OCCASIONAL PAPERS SAM NOBLE OKLAHOMA MUSEUM OF NATURAL HISTORY

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1 OCCASIONAL PAPERS SAM NOBLE OKLAHOMA MUSEUM OF NATURAL HISTORY UNIVERSITY OF OKLAHOMA, NORMAN, OKLAHOMA NUMBER 14, PAGES MAY 2003 A NEW SPECIES OF CNEMIDOPHORUS (SQUAMATA, TEIIDAE) FROM THE CERRADO BIOME IN CENTRAL BRAZIL GUARINO R. COLLI 1, JANALEE P. CALDWELL 2, GABRIEL C. COSTA 1, ALISON M. GAINSBURY 1, ADRIAN A. GARDA 2, DANIEL O. MESQUITA 1, CARLOS M. M. R. FILHO 1, ANA H. B. SOARES 1, VERÔNICA N. SILVA 1, PAULA H. VALDUJO 1, GUSTAVO H. C. VIEIRA 1, LAURIE J. VITT 2, FERNANDA P. WERNECK 1, HELGA C. WIEDERHECKER 1, AND MARIANA G. ZATZ 1 1 Departamento de Zoologia, Universidade de Brasília Brasília, DF Brazil 2 Sam Noble Oklahoma Museum of Natural History and Department of Zoology University of Oklahoma, Norman, OK U.S.A. grcolli@unb.br; phone/fax: ABSTRACT We describe a new species of Cnemidophorus from the northern portion of the Cerrado biome in Tocantins state, Brazil. This species is apparently endemic to the Jalapão, one of the least populated regions of central Brazil, characterized by large tracts of the cerrado physiognomy on sandy soils. A discriminant analysis indicated that scales around tail and femoral pores are the best discriminators among bisexual, Brazilian species of Cnemidophorus south of Amazonia. A naïve Bayesian network constructed with categorical (mostly coloration) variables indicated that the new species had high conditional probabilities of the following qualitative characters: vertebral field light, dorsolateral stripes interrupted, upper lateral stripes continuous, ventral caudals smooth, and dorsal caudals keeled. Ecologically, this species is similar to other New World whiptail lizards except that it is small in body size and females produce clutches of a single egg. Key words: Jalapão, Brazil, Cerrado, Cnemidophorus, Lizard, Tocantins. RESUMO Nós descrevemos uma nova espécie de Cnemidophorus da porção norte do Cerrado, no estado do Tocantins, Brasil. Essa espécie é aparentemente endêmica do Jalapão, uma das regiões menos povoadas do Brasil central, caracterizada por grandes extensões de cerrados sobre solos arenosos. Uma análise discriminante indicou que escamas ao redor da cauda e poros femorais são os melhores critérios de discriminação entre espécies brasileiras e bissexuais de Cnemidophorus ao sul da Amazônia. Uma rede Bayesiana ingênua, construída com variáveis categóricas (a maioria de coloração), indicou que a nova espécie possui altas probabilidades condicionais de possuir campo vertebral claro, listras dorsolaterais interrompidas, listras laterais superiores contínuas, caudais ventrais lisas e caudais dorsais quilhadas. Ecologicamente, essa espécie é similar aos seus parentes mais próximos, exceto pelo seu menor tamanho corporal e pelas fêmeas produzirem ninhadas com um único ovo Sam Noble Oklahoma Museum of Natural History ISSN:

2 2 COLLI ET AL. OCCASIONAL PAPERS Despite covering approximately one-quarter of Brazil s surface and being the most extensive Neotropical savanna, the Cerrado remains poorly studied (Oliveira and Marquis, 2002). Large tracts of this biome have never been adequately sampled and many undescribed species are known to exist (Ministério do Meio Ambiente, 1999; Colli et al., 2002). During the course of a herpetological survey conducted in the Jalapão region, Tocantins state, Brazil, we collected an undescribed species of Cnemidophorus. Herein we describe this new species, making detailed comparisons with three other congeneric species that range south of Amazonia for which comparable data are available. A brief comment is warranted regarding the systematics of Cnemidophorus, particularly the South American species. A combination of mitochondrial rdna, allozymic, and morphological data revealed that Cnemidophorus is paraphyletic and placed the North American species in the genus Aspidoscelis (Reeder et al., 2002). The lemniscatus group was paraphyletic, with the species in the C. lemniscatus complex being more related to species of Kentropyx. Due to weakly supported relationships, the genus name Cnemidophorus was retained for this species group. Until recently, all populations of Cnemidophorus in northern South America were assigned to a single species, C. lemniscatus, whereas most populations south of Amazonia were referred to as C. ocellifer. Several populations, however, have been recognized as new species (e.g., Rocha et al., 1997, 2000, 2002; Feltrim and Lema, 2000; Dias et al., 2002; Colli et al., 2003) and many more await adequate description. Consequently, diversity within these lizards has been grossly underestimated. MATERIALS AND METHODS We collected lizards with shotguns, pitfall traps, and drift fences from 13 February to 10 March 2002 in the Jalapão region, around the city of Mateiros (10 32' 46.69" S, 46 25' 13.20" W), Tocantins state, Brazil (Fig. 1). The vegetation in the study area consists of an open and low cerrado on sandy soils. For a recent review of the Cerrado biome, see Oliveira and Marquis (2002). The Jalapão covers approximately 53, km 2 of the eastern portion of the state of Tocantins, at the border with the states of Maranhão, Piauí, and Bahia (Fig. 1). Hence, the region lies primarily within the Cerrado biome but is also influenced by the Caatinga from northeastern Brazil. The Jalapão has one of the lowest Figure 1. Map of South America indicating the typelocality of Cnemidophorus mumbuca, at Mateiros, Brazil, and localities of other populations of Cnemidophorus used in comparisons. demographic densities in Brazil (1.21 human inhabitants per km 2 ), but is experiencing increased anthropic pressure, especially though ecotourism. Mean annual precipitation and temperature are 1500 mm and 26 C, respectively. Sandy soils ( neossolos quartzarênicos, Prado, 2001) dominate the landscape, being derived from Cretaceous sandstones of the Urucuia Formation (Campos and Dardenne, 1997a, b; Sgarbi, 2000). For comparisons, we obtained data on Cnemidophorus parecis Colli, Costa, Garda, Kopp, Mesquita, Péres, Valdujo, Veira, and Wiederhecker, 2003, C. littoralis Rocha, Araújo, Vrcibradic, and Costa, 2000, and C. ocellifer (Spix, 1825) from specimens housed in the Coleção Herpetológica da Universidade de Brasília (CHUNB) (Appendix 1). We recorded the following meristic variables for each specimen: supralabials (number of enlarged scales along the upper jaw, total on both sides), infralabials (number of enlarged scales along the lower jaw, total on both sides), chinshields (most anterior pair of chinshields separated from infralabials by row of small scales), supraoculars (number of supraoculars on right side), parietals (number of parietals plus interparietal scale), scales around midbody (counted midway between fore- and hindlimbs, excluding ventrals), transverse rows of ventrals (counted

3 Number 14 NEW SPECIES OF CNEMIDOPHORUS 3 along the midline, from gular fold to anterior margin of hindlimbs), ventrals in transverse row (counted midway between fore- and hindlimbs), femoral pores (total number on both sides), prefemorals (number of enlarged scales on anterior aspect of thigh, counted midway between the hip and the knee, on a row from femoral pores to granules on dorsal aspect of thigh), prefemoral rows (counted from hip to knee), infratibials (number of enlarged scales on longitudinal row from knee to base of first metatarsal), preanals (number of enlarged scales on preanal plate, from level of medialmost femoral pores to vent), fourth finger lamellae (counted under the finger), fourth toe lamellae (counted under the toe), scales around tail (counted on fifth transverse row), and dorsals (counted along the midline, from occiput to first transverse row of scales around tail). We used a discriminant function analysis to investigate differences among species in meristic characters (Tabachnick and Fidell, 2001). To identify the most powerful discriminators of the species of Cnemidophorus, we used a stepwise discriminant function analysis of meristic characters (Tabachnick and Fidell, 2001), using the METHOD = STEPWISE option in PROC STEPDISC of SAS (SAS Institute Inc., 1988). We evaluated linear discriminant functions through posterior probability error-rate estimates, based on crossvalidation, using PROC DISCRIM (SAS Institute Inc., 1988). We also recorded the following categorical variables: lower lateral fields (LLF, one on each side, area between ventral scales and lower lateral stripes: absent, light, spotted, or dark), upper lateral fields (ULF, one on each side, area between upper lateral and dorsolateral stripes: absent, light, spotted, or dark), dorsolateral fields (DLF, one on each side, dark area between dorsolateral and paravertebral stripes: absent, light, spotted, or dark), vertebral fields (VTF, one on each side, middorsal area between paravertebral stripes: absent, light, spotted, or dark), vertebral line (VTL, light stripe from interparietal scale to base of tail: absent, interrupted, continuous, or double), paravertebral stripes (PVS, one on each side, light stripe from parietal scale to first third of tail, between vertebral and dorsolateral fields: absent, interrupted, or continuous), dorsolateral stripes (DLS, one on each side, light stripe from superciliaries to first third of tail, between dorsolateral and upper lateral fields: absent, interrupted, or continuous), upper lateral stripes (ULS, one on each side, light stripe from suborbital region to hindlimb, between upper and lower lateral fields: absent, interrupted, or continuous), lower lateral stripes (LLS, one on each side, light stripe from axilla to hip, between lower lateral field and ventrals: absent, interrupted, or continuous), lateral spots (LTS, rounded light areas on flanks: absent, present), hindlimb spots (HLS, rounded light areas on hindlimbs: absent, present), chinshield contact (CHS, degree of contact between most anterior pair of chinshields: no contact, contact smaller than half of their lengths, or contact greater than half of their lengths), semicircles (SMC, degree of contact between supraoculars and medial head scales: no contact, no contact with semicircles isolating first supraocular, supraoculars contacting frontal and parietals, supraoculars contacting frontal, supraoculars contacting parietals), dorsal caudals (DCA, keels on dorsal, caudal scales, from most anterior third of tail: absent, present), ventral caudals (VCA, keels on ventral, caudal scales, from most anterior third of tail: absent, present), and preanal spur (PAS: absent, present). To model the conditional dependencies of each categorical variable within each species, we constructed a naïve Bayesian model using the software UNBARB (available at ftp:// ftp.cic.unb.br/pub/cic/wagner/software/bnets/ UnBARB.zip). In this model (Fig. 2), the variable species influences the chance of the occurrence of states of each categorical variable, assuming that categorical variables are conditionally independent for a given species and that the joint distribution of all variables satisfies the following: Figure 2. Diagram depicting naïve Bayesian network constructed to evaluate conditional probabilities of 16 categorical variables from species, assuming independence among categorical variables. See text for abbreviations.

4 4 COLLI ET AL. OCCASIONAL PAPERS PSC ( k,,..., C )= PC ( k i S ) 1 PS ( ) i= 1 where S is species, C is a categorical variable, P(C i S) is the posterior probability of C i given S, and P(S) is the prior probability of S (Cowell et al., 1999). We estimated P(S) and P(C i S) using Bayesian statistics (DeGroot, 1970; Bernardo and Smith, 2000) and the software Hugin Lite v. 5.3 (Jensen and Nielsen, 1999). Throughout the text we report means ±1 SD. SPECIES DESCRIPTION Cnemidophorus mumbuca sp. nov. Holotype. CHUNB (Figs. 3, 4), adult female, adjacent to Escola Municipal Dona Isabel Barreira de Oliveira (10 15' 46.02" S, 46 33' 55.69" W), ca. 35 km NW of Mateiros, Município Mateiros, Tocantins state, Brazil, about 428 m, collected on 27 February 2002 by Santos F. Balbino, Janalee P. Caldwell, Frederico G. R. França, Adrian A. Garda, Daniel O. Mesquita, and Laurie J. Vitt. Paratopotypes. (227) All specimens from cerrado areas in Município Mateiros, Tocantins, Brazil: CHUNB 28317, , , , 28753, collected in February and March 2002 by same collectors. Diagnosis. A species distinguished from all other members of the lemniscatus group by the following combination of characters: (1) small size, maximum SVL 59 mm for males and 57 mm for females, mean SVL ± 7.43, n = 223; (2) femoral pores; (3) scales around tail; (4) dorsals; (5) vertebral field light; (6) dorsolateral stripes incomplete; (7) upper lateral stripes continuous; (8) anal spurs absent; (9) ventral caudals smooth; (10) dorsal caudals keeled; and (11) fixed clutch size of one egg. Cnemidophorus mumbuca differs from C. littoralis in having ventral rows (30 38 in C. littoralis), femoral pores (28 36), scales around tail (25 34), and dorsals ( ). Cnemidophorus mumbuca differs from C. ocellifer in having femoral pores (16 28 in C. ocellifer), dorsolateral stripes incomplete, not reaching supraciliary region (continuous in most individuals), smaller body size (maximum SVL 118 mm, Vitt, 1983), and a fixed clutch size of one egg (1 to 5 eggs, Vitt, 1983). Cnemidophorus mumbuca differs from C. abaetensis in having femoral pores (21 30 in C. abaetensis, Figure 3. Cnemidophorus mumbuca, holotype, CHUNB 28466, adult female, SVL 56 mm. Dias et al., 2002), transverse rows of ventrals (29 35), dorsal aspect of tail brownish green (bright blue green to emerald green), smaller body size (maximum SVL 72 mm), and in lacking a dorsal tail stripe (bright green dorsal tail stripe). Cnemidophorus mumbuca differs from C. nativo in having femoral pores (22 26 in C. nativo, Rocha et al., 1997), ventral rows (29 32), brownish green dorsum (black with a faint midorsal stripe), and smaller body size (maximum 69 mm). Cnemidophorus mumbuca differs from C. parecis in having 0 2 pairs of chinshields not in contact with infralabials (1 3 in C. parecis), ventral rows (29 35), 6 8 ventrals in transverse row (8 10), femoral pores (25 33), 4 7 prefemorals (5 12), scales around tail (34 47), and dorsolateral stripes incomplete. Cnemidophorus mumbuca differs from C. lemniscatus in having 9 13 infralabials (15 19 in C. lemniscatus, Colli et al., 2003), femoral pores (44 54), 7 9 infratibial rows (9 12), and ventral caudals smooth (keeled). Cnemidophorus mum-

5 Number 14 NEW SPECIES OF CNEMIDOPHORUS 5 Figure 4. Top: Cerrado in Mateiros, Tocantins, Brazil. Middle: Adult female of Cnemidophorus mumbuca (holotype, CHUNB 28466). Bottom: Adult male of C. mumbuca. buca differs from C. gramivagus in having femoral pores (40 51 in C. gramivagus, Colli et al., 2003), 9 13 infralabials (13 18), ventral rows (29 33), 7 9 infratibial rows (9 14), dorsolateral stripes incomplete (complete), and ventral caudals smooth (keeled). Cnemidophorus mumbuca differs from C. cryptus in having 9 13 infralabials (13-17 in C. cryptus, Colli et al., 2003), femoral pores (38 48), dorsolateral stripes incomplete (complete), and ventral caudals smooth (keeled). Description of holotype. Adult female, 56 mm SVL, 115 mm complete tail length, 4.4 g total mass, rostral pentagonal, higher than wide, visible from above, bordered posteriorly by nasals. Nasals in contact along midline, each nasal divided by an oblique suture. Nostril in lower part of suture, directed posterolaterally, higher than wide. Frontonasal subhexagonal, suture with nasals and loreals forming a semicircle, sutures with prefrontals forming a wide angle. Prefrontals quadrilateral, with medial suture approximately as long as that between nasals, in contact laterally with loreal and first supraocular. Frontal approximately pentagonal, longer than wide, and wider anteriorly. Sutures with prefrontals straight, those with frontoparietals gently curved. Frontal separated from supraoculars by row of small scales. Frontoparietals pentagonal, longer than wide, with long, straight medial suture; separated from supraoculars by row of small scales; sutures with interparietal roundish. Interparietal sub-heptagonal, bordered at each side by irregular parietals, each divided by an oblique suture. Occipital scales irregular and variable in size. Four supraoculars on each side, second and third largest, followed posteriorly by group of small scales. First in contact with loreals, prefrontals, first supraciliaries, and second supraocular. Second, third, and fourth supraoculars separated from supraciliaries, frontal, frontoparietals, and parietals by row of small scales. Five supraciliaries on each side, first and second largest, others subequal. Loreal single, large, in contact with nasal, frontonasal, prefrontal, first supraciliary, frenocular, first subocular, and third and fourth supralabials on the left side, and second, third, and fourth supralabials on the right side. Frenocular narrow, height greater than width, in contact with first subocular, loreal, and small scales in ocular region. Three large suboculars, second largest, all in contact with supralabials. A continuous keel runs from frenocular to second subocular. Postoculars small, arranged in 2 3 rows. Lower eyelid with semiopaque disc, formed by transversally enlarged, convex scales. Five enlarged supralabials on each side, fifth below center of eye; followed by series of small scales extending to commissure of mouth. Temporal region with irregular scales, granular centrally, moderately enlarged peripherally. Ear opening large, oblique,

6 6 COLLI ET AL. OCCASIONAL PAPERS with smooth margins, anterior margin forming a semicircle, posterior margin straight. Tympanum recessed in a short auditory meatus. All dorsal and lateral head scales juxtaposed, smooth (except for keeled frenoculars and first and second suboculars). Symphysal anteriorly ellipsoid, posteriorly in contact with first infralabials and postsymphysal, forming two wide angles. Postsymphysal single, pentagonal, in contact with first and second infralabials, followed by four pairs of enlarged chinshields. First pair of chinshields in ample contact along midline; first and fourth pairs in contact with infralabials, second and third pair separated from infralabials by row of small scales; followed posteriorly by enlarged scales. Medial scales on chin small, smooth, elongate, arranged in longitudinal, posteriorly divergent rows; increasing in size and becoming roundish posteriorly. Five enlarged infralabials on each side, followed posteriorly by series of small scales extending to commissure of mouth; fifth infralabial below center of eye. Gular region divided in two areas: anterior region with enlarged, rounded scales, in transverse rows, delimited posteriorly by line uniting lower margin of ear openings; posterior region covered with granules, in transverse rows, bordered posteriorly by antegular fold. Gular and antegular folds marked by granules; scales between the two folds larger, irregular, slightly imbricate. Scales on nape and sides of neck similar to dorsals. Dorsals and scales on flanks granular, rounded, smooth, subimbricate; 235 scales from nape to base of tail; 104 scales around midbody (excluding ventrals). Ventrals large, smooth, rectangular (wider than long), imbricate, in 28 transverse rows; 8 ventral scales in transverse rows across midbody. Ventral scales separated from scales on flanks by row of moderately large scales. Preanal plate with three rows of enlarged scales, surrounded laterally by small scales. Preanal spurs absent. Femoral pores in a continuous row along each thigh, medially with a short gap; 8 pores on right side, 10 pores on left side. Scales on base of tail rectangular, smaller than ventrals, in transverse rows, longer than wide and keeled dorsally, gradually becoming wider than long and smooth ventrally. All transverse rows continuous around tail, except first row incomplete ventrally. Tail scales becoming longer and narrower posteriorly; subcaudal scales becoming keeled posteriorly. Limbs with large, smooth, imbricate scales on dorsal aspect of upper arms, Figure 5. Dorsal coloration patterns in four species of Cnemidophorus from Brazil. (A) C. littoralis, CHUNB (B) C. ocellifer, CHUNB (C) C. parecis, CHUNB (D) C. mumbuca, CHUNB anterodorsal aspect of forearms, anteroventral aspect of thighs, and ventral aspect of lower legs; elsewhere scales small, granular. Larger scales on upper arms in longitudinal rows. Forearms with one row of enlarged scales, wider than long. Anterior scales on thigh decreasing in size proximally. Lower legs with two rows of enlarged, hexagonal scales. Ventral aspect of hands and feet granular; three enlarged tubercles at base of pollex. Subdigital lamellae single; lamellae under left fourth finger 14, under right fourth finger 15; under left fourth toe 26; under right fourth toe 25. Color in life. Head brownish green dorsally, whitish laterally; labial regions and ventral aspect of head immaculate (Fig. 4). Dorsum, dorsal aspect of tail, hindlimbs, and forearms brownish green. Anterior aspect of thighs, proximal aspect of lower legs, lower flanks, and lateralmost longitudinal rows of ventrals yellowish green. Remainder of belly and ventral aspect of limbs and tail immaculate white. Paravertebral stripes whitish, interrupted, from parietal scales to base of tail, separated from dorsolateral stripes by ochre dorsolateral fields. Dorsolateral stripes whitish, incomplete, from behind supraciliary region to first third of tail, separated from upper lateral stripes by ochre upper lateral fields (Fig. 5). Upper lateral stripes whitish, continuous from suborbital region to hip, separated from lower lateral stripes by ochre lower lateral fields. Lower lateral stripes whitish, interrupted, extending from axilla to mid-body. Upper lateral fields

7 Number 14 NEW SPECIES OF CNEMIDOPHORUS 7 broader than dorsolateral fields; lower lateral fields thinnest. Color in fixative (stored in 70% ethanol, after preservation in 10% formalin). Head bluish brown dorsally, bluish laterally; labial regions and ventral aspect of head bluish white. Dorsum and dorsal aspect of tail bluish brown. Belly and ventral aspect of forelimbs bluish white; ventral aspect of tail and hindlimbs immaculate. Stripes bluish white and fields brown. Etymology. The name mumbuca refers to a small community of African descendents who migrated from the state of Bahia to the Jalapão region in This matriarchal community comprises approximately 22 families that survive from the production of handicraft using a locally abundant grass, called Capim-dourado (goldengrass, Syngonanthus nitens). Variation. Sexes are dimorphic in adult color pattern (Fig. 4). Light areas in anteriormost third of body bluish in males and whitish in females. Anterior aspect of thighs, sides of tail base, and lower flanks bright yellowish green in males and darker in females. Adult males generally with row of bluish white spots on lower lateral fields, whereas approximately 50% of females lack spots. Overall, juveniles of both sexes resemble adult females in coloration. Distribution and ecology. Known only from the type-locality (Fig. 1). Cnemidophorus mumbuca is the most abundant lizard species in the sandy cerrados around Mateiros. Other common lizard species at the type-locality are the tropidurid Tropidurus oreadicus, the gecko Gymnodactylus geckoides, the skink Mabuya heathi, the teiid Ameiva ameiva, and the gymnophthalmids Micrablepharus maximiliani and Vanzosaura rubricauda (Vitt et al., 2002). Cnemidophorus mumbuca is most common in open habitats with sandy soil with apparent density diminishing as the density of vegetation increases. They were not found in gallery forest. As an example of the effect of vegetation on their density, we monitored two pitfall trap arrays separated by only about 100 m (detailed data to be reported elsewhere). One was in open cerrado with few trees whereas the other contained a much higher tree density. From 15 February through 9 March, we collected 157 C. mumbuca in the array in the more open habitat and only 47 in the array with greater tree cover; they were more than three times as common in the open habitat. Both had sandy soil. In open grassy habitats, 35 of 36 (97.2%) individuals observed active were first seen on sandy soil; one was on a rock. Twenty-eight (77.8%) of those fled under shrubs, seven (19.4%) remained on sandy soil after fleeing, and one (2.8%) fled to a rock. Thirty-four (94.4%) stopped after initial flight, the other two (5.6%) continued fleeing. Cnemidophorus mumbuca becomes active when morning sun heats the ground. Twenty-three (63.9%) were first observed in sun, four (11.1%) were in shade, and 9 (25.0%) were in filtered sun. We observed individuals at 0800 h when we visited pitfall trap grids and observations on active lizards were made from h. Body temperatures of 36 active individuals averaged 36.9 ± 0.3 C (mean ± SE), substrate temperatures associated with lizards averaged 33.7 ± 0.6 C, air temperatures at 5 cm above ground averaged 32.5 ± 0.5 C, and air temperatures at 1 m averaged 31.9 ± 0.4 C. Lizard body temperatures averaged 3.2 ± 0.6 C higher than substrate temperatures and 4.4 ± 0.5 C higher than air temperatures at 5 cm. Although substrate temperatures explained only 16.2% of the variation in lizard body temperatures, the relationship between lizard body temperatures and substrate temperatures was highly significant (F 1,34 = 7.8, P = 0.009). The diet of 166 individuals included 21 prey types (ordinal level in most cases), most of which were insects. Numerically, termites were by far the most common prey type (64.98% of all prey) with orthopterans and spiders contributing 11.05% and 6.23% respectively. Volumetrically, orthopterans (35.54%), termites (14.90%), insect larvae (14.48%) and spiders (5.21%) accounted for 70% of the diet. Lizards most frequently ate orthopterans (54.8% of lizards), spiders (33.1%), termites (28.3%), and insect larvae (18.7%). Prey size, based on 1285 measurable items, averaged 4.45 ± 0.09 mm (range mm) in length, 1.73 ± 0.03 mm (range mm) in width, and ± 1.07 mm 3 (range mm 3 ) in volume. Among 80 females collected, five contained a single egg in one oviduct and 30 contained a single enlarged vitellogenic follicle. Thus, clutch size appears to be one egg. Oviductal eggs averaged ± 0.66 mm in length and 7.63 ± 0.43 mm in width. Based on the formula for a prolate spheroid, we estimate volume of an oviductal egg to be ± 67.9 mm 3. RESULTS AND DISCUSSION Meristic characters easily distinguish Cnemidophorus mumbuca from other congeners allied to C. ocellifer. The first two canonical discrimi-

8 8 COLLI ET AL. OCCASIONAL PAPERS Table 1. Canonical discriminant analysis of meristic characters of four species of Cnemidophorus. Canonical Variable Canonical Statistics Eigenvalue Cumulative proportion r 2 F P I <.0001 II <.0001 Variable Raw Canonical Coefficients Canonical Variable I Canonical Variable II Supralabials Infralabials Chinshields Supraoculars Parietals Scales around midbody Transverse rows of ventrals Ventrals in transverse row Femoral pores Prefemorals Prefemoral rows Infratibial rows Preanals Fourth finger lamellae Fourth toe lamellae Scales around tail Dorsals Species Means Canonical Variable I Canonical Variable II C. mumbuca C. littoralis C. ocellifer C. parecis nant variables explained approximately 97% of the total variation in the meristic variables (Table 1). The first canonical variable, representing primarily the influence of ventrals in transverse row (Table 1), promoted a clear separation between the four species (Fig. 6). Cnemidophorus parecis and C. littoralis, with positive means on the first canonical variable (Table 1), are characterized by a large number of ventrals in transverse row (Table 2). The second canonical discriminant variable, representing a contrast between femoral pores and supraoculars (positive coefficients) versus ventrals in transverse row and infralabials (Table 1), indicated a clear separation between C. littoralis and the remaining species (Fig. 6). Cnemidophorus littoralis, with the largest mean on the second canonical variable (Table 1), is mainly characterized by a large number of femoral pores (Table 2). The stepwise discriminant analysis of meristic characters selected 17 variables as the most powerful discriminators among the species of Cnemidophorus (Table 3). Scales around tail was selected first, correctly classifying 85.5% of the individuals, followed by femoral pores and fourth Figure 6. Scores on the first two canonical discriminant axes based on meristic variables in four species of Cnemidophorus from Brazil south of Amazonia.

9 Number 14 NEW SPECIES OF CNEMIDOPHORUS 9 Table 2. Meristic characters of four species of Cnemidophorus south of Amazonia in Brazil. Values indicate ± 1 SD, with range in parentheses. Variables Species C. mumbuca (n = 229) C. littoralis (n = 53) C. ocellifer (n = 101) C. parecis (n = 108) Supralabials ± ± ± ± 0.35 (12 18) (13 17) (11 16) (11 14) Infralabials ± ± ± ± 1.01 (9 13) (10 13) (10 14) (10 15) Chinshields 1.30 ± ± ± ± 0.30 (0 2) (1 2) (0 2) (1 3) Supraoculars 3.99 ± ± ± ± 0.10 (3 5) (3 5) (3 4) (4 5) Parietals 4.56 ± ± ± ± 0.82 (3 7) (3 5) (3 5) (2 5) Scales around midbody ± ± ± ± 5.85 (91 117) (96 123) (81 141) (96 127) Transverse rows of ventrals ± ± ± ± 0.97 (24 29) (30 38) (25 31) (29 35) Ventrals in transverse row 8.00 ± ± ± ± 0.49 (6 8) (8 10) (5 8) (8 10) Femoral pores ± ± ± ± 1.41 (14 20) (28 36) (16 28) (25 33) Prefemorals 4.90 ± ± ± ± 1.06 (4 7) (4 11) (4 8) (5 12) Prefemoral rows 9.49 ± ± ± ± 0.81 (8 12) (8 14) (8 11) (10 14) Infratibial rows 8.10 ± ± ± ± 0.70 (7 9) (6 13) (7 10) (8 12) Preanals 3.01 ± ± ± ± 0.42 (3 4) (3 5) (3 5) (4 5) Fourth finger lamellae ± ± ± ± 0.90 (13 19) (16 24) (13 20) (13 19) Fourth toe lamellae ± ± ± ± 1.61 (24 32) (29 37) (24 38) (23 31) Scales around tail ± ± ± ± 2.04 (19 27) (25 34) (21 30) (34 47) Dorsals ± ± ± ± ( ) ( ) ( ) ( )

10 10 COLLI ET AL. OCCASIONAL PAPERS Table 3. Stepwise discriminant analysis of meristic characters from four species of Cnemidophorus, with error-rate estimates based on cross-validation. Step Variable entered F P Error-rate 1 Scales around tail < Femoral pores < Fourth toe lamellae < Ventrals in transverse row < Supralabials < Dorsals < Scales around midbody < Transverse rows of ventrals < Infralabials < Chinshields < Prefemorals < Fourth finger lamellae < Infratibial rows 7.21 < Parietals 6.67 < Prefemoral rows 4.97 < Supraoculars 4.37 < Preanals 2.74 < toe lamellae, whose addition improved the classification criterion to 93.5% and 95.3%, respectively (Table 3). To determine if important variables were excluded from the analysis because of correlations among the original variables (Tabachnick and Fidell, 2001), we removed scales around tail and repeated the analysis. Femoral pores were then entered in the first step, correctly classifying 88.6% of the lizards (error-rate = 0.114, F = , P < 0.001). We then removed femoral pores and repeated the analysis once more. This time, ventrals in transverse row was the first variable to be selected, correctly classifying about 68.8% of the lizards (error-rate = , F = , P < 0.001). These analyses indicated that scales around tail, femoral pores, Table 4. Conditional probabilities of states for qualitative characters for four Brazilian species of Cnemidophorus, assuming a naïve Bayesian model. Variables Species C. mumbuca C. littoralis C. ocellifer C. parecis Lower lateral fields D= 61.80% L= 50.88% L= 71.43% L= 91.96% Upper lateral fields Sp= 51.93% D= 92.98% D= 48.57% L= 91.07% Dorsolateral fields D= 64.38% D= 64.91% D= 47.62% A= 96.43% Vertebral field L= 95.28% D= 64.91% L= 80.00% Sp= 96.43% Paravertebral stripes I= 67.24% I= 96.43% I= 61.54% A= 98.20% Dorsolateral stripes I= 98.71% C = 82.14% C= 64.42% C= 84.68% Upper lateral stripes C= 99.14% C = 96.43% C= 57.69% C= 90.99% Lower lateral stripes I= 85.34% I= 66.07% A= I= 95.50% Vertebral line A= 91.81% I= 91.07% A= A= 98.20% Lateral spots P= 67.10% A= 98.18% P= A= 99.09% Hindlimb spots P= 61.90% A= 98.18% A= 98.06% A= 99.09% Chinshields >= 87.07% >= 80.36% >= 98.08% >= 46.85% Lower lateral fields D= 61.80% L= 50.88% L= 71.43% L= 91.96% Preanal spur A= 100% A= 100% A= 100% A= 100% Semicircles NSS= 59.23% IFP= 59.65% NC= 53.33% IFP= 96.43% Ventral caudals S= 99.57% S= 98.18% S= 91.26% S= 99.09% Dorsal caudals K= 99.57% K= 98.18% K= 99.03% K= 89.09% Note: values in bold indicate probabilities greater than 95%. D: dark; L: light; Sp: spotted; A: absent; P: present; C: continuous; I: interrupted; K: keeled; S: smooth; IFP: incomplete, supraoculars contacting frontals and parietals; NSS: no contact, with semicircles isolating first supraocular; NC: no contact; >: contact between first pair of chin shields greater than half of their lengths.

11 Number 14 NEW SPECIES OF CNEMIDOPHORUS 11 and ventrals in transverse row are the meristic characters that best discriminated the species of Cnemidophorus and that their discriminatory power was high. The naïve Bayesian model indicated that Cnemidophorus mumbuca determined high conditional probabilities (>95%) of 6 categorical variables: vertebral field light, dorsolateral stripes interrupted, upper lateral stripes continuous, preanal spur absent, ventral caudals smooth, and dorsal caudals keeled (Table 4). Further, only C. mumbuca determined high conditional probabilities of vertebral field light and dorsolateral stripes interrupted (Table 4). Our results revealed a greater similarity between Cnemidophorus mumbuca and C. ocellifer, suggesting that the two species may be close relatives. However, a phylogenetic analysis of the species in the lemniscatus group is badly needed (Reeder et al., 2002). The nature of the biogeographic events that promoted the formation of C. mumbuca, in particular, and the diversification of the Cerrado herpetofauna, in general, are still poorly understood. Too much emphasis has been placed on relatively recent events, such as climatic fluctuations of the Quaternary (e.g., Vanzolini, 1970, 1974, 1976; Heyer, 1978; Duellman, 1979). However, several lines of evidence suggest that a great deal of the diversification of the Cerrado herpetofauna took place during the Tertiary, primarily as a consequence of the deepening of a latitudinal temperature gradient in South America (Pascual and Jaureguizar, 1990), the modernization of the Mixed Microfloral Province (Romero, 1993), the marine transgression that separated the Brazilian Shield from the southern portion of the continent (Räsänen et al., 1995; Webb, 1995), the uplift of the Brazilian Shield (Brasil and Alvarenga, 1989; Del Arco and Bezerra, 1989), and finally the arrival of immigrants from Central and North America (Estes and Báez, 1985; Vanzolini and Heyer, 1985). Apparently, Cnemidophorus mumbuca is an endemic of the Jalapão region and is strongly associated with sandy soils in open habitats, like other congeneric species (Magnusson et al., 1986). Given that the sands of the Urucuia Formation date back to the Cretaceous, the association of the new species with this geologic entity is not particularly enlightening with respect to its origin. We can only speculate that differentiation took place in situ and was shaped by prevailing ecological conditions, e.g., water stress and strong wet-dry seasonality. New World whiptail lizards (Cnemidophorus and Aspidoscelis) occur from the Great Basin Desert of North America through the deserts of Argentina (Wright, 1993). All species share a set of morphological and ecological characteristics including: elongate body and tail, active foraging mode, affinity for open habitats, high active body temperatures, high activity levels, and relatively low relative clutch mass (e.g., Pianka, 1970; Schall, 1977; Anderson and Karasov, 1981; Anderson, 1993; Casas-Andreu and Gurrola- Hidalgo, 1993; Vitt and Breitenbach, 1993; Vitt et al., 1993, 1997). Cnemidophorus mumbuca also shares this set of characteristics. Consequently, many aspects of the ecology of C. mumbuca are probably historical, reflecting a long history of success of whiptails in open habitats (see Pianka and Vitt, 2003; Vitt et al., 2003). Cnemidophorus mumbuca differs from most whiptails in body size (it is at the small end of the body size distribution for whiptails) and clutch size (a single egg). A history of low resource availability may have contributed to its small body size (see Tracy, 1999). Production of a single, relatively large egg may have resulted from selection favoring relatively large (and thus more competitive) offspring in a resource poor environment, an environment with small-bodied competitors (the two gymnophthalmids), or both. Clutch sizes of a single large egg are rare in whiptails, the most notable occurring in the large-bodied C. arubensis (Schall, 1977; Dearing and Schall, 1994), which lives in resource poor environments and has switched to herbivory (Dearing and Schall, 1992). ACKNOWLEDGEMENTS This work was developed under the project Proposta de levantamento da herpetofauna da micro-região do Jalapão, funded by Conservation International do Brasil, Universidade de Brasília, and SNOMNH. Santos F. Balbino and Frederico G. França assisted in fieldwork. We thank Dr. Marcos A. S. Silva for drawing the holotype. This work was supported by graduate student fellowships from CAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível Superior to AMG, AAG, DOM, and PHV; from Conselho Nacional do Desenvolvimento Científico e Tecnológico to GHCV, FPW, HCW, and MGZ; and by a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq to GRC (# /88-1).

12 12 COLLI ET AL. OCCASIONAL PAPERS LITERATURE CITED Anderson, R. A Analysis of foraging in a lizard, Cnemidophorus tigris: salient features and environmental effects. In Wright, J. W. and Vitt, L. J. (eds.), Biology of Whiptail Lizards (Genus Cnemidophorus), pp Oklahoma Museum of Natural History, Norman, Oklahoma. Anderson, R. A. and Karasov, W. H Contrasts in energy intake and expenditure in sit-and-wait and widely foraging lizards. Oecologia (Berlin) 49: Bernardo, J. M. and Smith, A. F. M Bayesian Theory. Wiley, New York, New York, U.S.A. Brasil, A. E. and Alvarenga, S. M Relevo. In Duarte, A. C. (ed.), Geografia do Brasil. Região Centro-Oeste, pp FIBGE-Diretoria de Geociências, Rio de Janeiro. Campos, J. E. G. and Dardenne, M. A. 1997a. Origem e evolução tectônica da Bacia Sanfranciscana. Revista Brasileira de Geociências 27: Campos, J. E. G. and Dardenne, M. A. 1997b. Estratigrafia e sedimentação da Bacia Sanfranciscana: uma revisão. Revista Brasileira de Geociências 27: Casas-Andreu, G. and Gurrola-Hidalgo, M. A Comparative ecology of two species of Cnemidophorus in coastal Jalisco, Mexico. In Wright, J. W. and Vitt, L. J. (eds.), Biology of Whiptail Lizards (Genus Cnemidophorus), pp The Oklahoma Museum of Natural History, Norman, Oklahoma. Colli, G. R., Bastos, R. P., and Araújo, A. F. B The character and dynamics of the Cerrado herpetofauna. In Oliveira, P. S. and Marquis, R. J. (eds.), The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna, pp Columbia University Press, New York, NY. Colli, G. R., Costa, G. C., Garda, A. A., Kopp, K. A., Mesquita, D. O., Péres, A. K., Jr., Valdujo, P. H., Vieira, G. H. C., and Wiederhecker, H. C A critically endangered new species of Cnemidophorus (Squamata, Teiidae) from a Cerrado enclave in southwestern Amazonia, Brazil. Herpetologica 59: Cowell, R. G., Dawid, A. P., Lauritzen, S. L., and Spiegelhalter, D. J Probabilistic Networks and Expert Systems. Springer-Verlag New York, Inc., New York, New York, U.S.A. Dearing, M. D. and Schall, J. J Testing models of optimal diet assembly by the generalist herbivorous lizard Cnemidophorus murinus. Ecology 73: Dearing, M. D. and Schall, J. J Atypical reproduction and sexual dimorphism of the tropical Bonaire Island whiptail lizard, Cnemidophorus murinus. Copeia 1994: DeGroot, M. H Optimal Statistic Decisions. McGraw-Hill, New York, New York, U.S.A. Del Arco, J. O. and Bezerra, P. E. L Geologia. In Fundação Instituto Brasileiro de Geografia e Estatística (ed.), Geografia do Brasil. Região Centro-Oeste. Volume 1., pp IBGE, Rio de Janeiro. Dias, E. J. R., Rocha, C. F. D., and Vrcibradic, D New Cnemidophorus (Squamata: Teiidae) from Bahia State, northeastern Brazil. Copeia 2002: Duellman, W. E. (ed.) The South American Herpetofauna: Its Origin, Evolution and Dispersal. Lawrence, Kansas, The Museum of Natural History, The University of Kansas. Estes, R. and Báez, A Herpetofaunas of North and South America during the late Cretaceous and Cenozoic: evidence for interchange? In Stehli, F. G. and Webb, S. D. (eds.), The Great American Biotic Interchange, pp Plenum Press, New York. Feltrim, A. C. and Lema, T Uma nova espécie de Cnemidophorus Wagler, 1830 do estado do Rio Grande do Sul, Brasil (Sauria, Teiidae). Biociências 8: Heyer, W. R Systematics of the fuscus group of the frog genus Leptodactylus (Amphibia, Leptodactylidae). Natural History Museum of Los Angeles County Science Bulletin 29:1-85. Jensen, F. and Nielsen, L. B Hugin Lite. Aalborg, Denmark, Hugin Expert A/S. Magnusson, W. E., Franke, C. R., and Kasper, L. A Factors affecting densities of Cnemidophorus lemniscatus. Copeia 1986: Ministério do Meio Ambiente Ações Prioritárias para a Conservação da Biodiversidade do Cerrado e Pantanal. Centro de Informação e Documentação Luís Eduardo Magalhães, Brasília, Distrito Federal. Oliveira, P. S. and Marquis, R. J The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York, New York. Pascual, R. and Jaureguizar, E. O Evolving climates and mammal faunas in Cenozoic South America. Journal of Human Evolution 19: Pianka, E. R Comparative antecology of the lizard Cnemidophorus tigres in different parts of its geographic range. Ecology 51: Pianka, E. R. and Vitt, L. J Lizards: Windows to the Evolution of Diversity. University of California Press, Berkeley, California. Prado, H Solos do Brasil: Gênese, Morfologia, Classificação e Levantamento (Second edition). H. do Prado, Piracicaba, São Paulo. Räsänen, M. E., Linna, A. M., Santos, J. C. R., and

13 Number 14 NEW SPECIES OF CNEMIDOPHORUS 13 Negri, F. R Late Miocene tidal deposits in the Amazonian foreland basin. Science 269: Reeder, T. W., Cole, C. J., and Dessauer, H. C Phylogenetic relationships of whiptail lizards of the genus Cnemidophorus (Squamata: Teiidae): a test of monophyly, reevaluation of karyotypic evolution, and review of hybrid origins. American Museum Novitates 3365:1-61. Rocha, C. F. D., Bergallo, H. G., and Peccinini-Seale, D Evidence of an unisexual population of the Brazilian whiptail lizard genus Cnemidophorus (Teiidae), with description of a new species. Herpetologica 53: Rocha, C. F. D., Araújo, A. F. B., Vrcibradic, D., and Costa, E. M. M New Cnemidophorus (Squamata; Teidae) from coastal Rio de Janeiro State, southeastern Brazil. Copeia 2000: Romero, E. J South American paleofloras. In Goldblatt, P. (ed.), Biological Relationships Between Africa and South America, pp Yale University Press, New Haven and London. SAS Institute Inc SAS/STAT User's Guide, Release 6.03 Edition. SAS Institute Inc., Cary, North Carolina, U.S.A. Schall, J. J Thermal ecology of five sympatric species of Cnemidophorus (Sauria: Teiidae). Herpetologica 33: Sgarbi, G. N. C The Cretaceous Sanfranciscan Basin, eastern Plateau of Brazil. Revista Brasileira de Geociências 30: Tabachnick, B. G. and Fidell, L. S Using Multivariate Statistics. Allyn & Bacon, Needham Heights, Massachussetts, U.S.A. Tracy, C. R Differences in body size among chuckwalla (Sauromalus obesus) populations. Ecology 80: Vanzolini, P. E Zoologia Sistemática, Geografia e a Origem das Espécies. Universidade de São Paulo, Instituto de Geografia, São Paulo. Vanzolini, P. E Ecological and geographical distribution of lizards in Pernambuco, northeastern Brazil (Sauria). Papéis Avulsos de Zoologia, São Paulo 28: Vanzolini, P. E On the lizards of a cerradocaatinga contact, evolutionary and zoogeographical implications (Sauria). Papéis Avulsos de Zoologia, São Paulo 29: Vanzolini, P. E. and Heyer, W. R The American herpetofauna and the interchange. In Stehli, F. G. and Webb, S. D. (eds.), The Great American Biotic Interchange, pp Plenum Press, New York. Vitt, L. J Reproduction and sexual dimorphism in the tropical teiid lizard, Cnemidophorus ocellifer. Copeia 1983: Vitt, L. J. and Breitenbach, G. L Life histories and reproductive tactics among lizards in the genus Cnemidophorus (Sauria: Teiidae). In Wright, J. W. and Vitt, L. J. (eds.). Biology of whiptail lizards (genus Cnemidophorus), pp Oklahoma Museum of Natural History, Norman, Oklahoma, USA. Vitt, L. J., Zani, P. A., Caldwell, J. P., and Durtsche, R. D Ecology of the whiptail lizard Cnemidophorus deppii on a tropical beach. Canadian Journal of Zoology 71: Vitt, L. J., Pianka, E. R., Cooper, J., W. E., Jr., and Schwenk, K History and the global ecology of squamate reptiles. American Naturalist in press. Vitt, L. J., Zani, P. A., Caldwell, J. P., Araújo, M. C. D., and Magnusson, W. E Ecology of whiptail lizards (Cnemidophorus) in the Amazon Region of Brazil. Copeia 1997: Vitt, L. J., Caldwell, J. P., Colli, G. R., Garda, A. A., Mesquita, D. O., França, F. G. R., and Balbino, S. F Um guia fotográfico dos répteis e anfíbios da região do Jalapão no Cerrado brasileiro. Special Publications in Herpetology, Sam Noble Oklahoma Museum of Natural History 1:1-17. Webb, S. D Biological implications of the Middle Miocene Amazon Seaway. Science 269: Wright, J. W Evolution of the lizards of the genus Cnemidophorus. In Wright, J. W. and Vitt, L. J. (eds.), Biology of Whiptail Lizards (Genus Cnemidophorus), pp The Oklahoma Museum of Natural History, Norman, Oklahoma, U.S.A.

14 14 COLLI ET AL. OCCASIONAL PAPERS APPENDIX I Specimens Examined Cnemidophorus littoralis (53). BRAZIL: Rio de Janeiro: Barra de Maricá, CHUNB , , 24110, 24111, 24117, 24867, Cnemidophorus mumbuca (228). BRAZIL: Tocantins: Mateiros, CHUNB 28317, , , Cnemidophorus ocellifer (101). BRAZIL: Bahia: Ibipeba, CHUNB , 03265, 03273, 03274, 03358, 03360, 03369, 03370, 03372, 03375, 03376, 03378, 03401, 03405, 03414, 03421, 08481, 08484, 08485; Irecê, CHUNB 03266, 03267, , 03359, , 03373, 03374, 03377, 03379, 03380, 03382, ; Lençóis, CHUNB 05591; Paulo Afonso, CHUNB ; Salvador, CHUNB 08138, 08139, 08152; Pernambuco: Buíque, CHUNB 23529; Exu, CHUNB 12855, 13590; Petrolina, CHUNB , , , , 13614, 24109, Cnemidophorus parecis (108). BRAZIL: Rondônia: Vilhena, CHUNB , , 14229,

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