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Lizards, Snakes, and Amphisbaenians from the Quaternary

Sand Dunes of the Middle Rio Sao Francisco, Bahia, Brazil

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DOI: 10.2307/1565694

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 OSSIFICATION IN BUFO 513

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Accepted:1 August 1996.

Journalof Herpetology, Vol. 30, No. 4, pp. 513-523, 1996

Copyright 1996 Society for the Study of Amphibians and Reptiles

Lizards, Snakes, and Amphisbaenians from the Quaternary

Sand Dunes of the Middle Rio SAoFrancisco,Bahia, Brazil

MIGUELTREFAUTRODRIGUES

Universidadede Sao Paulo, Instituto de Biociencias,Departamentode Zoologia,

Caixa Postal 11461, CEP 05422-970, Sao Paulo, SP, Brazil

ABSTRACT.- A Quaternarysand dune area was discovered in the morphoclimaticdomain of the semiarid
Brazilian Caatinga.This site consists of high continental dunes located on both banks of the middle Rio
Sao Francisco, Bahia, Brazil. The area contains a very unique fauna presenting striking adaptations to
psammophily and high levels of species richness and endemism. A total of 6904 specimens comprising 36
lizard (including amphisbaenians) and 25 snake species were collected at the study sites. This area of
approximately5000 km2includes 20 endemic reptiles and several newly described genera and species. This
fauna is particularly characterizedby an abundance and high diversity of fossorial and nocturnal forms
differing strongly in ecological composition from Caatingafaunas and previously studied North American,
Kalaharian,and Australian desert faunas. These differences may be a result of an association of an eco-
geographic mechanism of speciation initially synchronic and latter replaced by a classic allopatric spe-
ciation which occurred in an ancestral Caatinga fauna. It is postulated that the last event of speciation
possibly took place when the Sao Francisco river attained full exorrheism dividing formally continous
sands and isolating ancestralpsammophilic populations on opposite banks. At present, four closely related
species pairs isolated by the river support this model. The last period of species differentiation most likely
corresponded to the end of Wurm-Wisconsinglacial period.

A major task for herpetologists in South
America has been to identify faunal uniqueness
and to work out taxonomic relationships nec-
essary for interpretation of zoogeographic and
evolutionary patterns. Relatively few studies on
assemblages of squamates have been made for
this region, most of them in forest areas (see
Duellman, 1990 for a review). For Brazilian open-
canopy scrublands, the only studies available
are a comprehensive account on the reptiles of
northeastern Brazil (Vanzolini et al., 1980), an
ecological study on a snake assemblage in the
caatinga (Vitt and Vangilder, 1983), two prelim-
inary studies on the cerrado lizard communities
(Vitt, 1991; Vitt and Caldwell, 1993), and a few
studies of lizards in Amazonian savanna regions
(Magnusson et al. 1985; Magnusson 1987, Mag-
nusson and Silva, 1993; Vitt and Carvalho 1995).
The present study began in 1980 with a sur-
vey of amphibians and reptiles in a semiarid
and physionomically characteristic region of
northeastern Brazil encompassing ca. 800,000
514 MIGUEL TREFAUTRODRIGUES
km2 locally known as Caatinga. Although the
herpetological fauna of the caatinga is among
the best known compared to that of other mor-
phoclimatic domains of Brazil (i.e., Ab'Saber,
1977) previous work has been restricted to the
core area (e.g., Vanzolini, 1974; Vanzolini et al.
1980). I describe a faunistically unknown de-
sertlike area of caatinga adjacent to the banks
of the Rio Sao Francisco in the state of Bahia.
Preliminary work indicated that the area con-
tained a very peculiar lizard fauna character-
ized by striking adaptations for psammophily
in all species. After several expeditions to these
sand dunes, the faunal survey of its reptiles still
remains incomplete, but clearly species rich-
ness and endemism are unparalleled to those
elsewhere in South America. In an area com-
prising roughly 5.000 km2 (Barreto, 1993), 36
species of lizards and amphisbaenians can be
found, a local species richness greater than that
of Amazonia and probably rivalled only by those
in Australian deserts. In addition, 25 species of
snakes are known to this area and the presently
known endemic species of squamates reached
a total of 20 (32% of the fauna). Although the
area today cannot be adequately described as a
desert, it was certainly one by the end of the
Wiirm-Wisconsin glacial period (Tricart, 1974
Barreto, 1993); when at least some of the en-
demic species probably evolved. Some of the
adaptations presented by its species, as psam-
mophily and nocturnality, are similar to species
typical of many deserts (e.g., Pianka, 1986). Fol-
lowing formal description of the majority of
several new genera and species (Rodrigues,
1991a, b, c, d; 1993a, b; Vanzolini, 1991a, b), my
main objective in this paper is to summarize the
available information on the area and to bring
this unique fauna to the attention of the her-
petological community to facilitate future stud-
ies. In addition, it is possible that this rich sandy
enclave in caatingas will become a useful model
in testing recent hypothesis on desert lizard
diversity developed after the studies of Pianka
and collaborators in the Kalahari, North Amer-
ican, and Australian systems (Pianka, 1986).
MATERIALS
AND METHODS
The study area is located at Rio Sao Francisco
(approximately 9-11?S, 41-43?W) where the riv-
er flows across quaternary dunes (Fig. 1). Serra
do Estreito is a large and linear quartzitic out-
crop emerging from the alluvial plain of the
river to a height of 600 m above sea level on
the left bank. Situated between the Serra do
Estreito and the river is a large field of sand
dunes, hereafter referred as the Xique-Xique
dune field. These white to yellowish eollic par-
abolic dunes are the largest found in South
America and are formed by fine dystrophic
sands. The sand dunes are variable in elevation
(20-100 m) and held together by thickets of a
thorny and xeromorphic vegetation. Dominant
thickets are formed by the associations of Cac-
taceae (Opuntia and Cereus) and Bromeliaceae
(Bromeliasp.), with scattered shrubs of Euphor-
biaceae, Mirtaceae, Bombacaceae, Celastraceae,
Leguminosae, or Simaroubaceae. Some individ-
uals of a thorny and low Olacaceae and Mir-
taceae form isolated thickets. Large spaces of
bare sand intercalate the clumps of vegetation,
below which a leaf litter mat is also present.
Only rarely do some of the shrubs reach 5 m.
The only perennial river flowing across this area
is the Rio Icatu, a small tributary of Sao Fran-
cisco. Williams (1925), Rodrigues (1991a), Bar-
reto (1993), Martins (1995), and Rocha (1995)
provide additional information on this area.
Study sites at Xique-Xique dune field were
concentrated at Ibiraba and Queimadas, State of
Bahia. The Casanova dune field was studied at
Alagoado downstream on the north bank of the
river (Fig. 1). Although the vegetation, soil, and
general physiognomy are similar at the two sites,
the relief is less accentuated with smaller and
sometimes indistinct dunes at Alagoado. At the
right margin of the river, field work was cen-
tered in Santo Inacio and Vacaria. Santo Inacio
is a contact zone where the terminal northern
portion of the large Serra do Espinhaco (locally
Serra do Assurua) meets the alluvial plain of
the Sao Francisco. The Serra do Assurua is a
local mountain range with typical "campos ru-
pestres" (an open type of vegetation character-
istic of rocky substrates). Local habitats are a
complex mosaic of several vegetation types.
There are large outcrops of quartzitic rocks and
conglomerates separated by sand-gravel areas.
Vegetation is also clumped in thickets where
leaf litter is present. Some twisted cerrado trees
(characterized by a thickened bark and leathery
leaves reaching 4-10 m) and scattered individ-
uals of Velloziaceae are also found. In the al-
luvial plain of the river at Lagoa the Itaparica
are dunes identical to that of the opposite side.
At Vacaria the vegetation is characteristic of the
caatingas although the soils are sandy with low,
thorny, and xeromorphic plant species. In all
intervening areas typical caatinga with rocky
soils occurs. The region is subject to the same
general climatic regime despite its high levels
of habitat heterogeneity. Annual precipitation
reaches 700 mm but is characteristically irreg-
ular with rains concentrated from April to Oc-
tober. A dry season, characterized by the com-
plete lack of rain, extends from November to
March. Temperatures are relatively constant
throughout the year (24 to 28 C) with absolute
maxima near 40 C and minima close to 10 C
(Nimer, 1979).
 LIZARDS, SNAKES, AND AMPHISBAENIANS 515

FIG.1. The palaeoquaternarydune fields of the middle Sao Franciscoriver:Bahia:Brazilin the context of
the semiarid morphoclimatic domain of Caatingas. Study sites and other localities cited in the text are showed.

A total of sampling period of 1190 man-hours
has occurred since 1980. Except for the period
in February 1989 that took place during the
rainy season, all sampling occurred during the
dry season. Specimens were collected by hand,
firearms, or digging them from the sand, during
which information on habitat, microhabitat, and
other pertinent observations were obtained. All
the specimens obtained are deposited in the
Museum of Zoology, University of Sao Paulo,
Sao Paulo, Brazil (MZUSP).
RESULTSAND DISCUSSION
Lizards and Amphisbaenians.-A total of 6904
lizards and amphisbaenians were obtained; the
species, number, and relative frequency are giv-
en in the Table 1. Table 2 summarizes the eco-
logical information obtained and Fig. 2 com-
pares the major microhabitat preference by the
species at the study sites. Comparisons of Tables
1 and 2 indicate a surprisingly high number of
fossorial, nocturnal, and psamophilous forms.
Table 3 shows family distributions among sites
and compares present data with those obtained
for Cabaceiras: State of Paraiba (Rodrigues,
1986b), and Exu: State of Pernambuco (Vanzo-
lini et al. 1980; data in the MZUSP collection),
the two herpetologically best known localities
in typical caatinga habitats. Except for three
otherwise rare lizards occuring at Cabaceiras
(the gekkonid Phyllopezus periosus, the scincid
Mabuya macrorhyncha, and the gymnophthal-
mid Anotosaura vanzolinia) the fauna occurring
at Cabaceiras and Exu comprises only the typ-
ical caatinga forms.
A first important remark comparing dunes
and caatingas is the depauperate fauna of gek-
konids at study sites. At Santo Inacio, Ibiraba,
Queimadas, and Alagoado the only gekkonids
present were Briba brasiliana, Hemidactylus ma-
bouia, Phyllopezus pollicaris, and Lygodactylus
klugei, all present elsewhere in the caatingas.
Vacaria is the only locality in the study area
where Gymnodactylusgeckoides occurs; it is ab-
sent from the other localities in the study area
although its habitat is present there. I have no
516 MIGUEL TREFAUTRODRIGUES

TABLE1. Lizards and amphisbaenians from the pa-pauperate when compared with the diverse
laeoquaternary dune region of the middle Sao Fran-fauna of study sites. Diploglossus lessonae, the
cisco river, an * indicates endemic species. only Anguidae of the domain, is probably ab-
sent from the sands at the study sites.
Num- Fre- Of the 14 species found at study sites and not
Species ber quency known to occur in other caatinga localities, all
Bribabrasiliana 47 0.68 are endemic (Table 1) and 13 are psammophils.
Coleodactylusmeridionalis 1 0.01 Only Tropiduruspinima is saxicolous occurring
Gymnodactylusgeckoides 10 0.14 only at Santo Inacio. Santo Inacio, Alagoado,
Hemidactylus mabouia 4 0.05 Ibiraba, and Queimadas have six endemic spe-
Lygodactylusklugei 114 1.65
cies; Vacariaonly two, but none in pure caatinga
Phyllopezuspollicaris 14 0.20
localities. It is also clear that with the above
Ameiva ameiva 12 0.17
Cnemidophorus ocellifer 223 3.23 exceptions the caatinga lizard species are pres-
ent elsewhere in the study sites and they have
Cnemidophorussp. n. 11 0.15
Tupinambisteguixin 1 0.01 in addition locally endemic forms showing
Calyptommatusleiolepis* 1813 26.26 striking adaptations to psammophily, noctur-
Calyptommatusnicterus* 1415 20.49 nality, and fossoriality that are absent from the
Calyptommatussinebrachiatus* 448 6.48 intervening caatingas (Tables 2 and 4). Table 4
Colobosaura mentalis 3 0.04 also compares the ecological composition of the
Nothobachiaablephara* 379 5.48 fauna of Cabaceiras and Exu with those of the
Procellosaurinuserythrocercus* 90 1.30
Procellosaurinus 39 sand dune area. Although the number of ter-
tetradactylus* 0.56
115 1.66 restrial and arboreal species are similar in caa-
Psilophthalmuspaeminosus*
Vanzosaura rubricauda 847 12.2 tingas and dunes, the number of fossorial spe-
Iguana iguana 8 0.11 cies is much increased at study sites.
Polychrusacutirostris 1 0.01 In order to account for size differences among
Tropidurusamathites* 143 2.07 these faunas I further divided the lizards and
Tropidurus cocorobensis 7 0.10 amphisbaenians in five arbitrarily assigned size
Tropidurus divaricatus* 219 3.17 classes: very small, small, medium-sized, large,
Tropidurus erythrocephalus 139 2.01 and very large. It is evident that major differ-
Tropidurushispidus 443 6.41
0.84 ences between caatingas and dunes should be
Tropidurus psammonastes* 58
207 3.00 attributed to the number of very small and me-
Tropiduruspinima*
Tropidurussemitaeniatus 13 0.18 dium-sized forms. Small, large, and very large
Mabuya heathi 21 0.30 animals are practically the same in the caatingas
Amphisbaenafrontalis* 13 0.18 and in the sand dune area.
Amphisbaena hastata* 13 0.18 As a fauna of a semiarid region I also make
Amphisbaena ignatiana* 9 0.13 comparisons of the present data with data ob-
Amphisbaenapretrei 1 0.01 tained by Pianka in the Kalahari, North Amer-
Amphisbaena vermicularis 19 0.27
ican, and Australian deserts. If we compare the
Leposternon polystegum 4 0.05
number of specimens collected or observed in
Total 6904 100% the three ecological categories refered to above,
the differences are very large (Fig. 3). The fauna
of the sand dune area is immediately set apart
answer for this pattern but the absence of en- by a predominantly subterranean fauna. Con-
demic geckos from the area is striking. The com- sidering the number of species per site, this
position of Polychridae and Iguanidae of the sand dune region has more species than North
dunes and caatinga are identical. Among Scin- American deserts and close to the Kalahari
cidae and Teiidae there are few differences: a semidesert. But if we considered the total num-
new species of Cnemidophorusin Santo Inacio ber of species present in this small region, (36
and the presence of Mabuya macrorhynchaat Ca- including amphisbaenians or 30 lizards), the
baceiras, compared with the other localities species diversity is only rivaled by the Austra-
where only Mabuyaheathioccurs. The only tro- lian deserts. Furthermore if we compare the
pidurids present at Cabaceiras and Exfi and ecological composition of Caatingas, Kalahari,
widespread in the caatingas are Tropidurushis- Australian, North American, and the dunes, the
pidus and Tropidurussemitaeniatus; tropidurid first four are similar in the scarcity of fossorial
richness at study sites is higher. Similarly, the forms, whereas the present study area is im-
only gymnophthalmids present at Exu are Mi- mediately recognized by its predominantly fos-
crablepharusmaximilianiand Vanzosaurarubricau- sorial or semifossorial fauna.
da. Although two other gymnophthalmid spe- Snakes.-A total of 133 snakes were collected
cies, Colobosauramentalis and Anotosauravanzo- (Table 5). Habitat categories were assigned ac-
linia, also occur at Cabaceiras its fauna is de- cording to Vitt and Vangilder (1983). For the
 TABLE2. Ecological data for lizards and amphisbaenians of the palaeoquaternary sand dunes of the

Activity Terrestrial Arboreal

Habitatand ecology species Diur. Noct. Sand Rocks Leaves Trunk Oth
Bribabrasiliana X X X
Coleodactylusmeridionalis X X
Gymnodactylusgeckoides X X
Hemidactylus mabouia X X
Phyllopezus pollicaris X X X
Lygodactylusklugei x X
Ameiva ameiva x x X X
Cnemidophorusocellifer x x X
Cnemidophorussp. n. x X X
Calyptommatusleiolepis x
Calyptommatusnicterus x
Calyptommatussinebrachiatus x
Colobosauramentalis x x
Nothobachiaablephara x x x
Procellosaurinuserythrocercus x x
Procellosaurinustetradactylus x x
Psilophthalmuspaeminosus x x
Tupinambisteguixin x x x x
Vanzosaurarubricauda x x
Iguana iguana x x x
Polychrus acutirostris x x x
Tropidurusamathites x x
Tropiduruscocorobensis x x
Tropidurusdivaricatus x x
Tropiduruserythrocephalus x x
Tropidurushispidus x x x x
Tropiduruspsammonastes x x
Tropiduruspinima x x
Tropidurussemitaeniatus x x
Mabuya heathi x x
Amphisbaenafrontalis x
Amphisbaenahastata x
Amphisbaenaignatiana x
Amphisbaenapretrei x
Amphisbaenavermicularis x
Leposternonpolystegum x
 IBIRABA AND QUEIMADAS

ALAGOADO

33 34 35
Sio Francisco
River

SANTO INACIO

20.21

FIG.2. Habitat distribution of lizards and amphisbaenians at study sites in the region of the palaeoqua-
ternary sand dunes of the middle Sao Francisco river. Species are: (1) Bribabrasiliana,(2) Coleodactylusmeridionalis,
(3) Gymnodactylusgeckoides, (4) Hemidactylus mabouia,(5) Phyllopezus pollicaris, (6) Lygodactylusklugei, (7) Ameiva
ameiva, (8) Cnemidophorusocellifer, (9) Cnemidophorussp., (10) Tupinambisteguixin, (11) Calyptommatusleiolepis,
(12) Calyptommatusnicterus,(13) Calyptommatussinebrachiatus,(14) Colobosauramentalis, (15) Nothobachiaablephara,
(16) Procellosaurinuserythrocercus,(17) Procellosaurinustetradactylus,(18) Psilophthalmuspaeminosus,(19) Vanzosaura
rubricauda,(20) Iguana iguana, (21) Polychrus acutirostris,(22) Tropidurusamathites,(23) Tropiduruscocorobensis,(24)
Tropidurusdivaricatus,(25) Tropiduruserythrocephalus,(26) Tropidurushispidus, (27) Tropiduruspsammonastes,(28)
Tropiduruspinima, (29) Tropidurussemitaeniatus, (30) Mabuya heathi, (31) Amphisbaenafrontalis, (32) Amphisbaena
hastata, (33) Amphisbaenaignatiana, (34) Amphisbaenapretrei, (35) Amphisbaenavermicularis,(36) Leposternonpo-
lystegum.
 LIZARDS, SNAKES, AND AMPHISBAENIANS 519

TABLE3. Species composition of lizard faunas from six semiarid sites in northeasternBrazil;number in
parenthesesincludes amphisbaenians.
Number
of Iguani- Polych- Tropidur- Gekkon- Scinc- Gymnoph- Angu-
Site species dae ridae idae idae idae Teiidae thalmidae idae
Santo Inacio 19 (22) 1 1 4 4 1 4 4 -
Ibiraba 17 (19) 1 1 3 4 1 3 4 -
Alagoado 17 (19) 1 1 3 4 1 3 4 -
Vacaria 17 (19) 1 1 3 5 1 3 3 -
Cabaceiras 18 (19) 1 1 2 6 1 3 3 1
Exf 15 (17) 1 1 2 4 1 3 2 1

study area, 25 species were found, six of them
endemic. There are two sources of data for com-
parison: an intensive survey conduced by Vitt
and Vangilder (1983) at Exu, and a comprehen-
sive list of caatinga snakes encompassing all the
geographic area of the domain based on the
MZUSP snake collection improved with data
from the literature (Vanzolini et al., 1980).
Nineteen species were found at Exu and 25 for
all the caatinga area. The point that I would
emphasize here is the predominance of terres-
trial snakes at Exu and in the general area of
caatingas and the scarcity of fossorial forms.
This pattern is in direct contrast to the snake
fauna of the sandy dunes of the middle Sao
Francisco. Figure 4 compares the species num-
bers in the three areas for major habitat cate-
gories. Although terrestrial snakes are also im-
portant there in terms of numbers of species,
the fossorial snake fauna is much richer than
the adjacent caatingas. Similar to lizards and
amphisbaenians, the snake fauna is character-
ized by fossoriality and psammophily. Of the
six endemic species, all are very small or small
snakes, fossorial, predominantly nocturnal, and
psamophilous. Curiously these snakes are mem-
bers of the Typhlopidae and Colubridae, both
including fossorial representatives in other ar-
eas. The arboreal-terrestrial Boidae and the ter-
restrial Viperidae have no endemics in the area.
Adaptations to an arenicolous mode of life are
particularly evident in the sand swimming spe-
cies of the genus Phimophis.
The Historical,Geographicand EvolutionaryCon-
text.-The Quaternary dunes region of the mid-
dle Sao Francisco river harbors a rich, diverse,
endemic, markedly fossorial, and psamophilous
fauna of lizards, snakes, and amphisbaenians
differing substantially from that of adjacent caa-
tinga. Considering the small dimensions of the
area and its stranded condition in the caatingas,
the mechanisms responsible for such a high di-
versity are not immediately obvious. Similar
patches of sandy habitats occur in the domain,
but contain the current caatinga species with
no endemic species and no psamophilic adap-
tations present in this segment of the herpe-
tofauna of the dunes. The Raso da Catarina
("raso" is a local term for sandy soils in north-
eastern Brazil) and Raso da Gloria in the State
of Bahia are prime examples. The reptile faunas
of such sandy soil regions are comparable, with
the possible exception of Amphisbaenaarenaria
(Vanzolini, 1991b) recently described from Raso
da Catarina in Bahia, where there are no en-
demics. Intensive field work at these areas at-
tests to the absence of other endemic forms.
Similarly, the "brejos" (isolated patches of for-
est in the semiarid caatinga) have fewer species
than the Amazonian or Atlantic forests, with
which they were connected in the past (see Van-
zolini and Williams, 1981 for a review), with
very few endemics. In South America we have
found the same pattern in the coastal islands of
continental shelf now isolated by the sea level
(Rodrigues, 1991e). One or occasionally, two
species are typically endemic within these iso-
lates. What were the mechanisms involved in
the origin of such a high diversity and the strik-
ing adaptations to psammophily in this fauna?
Although we can invoke ecological causes to
explain their present coexistence, the elevated
number of endemic species and genera lead us
to consider of historical reasons.
In previous papers (Rodrigues 1986a, 1988,
1991a, 1993b; Kasahara et al., 1987) I proposed
a model to explain the speciation of some liz-
ards from the area based on geomorphological
TABLE 4. Number of species per majorhabitatcat-
egories for lizardfaunasin six semiaridareasof Brazil,
numbersin parenthesesinclude amphisbaenians.
Site Terrestrial Arboreal Fossorial
Santo Inacio 10 6 3 (6)
Ibiraba 7 6 4 (6)
Alagoado 8 5 4 (6)
Vacaria 8 6 3 (5)
Cabaceiras 9 7 2 (3)
Exfi 8 5 2 (4)
520 MIGUEL TREFAUT RODRIGUES

6000

5000

n
0 4000
E
0.
0 3000
o0O

E 2000

1000

0
USA Kalahari Australia Dunes Exu

FIG.3. Numbers of specimens of fossorial, terrestrial and arboreal lizards and amphisbaenians collected
at five arid or semiarid study sites. Data for North America, Kalahari and Australia are from Pianka (1986).

and paleoclimatic data on the Sao Francisco sand-
dunes (Ab'Saber, 1969; Tricart, 1974). According
to this model the Sao Francisco river had an
endorrheic pattern of drainage until the end of
the last glacial period, flowing and carrying
sands to lacustrine or palustrine depressions lo-
cated in the proximity of the area. In a subse-
quent humid period, the river found its way
out to the sea isolating in opposite margins
patches of sands of an otherwise continuous

TABLE 5. Number, relative frequency, habitat categories and period of activity for 25 species of snakes of
the study area. (*) indicates endemic species.

Species Number Frequency Habitat Activity

Typhlopsyonenagae* 4 3.00 Fossorial Nocturnal-Diurnal
Leptotyphlopsalbifrons 31 23.30 Fossorial Nocturnal-Diurnal
Boa constrictor 1 0.75 Terrestrial-Arboreal Nocturnal
Corallus enydris 3 2.25 Arboreal Nocturnal
Apostolepis arenarius* 7 5.26 Fossorial Nocturnal-Diurnal
Apostolepisgaboi* 1 0.75 Fossorial Nocturnal-Diurnal
Apostolepis sp. n.* 3 2.25 Fossorial Nocturnal-Diurnal
Drymoluberbrazili 1 0.75 Terrestrial Diurnal
Helicops leopardinus 16 12.03 Aquatic Diurnal
Liophisdilepis 3 2.25 Terrestrial-Aquatic Diurnal
Liophispoecilogyrus 1 0.75 Terrestrial-Aquatic Diurnal
Liophisviridis 2 1.50 Terrestrial Diurnal
Mastigodryas bifossatus 1 0.75 Terrestrial-Aquatic Diurnal
Oxybelis aeneus 1 0.75 Arboreal Diurnal
Oxyrhopus trigeminus 8 6.01 Terrestrial Nocturnal-Diurnal
Philodryas nattereri 6 4.51 Terrestrial Diurnal
Phimophischui* 3 2.25 Fossorial Nocturnal-Diurnal
Phimophisiglesiasi 1 0.75 Fossorial Nocturnal-Diurnal
Phimophisscriptorcibatus* 14 10.52 Fossorial Nocturnal-Diurnal
Thamnodynastessp. 1 4 3.00 Terrestrial Nocturnal
Thamnodynastessp. 2 1 0.75 Terrestrial-Arboreal Nocturnal
Waglerophismerremii 6 4.51 Terrestrial Diurnal
Micrurus ibiboboca 2 1.50 Terrestrial fossorial Nocturnal-Diurnal
Bothropserythromelas 5 3.75 Terrestrial Nocturnal
Crotalusdurissus 8 6.01 Terrestrial Nocturnal
 LIZARDS, SNAKES, AND AMPHISBAENIANS
12-
10 -
(n 8
U a Fos-Ter
'I,
.0
6
E
C
4
0. DunesCaatI
Dunes
FIG.4. Snake species number for seven majorecological categoriesat the study area, Exu and Caatinga.
dune field. Psamophilous animals could then
evolve allopatrically to attain their present day
species status. Although originally designed to
account for the speciation of just one closely
related species pair (Rodrigues, 1986a), it was
subsequently and independently corroborated
by the discovery of other psamophilous species
pairs of lizards, snakes, and amphisbaenians.
The presence of four species pairs support this
allopatric model of differentiation: the tropi-
durid lizards Tropidurusamathites/Tropidurusdi-
varicatus, the gymnophthalmid lizards Calyp-
tommatussinebrachiatus/ leiolepis-nicterus,the col-
ubrid snakes Phimophis chui/Phimophis scriptor-
cibatus, and the amphisbaenians Amphisbaena
ignatiana/Amphisbaenahasataa.Each group has a
species (the first) occurring on the right bank
of the river whereas the other member of the
pair (two in the case of Calyptommatus)occur on
the opposite bank. Speciation occurred when
the Sao Francisco attained full exorreism divid-
ing formerly continuos sands and isolating their
psamophilous ancestral populations on oppo-
site banks. Possibly this period corresponded to
the end of the Wurm-Wisconsin glacial, rough-
ly 12000 years before present (Tricart, 1974). I
suggest that these species pairs speciated con-
temporaneously. Although this model explains
final phase of speciation in the area, and a por-
tion of the diversity, another sequence of events
is necessary to account on the origin of adap-
tations to psammophily and fossoriality. In a
recent paper (Rodrigues, 1993b) I hypothesized
that in a period previous to the origin of psa-
mophilic adaptations, the local fauna lived in
521
mArbor
* Arb-Terr
a Ter-Aq
n Terr
* Aqua
aFos
ng
Caatinga Exu
typical caatinga depressions with inselbergs and
isolated hills. During a subsequent endorrheic
phase these habitats became submerged, and
sand accumulated from lacustrine deposition,
isolating some elements of the fauna on disjunct
hills that remained above the flooded lowlands.
Later, with the onset of a semiarid climate, the
water level dropped exposing sand deposits to
sun and wind. These hills were vanishing fau-
nal refugia in a sandy desert. Species with pre-
adaptations for life in sand expanded into a
recent dune fields whereas others became ex-
tinct. This sequence of events corresponds in
essence to the ecogeographical model of spe-
ciation (Vanzolini and Williams, 1981). As
stressed previously (Rodrigues, 1991a), al-
though the paleolacustrine hypothesis can ac-
count for the final phase of speciation in the
area, we cannot dismiss the possibility that a
forsaken meander of the river was responsible
for the species multiplication.
I am convinced that a conjunction of histor-
ical and ecological contingencies operating in
the area were the determinant factors respon-
sible for the origin of this ecologically and mor-
phologically peculiar fauna; in other words, the
association of an ecogeographic mechanism of
speciation initially synchronic with, and later
replaced by, classic allopatric speciation.
The occurrence of the endemic Tropiduruspin-
ima, a saxicolous lizard closely related to Tro-
pidurussemitaeniatus,a widespread species in the
caatingas, indicates that a different round of
geographic speciation was initiated there, at least
in terms of the habitats isolated. Presently, we
522 MIGUEL TREFAUTRODRIGUES
do not know whether this episode was or was
not contemporaneous with the multiplication
phase of arenicolous forms.
Previous stocks of endemic psamophilous
groups certainly occurred in the region since
preadaptations for a psamophilic and fossorial
existence were already present. Several tropi-
durids are sand specialists (Rodrigues, 1987),
and Micrablepharusand Gymnophthalmus,the
more basal genera of the diverse gymnophthal-
mid radiation of the study area (Rodrigues,
1991b), already show striking adaptations to a
sand lifestyle: absence of eyelids, small size, and
limb reduction. The Amphisbaenidae and Ty-
phlopidae are acknowledged traditional fosso-
rial groups and Phimophis and Apostolepis are
also two entirely fossorial genera of xenodon-
tine snakes. Other families present in study area
as Boidae, Viperidae, Gekkonidae, and Teiidae
do not include fossorial forms in South Amer-
ica. The absence of endemic leptotyphlopids in
the study area may be real or perhaps reflect
undersampling. Finally, Mabuya is the only
South American genus of Scincidae and is typ-
ically terrestrial. In summary the endemic forms
that account for the high species diversity of
this area are descendants of previous stocks
preadapted to a fossorial life.
Even withstanding the above, some of the
current patterns may be adequately explained
by presently operating or recent ecological
causes. For example, why is Vanzosaurarubri-
caudaabsent from the Casanova dune field while
Procellosaurinustetradactylusand Procellosaurinus
erythrocercusoccur there? Why does Vanzosaura
rubricaudaoccur at Xique-Xique dune field only
at the base of dunes and not at the dunes where
Procellosaurinuserythrocercusoccur ([Rodrigues,
1991c]; Moraes, 1993)? Because these lizards are
ecologically and morphologically very similar
this pattern could be attributed to competitive
exclusion. Likewise, only by attributing to eco-
logical factors the absence of some represen-
tative forms from the sandy habitats at the right
bank, could we come to accept the final stage
of speciation proposed by the model. Present
knowledge of microteiid phylogeny (Ro-
drigues, 1991c; in prep.) suggest that Nothoba-
chia and Procellosaurinuswere already present at
the time when the ancestors of Calyptommatus
were separated by the river. Why then are they
absent from the sands of the right margin of
the river? The same question applies to other
endemics of the left bank as Tropiduruspsam-
monastes,Amphisbaenafrontalis,and the endemic
psamophilous rodent of the genus Proechimys
(Leal-Mesquita et al., 1992; Rocha, 1995). Both
extinction and competition are good candidates
for explanations for these problems. Data on
body size, although very preliminary, are also
indicative that speciation affected only small
reptiles. Although historical ecology, e.g., the
scarcity of sufficient prey, can be hypothesized
to account for this pattern, I prefer to rely on
phylogenetic constraint to explain it. For ex-
ample, the Iguanidae, Teiidae, and Boidae,
which include the largest forms, are terrestrial
or arboreal reptiles that historically were not
adapted to a subterranean life.
Acknowledgments.-I thank Funda:ao de Am-
paro a Pesquisa do Estado de Sao Paulo (FA-
PESP) and Conselho Nacional Cientifico e Tec-
nol6gico (CNPq) for support. Jose Manoel Mar-
tins, Pedro Luis Bernardo da Rocha, Gabriel
Skuk, Rosana Carvalho Moraes, Alessandra Biz-
erra, Otavio Marques, Alina Fierros, Jean Pierre
Ybert, Alcina Barreto, Maria Elisa Xavier Freire,
Rosana Tidon, and Federico Lencioni gave in-
valuable aid in the field. Gabriel Skuk aided
with the drawings. I thank Paulo Emilio Van-
zolini, Charles W. Myers, William R. Heyer,
BarbaraZimmerman, Carlos Peres, Laurie Vitt,
and John Lynch for critically reading the manu-
script. I also thank Yatiyo Yonenaga-Yassuda,
Maria Licia Bennozzati and Joao Stenghel Mor-
gante.
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