ndash1
240
120
2plusmn3
304
18ndash1
777
(-00
26plusmn0
022
)(-0
067
ndash00
02)
(-00
10plusmn0
029
)(-0
069
ndash00
30)
(00
42plusmn0
025
)(0
002
ndash00
76)
(-00
42plusmn0
061
)(-0
127
ndash00
84)
Tail
leng
th98
60
plusmn67
589
72ndash
116
8713
155
plusmn12
5110
487
ndash149
18
122
44plusmn1
716
887
2ndash14
131
144
13plusmn1
902
111
62ndash1
713
6(-0
004
plusmn00
28)
(-00
36ndash0
070
)(0
078
plusmn00
42)
(-00
10ndash0
148
)(-0
111
plusmn00
56)
(-01
11ndash0
056
)(-0
014
plusmn00
55)
(-00
82ndash0
080
)Fo
rele
g le
ngth
326
6plusmn1
6429
99ndash
350
039
83plusmn
303
932
55ndash
444
340
41plusmn
256
361
3ndash43
83
460
5plusmn7
6233
27ndash
564
0(0
044
plusmn00
18)
(00
06ndash0
063
)(0
073
plusmn00
19)
(00
40ndash0
106
)(0
009
plusmn00
23)
(-00
42ndash0
042
)(-0
029
plusmn00
53)
(-01
14ndash0
074
)Hi
nd li
mb
leng
th45
25plusmn
262
402
1ndash48
89
570
5plusmn3
8249
61ndash
629
457
64plusmn
365
505
0ndash62
82
681
5plusmn9
7950
56ndash
807
2(0
022
plusmn00
20)
(-00
12ndash0
043
)(0
066
plusmn00
11)
(00
50ndash0
085
)(0
001
plusmn00
23)
(-00
42ndash0
034
)(-0
018
plusmn00
51)
(-00
97ndash0
090
)
31
Interact ion of sympatr ic Tropidur idae
nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to activity when sighted (G=04808 gl=4 p=09753 nT hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φ jk = 099) Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=1
3)M
ales
(n=1
7)Fe
mal
es (n
=15)
Mal
es (n
=18)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
100
plusmn04
90
25ndash2
01
295
plusmn16
00
75ndash6
17
388
plusmn17
81
37ndash6
84
395
plusmn17
11
15ndash6
44
Mas
s1
96plusmn0
88
075
ndash35
05
62plusmn3
84
110
ndash13
007
77plusmn3
78
200
ndash15
258
07plusmn3
38
250
ndash12
50(-0
009
plusmn00
63)
(-01
40ndash0
072
)(-0
015
plusmn00
74)
(-01
59ndash0
112
)(-0
029
plusmn01
11)
(-02
64ndash0
068
)(0
035
plusmn00
40)
(-00
24ndash0
104
)SV
L44
22plusmn
782
269
6ndash56
84
596
5plusmn10
67
416
7ndash72
76
574
2plusmn10
99
399
1ndash72
71
579
1plusmn8
7238
82ndash
693
6(-0
094
plusmn00
72)
(-02
76ndash-
000
8)(0
010
plusmn00
54)
(-00
98ndash0
075
)(-0
025
plusmn00
61)
(-01
67ndash0
031
)(-0
020
plusmn00
40)
(-01
35ndash0
022
)Bo
dy w
idth
117
2plusmn2
216
93ndash1
468
164
5plusmn3
7610
87ndash
226
615
38plusmn
330
112
6ndash21
02
154
4plusmn3
044
105
0ndash19
44
(-01
05plusmn0
086
)(-0
306
ndash-0
006)
(00
05plusmn0
073
)(-0
122
ndash00
92)
(-00
41plusmn0
060
)(-0
120
ndash00
45)
(-00
40plusmn0
058
)(-0
143
ndash00
35)
Body
hei
ght
465
plusmn11
53
37ndash7
69
626
plusmn14
803
51ndash8
73
889
plusmn21
65
38ndash1
230
897
plusmn23
25
57ndash1
219
(-01
13plusmn0
089
)(-0
256
ndash00
78)
(-00
53plusmn0
079
)(-0
224
ndash00
46)
(00
71plusmn0
068
)(-0
058
ndash01
43)
(00
72plusmn0
074
)(-0
036
ndash01
73)
Head
wid
th9
07plusmn1
80
606
ndash11
9411
91plusmn
243
762
ndash15
7212
05plusmn
171
933
ndash14
5012
28plusmn
180
920
ndash15
14(-0
082
plusmn00
74)
(-02
21ndash0
019
)(0
007
plusmn00
62)
(-01
34ndash0
075
)(-0
002
plusmn00
31)
(-00
57ndash0
053
)(0
004
plusmn00
34)
(-00
59ndash0
070
)He
ad le
ngth
129
6plusmn1
899
33ndash1
555
159
4plusmn3
129
45ndash2
022
175
7plusmn2
6013
14ndash
222
317
63plusmn
246
125
5ndash21
52
(-00
70plusmn0
057
)(-0
185
ndash00
10)
(-00
18plusmn0
075
)(-0
248
ndash00
47)
(00
10plusmn0
031
)(-0
062
ndash00
58)
(00
10plusmn0
033
)(-0
075
ndash00
53)
Head
hei
ght
402
plusmn05
52
99ndash4
97
562
plusmn09
83
99ndash7
20
744
plusmn10
95
71ndash8
73
773
plusmn12
25
69ndash9
55
(-01
20plusmn0
054
)(-0
224
ndash-0
049)
(-00
27plusmn0
044
)(-0
112
ndash00
30)
(00
72plusmn0
030
)(0
028
ndash01
32)
(00
86plusmn0
035
)(0
027
ndash01
61)
Tail
leng
th81
15plusmn
163
853
34ndash
102
4510
703
plusmn20
9876
87ndash
150
9097
02plusmn
118
475
06ndash
112
8797
32plusmn
119
269
96ndash
119
44(-0
072
plusmn00
89)
(-02
31ndash0
046
)(0
033
plusmn00
65)
(-00
73ndash0
144
)(-0
019
plusmn00
43)
(-00
91ndash0
056
)(-0
018
plusmn00
46)
(-01
18ndash0
058
)Fo
rele
g le
ngth
232
4plusmn4
2413
97ndash
293
730
57plusmn
572
194
6ndash37
79
294
0plusmn4
7721
03ndash
358
728
47plusmn
414
197
2ndash35
55
(-00
81plusmn0
077
)(-0
270
ndash00
13)
(00
15plusmn0
063
)(-0
135
ndash01
02)
(-00
17plusmn0
047
)(-0
112
ndash00
41)
(-00
31plusmn0
040
)(-0
136
ndash00
26)
Hind
lim
b le
ngth
343
7plusmn5
5522
80ndash
434
444
36plusmn
755
311
5ndash53
59
434
5plusmn5
9532
67ndash
503
843
08plusmn
635
310
8ndash52
01
(-00
75plusmn0
064
)(-0
224
ndash-0
008)
(00
12plusmn0
055
)(-0
097
ndash00
77)
(-00
11plusmn0
039
)(-0
087
ndash00
24)
(-00
16plusmn0
043
)(-0
105
ndash00
40)
Tabl
e 2
Des
crip
tive
data
for m
orph
olog
ical
cha
ract
eristi
cs o
f non
-rep
rodu
ctive
indi
vidu
als
of T
hisp
idus
and
T s
emita
enia
tus
in th
e Co
nser
vatio
n U
nit o
f the
Sta
te
Mon
umen
to N
atur
al G
rota
do
Angi
co P
occedilo
Redo
ndo
- SE
Lin
ear m
easu
rem
ents
are
in m
illim
etre
s th
e w
eigh
t is
in g
ram
s an
d va
lues
in p
aren
thes
es re
fer
to s
ize-
adju
sted
var
iabl
es
32
FFA Gomes et a l
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931 nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)
Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus
Taxon Availability Tropidurus semitaeniatus (n=60) Tropidurus hispidus (n=60)
n n F F n n V (mm3) V F F n n V (mm3) V
Acarina 268 074 2 333 2 014 039 000 4 667 14 049 71176 231
Araneae 523 145 20 3333 35 236 27219 227 16 2667 26 090 69893 226
Blattaria 272 076 1 007 5 833 5 017 9811 032
Chilopoda 8 002 1 167 1 007 122 010 1 167 1 003 57009 185
Coleoptera 3497 971 19 3167 32 216 13121 109 36 6000 98 341 148896 482
Dermaptera 3 001
Diplopoda 92 026 1 167 1 003 2925 009
Diplura 1 000
Diptera 5386 1495 15 2500 33 223 24458 204 10 1667 12 042 10033 033
Embioptera 1 000
Ephemeoptera 6 002
Gastropoda 24 007 2 333 4 027 3754 031 1 167 1 003 347 001
Hemiptera 20 006 2 333 2 007 30919 100
Homoptera 56 016 2 333 5 034 1739 014 3 500 10 035 2731 009
Hymenoptera 24908 6916 54 9000 989 6682 277634 2313 56 9333 2088 7265 867513 2811
Isopoda 9 002 1 167 1 003 2028 007
Isoptera 72 020 7 1167 39 264 4505 038 8 1333 412 1434 114157 370
Insect larvae 118 033 30 5000 309 2088 767065 6390 30 5000 175 609 1342030 4348
Lepidoptera 693 192 15 2500 21 142 32576 271 15 2500 22 077 39560 128
Mantodea 1 lt001
Organic material 5 833 055 00046 17 2833 1730 560
Mecoptera 1 lt001
Neuroptera 6 002
Odonata 3 001
Opilionidae 13 004
Orthoptera 4 667 4 027 45371 378 4 667 4 014 144351 468
Protura 2 001 000
Pseudoscorpionida 14 004 2 333 4 027 461 004 1 167 2 007 187 001
Pscoptera 1 lt001 000
Scorpionida 12 003 1 167 1 007 1299 011
Siphonoptera 1 lt001
Strepsitera 1 lt001
Thrichoptera 1 lt001
Thysanura 2 001
TOTAL 36015 100 1480 100 1200516 100 2874 100 3086566 100
B 202 296 206 226
Table 3 Summary of prey availability and diets of Tropidurus hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE n ndash number of prey n ndash percentage of prey F ndash frequency of prey V ndash volume V ndash percentage of volume
33
Interact ion of sympatr ic Tropidur idae
respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to
activity when sighted (G=04808 gl=4 p=09753 nT
hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT
semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φjk = 099)
Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
The first and second principal components of a PCA together explained 70 of the variation in morphology of the two species The first principal component was related to SVL anterior and posterior limb length and head width The two species did not significantly differ in shape (MANOVA Wilkrsquos Lambda=0893 p=0566) although T hispidus is slightly larger than T semitaeniatus with a larger and higher head longer limbs and a higher body
A total of 60 stomachs were analysed for T semitaeniatus and T hispidus each Eighteen prey categories were used by T hispidus and 15 were used by T semitaeniatus The most frequent prey categories for T hispidus were Hymenoptera Coleoptera insect larvae Araneae and Lepidoptera The corresponding groups for T semitaeniatus were Hymenoptera insect larvae Araneae Coleoptera Diptera and Lepidoptera The most abundant prey types were Hymenoptera and Isoptera for T hispidus and Hymenoptera and insect larvae for T semitaeniatus Highest prey volumes were represented by insect larvae and Hymenoptera for T hispidus and insect larvae and Hymenoptera for T semitaeniatus (Table 3) Formicidae represented 9995 of the Hymenoptera ingested by the two species (Table 3) Both species also consumed plant material (28 of T hispidus individuals representing 60 of the volume of food consumed and 833 of T semitaeniatus representing 00046 of food volume
The trophic niche widths estimated for T hispidus and T semitaeniatus were 206 and 202 for prey number and 226 and 296 for prey volume respectively Overlap
was higher with regards to prey number ( φjk=096 prey volume φ jk=097) but prey number and prey volume were significantly different from each other (prey number KolmogorovndashSmirnov Dmax=01584 plt001 prey volume KolmogorovndashSmirnov Dmax=01816 plt001 Table 3) A total of 36015 invertebrates distributed into 33 categories were used to estimate prey availability in the environment The distribution of available prey differed from the consumed prey for both species (T hispidus Dmax=02267 plt001 T semitaeniatus Dmax=02294 plt001)
The mean number of prey categories consumed for each species was seven (T semitaeniatus 5ndash11 T hispidus 4ndash11) Five categories comprised more than 10 in at least one monthly sample for T hispidus (Hymenoptera insect larvae Isoptera Coleoptera and Lepidoptera) and four of these also comprised more than 10 in at least one monthly sample for T semitaeniatus (all except Lepidoptera) The largest niche widths (B) were observed in February (254) June (248) April (245) and May (204) for T hispidus and in July (310) February (289) June (284) and May (221) for T semitaeniatus Diet overlap was high (Oslashgt050) in all months except April (011) and December (020) However significant differences between the diets were found in December February April May and August (Table 4)
The proportion of items most used in the diets was similar to available prey in January April September and October for T hispidus and in December January September and October for T semitaeniatus (Table 4) The prey availability occurred between December 2008 and March 2009 and between October and November 2009 (Table 4) The numbers of available prey categories ranged from eight (August) to 19 (February) The highest diversity of available prey was observed in May (378) (Table 4)
Focusing on the two most common food items Hymenoptera were most abundantly available in December 2008 and January 2009 and between September and November 2009 (Table 4) Tropidurus semitaeniatus largely consumed Hymenoptera (over 50 of diet) in the months of December 2008 January March and July to November 2009 whereas insect larvae were more consumed in February April May and June For T hispidus Hymenoptera comprised gt50 of the diet in all month except December and February (Table 4) Insect larvae never exceeded 50 of the number of prey consumed
A strong relationship was seen when comparing the morphology of the head of each species Tropidurus with the dimensions of prey actually consumed by them (Table 5) The first canonical variable for T semitaeniatus showed an inverse relationship in which animals with narrower heads were related to larger prey (Table 5) Already T hispidus for the first canonical variable was significantly positive for the relation between animals with large heads and longer prey (Table 5)
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
29
Interact ion of sympatr ic Tropidur idae
where p is the proportion of resource category (trophic spatial or temporal) used and n is the number of resource categories adopted B ranges between 1 (exclusive use of a resource type) and 0 (homogeneous use of all types of resources) The estimated availability (total and monthly) of food resources was also measured using this method
The overlap between the food spatial and temporal niches were calculated using the formula for symmetrical overlap (Pianka 1973)
sum sum
sum
= =
==n
i
n
iikij
nikij
jk
pp
pp
1 1
22
1φ
where j and k represent different species Values close to zero indicate no similarity in resource use and values close to one indicate the similar use of such resources This index was also adopted to compare prey categories ingested with those available in the environments A canonical correlation between two set of variables (maximum length and maximum width of prey versus length width and height of the head) was used to investigate the relationship between the prey dimensions and head measurements
RESULTSIn total 1760 observations were made (422 for T hispidus and 1338 for T semitaeniatus) Morphometric and diet analyses were performed using a total of 102 specimens comprising 51 T hispidus (9 males 9 females and 33 young) and 51 T semitaeniatus (12 males 9 females and 30 young)
No significant differences were observed between both species with respect to substrate use (G=93421 gl=7 p=0229 nT hispidus=421 nT semitaeniatus=1333) In total 8313 and 9317 of T hispidus and T semitaeniatus were found on rocks (Fig 2A) and niche space width (B) was 142 and 115 respectively Overlap in use of microhabitats was high ( φjk=099) The average perch height was 6322plusmn6607 cm (n=300) for T hispidus and 5636plusmn5130 cm (n=912) for T semitaeniatus (including animals found on the ground Fig 2B) without significant differences (MannndashWhitney U=4250 p=05708 n=1212) Niche widths (B) of perch height were 289 for T hispidus and 273 for T semitaeniatus with a high overlap between species ( φjk=099)
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931
Fig 2 Relative frequencies of (A) substrate use when located (B) perch height use (C) weather condition (D) sun exposure (E) activity levels across the day (F) behaviour when sighted (G) behaviour when escaping from the observer (H) substrate use after the approach of the observer of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE
30
FFA Gomes et a l
Tabl
e 1
Des
crip
tive
data
for
mor
phol
ogic
al c
hara
cter
istics
of r
epro
ducti
ve in
divi
dual
s of
T h
ispi
dus
and
T s
emita
enia
tus
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E L
inea
r mea
sure
men
ts a
re in
mill
imet
res
the
wei
ght i
s in
gra
ms
and
valu
es in
par
enth
eses
refe
r to
size-
adju
sted
var
iabl
es
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=9
)M
ales
(n=1
2)Fe
mal
es (n
=9)
Mal
es (n
=9)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
352
plusmn05
32
68ndash4
25
648
plusmn13
43
48ndash8
33
105
0plusmn2
197
81ndash1
358
155
5plusmn6
342
09ndash2
399
Mas
s6
99plusmn1
00
585
ndash90
014
69plusmn
391
800
ndash20
2523
48plusmn
553
165
0ndash31
00
312
2plusmn14
17
142
5ndash52
00
(00
52plusmn0
110
)(-0
068
ndash02
42)
(-00
94plusmn0
268
)(-0
846
ndash01
60)
(00
75plusmn0
127
)(-0
085
ndash03
27)
(00
04plusmn0
061
)(-0
100
ndash00
81)
SVL
651
6plusmn3
6759
69-
719
979
68plusmn
456
731
7ndash87
32
840
5plusmn7
9074
16-
961
195
54plusmn
136
471
19ndash
114
08(0
047
plusmn00
20)
(00
17ndash0
073
)(0
073
plusmn00
14)
(00
49ndash0
095
)(0
017
plusmn00
15)
(-00
10ndash0
043
)(-0
028
plusmn00
65)
(-01
25ndash0
110
)Bo
dy w
idth
202
5plusmn1
5417
61ndash
223
723
08plusmn
414
152
3ndash29
83
250
0plusmn2
0619
74-
282
124
82plusmn
404
164
2ndash31
06
(00
97plusmn0
030
)(0
043
ndash01
33)
(00
86plusmn0
061
)(-0
062
ndash01
76)
(00
46plusmn0
039
)(-0
015
ndash01
01)
(-00
62plusmn0
056
)(-0
148
ndash00
32)
Body
hei
ght
745
plusmn11
15
36ndash9
10
848
plusmn10
96
64ndash9
93
140
7plusmn1
4611
22ndash
163
915
64plusmn
439
439
ndash22
09(0
015
plusmn00
60)
(-01
00ndash0
097
)(-0
021
plusmn00
54)
(-01
67ndash0
048
)(0
077
plusmn00
55)
(-00
07ndash0
162
)(-0
055
plusmn01
01)
(-02
26ndash0
073
)He
ad w
idth
120
3plusmn0
7311
04ndash
135
015
61plusmn
172
112
5ndash18
00
171
9plusmn1
7115
21ndash
197
419
93plusmn
395
116
2ndash23
99
(00
11plusmn0
020
)(-0
017
ndash00
49)
(00
57plusmn0
037
)(-0
020
ndash01
02)
(00
16plusmn0
020
)(-0
018
ndash00
49)
(-00
32plusmn0
047
)(-0
109
ndash00
45)
Head
leng
th17
16plusmn
164
125
7ndash18
84
214
4plusmn1
8117
24ndash
248
023
64plusmn
239
208
5ndash26
86
326
1plusmn18
45
168
1ndash91
82
(00
08plusmn0
044
)(-0
112
ndash00
43)
(00
44plusmn0
019
)(0
014
ndash00
79)
(00
02plusmn0
013
)(-0
017
ndash00
33)
(-00
01plusmn0
177
)(-0
153
ndash05
62)
Head
hei
ght
580
plusmn03
74
97ndash6
37
717
plusmn07
65
44ndash8
40
103
1plusmn1
009
23ndash1
240
120
2plusmn3
304
18ndash1
777
(-00
26plusmn0
022
)(-0
067
ndash00
02)
(-00
10plusmn0
029
)(-0
069
ndash00
30)
(00
42plusmn0
025
)(0
002
ndash00
76)
(-00
42plusmn0
061
)(-0
127
ndash00
84)
Tail
leng
th98
60
plusmn67
589
72ndash
116
8713
155
plusmn12
5110
487
ndash149
18
122
44plusmn1
716
887
2ndash14
131
144
13plusmn1
902
111
62ndash1
713
6(-0
004
plusmn00
28)
(-00
36ndash0
070
)(0
078
plusmn00
42)
(-00
10ndash0
148
)(-0
111
plusmn00
56)
(-01
11ndash0
056
)(-0
014
plusmn00
55)
(-00
82ndash0
080
)Fo
rele
g le
ngth
326
6plusmn1
6429
99ndash
350
039
83plusmn
303
932
55ndash
444
340
41plusmn
256
361
3ndash43
83
460
5plusmn7
6233
27ndash
564
0(0
044
plusmn00
18)
(00
06ndash0
063
)(0
073
plusmn00
19)
(00
40ndash0
106
)(0
009
plusmn00
23)
(-00
42ndash0
042
)(-0
029
plusmn00
53)
(-01
14ndash0
074
)Hi
nd li
mb
leng
th45
25plusmn
262
402
1ndash48
89
570
5plusmn3
8249
61ndash
629
457
64plusmn
365
505
0ndash62
82
681
5plusmn9
7950
56ndash
807
2(0
022
plusmn00
20)
(-00
12ndash0
043
)(0
066
plusmn00
11)
(00
50ndash0
085
)(0
001
plusmn00
23)
(-00
42ndash0
034
)(-0
018
plusmn00
51)
(-00
97ndash0
090
)
31
Interact ion of sympatr ic Tropidur idae
nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to activity when sighted (G=04808 gl=4 p=09753 nT hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φ jk = 099) Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=1
3)M
ales
(n=1
7)Fe
mal
es (n
=15)
Mal
es (n
=18)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
100
plusmn04
90
25ndash2
01
295
plusmn16
00
75ndash6
17
388
plusmn17
81
37ndash6
84
395
plusmn17
11
15ndash6
44
Mas
s1
96plusmn0
88
075
ndash35
05
62plusmn3
84
110
ndash13
007
77plusmn3
78
200
ndash15
258
07plusmn3
38
250
ndash12
50(-0
009
plusmn00
63)
(-01
40ndash0
072
)(-0
015
plusmn00
74)
(-01
59ndash0
112
)(-0
029
plusmn01
11)
(-02
64ndash0
068
)(0
035
plusmn00
40)
(-00
24ndash0
104
)SV
L44
22plusmn
782
269
6ndash56
84
596
5plusmn10
67
416
7ndash72
76
574
2plusmn10
99
399
1ndash72
71
579
1plusmn8
7238
82ndash
693
6(-0
094
plusmn00
72)
(-02
76ndash-
000
8)(0
010
plusmn00
54)
(-00
98ndash0
075
)(-0
025
plusmn00
61)
(-01
67ndash0
031
)(-0
020
plusmn00
40)
(-01
35ndash0
022
)Bo
dy w
idth
117
2plusmn2
216
93ndash1
468
164
5plusmn3
7610
87ndash
226
615
38plusmn
330
112
6ndash21
02
154
4plusmn3
044
105
0ndash19
44
(-01
05plusmn0
086
)(-0
306
ndash-0
006)
(00
05plusmn0
073
)(-0
122
ndash00
92)
(-00
41plusmn0
060
)(-0
120
ndash00
45)
(-00
40plusmn0
058
)(-0
143
ndash00
35)
Body
hei
ght
465
plusmn11
53
37ndash7
69
626
plusmn14
803
51ndash8
73
889
plusmn21
65
38ndash1
230
897
plusmn23
25
57ndash1
219
(-01
13plusmn0
089
)(-0
256
ndash00
78)
(-00
53plusmn0
079
)(-0
224
ndash00
46)
(00
71plusmn0
068
)(-0
058
ndash01
43)
(00
72plusmn0
074
)(-0
036
ndash01
73)
Head
wid
th9
07plusmn1
80
606
ndash11
9411
91plusmn
243
762
ndash15
7212
05plusmn
171
933
ndash14
5012
28plusmn
180
920
ndash15
14(-0
082
plusmn00
74)
(-02
21ndash0
019
)(0
007
plusmn00
62)
(-01
34ndash0
075
)(-0
002
plusmn00
31)
(-00
57ndash0
053
)(0
004
plusmn00
34)
(-00
59ndash0
070
)He
ad le
ngth
129
6plusmn1
899
33ndash1
555
159
4plusmn3
129
45ndash2
022
175
7plusmn2
6013
14ndash
222
317
63plusmn
246
125
5ndash21
52
(-00
70plusmn0
057
)(-0
185
ndash00
10)
(-00
18plusmn0
075
)(-0
248
ndash00
47)
(00
10plusmn0
031
)(-0
062
ndash00
58)
(00
10plusmn0
033
)(-0
075
ndash00
53)
Head
hei
ght
402
plusmn05
52
99ndash4
97
562
plusmn09
83
99ndash7
20
744
plusmn10
95
71ndash8
73
773
plusmn12
25
69ndash9
55
(-01
20plusmn0
054
)(-0
224
ndash-0
049)
(-00
27plusmn0
044
)(-0
112
ndash00
30)
(00
72plusmn0
030
)(0
028
ndash01
32)
(00
86plusmn0
035
)(0
027
ndash01
61)
Tail
leng
th81
15plusmn
163
853
34ndash
102
4510
703
plusmn20
9876
87ndash
150
9097
02plusmn
118
475
06ndash
112
8797
32plusmn
119
269
96ndash
119
44(-0
072
plusmn00
89)
(-02
31ndash0
046
)(0
033
plusmn00
65)
(-00
73ndash0
144
)(-0
019
plusmn00
43)
(-00
91ndash0
056
)(-0
018
plusmn00
46)
(-01
18ndash0
058
)Fo
rele
g le
ngth
232
4plusmn4
2413
97ndash
293
730
57plusmn
572
194
6ndash37
79
294
0plusmn4
7721
03ndash
358
728
47plusmn
414
197
2ndash35
55
(-00
81plusmn0
077
)(-0
270
ndash00
13)
(00
15plusmn0
063
)(-0
135
ndash01
02)
(-00
17plusmn0
047
)(-0
112
ndash00
41)
(-00
31plusmn0
040
)(-0
136
ndash00
26)
Hind
lim
b le
ngth
343
7plusmn5
5522
80ndash
434
444
36plusmn
755
311
5ndash53
59
434
5plusmn5
9532
67ndash
503
843
08plusmn
635
310
8ndash52
01
(-00
75plusmn0
064
)(-0
224
ndash-0
008)
(00
12plusmn0
055
)(-0
097
ndash00
77)
(-00
11plusmn0
039
)(-0
087
ndash00
24)
(-00
16plusmn0
043
)(-0
105
ndash00
40)
Tabl
e 2
Des
crip
tive
data
for m
orph
olog
ical
cha
ract
eristi
cs o
f non
-rep
rodu
ctive
indi
vidu
als
of T
hisp
idus
and
T s
emita
enia
tus
in th
e Co
nser
vatio
n U
nit o
f the
Sta
te
Mon
umen
to N
atur
al G
rota
do
Angi
co P
occedilo
Redo
ndo
- SE
Lin
ear m
easu
rem
ents
are
in m
illim
etre
s th
e w
eigh
t is
in g
ram
s an
d va
lues
in p
aren
thes
es re
fer
to s
ize-
adju
sted
var
iabl
es
32
FFA Gomes et a l
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931 nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)
Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus
Taxon Availability Tropidurus semitaeniatus (n=60) Tropidurus hispidus (n=60)
n n F F n n V (mm3) V F F n n V (mm3) V
Acarina 268 074 2 333 2 014 039 000 4 667 14 049 71176 231
Araneae 523 145 20 3333 35 236 27219 227 16 2667 26 090 69893 226
Blattaria 272 076 1 007 5 833 5 017 9811 032
Chilopoda 8 002 1 167 1 007 122 010 1 167 1 003 57009 185
Coleoptera 3497 971 19 3167 32 216 13121 109 36 6000 98 341 148896 482
Dermaptera 3 001
Diplopoda 92 026 1 167 1 003 2925 009
Diplura 1 000
Diptera 5386 1495 15 2500 33 223 24458 204 10 1667 12 042 10033 033
Embioptera 1 000
Ephemeoptera 6 002
Gastropoda 24 007 2 333 4 027 3754 031 1 167 1 003 347 001
Hemiptera 20 006 2 333 2 007 30919 100
Homoptera 56 016 2 333 5 034 1739 014 3 500 10 035 2731 009
Hymenoptera 24908 6916 54 9000 989 6682 277634 2313 56 9333 2088 7265 867513 2811
Isopoda 9 002 1 167 1 003 2028 007
Isoptera 72 020 7 1167 39 264 4505 038 8 1333 412 1434 114157 370
Insect larvae 118 033 30 5000 309 2088 767065 6390 30 5000 175 609 1342030 4348
Lepidoptera 693 192 15 2500 21 142 32576 271 15 2500 22 077 39560 128
Mantodea 1 lt001
Organic material 5 833 055 00046 17 2833 1730 560
Mecoptera 1 lt001
Neuroptera 6 002
Odonata 3 001
Opilionidae 13 004
Orthoptera 4 667 4 027 45371 378 4 667 4 014 144351 468
Protura 2 001 000
Pseudoscorpionida 14 004 2 333 4 027 461 004 1 167 2 007 187 001
Pscoptera 1 lt001 000
Scorpionida 12 003 1 167 1 007 1299 011
Siphonoptera 1 lt001
Strepsitera 1 lt001
Thrichoptera 1 lt001
Thysanura 2 001
TOTAL 36015 100 1480 100 1200516 100 2874 100 3086566 100
B 202 296 206 226
Table 3 Summary of prey availability and diets of Tropidurus hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE n ndash number of prey n ndash percentage of prey F ndash frequency of prey V ndash volume V ndash percentage of volume
33
Interact ion of sympatr ic Tropidur idae
respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to
activity when sighted (G=04808 gl=4 p=09753 nT
hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT
semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φjk = 099)
Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
The first and second principal components of a PCA together explained 70 of the variation in morphology of the two species The first principal component was related to SVL anterior and posterior limb length and head width The two species did not significantly differ in shape (MANOVA Wilkrsquos Lambda=0893 p=0566) although T hispidus is slightly larger than T semitaeniatus with a larger and higher head longer limbs and a higher body
A total of 60 stomachs were analysed for T semitaeniatus and T hispidus each Eighteen prey categories were used by T hispidus and 15 were used by T semitaeniatus The most frequent prey categories for T hispidus were Hymenoptera Coleoptera insect larvae Araneae and Lepidoptera The corresponding groups for T semitaeniatus were Hymenoptera insect larvae Araneae Coleoptera Diptera and Lepidoptera The most abundant prey types were Hymenoptera and Isoptera for T hispidus and Hymenoptera and insect larvae for T semitaeniatus Highest prey volumes were represented by insect larvae and Hymenoptera for T hispidus and insect larvae and Hymenoptera for T semitaeniatus (Table 3) Formicidae represented 9995 of the Hymenoptera ingested by the two species (Table 3) Both species also consumed plant material (28 of T hispidus individuals representing 60 of the volume of food consumed and 833 of T semitaeniatus representing 00046 of food volume
The trophic niche widths estimated for T hispidus and T semitaeniatus were 206 and 202 for prey number and 226 and 296 for prey volume respectively Overlap
was higher with regards to prey number ( φjk=096 prey volume φ jk=097) but prey number and prey volume were significantly different from each other (prey number KolmogorovndashSmirnov Dmax=01584 plt001 prey volume KolmogorovndashSmirnov Dmax=01816 plt001 Table 3) A total of 36015 invertebrates distributed into 33 categories were used to estimate prey availability in the environment The distribution of available prey differed from the consumed prey for both species (T hispidus Dmax=02267 plt001 T semitaeniatus Dmax=02294 plt001)
The mean number of prey categories consumed for each species was seven (T semitaeniatus 5ndash11 T hispidus 4ndash11) Five categories comprised more than 10 in at least one monthly sample for T hispidus (Hymenoptera insect larvae Isoptera Coleoptera and Lepidoptera) and four of these also comprised more than 10 in at least one monthly sample for T semitaeniatus (all except Lepidoptera) The largest niche widths (B) were observed in February (254) June (248) April (245) and May (204) for T hispidus and in July (310) February (289) June (284) and May (221) for T semitaeniatus Diet overlap was high (Oslashgt050) in all months except April (011) and December (020) However significant differences between the diets were found in December February April May and August (Table 4)
The proportion of items most used in the diets was similar to available prey in January April September and October for T hispidus and in December January September and October for T semitaeniatus (Table 4) The prey availability occurred between December 2008 and March 2009 and between October and November 2009 (Table 4) The numbers of available prey categories ranged from eight (August) to 19 (February) The highest diversity of available prey was observed in May (378) (Table 4)
Focusing on the two most common food items Hymenoptera were most abundantly available in December 2008 and January 2009 and between September and November 2009 (Table 4) Tropidurus semitaeniatus largely consumed Hymenoptera (over 50 of diet) in the months of December 2008 January March and July to November 2009 whereas insect larvae were more consumed in February April May and June For T hispidus Hymenoptera comprised gt50 of the diet in all month except December and February (Table 4) Insect larvae never exceeded 50 of the number of prey consumed
A strong relationship was seen when comparing the morphology of the head of each species Tropidurus with the dimensions of prey actually consumed by them (Table 5) The first canonical variable for T semitaeniatus showed an inverse relationship in which animals with narrower heads were related to larger prey (Table 5) Already T hispidus for the first canonical variable was significantly positive for the relation between animals with large heads and longer prey (Table 5)
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
30
FFA Gomes et a l
Tabl
e 1
Des
crip
tive
data
for
mor
phol
ogic
al c
hara
cter
istics
of r
epro
ducti
ve in
divi
dual
s of
T h
ispi
dus
and
T s
emita
enia
tus
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E L
inea
r mea
sure
men
ts a
re in
mill
imet
res
the
wei
ght i
s in
gra
ms
and
valu
es in
par
enth
eses
refe
r to
size-
adju
sted
var
iabl
es
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=9
)M
ales
(n=1
2)Fe
mal
es (n
=9)
Mal
es (n
=9)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
352
plusmn05
32
68ndash4
25
648
plusmn13
43
48ndash8
33
105
0plusmn2
197
81ndash1
358
155
5plusmn6
342
09ndash2
399
Mas
s6
99plusmn1
00
585
ndash90
014
69plusmn
391
800
ndash20
2523
48plusmn
553
165
0ndash31
00
312
2plusmn14
17
142
5ndash52
00
(00
52plusmn0
110
)(-0
068
ndash02
42)
(-00
94plusmn0
268
)(-0
846
ndash01
60)
(00
75plusmn0
127
)(-0
085
ndash03
27)
(00
04plusmn0
061
)(-0
100
ndash00
81)
SVL
651
6plusmn3
6759
69-
719
979
68plusmn
456
731
7ndash87
32
840
5plusmn7
9074
16-
961
195
54plusmn
136
471
19ndash
114
08(0
047
plusmn00
20)
(00
17ndash0
073
)(0
073
plusmn00
14)
(00
49ndash0
095
)(0
017
plusmn00
15)
(-00
10ndash0
043
)(-0
028
plusmn00
65)
(-01
25ndash0
110
)Bo
dy w
idth
202
5plusmn1
5417
61ndash
223
723
08plusmn
414
152
3ndash29
83
250
0plusmn2
0619
74-
282
124
82plusmn
404
164
2ndash31
06
(00
97plusmn0
030
)(0
043
ndash01
33)
(00
86plusmn0
061
)(-0
062
ndash01
76)
(00
46plusmn0
039
)(-0
015
ndash01
01)
(-00
62plusmn0
056
)(-0
148
ndash00
32)
Body
hei
ght
745
plusmn11
15
36ndash9
10
848
plusmn10
96
64ndash9
93
140
7plusmn1
4611
22ndash
163
915
64plusmn
439
439
ndash22
09(0
015
plusmn00
60)
(-01
00ndash0
097
)(-0
021
plusmn00
54)
(-01
67ndash0
048
)(0
077
plusmn00
55)
(-00
07ndash0
162
)(-0
055
plusmn01
01)
(-02
26ndash0
073
)He
ad w
idth
120
3plusmn0
7311
04ndash
135
015
61plusmn
172
112
5ndash18
00
171
9plusmn1
7115
21ndash
197
419
93plusmn
395
116
2ndash23
99
(00
11plusmn0
020
)(-0
017
ndash00
49)
(00
57plusmn0
037
)(-0
020
ndash01
02)
(00
16plusmn0
020
)(-0
018
ndash00
49)
(-00
32plusmn0
047
)(-0
109
ndash00
45)
Head
leng
th17
16plusmn
164
125
7ndash18
84
214
4plusmn1
8117
24ndash
248
023
64plusmn
239
208
5ndash26
86
326
1plusmn18
45
168
1ndash91
82
(00
08plusmn0
044
)(-0
112
ndash00
43)
(00
44plusmn0
019
)(0
014
ndash00
79)
(00
02plusmn0
013
)(-0
017
ndash00
33)
(-00
01plusmn0
177
)(-0
153
ndash05
62)
Head
hei
ght
580
plusmn03
74
97ndash6
37
717
plusmn07
65
44ndash8
40
103
1plusmn1
009
23ndash1
240
120
2plusmn3
304
18ndash1
777
(-00
26plusmn0
022
)(-0
067
ndash00
02)
(-00
10plusmn0
029
)(-0
069
ndash00
30)
(00
42plusmn0
025
)(0
002
ndash00
76)
(-00
42plusmn0
061
)(-0
127
ndash00
84)
Tail
leng
th98
60
plusmn67
589
72ndash
116
8713
155
plusmn12
5110
487
ndash149
18
122
44plusmn1
716
887
2ndash14
131
144
13plusmn1
902
111
62ndash1
713
6(-0
004
plusmn00
28)
(-00
36ndash0
070
)(0
078
plusmn00
42)
(-00
10ndash0
148
)(-0
111
plusmn00
56)
(-01
11ndash0
056
)(-0
014
plusmn00
55)
(-00
82ndash0
080
)Fo
rele
g le
ngth
326
6plusmn1
6429
99ndash
350
039
83plusmn
303
932
55ndash
444
340
41plusmn
256
361
3ndash43
83
460
5plusmn7
6233
27ndash
564
0(0
044
plusmn00
18)
(00
06ndash0
063
)(0
073
plusmn00
19)
(00
40ndash0
106
)(0
009
plusmn00
23)
(-00
42ndash0
042
)(-0
029
plusmn00
53)
(-01
14ndash0
074
)Hi
nd li
mb
leng
th45
25plusmn
262
402
1ndash48
89
570
5plusmn3
8249
61ndash
629
457
64plusmn
365
505
0ndash62
82
681
5plusmn9
7950
56ndash
807
2(0
022
plusmn00
20)
(-00
12ndash0
043
)(0
066
plusmn00
11)
(00
50ndash0
085
)(0
001
plusmn00
23)
(-00
42ndash0
034
)(-0
018
plusmn00
51)
(-00
97ndash0
090
)
31
Interact ion of sympatr ic Tropidur idae
nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to activity when sighted (G=04808 gl=4 p=09753 nT hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φ jk = 099) Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=1
3)M
ales
(n=1
7)Fe
mal
es (n
=15)
Mal
es (n
=18)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
100
plusmn04
90
25ndash2
01
295
plusmn16
00
75ndash6
17
388
plusmn17
81
37ndash6
84
395
plusmn17
11
15ndash6
44
Mas
s1
96plusmn0
88
075
ndash35
05
62plusmn3
84
110
ndash13
007
77plusmn3
78
200
ndash15
258
07plusmn3
38
250
ndash12
50(-0
009
plusmn00
63)
(-01
40ndash0
072
)(-0
015
plusmn00
74)
(-01
59ndash0
112
)(-0
029
plusmn01
11)
(-02
64ndash0
068
)(0
035
plusmn00
40)
(-00
24ndash0
104
)SV
L44
22plusmn
782
269
6ndash56
84
596
5plusmn10
67
416
7ndash72
76
574
2plusmn10
99
399
1ndash72
71
579
1plusmn8
7238
82ndash
693
6(-0
094
plusmn00
72)
(-02
76ndash-
000
8)(0
010
plusmn00
54)
(-00
98ndash0
075
)(-0
025
plusmn00
61)
(-01
67ndash0
031
)(-0
020
plusmn00
40)
(-01
35ndash0
022
)Bo
dy w
idth
117
2plusmn2
216
93ndash1
468
164
5plusmn3
7610
87ndash
226
615
38plusmn
330
112
6ndash21
02
154
4plusmn3
044
105
0ndash19
44
(-01
05plusmn0
086
)(-0
306
ndash-0
006)
(00
05plusmn0
073
)(-0
122
ndash00
92)
(-00
41plusmn0
060
)(-0
120
ndash00
45)
(-00
40plusmn0
058
)(-0
143
ndash00
35)
Body
hei
ght
465
plusmn11
53
37ndash7
69
626
plusmn14
803
51ndash8
73
889
plusmn21
65
38ndash1
230
897
plusmn23
25
57ndash1
219
(-01
13plusmn0
089
)(-0
256
ndash00
78)
(-00
53plusmn0
079
)(-0
224
ndash00
46)
(00
71plusmn0
068
)(-0
058
ndash01
43)
(00
72plusmn0
074
)(-0
036
ndash01
73)
Head
wid
th9
07plusmn1
80
606
ndash11
9411
91plusmn
243
762
ndash15
7212
05plusmn
171
933
ndash14
5012
28plusmn
180
920
ndash15
14(-0
082
plusmn00
74)
(-02
21ndash0
019
)(0
007
plusmn00
62)
(-01
34ndash0
075
)(-0
002
plusmn00
31)
(-00
57ndash0
053
)(0
004
plusmn00
34)
(-00
59ndash0
070
)He
ad le
ngth
129
6plusmn1
899
33ndash1
555
159
4plusmn3
129
45ndash2
022
175
7plusmn2
6013
14ndash
222
317
63plusmn
246
125
5ndash21
52
(-00
70plusmn0
057
)(-0
185
ndash00
10)
(-00
18plusmn0
075
)(-0
248
ndash00
47)
(00
10plusmn0
031
)(-0
062
ndash00
58)
(00
10plusmn0
033
)(-0
075
ndash00
53)
Head
hei
ght
402
plusmn05
52
99ndash4
97
562
plusmn09
83
99ndash7
20
744
plusmn10
95
71ndash8
73
773
plusmn12
25
69ndash9
55
(-01
20plusmn0
054
)(-0
224
ndash-0
049)
(-00
27plusmn0
044
)(-0
112
ndash00
30)
(00
72plusmn0
030
)(0
028
ndash01
32)
(00
86plusmn0
035
)(0
027
ndash01
61)
Tail
leng
th81
15plusmn
163
853
34ndash
102
4510
703
plusmn20
9876
87ndash
150
9097
02plusmn
118
475
06ndash
112
8797
32plusmn
119
269
96ndash
119
44(-0
072
plusmn00
89)
(-02
31ndash0
046
)(0
033
plusmn00
65)
(-00
73ndash0
144
)(-0
019
plusmn00
43)
(-00
91ndash0
056
)(-0
018
plusmn00
46)
(-01
18ndash0
058
)Fo
rele
g le
ngth
232
4plusmn4
2413
97ndash
293
730
57plusmn
572
194
6ndash37
79
294
0plusmn4
7721
03ndash
358
728
47plusmn
414
197
2ndash35
55
(-00
81plusmn0
077
)(-0
270
ndash00
13)
(00
15plusmn0
063
)(-0
135
ndash01
02)
(-00
17plusmn0
047
)(-0
112
ndash00
41)
(-00
31plusmn0
040
)(-0
136
ndash00
26)
Hind
lim
b le
ngth
343
7plusmn5
5522
80ndash
434
444
36plusmn
755
311
5ndash53
59
434
5plusmn5
9532
67ndash
503
843
08plusmn
635
310
8ndash52
01
(-00
75plusmn0
064
)(-0
224
ndash-0
008)
(00
12plusmn0
055
)(-0
097
ndash00
77)
(-00
11plusmn0
039
)(-0
087
ndash00
24)
(-00
16plusmn0
043
)(-0
105
ndash00
40)
Tabl
e 2
Des
crip
tive
data
for m
orph
olog
ical
cha
ract
eristi
cs o
f non
-rep
rodu
ctive
indi
vidu
als
of T
hisp
idus
and
T s
emita
enia
tus
in th
e Co
nser
vatio
n U
nit o
f the
Sta
te
Mon
umen
to N
atur
al G
rota
do
Angi
co P
occedilo
Redo
ndo
- SE
Lin
ear m
easu
rem
ents
are
in m
illim
etre
s th
e w
eigh
t is
in g
ram
s an
d va
lues
in p
aren
thes
es re
fer
to s
ize-
adju
sted
var
iabl
es
32
FFA Gomes et a l
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931 nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)
Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus
Taxon Availability Tropidurus semitaeniatus (n=60) Tropidurus hispidus (n=60)
n n F F n n V (mm3) V F F n n V (mm3) V
Acarina 268 074 2 333 2 014 039 000 4 667 14 049 71176 231
Araneae 523 145 20 3333 35 236 27219 227 16 2667 26 090 69893 226
Blattaria 272 076 1 007 5 833 5 017 9811 032
Chilopoda 8 002 1 167 1 007 122 010 1 167 1 003 57009 185
Coleoptera 3497 971 19 3167 32 216 13121 109 36 6000 98 341 148896 482
Dermaptera 3 001
Diplopoda 92 026 1 167 1 003 2925 009
Diplura 1 000
Diptera 5386 1495 15 2500 33 223 24458 204 10 1667 12 042 10033 033
Embioptera 1 000
Ephemeoptera 6 002
Gastropoda 24 007 2 333 4 027 3754 031 1 167 1 003 347 001
Hemiptera 20 006 2 333 2 007 30919 100
Homoptera 56 016 2 333 5 034 1739 014 3 500 10 035 2731 009
Hymenoptera 24908 6916 54 9000 989 6682 277634 2313 56 9333 2088 7265 867513 2811
Isopoda 9 002 1 167 1 003 2028 007
Isoptera 72 020 7 1167 39 264 4505 038 8 1333 412 1434 114157 370
Insect larvae 118 033 30 5000 309 2088 767065 6390 30 5000 175 609 1342030 4348
Lepidoptera 693 192 15 2500 21 142 32576 271 15 2500 22 077 39560 128
Mantodea 1 lt001
Organic material 5 833 055 00046 17 2833 1730 560
Mecoptera 1 lt001
Neuroptera 6 002
Odonata 3 001
Opilionidae 13 004
Orthoptera 4 667 4 027 45371 378 4 667 4 014 144351 468
Protura 2 001 000
Pseudoscorpionida 14 004 2 333 4 027 461 004 1 167 2 007 187 001
Pscoptera 1 lt001 000
Scorpionida 12 003 1 167 1 007 1299 011
Siphonoptera 1 lt001
Strepsitera 1 lt001
Thrichoptera 1 lt001
Thysanura 2 001
TOTAL 36015 100 1480 100 1200516 100 2874 100 3086566 100
B 202 296 206 226
Table 3 Summary of prey availability and diets of Tropidurus hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE n ndash number of prey n ndash percentage of prey F ndash frequency of prey V ndash volume V ndash percentage of volume
33
Interact ion of sympatr ic Tropidur idae
respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to
activity when sighted (G=04808 gl=4 p=09753 nT
hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT
semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φjk = 099)
Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
The first and second principal components of a PCA together explained 70 of the variation in morphology of the two species The first principal component was related to SVL anterior and posterior limb length and head width The two species did not significantly differ in shape (MANOVA Wilkrsquos Lambda=0893 p=0566) although T hispidus is slightly larger than T semitaeniatus with a larger and higher head longer limbs and a higher body
A total of 60 stomachs were analysed for T semitaeniatus and T hispidus each Eighteen prey categories were used by T hispidus and 15 were used by T semitaeniatus The most frequent prey categories for T hispidus were Hymenoptera Coleoptera insect larvae Araneae and Lepidoptera The corresponding groups for T semitaeniatus were Hymenoptera insect larvae Araneae Coleoptera Diptera and Lepidoptera The most abundant prey types were Hymenoptera and Isoptera for T hispidus and Hymenoptera and insect larvae for T semitaeniatus Highest prey volumes were represented by insect larvae and Hymenoptera for T hispidus and insect larvae and Hymenoptera for T semitaeniatus (Table 3) Formicidae represented 9995 of the Hymenoptera ingested by the two species (Table 3) Both species also consumed plant material (28 of T hispidus individuals representing 60 of the volume of food consumed and 833 of T semitaeniatus representing 00046 of food volume
The trophic niche widths estimated for T hispidus and T semitaeniatus were 206 and 202 for prey number and 226 and 296 for prey volume respectively Overlap
was higher with regards to prey number ( φjk=096 prey volume φ jk=097) but prey number and prey volume were significantly different from each other (prey number KolmogorovndashSmirnov Dmax=01584 plt001 prey volume KolmogorovndashSmirnov Dmax=01816 plt001 Table 3) A total of 36015 invertebrates distributed into 33 categories were used to estimate prey availability in the environment The distribution of available prey differed from the consumed prey for both species (T hispidus Dmax=02267 plt001 T semitaeniatus Dmax=02294 plt001)
The mean number of prey categories consumed for each species was seven (T semitaeniatus 5ndash11 T hispidus 4ndash11) Five categories comprised more than 10 in at least one monthly sample for T hispidus (Hymenoptera insect larvae Isoptera Coleoptera and Lepidoptera) and four of these also comprised more than 10 in at least one monthly sample for T semitaeniatus (all except Lepidoptera) The largest niche widths (B) were observed in February (254) June (248) April (245) and May (204) for T hispidus and in July (310) February (289) June (284) and May (221) for T semitaeniatus Diet overlap was high (Oslashgt050) in all months except April (011) and December (020) However significant differences between the diets were found in December February April May and August (Table 4)
The proportion of items most used in the diets was similar to available prey in January April September and October for T hispidus and in December January September and October for T semitaeniatus (Table 4) The prey availability occurred between December 2008 and March 2009 and between October and November 2009 (Table 4) The numbers of available prey categories ranged from eight (August) to 19 (February) The highest diversity of available prey was observed in May (378) (Table 4)
Focusing on the two most common food items Hymenoptera were most abundantly available in December 2008 and January 2009 and between September and November 2009 (Table 4) Tropidurus semitaeniatus largely consumed Hymenoptera (over 50 of diet) in the months of December 2008 January March and July to November 2009 whereas insect larvae were more consumed in February April May and June For T hispidus Hymenoptera comprised gt50 of the diet in all month except December and February (Table 4) Insect larvae never exceeded 50 of the number of prey consumed
A strong relationship was seen when comparing the morphology of the head of each species Tropidurus with the dimensions of prey actually consumed by them (Table 5) The first canonical variable for T semitaeniatus showed an inverse relationship in which animals with narrower heads were related to larger prey (Table 5) Already T hispidus for the first canonical variable was significantly positive for the relation between animals with large heads and longer prey (Table 5)
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
31
Interact ion of sympatr ic Tropidur idae
nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to activity when sighted (G=04808 gl=4 p=09753 nT hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φ jk = 099) Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
Trop
idur
us se
mita
enia
tus
Trop
idur
us h
ispid
us
Varia
bles
Fem
ales
(n=1
3)M
ales
(n=1
7)Fe
mal
es (n
=15)
Mal
es (n
=18)
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Aver
ageplusmn
sdM
inndash
Max
Av
erag
eplusmnsd
Min
ndashM
ax
Body
size
100
plusmn04
90
25ndash2
01
295
plusmn16
00
75ndash6
17
388
plusmn17
81
37ndash6
84
395
plusmn17
11
15ndash6
44
Mas
s1
96plusmn0
88
075
ndash35
05
62plusmn3
84
110
ndash13
007
77plusmn3
78
200
ndash15
258
07plusmn3
38
250
ndash12
50(-0
009
plusmn00
63)
(-01
40ndash0
072
)(-0
015
plusmn00
74)
(-01
59ndash0
112
)(-0
029
plusmn01
11)
(-02
64ndash0
068
)(0
035
plusmn00
40)
(-00
24ndash0
104
)SV
L44
22plusmn
782
269
6ndash56
84
596
5plusmn10
67
416
7ndash72
76
574
2plusmn10
99
399
1ndash72
71
579
1plusmn8
7238
82ndash
693
6(-0
094
plusmn00
72)
(-02
76ndash-
000
8)(0
010
plusmn00
54)
(-00
98ndash0
075
)(-0
025
plusmn00
61)
(-01
67ndash0
031
)(-0
020
plusmn00
40)
(-01
35ndash0
022
)Bo
dy w
idth
117
2plusmn2
216
93ndash1
468
164
5plusmn3
7610
87ndash
226
615
38plusmn
330
112
6ndash21
02
154
4plusmn3
044
105
0ndash19
44
(-01
05plusmn0
086
)(-0
306
ndash-0
006)
(00
05plusmn0
073
)(-0
122
ndash00
92)
(-00
41plusmn0
060
)(-0
120
ndash00
45)
(-00
40plusmn0
058
)(-0
143
ndash00
35)
Body
hei
ght
465
plusmn11
53
37ndash7
69
626
plusmn14
803
51ndash8
73
889
plusmn21
65
38ndash1
230
897
plusmn23
25
57ndash1
219
(-01
13plusmn0
089
)(-0
256
ndash00
78)
(-00
53plusmn0
079
)(-0
224
ndash00
46)
(00
71plusmn0
068
)(-0
058
ndash01
43)
(00
72plusmn0
074
)(-0
036
ndash01
73)
Head
wid
th9
07plusmn1
80
606
ndash11
9411
91plusmn
243
762
ndash15
7212
05plusmn
171
933
ndash14
5012
28plusmn
180
920
ndash15
14(-0
082
plusmn00
74)
(-02
21ndash0
019
)(0
007
plusmn00
62)
(-01
34ndash0
075
)(-0
002
plusmn00
31)
(-00
57ndash0
053
)(0
004
plusmn00
34)
(-00
59ndash0
070
)He
ad le
ngth
129
6plusmn1
899
33ndash1
555
159
4plusmn3
129
45ndash2
022
175
7plusmn2
6013
14ndash
222
317
63plusmn
246
125
5ndash21
52
(-00
70plusmn0
057
)(-0
185
ndash00
10)
(-00
18plusmn0
075
)(-0
248
ndash00
47)
(00
10plusmn0
031
)(-0
062
ndash00
58)
(00
10plusmn0
033
)(-0
075
ndash00
53)
Head
hei
ght
402
plusmn05
52
99ndash4
97
562
plusmn09
83
99ndash7
20
744
plusmn10
95
71ndash8
73
773
plusmn12
25
69ndash9
55
(-01
20plusmn0
054
)(-0
224
ndash-0
049)
(-00
27plusmn0
044
)(-0
112
ndash00
30)
(00
72plusmn0
030
)(0
028
ndash01
32)
(00
86plusmn0
035
)(0
027
ndash01
61)
Tail
leng
th81
15plusmn
163
853
34ndash
102
4510
703
plusmn20
9876
87ndash
150
9097
02plusmn
118
475
06ndash
112
8797
32plusmn
119
269
96ndash
119
44(-0
072
plusmn00
89)
(-02
31ndash0
046
)(0
033
plusmn00
65)
(-00
73ndash0
144
)(-0
019
plusmn00
43)
(-00
91ndash0
056
)(-0
018
plusmn00
46)
(-01
18ndash0
058
)Fo
rele
g le
ngth
232
4plusmn4
2413
97ndash
293
730
57plusmn
572
194
6ndash37
79
294
0plusmn4
7721
03ndash
358
728
47plusmn
414
197
2ndash35
55
(-00
81plusmn0
077
)(-0
270
ndash00
13)
(00
15plusmn0
063
)(-0
135
ndash01
02)
(-00
17plusmn0
047
)(-0
112
ndash00
41)
(-00
31plusmn0
040
)(-0
136
ndash00
26)
Hind
lim
b le
ngth
343
7plusmn5
5522
80ndash
434
444
36plusmn
755
311
5ndash53
59
434
5plusmn5
9532
67ndash
503
843
08plusmn
635
310
8ndash52
01
(-00
75plusmn0
064
)(-0
224
ndash-0
008)
(00
12plusmn0
055
)(-0
097
ndash00
77)
(-00
11plusmn0
039
)(-0
087
ndash00
24)
(-00
16plusmn0
043
)(-0
105
ndash00
40)
Tabl
e 2
Des
crip
tive
data
for m
orph
olog
ical
cha
ract
eristi
cs o
f non
-rep
rodu
ctive
indi
vidu
als
of T
hisp
idus
and
T s
emita
enia
tus
in th
e Co
nser
vatio
n U
nit o
f the
Sta
te
Mon
umen
to N
atur
al G
rota
do
Angi
co P
occedilo
Redo
ndo
- SE
Lin
ear m
easu
rem
ents
are
in m
illim
etre
s th
e w
eigh
t is
in g
ram
s an
d va
lues
in p
aren
thes
es re
fer
to s
ize-
adju
sted
var
iabl
es
32
FFA Gomes et a l
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931 nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)
Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus
Taxon Availability Tropidurus semitaeniatus (n=60) Tropidurus hispidus (n=60)
n n F F n n V (mm3) V F F n n V (mm3) V
Acarina 268 074 2 333 2 014 039 000 4 667 14 049 71176 231
Araneae 523 145 20 3333 35 236 27219 227 16 2667 26 090 69893 226
Blattaria 272 076 1 007 5 833 5 017 9811 032
Chilopoda 8 002 1 167 1 007 122 010 1 167 1 003 57009 185
Coleoptera 3497 971 19 3167 32 216 13121 109 36 6000 98 341 148896 482
Dermaptera 3 001
Diplopoda 92 026 1 167 1 003 2925 009
Diplura 1 000
Diptera 5386 1495 15 2500 33 223 24458 204 10 1667 12 042 10033 033
Embioptera 1 000
Ephemeoptera 6 002
Gastropoda 24 007 2 333 4 027 3754 031 1 167 1 003 347 001
Hemiptera 20 006 2 333 2 007 30919 100
Homoptera 56 016 2 333 5 034 1739 014 3 500 10 035 2731 009
Hymenoptera 24908 6916 54 9000 989 6682 277634 2313 56 9333 2088 7265 867513 2811
Isopoda 9 002 1 167 1 003 2028 007
Isoptera 72 020 7 1167 39 264 4505 038 8 1333 412 1434 114157 370
Insect larvae 118 033 30 5000 309 2088 767065 6390 30 5000 175 609 1342030 4348
Lepidoptera 693 192 15 2500 21 142 32576 271 15 2500 22 077 39560 128
Mantodea 1 lt001
Organic material 5 833 055 00046 17 2833 1730 560
Mecoptera 1 lt001
Neuroptera 6 002
Odonata 3 001
Opilionidae 13 004
Orthoptera 4 667 4 027 45371 378 4 667 4 014 144351 468
Protura 2 001 000
Pseudoscorpionida 14 004 2 333 4 027 461 004 1 167 2 007 187 001
Pscoptera 1 lt001 000
Scorpionida 12 003 1 167 1 007 1299 011
Siphonoptera 1 lt001
Strepsitera 1 lt001
Thrichoptera 1 lt001
Thysanura 2 001
TOTAL 36015 100 1480 100 1200516 100 2874 100 3086566 100
B 202 296 206 226
Table 3 Summary of prey availability and diets of Tropidurus hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE n ndash number of prey n ndash percentage of prey F ndash frequency of prey V ndash volume V ndash percentage of volume
33
Interact ion of sympatr ic Tropidur idae
respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to
activity when sighted (G=04808 gl=4 p=09753 nT
hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT
semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φjk = 099)
Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
The first and second principal components of a PCA together explained 70 of the variation in morphology of the two species The first principal component was related to SVL anterior and posterior limb length and head width The two species did not significantly differ in shape (MANOVA Wilkrsquos Lambda=0893 p=0566) although T hispidus is slightly larger than T semitaeniatus with a larger and higher head longer limbs and a higher body
A total of 60 stomachs were analysed for T semitaeniatus and T hispidus each Eighteen prey categories were used by T hispidus and 15 were used by T semitaeniatus The most frequent prey categories for T hispidus were Hymenoptera Coleoptera insect larvae Araneae and Lepidoptera The corresponding groups for T semitaeniatus were Hymenoptera insect larvae Araneae Coleoptera Diptera and Lepidoptera The most abundant prey types were Hymenoptera and Isoptera for T hispidus and Hymenoptera and insect larvae for T semitaeniatus Highest prey volumes were represented by insect larvae and Hymenoptera for T hispidus and insect larvae and Hymenoptera for T semitaeniatus (Table 3) Formicidae represented 9995 of the Hymenoptera ingested by the two species (Table 3) Both species also consumed plant material (28 of T hispidus individuals representing 60 of the volume of food consumed and 833 of T semitaeniatus representing 00046 of food volume
The trophic niche widths estimated for T hispidus and T semitaeniatus were 206 and 202 for prey number and 226 and 296 for prey volume respectively Overlap
was higher with regards to prey number ( φjk=096 prey volume φ jk=097) but prey number and prey volume were significantly different from each other (prey number KolmogorovndashSmirnov Dmax=01584 plt001 prey volume KolmogorovndashSmirnov Dmax=01816 plt001 Table 3) A total of 36015 invertebrates distributed into 33 categories were used to estimate prey availability in the environment The distribution of available prey differed from the consumed prey for both species (T hispidus Dmax=02267 plt001 T semitaeniatus Dmax=02294 plt001)
The mean number of prey categories consumed for each species was seven (T semitaeniatus 5ndash11 T hispidus 4ndash11) Five categories comprised more than 10 in at least one monthly sample for T hispidus (Hymenoptera insect larvae Isoptera Coleoptera and Lepidoptera) and four of these also comprised more than 10 in at least one monthly sample for T semitaeniatus (all except Lepidoptera) The largest niche widths (B) were observed in February (254) June (248) April (245) and May (204) for T hispidus and in July (310) February (289) June (284) and May (221) for T semitaeniatus Diet overlap was high (Oslashgt050) in all months except April (011) and December (020) However significant differences between the diets were found in December February April May and August (Table 4)
The proportion of items most used in the diets was similar to available prey in January April September and October for T hispidus and in December January September and October for T semitaeniatus (Table 4) The prey availability occurred between December 2008 and March 2009 and between October and November 2009 (Table 4) The numbers of available prey categories ranged from eight (August) to 19 (February) The highest diversity of available prey was observed in May (378) (Table 4)
Focusing on the two most common food items Hymenoptera were most abundantly available in December 2008 and January 2009 and between September and November 2009 (Table 4) Tropidurus semitaeniatus largely consumed Hymenoptera (over 50 of diet) in the months of December 2008 January March and July to November 2009 whereas insect larvae were more consumed in February April May and June For T hispidus Hymenoptera comprised gt50 of the diet in all month except December and February (Table 4) Insect larvae never exceeded 50 of the number of prey consumed
A strong relationship was seen when comparing the morphology of the head of each species Tropidurus with the dimensions of prey actually consumed by them (Table 5) The first canonical variable for T semitaeniatus showed an inverse relationship in which animals with narrower heads were related to larger prey (Table 5) Already T hispidus for the first canonical variable was significantly positive for the relation between animals with large heads and longer prey (Table 5)
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
32
FFA Gomes et a l
Both T hispidus (7867) and T semitaeniatus (8303) preferred sunny days (Fig 2C) without differences between them (G=14534 gl=3 p=06931 nT hispidus=422 and nT semitaeniatus=1338) Tropidurus hispidus was most often observed in shaded (3871) and mosaic sites (3776) whereas T semitaeniatus was most often found at sites exposed to the sun (3638) followed by mosaic sites (3443) (Fig 2D) The difference between species was significant (T=8597 df=364 plt0001 nT
hispidus=421 and nT semitaeniatus =1333)
Tropidurus hispidus and T semitaeniatus showed the same temporal activity patterns (G=82992 gl=11 p=06863 nT hispidus=422 and nT semitaeniatus=1356) Both species were bi-modally active Tropidurus hispidus activity was highest between 0800 and 1100 hours declining at midday and rising again between 1400 and 1600 (Fig 2E) For T semitaeniatus the highest peaks occurred between 0700 and 1000 and between 1400 and 1700 (Fig 2E) The niche widths for activity times were 1078 and 1041 for T hispidus and T semitaeniatus
Taxon Availability Tropidurus semitaeniatus (n=60) Tropidurus hispidus (n=60)
n n F F n n V (mm3) V F F n n V (mm3) V
Acarina 268 074 2 333 2 014 039 000 4 667 14 049 71176 231
Araneae 523 145 20 3333 35 236 27219 227 16 2667 26 090 69893 226
Blattaria 272 076 1 007 5 833 5 017 9811 032
Chilopoda 8 002 1 167 1 007 122 010 1 167 1 003 57009 185
Coleoptera 3497 971 19 3167 32 216 13121 109 36 6000 98 341 148896 482
Dermaptera 3 001
Diplopoda 92 026 1 167 1 003 2925 009
Diplura 1 000
Diptera 5386 1495 15 2500 33 223 24458 204 10 1667 12 042 10033 033
Embioptera 1 000
Ephemeoptera 6 002
Gastropoda 24 007 2 333 4 027 3754 031 1 167 1 003 347 001
Hemiptera 20 006 2 333 2 007 30919 100
Homoptera 56 016 2 333 5 034 1739 014 3 500 10 035 2731 009
Hymenoptera 24908 6916 54 9000 989 6682 277634 2313 56 9333 2088 7265 867513 2811
Isopoda 9 002 1 167 1 003 2028 007
Isoptera 72 020 7 1167 39 264 4505 038 8 1333 412 1434 114157 370
Insect larvae 118 033 30 5000 309 2088 767065 6390 30 5000 175 609 1342030 4348
Lepidoptera 693 192 15 2500 21 142 32576 271 15 2500 22 077 39560 128
Mantodea 1 lt001
Organic material 5 833 055 00046 17 2833 1730 560
Mecoptera 1 lt001
Neuroptera 6 002
Odonata 3 001
Opilionidae 13 004
Orthoptera 4 667 4 027 45371 378 4 667 4 014 144351 468
Protura 2 001 000
Pseudoscorpionida 14 004 2 333 4 027 461 004 1 167 2 007 187 001
Pscoptera 1 lt001 000
Scorpionida 12 003 1 167 1 007 1299 011
Siphonoptera 1 lt001
Strepsitera 1 lt001
Thrichoptera 1 lt001
Thysanura 2 001
TOTAL 36015 100 1480 100 1200516 100 2874 100 3086566 100
B 202 296 206 226
Table 3 Summary of prey availability and diets of Tropidurus hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo - SE n ndash number of prey n ndash percentage of prey F ndash frequency of prey V ndash volume V ndash percentage of volume
33
Interact ion of sympatr ic Tropidur idae
respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to
activity when sighted (G=04808 gl=4 p=09753 nT
hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT
semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φjk = 099)
Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
The first and second principal components of a PCA together explained 70 of the variation in morphology of the two species The first principal component was related to SVL anterior and posterior limb length and head width The two species did not significantly differ in shape (MANOVA Wilkrsquos Lambda=0893 p=0566) although T hispidus is slightly larger than T semitaeniatus with a larger and higher head longer limbs and a higher body
A total of 60 stomachs were analysed for T semitaeniatus and T hispidus each Eighteen prey categories were used by T hispidus and 15 were used by T semitaeniatus The most frequent prey categories for T hispidus were Hymenoptera Coleoptera insect larvae Araneae and Lepidoptera The corresponding groups for T semitaeniatus were Hymenoptera insect larvae Araneae Coleoptera Diptera and Lepidoptera The most abundant prey types were Hymenoptera and Isoptera for T hispidus and Hymenoptera and insect larvae for T semitaeniatus Highest prey volumes were represented by insect larvae and Hymenoptera for T hispidus and insect larvae and Hymenoptera for T semitaeniatus (Table 3) Formicidae represented 9995 of the Hymenoptera ingested by the two species (Table 3) Both species also consumed plant material (28 of T hispidus individuals representing 60 of the volume of food consumed and 833 of T semitaeniatus representing 00046 of food volume
The trophic niche widths estimated for T hispidus and T semitaeniatus were 206 and 202 for prey number and 226 and 296 for prey volume respectively Overlap
was higher with regards to prey number ( φjk=096 prey volume φ jk=097) but prey number and prey volume were significantly different from each other (prey number KolmogorovndashSmirnov Dmax=01584 plt001 prey volume KolmogorovndashSmirnov Dmax=01816 plt001 Table 3) A total of 36015 invertebrates distributed into 33 categories were used to estimate prey availability in the environment The distribution of available prey differed from the consumed prey for both species (T hispidus Dmax=02267 plt001 T semitaeniatus Dmax=02294 plt001)
The mean number of prey categories consumed for each species was seven (T semitaeniatus 5ndash11 T hispidus 4ndash11) Five categories comprised more than 10 in at least one monthly sample for T hispidus (Hymenoptera insect larvae Isoptera Coleoptera and Lepidoptera) and four of these also comprised more than 10 in at least one monthly sample for T semitaeniatus (all except Lepidoptera) The largest niche widths (B) were observed in February (254) June (248) April (245) and May (204) for T hispidus and in July (310) February (289) June (284) and May (221) for T semitaeniatus Diet overlap was high (Oslashgt050) in all months except April (011) and December (020) However significant differences between the diets were found in December February April May and August (Table 4)
The proportion of items most used in the diets was similar to available prey in January April September and October for T hispidus and in December January September and October for T semitaeniatus (Table 4) The prey availability occurred between December 2008 and March 2009 and between October and November 2009 (Table 4) The numbers of available prey categories ranged from eight (August) to 19 (February) The highest diversity of available prey was observed in May (378) (Table 4)
Focusing on the two most common food items Hymenoptera were most abundantly available in December 2008 and January 2009 and between September and November 2009 (Table 4) Tropidurus semitaeniatus largely consumed Hymenoptera (over 50 of diet) in the months of December 2008 January March and July to November 2009 whereas insect larvae were more consumed in February April May and June For T hispidus Hymenoptera comprised gt50 of the diet in all month except December and February (Table 4) Insect larvae never exceeded 50 of the number of prey consumed
A strong relationship was seen when comparing the morphology of the head of each species Tropidurus with the dimensions of prey actually consumed by them (Table 5) The first canonical variable for T semitaeniatus showed an inverse relationship in which animals with narrower heads were related to larger prey (Table 5) Already T hispidus for the first canonical variable was significantly positive for the relation between animals with large heads and longer prey (Table 5)
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
33
Interact ion of sympatr ic Tropidur idae
respectively with a high overlap of these schedules ( φ
jk=092) The two species were indiscernible with regard to
activity when sighted (G=04808 gl=4 p=09753 nT
hispidus=461 and nT semitaeniatus=1338) A standing position dominated for both T hispidus (8178) and T semitaeniatus (8079) (Fig 2F) Running for shelter was the main activity after having been encountered for both species (Tropidurus hispidus 6580 T semitaeniatus 7427) (Fig 2G) without statistical differences (G=72499 gl=6 p=02984 nT hispidus=421 and nT
semitaeniatus=1337) Similar shelters were chosen by the two species (G=133158 gl=7 p=00648 nT hispidus=421 and nT semitaeniatus=1331) Rocks were used most frequently (T hispidus 6674 and T semitaeniatus 8136) followed by crevices (T hispidus 1069 and T semitaeniatus 1254) (Fig 2H) Niche width for shelters use was 211 and 147 for T hispidus and T semitaeniatus respectively with a high overlap ( φjk = 099)
Adult T hispidus were larger than T semitaeniatus (ANOVA F136=42119 plt0001 n=382 Table 1) Average SVL of T hispidus was 9268plusmn1358 mm for adults and 6391plusmn1413 mm for juveniles average SVL of T semitaeniatus adults and young was 7366plusmn904 mm and 5555plusmn1303 mm respectively The size-adjusted masses (adults) were similar between the species (ANOVA F128=1283 p=0267 n=30 Table 1) Adults and young of T hispidus had masses of 3208plusmn1151 g and 1095plusmn646 g T semitaeniatus weighed 1219plusmn506 g and 507plusmn381 g respectively (Tables 1 and 2)
The first and second principal components of a PCA together explained 70 of the variation in morphology of the two species The first principal component was related to SVL anterior and posterior limb length and head width The two species did not significantly differ in shape (MANOVA Wilkrsquos Lambda=0893 p=0566) although T hispidus is slightly larger than T semitaeniatus with a larger and higher head longer limbs and a higher body
A total of 60 stomachs were analysed for T semitaeniatus and T hispidus each Eighteen prey categories were used by T hispidus and 15 were used by T semitaeniatus The most frequent prey categories for T hispidus were Hymenoptera Coleoptera insect larvae Araneae and Lepidoptera The corresponding groups for T semitaeniatus were Hymenoptera insect larvae Araneae Coleoptera Diptera and Lepidoptera The most abundant prey types were Hymenoptera and Isoptera for T hispidus and Hymenoptera and insect larvae for T semitaeniatus Highest prey volumes were represented by insect larvae and Hymenoptera for T hispidus and insect larvae and Hymenoptera for T semitaeniatus (Table 3) Formicidae represented 9995 of the Hymenoptera ingested by the two species (Table 3) Both species also consumed plant material (28 of T hispidus individuals representing 60 of the volume of food consumed and 833 of T semitaeniatus representing 00046 of food volume
The trophic niche widths estimated for T hispidus and T semitaeniatus were 206 and 202 for prey number and 226 and 296 for prey volume respectively Overlap
was higher with regards to prey number ( φjk=096 prey volume φ jk=097) but prey number and prey volume were significantly different from each other (prey number KolmogorovndashSmirnov Dmax=01584 plt001 prey volume KolmogorovndashSmirnov Dmax=01816 plt001 Table 3) A total of 36015 invertebrates distributed into 33 categories were used to estimate prey availability in the environment The distribution of available prey differed from the consumed prey for both species (T hispidus Dmax=02267 plt001 T semitaeniatus Dmax=02294 plt001)
The mean number of prey categories consumed for each species was seven (T semitaeniatus 5ndash11 T hispidus 4ndash11) Five categories comprised more than 10 in at least one monthly sample for T hispidus (Hymenoptera insect larvae Isoptera Coleoptera and Lepidoptera) and four of these also comprised more than 10 in at least one monthly sample for T semitaeniatus (all except Lepidoptera) The largest niche widths (B) were observed in February (254) June (248) April (245) and May (204) for T hispidus and in July (310) February (289) June (284) and May (221) for T semitaeniatus Diet overlap was high (Oslashgt050) in all months except April (011) and December (020) However significant differences between the diets were found in December February April May and August (Table 4)
The proportion of items most used in the diets was similar to available prey in January April September and October for T hispidus and in December January September and October for T semitaeniatus (Table 4) The prey availability occurred between December 2008 and March 2009 and between October and November 2009 (Table 4) The numbers of available prey categories ranged from eight (August) to 19 (February) The highest diversity of available prey was observed in May (378) (Table 4)
Focusing on the two most common food items Hymenoptera were most abundantly available in December 2008 and January 2009 and between September and November 2009 (Table 4) Tropidurus semitaeniatus largely consumed Hymenoptera (over 50 of diet) in the months of December 2008 January March and July to November 2009 whereas insect larvae were more consumed in February April May and June For T hispidus Hymenoptera comprised gt50 of the diet in all month except December and February (Table 4) Insect larvae never exceeded 50 of the number of prey consumed
A strong relationship was seen when comparing the morphology of the head of each species Tropidurus with the dimensions of prey actually consumed by them (Table 5) The first canonical variable for T semitaeniatus showed an inverse relationship in which animals with narrower heads were related to larger prey (Table 5) Already T hispidus for the first canonical variable was significantly positive for the relation between animals with large heads and longer prey (Table 5)
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
34
FFA Gomes et a l
Dece
mbe
rJa
nuar
yFe
brua
ryM
arch
April
May
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
(126
)(4
51)
(407
2)(9
0)(5
05)
(141
85)
(73)
(83)
(430
8)(1
07)
(151
)(3
895)
(178
)(4
5)(7
99)
(108
)(2
67)
(826
)Ac
arin
a1
650
590
570
070
030
750
36Ar
anea
e1
590
440
612
250
200
731
371
201
183
740
631
826
133
700
75Bl
attar
ia0
440
101
120
200
480
260
100
380
370
12Ch
ilopo
da0
220
010
030
48Co
leop
tera
317
044
447
562
079
851
274
361
474
093
125
137
62
2524
44
160
20
934
8718
52
Derm
apte
ra0
08Di
plop
oda
009
138
037
763
Dipl
ura
002
Dipt
era
142
91
922
250
592
874
8247
47
187
188
447
215
77
377
7Em
biop
tera
013
Ephe
meo
pter
a0
75Ga
stro
poda
100
109
Hem
ipte
ra0
010
020
030
371
21Ho
mop
tera
007
001
063
093
037
073
Hym
enop
tera
793
716
41
908
480
90
906
986
75
397
346
99
389
784
11
800
028
11
337
577
852
44
314
865
17
284
5Is
opod
a0
22Is
opte
ra0
7981
82
002
112
634
424
70
911
870
562
220
631
120
61In
sect
larv
a0
790
223
370
016
8540
96
042
093
938
036
932
64
443
7559
26
250
91
94Le
pido
pter
a2
250
592
742
415
646
546
2510
94
056
111
10
501
851
120
85M
anto
dea
002
Mec
opte
ra0
02N
euro
pter
aO
dona
ta0
05O
pilio
nida
e0
03O
rtho
pter
a1
121
850
37Pr
otur
a0
010
02Ps
eudo
scor
pion
ida
002
411
025
024
Pscoacute
pter
a0
02Sc
orpi
onid
a0
050
020
050
13Si
phon
opte
ra0
02St
reps
itera
002
Thric
hopt
era
002
Thys
anur
a0
01 B
153
143
121
151
121
131
289
254
261
140
153
322
115
245
302
221
204
378
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
099
010
gt00
51
000
08gt0
05
044
050
lt00
10
540
54lt0
01
010
089
lt00
10
300
63lt0
01
Th x
Disp
020
082
lt00
10
990
11gt0
05
054
044
lt00
10
540
57lt0
01
094
018
gt00
50
550
61lt0
01
Ts x
Th
020
080
lt00
10
990
09gt0
05
059
030
lt00
10
990
08gt0
05
011
078
lt00
10
750
36lt0
01
Tabl
e 4
Mon
thly
dist
ributi
on o
f foo
d av
aila
bilty
(D) a
nd o
f the
sto
mac
h co
nten
ts o
f T h
ispi
dus
(Th)
and
T s
emita
enia
tus
(Ts)
in t
he C
onse
rvati
on U
nit
of t
he S
tate
M
onum
ento
Nat
ural
Gro
ta d
o An
gico
Poccedil
o Re
dond
o - S
E (B
razil
) Th
e va
lues
in p
aren
thes
es re
fer t
o th
e nu
mbe
r of i
nver
tebr
ates
per
sam
ple
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
35
Interact ion of sympatr ic Tropidur idae
Tabl
e 4
(Con
tinue
d)
June
July
Augu
stSe
ptem
ber
Oct
ober
Nov
embe
rTs
ThD
TsTh
DTs
ThD
TsTh
DTs
ThD
TsTh
D
(95)
(120
)(9
33)
(59)
(156
)(8
99)
(46)
(63)
(219
)(1
50)
(170
)(1
023)
(240
)(5
64)
(242
4)(2
09)
(294
)(2
432)
Acar
ina
169
011
317
042
160
223
214
Aran
eae
421
244
493
678
445
100
52
671
762
251
251
241
533
350
342
26Bl
attar
ia0
430
640
220
490
176
83Ch
ilopo
da0
111
690
11Co
leop
tera
421
732
202
63
396
4126
59
476
168
93
3312
35
181
80
421
425
901
444
0812
05
Derm
apte
raDi
plop
oda
150
Dipl
ura
Dipt
era
316
081
390
13
3913
90
435
913
067
059
225
042
239
096
354
Embi
opte
raEp
hem
eopt
era
Gast
ropo
da5
081
370
590
200
040
480
04He
mip
tera
081
032
011
046
008
Hom
opte
ra0
810
963
390
641
454
353
171
832
350
290
620
08Hy
men
opte
ra42
11
561
029
26
525
485
26
525
065
22
746
058
45
906
779
41
742
996
67
937
986
10
904
394
90
722
0Is
opod
a1
59Is
opte
ra1
6911
11
133
059
058
008
Inse
ct la
rva
410
528
46
236
186
47
050
2223
91
159
067
176
039
071
017
335
068
029
Lepi
dopt
era
316
244
021
169
033
217
183
059
039
083
071
Man
tode
aM
ecop
tera
Neu
ropt
era
064
Odo
nata
004
Opi
lioni
dae
039
012
021
Ort
hopt
era
105
081
059
018
Prot
ura
Pseu
dosc
orpi
onid
a1
050
350
080
21Ps
coacutept
era
Scor
pion
ida
067
029
004
Siph
onop
tera
Stre
psite
raTh
richo
pter
aTh
ysan
ura
B2
842
483
543
101
362
722
051
742
571
211
541
711
071
131
341
221
111
84
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
OslashDm
axp
Ts x
Disp
049
056
lt00
10
850
28lt0
01
089
001
lt00
10
980
17gt0
05
100
010
gt00
50
980
21lt0
05
Th x
Disp
056
056
lt00
10
560
39lt0
01
094
030
lt00
11
000
08gt0
05
100
009
gt00
50
990
23lt0
05
Ts x
Th
095
015
gt00
50
950
18gt0
05
093
025
lt00
10
990
11gt0
05
100
002
gt00
51
000
03gt0
05
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
36
DIsCUssION The presence of a species in an environment may be related to specific physiological needs improved access to food availability of resources presence of refuges morphological adaptations inter and intraspecific interactions as well as historical factors (Pianka 1973 Herfindal et al 2005 Borger et al 2006 Silva amp Arauacutejo 2008) The habitat and microhabitat chosen by a species should meet their essential needs to allow viable populations (Silva amp Arauacutejo 2008) In the study area T hispidus and T semitaeniatus largely were active on rocky substrates Such sites are able to maximise the uptake of heat necessary for thermoregulation both through direct exposure and contact with heated surfaces (Rocha amp Bergallo 1990 VanSluys 1992 Meira et al 2007)
Tropidurus semitaeniatus is considered to be a saxicolous species endemic of Caatinga environments whereas T hispidus occupies a generalist habitat in open formations of various biomes (Rodrigues 1987) Despite this variation in the use of microhabitats T hispidus tends towards a saxicolous habit in places where rocks are abundant Vitt et al (1997) found that where T hispidus use rocks individuals displayed greater dorso-ventral flattening than when in habitat areas without rocks This suggests that the flattening in these individuals could be adaptive to the use of cracks in rock outcrops In the present study no differences were established in body shape between the species
The preference of these species for rocks has been recorded in other localities and environments Tropidurus hispidus uses rocks in Caatinga environments (Vitt 1981 Dias amp Lira-da-Silva 1998 Kolodiuk et al 2009) in the Amazonian rainforest (Vitt amp Carvalho 1995 Vitt et al 1996 Vitt amp Zani 1998) Amazonian savannahs (Mesquita et al 2006) and fields in Minas Gerais (VanSluys et al 2004) T semitaeniatus uses rocky substrates in the Caatinga biome (Vitt 1981 Kolodiuk et al 2009 Ribeiro amp Freire 2010) and in Agreste Sergipe (Fernandes amp Oliveira 1997 Ramos amp Denisson 1997) The use of rocks is common to others species of the semitaeniatus group (T helenae and T pinima Rodrigues 1984 Manzani amp Abe 1990 Rodrigues 2005) as well as for several
Table 5 Canonical correlation between the measurements of the head and the size of prey of T hispidus and T semitaeniatus in the Conservation Unit of the State Monumento Natural Grota do Angico Poccedilo Redondo ndash SE (Brazil)
species of the torquatus group (T montanus T itambere and T oreadicus Rodrigues 1987 Faria amp Araujo 2004 VanSluys et al 2004 Meira et al 2007) Both species adopted vertical positions which were in most cases lt40 cm above ground (5064 and 5178 of observations for T hispidus and T semitaeniatus respectively) Teixeira-Filho et al (1996) suggest that layers close to the ground are heated up more quickly with advantages for thermoregulation and a consequently lower risk of predation and more time for other activities such as foraging
Tropidurus individuals were active throughout the data collection period Both species are sit-and-wait predators implying a shorter time searching for prey and more energy invested in prey capture than is the case for more active foragers (Dias amp Lira-da-Silva 1998 Pianka amp Vitt 2003) Similar findings were already obtained for T hispidus (Vitt 1995 Vitt amp Zani 1998 VanSluys et al 2004) T semitaeniatus (Vitt 1995) T torquatus (Bergallo amp Rocha 1993 Teixeira-Filho et al 1996 Hatano et al 2001) T itambere (VanSluys 1992 Faria amp Araujo 2004) T montanus (VanSluys et al 2004) and T oreadicus (Faria amp Araujo 2004 Meira et al 2007) The observed bimodal patterns of activity have previously been found by VanSluys (1992) for T itambere and by Vrcibradic amp Rocha (1998) for Mabuya frenata during the wet season at high temperatures The Caatinga biome is characterised by particularly hot temperatures (Prado 2005) explaining the observed bimodal pattern for the present study species
According to Huey amp Slatkin (1976) thermoregulation in diurnal lizards involves a set of behavioural activities and options for microhabitat use Displacement between environments with a differential exposure to sun will help to achieve the optimum temperature sought (Rocha amp Bergallo 1990 Vitt amp Carvalho 1995 Hatano et al 2001) We observed a preference for sunny days and exposure to sun was distributed between categories (sun mosaic shadow) for both species with T semitaeniatus having a preference for sun and T hispidus having a preference for shadow The difference in exposure adopted by each species may reflect their physiological needs Vitt (1995) and Ribeiro amp Freire (2010) verified that T semitaeniatus
FFA Gomes et a l
Tropidurus semitaeniatus Tropidurus hispidus
Canonical coefficients Canonical coefficients
Head 1st Canonical Variable 2nd Canonical Variable 1st Canonical Variable 2nd Canonical Variable
Length 165 645 025 123
Height -217 -686 136 028
Width 151 032 -064 -160
Prey
Greater Length 038 139 129 -164
Greater Width 068 -127 -035 206
Canonical Correlation c2 p Canonical Correlation c2 p
I 095 13634 lt00001 053 14437 00251
II 055 1883 lt00001 014 0865 06488
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
37
presents a mean body temperature that is higher than T hispidus In the study area of the present work T hispidus may prefer shady places to avoid negative effects of high temperatures (Teixeira-Filho et al 1996)
Ecological historical and behavioural factors must be considered when evaluating the reasons why certain species consume particular types of prey (Vitt amp Zani 1998 Pianka amp Vitt 2003) and morphological limitations may further interfere with the type of food consumed (Toft 1985 Magnusson amp Silva 1993) An opportunistic pattern in food use was observed for both species in this study given the strong correlation between use and availability The use of ants is widely observed in the diet of the genus Tropidurus and has been reported for several species (T hispidus Dias amp Lira-da-Silva 1998 T torquatus group Arauacutejo 1987 T itambere VanSluys 1995 T oreadicus and T spinulosos Colli et al 1992 T torquatus Bergallo amp Rocha 1994 T hispidus T oreadicus T semitaeniatus Vitt 1993 T semitaeniatus and T hispidus Ribeiro amp Freire 2011) Ants are abundant in the Caatinga (Santos et al 1999) Insect larvae were mainly used in the rainy season probably due to their higher availability during this period
For lizards prey composition is largely related to the type of foraging used and the habitat they occupy (Vitt 1991 Toft 1985) Diet overlap is common among sympatric species that hunt by stalking since they have a preference for active prey (Zug et al 2001 Silva amp Arauacutejo 2008) In periods of higher rainfall both species became more selective since the number of invertebrates in the environment was larger Tropidurus semitaeniatus changed their diet towards insect larvae which were not the most abundant prey category T hispidus continued to consume Hymenoptera as the main item in their diet Considering the reduction in availability of Hymenoptera during the rainy season it is likely that individuals of Tropidurus species broaden the diversity of food items to meet their daily nutritional needs The seasonal change in food habits of T semitaeniatus during the rainy season might be due to avoidance of competition during this period Head morphology is reflected in the consumption of prey of different dimensions it is expected that animals with larger heads consume larger prey (Pianka 1969) However this pattern was not observed for the target species of this study Since T semitaeniatus that has a smaller width head was observed consuming relatively larger prey whereas T hispidus with larger heads prefers more elongated prey Food availability in the environment probably best explains the observed pattern Besides invertebrates large quantities of plant material (flowers leaves and seeds) were found in stomachs and T hispidus consumed more plants than T semitaeniatus Ingestion of plant material in Tropidurus and other lizards is relatively common to provide energy as well as possibly water (Rocha amp Bergallo 1992 VanSluys 1993 Dias amp Lira-da-Silva 1998) In our study area the coexistence of T hispidus and T semitaeniatus on rocky outcrops is probably facilitated by small variations in spatial arrangement the morphology of the trophic apparatus and temporary niche shifts in their diets depending on rather unpredictable rainfall patterns
ACKNOWLEDGEMENTs
We thank Mr Manuel Messias and his entire family for their support in the collection area We are grateful to CAPES for providing the research grant and SISBIO for licensing the collection the Secretaria do Meio-Ambiente e Recursos Hiacutedricos de Sergipe (SEMARH SE) for support with transport to the area and other aid at UC and the Nuacutecleo de Pesquisa em Ecologia e Conservaccedilatildeo (NPEC) and the Universidade Federal de Sergipe (UFS) for logistical support The data collection was authorised by license number 19237-1 issued by SISBIO (System of Authorization and Information on Biodiversity)
REFERENCEs
Arauacutejo AFB (1987) Comportamento alimentar dos lagartos o caso dos Tropidurus da Serra dos Carajaacutes Paraacute (Sauria Iguanidae) In Anais de Etologia 203ndash234 Encontro Anual de Etologia (1987) Ribeiratildeo Preto Jaboticabal FUNEP 5
Bergallo HG amp Rocha D (1993) Activity patterns and body temperatures of two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics in southeastern Brazil Amphibia-Reptilia 14 312ndash315
Bergallo HG amp Rocha D (1994) Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics Australian Journal of Ecology 19 72ndash75
Beacuternils RS amp Costa HC (2012) Reacutepteis brasileiros lista de espeacutecies Versatildeo 20122 Available from lthttpwwwsbherpetologiaorgbrgt Sociedade Brasileira de Herpetologia Accessed 2 October 2013
Borger L Franconi N De Michele G Gantz A et al (2006) Effects of sampling regime on the mean and variance of home range size estimates Journal of Animal Ecology 75 1393ndash1405
Carvalho ALG Brito MR amp Fernandes DS (2013) Biogeography of the lizard genus Tropidurus Wied-Neuwied 1825 (Squamata Tropiduridae) distribution endemism and area relationships in South America Public Library of Science 8 1ndash14
Carvalho CM Vilar JC amp Oliveira FF (2005) Reacutepteis e anfiacutebios In Parque Nacional Serra de Itabaiana - Levantamento da Biota 39ndash61 Carvalho CM and Vilar JC (eds) Aracaju Ibama Biologia Geral e Experimental ndash UFS
Chiang JCH amp Koutavas A (2004) Tropical Flip-flop connections Nature 432 684ndash685
Colli GR Arauacutejo AFB Silveira R amp Roma F (1992) Niche partitioning and morphology of two syntopic Tropidurus (Sauria Tropiduridae) in Mato Grasso Brazil Journal of Herpetology 26 66ndash69
Cooper Jr WE (1994) Prey chemical discrimination foraging mode and phylogeny In Lizard ecology historical and experimental perspectives 95ndash116 Vitt LJ amp Pianka ER (eds) New Jersey Princeton University Press
Dias EJR amp Lira-da-Silva RM (1998) Utilizaccedilatildeo dos recursos alimentares por quatro espeacutecies de lagartos (Phyllopezus pollicaris Tropidurus hispidus Mabuya macrorhyncha e Vanzossaura rubricauda) da caatinga (Usina Hidroeleacutetrica de Xingoacute) Brazilian Journal of Ecology 2 97ndash101
Faria RG amp Arauacutejo AFB (2004) Sintopy of two Tropidurus
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
38
lizard species (Squamata Tropiduridae) on a rocky cerrado habitat in Central Brazil Brazilian Journal of Biology 64 775ndash786
Fernandes ACM amp Oliveira EF (1997) Diversidade na dieta e aspectos reprodutivos de duas espeacutecies simpaacutetricas e sintoacutepicas de Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 35ndash40
Freitas MA amp Silva TFS (2007) Guia ilustrado A herpetofauna das caatingas e aacutereas de altitudes do Nordeste Brasileiro Pelotas USEB (Coleccedilatildeo Manuais de Campo USEB 6) 384 pp
Frost DR Rodrigues MT Grant T amp Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata Tropiduridae Tropidurinae) Direct optimization descriptive efficiency and analysis of congruence between molecular data and morphology Molecular Plylogenetics and Evolution 21 352ndash371
Hatano FH Vrcibradic D Galdino CAB Cunha-Barros M et al (2001) Thermal ecology and activity patterns of the lizard community of the restinga of Jurubatiba Macaeacute RJ Revista Brasileira de Biologia 61 287ndash294
Herfindal I Linnell JDC Odden J Birkeland Nilsen E amp Andersen R (2005) Prey density environmental productivity and home-range size in the Eurasian lynx (Lynx lynx) Journal of Zoology 265 63ndash71
Huey RB amp Pianka ER (1977) Patterns of niche overlap among broadly sympatric versus narrowly sympatric Kalahari lizards (Scincidae Mabuya) Ecology 58 119ndash128
Huey RB amp Slatkin M (1976) Cost and benefits of lizard thermoregulation The Quarterly Review of Biology 51 363ndash384
Hutchinson GE (1957) Concluding remarks Cold Spring Harbour Symposium on Quantitative Biology 22 415ndash427
Janzen DH amp Schoener TW (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season Ecology 49 96ndash110
Jolicoeur P (1963) The multivariate generalization of the allometry equation Biometrics 19 497ndash499
Kolodiuk MF Ribeiro LB amp Freire EMX (2009) The effects of seasonality on the foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) living in sympatry in the caatinga of northeastern Brazil Revista Brasileira de Zoologia 26 581ndash585
Krol MS Jaegar A Bronstert A amp Krywkow J (2001) The semiarid integrated model (SDIM) a regional integrated model assessing water availability vulnerability of ecosystems and society in NE-Brazil Physics and Chemistry of the Earth 26 529ndash533
Losos JB (1990) Ecomorphology performance capability and scaling of west Indian Anolis lizards an evolutionary analysis Ecological Monographs 60 369ndash388
Losos JB (2008) Phylogenetic niche conservatism phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species Ecology Letters 11 995ndash1007
Magnusson WE amp Silva EV (1993) Relative effects of size season and species on the diets of some Amazonian Savanna lizards Journal of Herpetology 27 380ndash385
Magnusson WE Lima PA Silva WA amp Arauacutejo MC (2003) Use of geometric forms to estimate volume of invertebrates
in ecological studies of dietary overlap Copeia 2003 13ndash19Manzani PR amp Abe AS (1990) A new species of Tapinurus
from the Caatinga of Piauiacute Northeastern Brazil (Squamata Tropiduridae) Herpetologica 46 462ndash467
MrsquoCloskey RT amp Hecnar ESJ (1994) Interspecific spatial overlap Oikos 71 65ndash74
Meira KT Faria RG Silva MDM Miranda VT amp Zahn-Silva W (2007) Histoacuteria natural de Tropidurus oreadicus em uma aacuterea de cerrado rupestre do Brasil Central Biota Neotropica 7 155ndash163
Mesquita DO Costa GC amp Colli GR (2006) Ecology of an Amazonian savanna lizard assemblage in Monte Alegre Paraacute state Brazil South American Journal of Herpetology 1 61ndash71
Milstead WW (1965) Changes in competing populations of whiptail lizards (Cnemidophorus) in southwestern Texas The American Midland Naturalist 7375ndash80
Nimer E (1972) Climatologia da Regiatildeo Nordeste do Brasil In Introduccedilatildeo agrave Climatologia Dinacircmica Revista Brasileira de Geografia 34 3ndash51
Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia Ecology 50 1012ndash 1030
Pianka ER (1973) The structure of lizard communities Annual Review of Ecology and Systematics 4 53ndash74
Pianka ER amp Vitt LJ (2003) Lizards Windows to The Evolution of Diversity Berkeley University of California Press 333 pp
Prado D (2005) As Caatingas da Ameacuterica do Sul In Ecologia e Conservaccedilatildeo da Caatinga 3ndash73 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ramos L amp Denisson S (1997) Notas sobre os habitats e microhabitats de duas espeacutecies simpaacutetricas de lagartos do gecircnero Tropidurus da Serra de Itabaiana Sergipe (Sauria Tropiduridae) Publicaccedilotildees Avulsas do Centro Acadecircmico Livre de Biologia 1 29ndash34
Reis AMS Arauacutejo EL Ferraz EMN amp Moura AN (2006) Inter-annual variations in the floristic and population structure of an herbaceous community of ldquocaatingardquo vegetation in Pernambuco Brazil Revista Brasileira de Botacircnica 29 497ndash508
Ribeiro LB amp Freire EMX (2009) Tropidurus semitaeniatus (NCN) Drinking behavior Herpetological Review 40 228ndash229
Ribeiro LB amp Freire EMX (2010) Thermal ecology and thermoregulatory behaviour of Tropidurus hispidus and T semitaeniatus in a caatinga area of northeastern Brazil Herpetological Journal 20 201ndash208
Ribeiro LB amp Freire EMX (2011) Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata Tropiduridae) in a caatinga area of northeastern Brazil Iheringia Seacuterie Zoologia 101 225ndash232
Ricklefs RE Cochran D amp Pianka ER (1981) A morphological analysis of the structure of communities of lizards in desert habitats Ecology 62 1474ndash1478
Rocha CFD amp Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil Ethology Ecology amp Evolution 2 263ndash268
Rocha CFD amp Bergallo HG (1992) Tropidurus torquatus (collared lizard) diet Herpetological Review 25 69
Rodrigues MT (1984) Uma nova espeacutecie brasileira de
FFA Gomes et a l
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae
39
Tropidurus com crista dorsal (Sauria Iguanidae) Papeacuteis Avulsos de Zoologia 35 169ndash175
Rodrigues MT (1987) Sistemaacutetica ecologia e zoogeografia dos Tropidurus do grupo torquatus ao sul do Rio Amazonas (Sauridae Iguanidae) Arquivos de Zoologia 31 105ndash230
Rodrigues MT (2005) Herpetofauna da Caatinga In Ecologia e Conservaccedilatildeo da Caatinga 181ndash236 Leal IR Tabareli M amp Silva JMC (eds) Recife Editora da UFPE
Ruiz-Esparza J Gouveia SF Rocha PA Ribeiro AS amp Ferrari SF (2011) Birds of the Grota do Angico Natural Monument in the semi-arid caatinga scrublands of northeastern Brazil Biota Neotropica 11 1ndash8
Santos GMM Delabie JHC amp Resende JJ (1999) Caracterizaccedilatildeo da mirmecofauna (Hymenoptera-Formicidae) associada agrave vegetaccedilatildeo perifeacuterica de inselbergs (caatinga-arboacuterea-estacional-semi-deciacutedua) em Itatim ndash Bahia ndash Brasil Sitientibus 20 33ndash43
Sampaio EVSB (1995) Overview of the Brazilian Caatinga In Seasonally Dry Forests 35ndash58 Bullock HA Mooney HA amp Medina E (eds) Reino Unido Cambridge University Press
Schoener TW (1975) Presence and absence of habitat shift in some widespread lizards species Ecological Monographs 45 233ndash258
Silva VN amp Arauacutejo AFB (2008) Ecologia dos Lagartos Brasileiros 1st ed Rio de Janeiro Technical Books 271p
Simpson EH (1949) Measurement of diversity Nature 163 688
Somers KM (1986) Multivariate allometry and removal of size with principal components analysis Systematic Zoology 35 359ndash368
Teixeira-Filho P Rocha CFD amp Ribas S (1996) Ecologia termal e uso do habitat por Tropidurus torquatus (Sauria Tropiduridae) em uma aacuterea de restinga do sudeste do Brasil In Herpetologia Neotropical 255ndash267 Peacutefaur JE (ed) Actas del II Congreso Latinoamericano de Herpetologia II Volumen Universidad de Los Andes Merida Venezuela Consejo de Publicaciones
Toft CA (1985) Resource partitioning in amphibians and reptilies Copeia 1 1ndash21
VanSluys M (1992) Aspectos da ecologia do lagarto Tropidurus itambere (Tropiduridae) em uma aacuterea do sudeste do Brasil Revista Brasileira de Biologia 52 181ndash185
VanSluys M (1993) Food habits of the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Journal of Herpetology 27 347ndash351
VanSluys M (1995) Seasonal variation in prey choice by the lizard Tropidurus itambere (Tropiduridae) in Southeastern Brazil Ciecircncia e Cultura 47 61ndash65
VanSluys M Rocha CFD Vrcibradic D Galdino CAB amp Fontes AF (2004) Diet activity and microhabitat use of two syntopic Tropidurus species (Lacertilia Tropiduridae) in Minas Gerais Brazil Journal of Herpetology 38 606ndash611
Vitt LJ (1981) Lizard reproduction habitat specificity and constraints on relative clutch mass The American Naturalist 117 506ndash514
Vitt LJ (1991) An introduction to the ecology of cerrado lizards Journal of Herpetology 25 79ndash90
Vitt LJ (1993) Ecology of isolated open-formation Tropidurus (Reptilia Tropiduridae) in Amazonian lowland rain forest Canadian Journal of Zoology 71 2370ndash2390
Vitt LJ (1995) The ecology of tropical lizards in the caatinga of northeast Brazil Occasional Papers of the Oklahoma Museum of Natural History 1 29ndash34
Vitt LJ Zani PA amp Caldwell JP (1996) Behavioural ecology of Tropidurus hispidus on isolated rock outcrops in Amazonia Journal of Tropical Ecology 12 81ndash101
Vitt LJ Caldwell JP Zani PA amp Titus TA (1997) The role of habitat shift in the evolution of lizard morphology evidence from tropical Tropidurus Proceedings of the National Academy of Sciences 94 3828ndash3832
Vitt LJ amp Carvalho CM (1995) Niche partitioning in a tropical wet season lizards in the Lavrado area of Northern Brazil Copeia 2 305ndash329
Vitt LJ amp Pianka ER (1994) Introduction and Acknowledgments In Lizard Ecology Historical and Experimental Perspectives 9ndash12 Vitt LJ amp Pianka ER (eds) Princeton University Press 403 pp
Vitt LJ amp Zani PA (1998) Ecological relationships among sympatric lizards in a transitional forest in the northern Amazon of Brazil Journal of Tropical Ecology 14 63ndash86
Vrcibradic D amp Rocha CFD (1998) Ecology of the skink Mabuya frenata in an area of rock outcrops in Southeastern Brazil Journal of Herpetology 32 229ndash237
Webb CO Ackerly DD McPeek MA amp Donoghue MJ (2002) Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505
Zug GR Vitt LJ amp Caldwell JP (2001) Herpetology An Introductory Biology of Amphibians and Reptiles 2nd ed San Diego Academic Press 630 pp
Accepted 8 July 2014
Interact ion of sympatr ic Tropidur idae