Amerotyphlops martis, Graboski & Arredondo & Grazziotin & Guerra-Fuentes & Da Silva & Prudente & Pinto & Rodrigues & Bonatto & Zaher, 2023

Graboski, Roberta, Arredondo, Juan C., Grazziotin, Felipe G., Guerra-Fuentes, Ricardo Arturo, Da Silva, Ariane A. A., Prudente, Ana L. C., Pinto, Roberta R., Rodrigues, Miguel T., Bonatto, Sandro L. & Zaher, Hussam, 2023, Revealing the cryptic diversity of the widespread and poorly known South American blind snake genus Amerotyphlops (Typhlopidae: Scolecophidia) through integrative taxonomy, Zoological Journal of the Linnean Society 197, pp. 719-751 : 735-738

AMEROTYPHLOPS MARTIS SP. NOV.

( FIG. 12 ; SUPPORTING INFORMATION, FIGS S5 , S 6 )

Z o o b a n k r e g i s t r a t i o n: u r n: l s i d: z o o b a n k. org:act: 0FDB6570-F072-4B5E-BE52-0BF93785AC88

Holotype: An adult male, MNRJ 18744 , collected by Ana C. C. Lourenço and Délio Baêta between 2 and 8 September 2009 from Praia das Neves (21° 16 ′ 45.59 ′′ S, 40° 57 ′ 47.86 ′′ W), municipality of Presidente Kennedy, state of Espírito Santo, Brazil ( Fig. 12 ; Supporting Information, Fig. S5 ).

Paratypes: Three male specimens, MNRJ 18743 , MNRJ 18745 and MNRJ 18747 , collected in the same locality of the holotype by Ana C. C. Lourenço and Délio Baêta between 2 and 8 September 2009 (Supporting Information, Fig. S6A–F ) .

Matos, 2009; Reis & Fontoura, 2009), with an elevational gradient ranging from sea level to more than 1000 m a.s.l., with an annual average of temperature between 23.3 and 23.6 °C and rainfall between 1300 and 1600 mm ( Silveira et al., 2005; Amorim & Matos, 2009; Nacif et al., 2009; Reis & Fontoura, 2009). These areas have different levels of successional forests according to elevational gradients. Areas between 400 and 800 m, presenting a high and dense forest, with large height trees (taller than 30 m), a well-defined canopy structure, with abundant Diagnosis: This species is distinguished from all other South American congeneric species by the unique combination of the following of characters: (1) nasal suture incomplete; (2) rostral scale oval; (3) supralabial scales four; (4) infralabial scales three; (5) rows scales around the body 20/20/18–20; (6) mid-dorsal scales 208– 217; (7) ventral scales 195–211; (8) rows of dorsal scales pale brown 12–13; (9) rows of ventral scales yellowish cream and immaculate four to five; (10) caudal spine pale brown; (11) subcaudal scales ten to 12; (12) maximum TTL 170 mm; (13) maximum TL 6.13 mm; (14) nasal process of premaxilla contacting the vertical laminae of the nasals in the anterodorsal and posteroventral portions, with the central portion not in contact, leaving a large round canal between the olfactory chambers; (15) large palatine fossa on the lateral side of the maxilla; (16) maxilla with a concave medial border; (17) ventral pterygoid process of palatine straight; (18) ratio between length of ventral pterygoid process of palatine and skull length 0.06; (19) angle between mandibular condyle articulation and the retroarticular process of the compound bone close to 90°; (20) Dorsal surface of dentary bone with two evident foramina; and (21) hemipenis single, with an additional structure in the apical cup, with a tissue projection in the form of a curved papilla.

Amerotyphlops martis differs from A. costaricensis , A. lehneri , A. microstomus , A. stadelmani , A. tasymicris , A. tenuis , A. trinitatus and A. tycherus by having an incomplete nasal suture (vs. complete nasal suture); from A. arenensis , A. caetanoi , A. amoipira , A. minuisquamus , A. paucisquamus and A. yonenagae by having 20/20/18 or 20/20/20 rows scales around the body (vs. 18/16/14, 18/18/14, 20/18/14 or 20/18/ 15 in A. minuisquamus and 18/18/ 18 in A. arenensis , A. caetanoi , A. amoipira , A. paucisquamus and A. yonenagae ); from A. reticulatus by having pigmented cephalic scales with a pale brown dorsum and tail (vs. a yellowish and few pigmented cephalic scales, dorsum brown or black and dorsum tail black with cream or yellow spot); from A. montanus by having a smaller total length (TTL), between 130 and 170 mm (vs. larger total length 216 mm); and from A. brongermianus by having a small midbody diameter (MBD), between 4.090 and 5.133 mm and a single hemipenis with an additional structure in the apical cup, a large papillae projected laterally from the tip that extends horizontally over the proximal portion of the apical cup (vs. robust midbody diameter, between 5.03 and 14.76 mm and a single hemipenis with an unornamented apical cup). Table 1 shows additional morphometric characters and scale patterns found in A. martis and morphologically similar species distributed in southern and north-eastern Brazil. Description of the holotype: Adult male, TTL 157 mm, TL 6.13 mm, MBD/(SVL-HR) 0.032 mm and TL/SVL 24.61 mm. Head slightly depressed dorsoventrally, not wider than ‘neck’. Snout round in dorsal and ventral views. Rostral oval, longer than wide, narrow at anteroposterior region and wider at medial region; visible in dorsal view, extending ventrodorsally without reaching the imaginary transverse line between anterior borders of eyes. Rostral contacting nasal (anterior and posterior) dorsolaterally and first supralabial and anterior nasal scales ventrally. Nasal suture incomplete, only partially dividing the anterior and posterior portions of nasal scale. Suture begins in the upper edge of second supralabial, passes through nostril, but fails to reach rostral. Anterior nasal in contact with first infralabial and upper edge of second infralabial. Posterior nasal longer than wide, contacting upper margin of second supralabial and preocular. Supralabials four, fourth twice longer than third. Infralabials three, third largest. Eye diameter 0.90 mm; eyes not visible in ventral view, located dorsolaterally, close to suture between preocular and ocular scales, completely covered by ocular scale. Ocular scales contacting frontal. Body cylindrical and robust. Midbody diameter 4.86 mm. Dorsal and ventral scales cycloid, wider than long, highly imbricated and arranged in diagonal series; scale rows around the body 20/20/18. Mid-dorsal scales 215. Ventral scales 211. Cloacal plate rounded, bordered anteriorly by three rows of scales and posteriorly by five rows of scales. Subcaudal scales 11, excluding the terminal spine.

Skull osteology (N = 1; MNRJ 18743): The length of the skull is 6.52 mm, the width is 2.96 mm. The snout region has a globular enlarged-shape and highly consolidated. The snout articulates with the braincase by the nasal and prefrontal sutures and with the frontal bone. The anteroventral region of the premaxilla has a short backward process. The midsagittal lamina separates both sides of the premaxilla ( Fig. 5 ). The lamina of the premaxilla is confluent with the mid-dorsal laminae of the nasals and with the mid-dorsal ridges of the vomeronasal cupola of the septomaxillae ( Fig. 5 ). The nasal process of premaxilla contacts the vertical laminae of the nasals in the anterodorsal and posteroventral portions, with the central portion not in contact, leaving a large round canal between the olfactory chambers ( Fig. 5A ). The medial side of the maxilla has a shallow depression (or fossa), where lodges the maxillary process of the palatine. The palatine fossa is on the lateral side of the maxilla, in the region of the articular fossa. The palatine fossa is large ( Fig. 6A ), with a diameter of 0.27 mm. The medial border of the maxilla is concaveshaped ( Fig. 6C ). The ventral pterygoid process of the palatine is straight-shaped and ventrally directed ( Fig. 7A ). The retroarticular process projects in parallel to the horizontal plane of the articular. The angle between mandibular condyle articulation and the retroarticular process of the compound bone is close to 90° ( Fig. 8A ). The edentulous dentary is restricted to the distal end of the mandible, articulating mainly with the splenial. The dorsal side of the dentary is flat and pierced by two foramina ( Fig. 9A ).

H e m i p e n i a l m o r p h o l o g y (N = 4; o r g a n s f u l l y eƲerted and inflated): Hemipenis single, with a long cylindrical body and conical in the distal region (apical cup) ( Fig. 13A–D ); a tissue sheet extends from the lateral surface of the apical cup, it folds and runs transversely forming a curved papilla ( Fig. 13A ); the region between this flounce and the lateral sheet is deeper, forming a pocket on the sulcate side ( Fig. 13A ); internal surfaces of the flounce and the conical termination covered with smooth and shallow striations ( Fig. 13A, B ); sulcus spermaticus single, protruding over the surface of the hemipenial body, originating on the medial surface of the basal region of the hemipenis and running distally sinuously, reaching the flounce and draining to the pocket of the sulcate side ( Fig. 13C ); proximal region of the asulcate side of the hemipenial body with a transversal groove ( Fig. 13D ); medial region of the sulcate and asulcate sides (including the sulcus walls) covered with smooth and shallow striations ( Fig. 13C, D ).

Coloration of the holotype in preserƲatiƲe: Dorsum (13/11/13 rows scales) pale brown. In the dorsal part of the body up to the tail, a fine darker brown reticulum, particularly concentrated in the central part of dorsal scales (Supporting Information, Fig. S5A ). Venter (7/9/5 rows scales) pale cream (Supporting Information, Fig. S5B ). Dorsal portions of snout pale cream, with a few light brown spots, covering partially both rostral and nasal scales ( Fig. 12A, B ). The ventral portion of snout pale cream and immaculate ( Fig. 12C ). Symphysial region pale cream and immaculate ( Fig. 12C ). Dorsal head scales (supraoculars, frontal, postfrontal, parietals and occipitals) and dorsal portions of lateral head scales (ocular, nasal and lower nasal) predominantly pale cream with few pale brown spots ( Fig. 12A, B ) and ventral portions pale cream ( Fig. 12C ). Cloacal plate pale cream and terminal spine creamy pale brown (Supporting Information, Fig. S5B ).

Variation of paratypes: Number of subcaudal scales ten to 12 (mean = 11, SD = 1, N = 3). Tail length 2.95– 3.20% of TTL (N = 3). Largest male with 170 mm TTL. MBD 4.09–5.13 mm (mean = 4.61, SD = 0.52, N = 3); number of mid-dorsal scales 208–217 (mean = 212.3, SD = 4.50, N = 3); number of ventral scales 195–208 (mean = 201.0, SD = 6.55, N = 3); and number of scale rows around the body 20/20/18 (N = 2) or 20/20/20 (N = 1). The colour patterns of the paratypes are similar to that found in the holotype (Supporting Information, Fig. S6A–F ).

Etymology: The specific epithet is derived from the Latin name ‘ Mars ’, in allusion to the Mars symbol, used to represent the male gender. The choice of the name is a reference to the distinct hemipenial morphology of this species that differs from all other species of Amerotyphlops .

Distribution and habitat: Amerotyphlops martis is only known from Praia das Neves, situated at 20 km from the municipality of Presidente Kennedy, state of Espírito Santo, Brazil ( Fig. 10B ). This region is considered as part of the Atlantic Forest morphoclimatic domain, in the Atlantic Coast Restingas ecoregion, a sandy plain located along to the coast of Brazil ( Olson et al., 2001).

The prevalent phytophysiognomy in Praia das Neves is heterogeneous, presenting an herbaceous, shrubs and arboreous forest usually distributed in parallels ridges to the shoreline ( Braz et al., 2013), with an annual average of temperature and rainfall of 20 °C and 1561 mm, respectively ( Peel et al., 2007). Praia das Neves has several different levels of successional vegetation, with areas close to the beach line presenting herbaceous and shrubby vegetation, with stretches of graminoid beach communities, changing the vegetation in the interior, where presenting a fragmented Ridge forest, with medium height trees (between 15 and 20 m), with lianas, epiphytes and herbaceous understory ( Braz et al., 2013).

Figures

Figure 5. Three-dimensional cutaway views along the sagittal axis of the nasal cavity in Amerotyphlops species based on HRXCT data. A, Amerotyphlops brongersmianus (MZUSP 14689); B, Amerotyphlops caetanoi sp. nov. (MZUSP S-023380). Insert show a lateral profile of the skull of A. brongersmianus presenting in red the position of the detailed region. Scales bars equal to 5 mm. Abbreviations: pmx, premaxilla; smx, septomaxilla; vm, vomer; na, nasal.

Figure 6. Three-dimensional reconstruction of the lateral region of the skull in Amerotyphlops species based on HRXCT data. A, Amerotyphlops caetanoi sp. nov. (MZUSP S-023380); B, Amerotyphlops montanum sp. nov. (MZUSP 20065); C, Amerotyphlops brongersmianus (MZUSP 14674). Insert shows a lateral profile of the skull of A. brongersmianus presenting in red the position of the detailed region. Scales bars equal to 5 mm.Abbreviations:mx, maxilla; mxpalf, palatine articulation fossa of the maxilla.

Figure 7. Three-dimensional reconstruction of the lateroventral region of the skull in Amerotyphlops species based on HRXCT data. A, Amerotyphlops caetanoi sp. nov. (MZUSP S-023380); B, Amerotyphlops brongersmianus (MZUSP 14674). Insert shows a lateral profile of the skull of A. brongersmianus presenting in red the position of the detailed region. Scales bars equal to 5 mm. Abbreviations: mx, maxilla; palmx, palatine maxillary process; palptv, palatine pterygoid ventral process; pt, pterygoid.

Figure 8. Three-dimensional reconstruction of the posterior region of the left mandible in Amerotyphlops speciesbased on HRXCTdata.A,Amerotyphlops caetanoisp. nov. (MZUSP S-023380); B, Amerotyphlops brongersmianus (MZUSP 14674). Insert shows a lateral profile of the skull of A. brongersmianus presenting in red the position of the detailed region. Scales bars equal to 5 mm. Abbreviations: cb, compound bone; q, quadrate; rp, retroarticular process.

Figure 9. Three-dimensional reconstruction of the anterior region of the left mandible in Amerotyphlops species based on HRXCT data. A, Amerotyphlops caetanoi sp. nov. (MZUSP S-023380); B, Amerotyphlops montanum sp. nov. (MZUSP 20065). Insert shows a lateral profile of the skull of A. brongersmianus presenting in red the position of the detailed region. Scales bars equal to 5 mm. Abbreviations: cb, compound bone; co, coronoid; d, dentary; sp, splenial.

Figure 10. Geographical distribution of nine species belonging to the genus Amerotyphlops from South America.A, zoomed map of species distributed in the north-eastern Brazil; B, zoomed map of four new species described in this work. Symbols: A. arenensis (black pentagons); A. amoipira (black diamonds); A. brongersmianus (black circles); A. yonenagae (black squares); A. pauciquamus (black inverted triangles); A. martis sp. nov. (black star); A. montanum sp. nov. (black triangles); A. illusorium sp. nov. (black cross); Amerotyphlops caetanoi sp. nov. (black asterisk).

Figure 12. Holotype of Amerotyphlops martis sp. nov. (MNRJ 18744). Head in left lateral (A), dorsal (B) and ventral (C) views. TTL = 157 mm. Scale bar equal to 5 mm.

Figure 13. Hemipenis of Amerotyphlops martis sp. nov. (MNRJ 18744), detail of the apical region on the sulcate (A) and asulcate views (B), sulcate (C) and asulcate sides (D). Scale bar equal to 1 mm.