Ctenomys pulcer, Verzi & De Santi & Olivares & Morgan & Basso & Brook, 2023

Verzi, Diego H., De Santi, Nahuel A., Olivares, A. Itati, Morgan, Cecilia C., Basso, Nestor G. & Brook, Federico, 2023, A new species of the highly polytypic South American rodent Ctenomys increases the diversity of the magellanicus clade, Vertebrate Zoology 73, pp. 289-312 : 289

Ctenomys pulcer sp. nov.

Ctenomys talarum - Massoia (1988: 6)

Ctenomys cf. Ctenomys talarum - Pardiñas (2001: 236, fig. 2c)

Ctenomys talarum - Massarini et al. (1995: 208, 211-212, fig. 4)

Ctenomys talarum - Mora et al. (2007: 3457, fig 2a)

Ctenomys sp. “monte” - Morgan and Verzi (2006: 1260)

Ctenomys “monte” - Morgan and Verzi (2011: 4)

Ctenomys sp. “monte” - Morgan et al. (2017: 121, fig. 2)

Ctenomys sp. - De Santi et al. (2018: 71)

Ctenomys sp. C - De Santi et al. (2021: 8, 10, figs 4, 5)

Ctenomys sp. C - Verzi et al. (2021: 5, fig. 1.1)

Holotype.

MLP-Mz 8.X.02.17 male, collected by D. Verzi and E. Etcheverry leg. on 5 July 1999, and prepared as study skin and skeleton.

Type locality.

Argentina, Buenos Aires Province, Monte Hermoso County, Estancia Delta (38°56 ’47” S; 61°15 ’22” W; Fig. 2 ).

Paratypes.

14 specimens from Estancia Delta, Monte Hermoso County, Buenos Aires Province, Argentina (MLP-Mz 27.XII.01.56 male, MLP-Mz 27.XII.01.57 male, MLP-Mz 27.XII.01.58 male, MLP-Mz 13.VI.02.1 male, MLP-Mz 13.VI.02.2 female, MLP-Mz 9.XII.02.1 female, MLP-Mz 9.XII.02.2 female, MLP-Mz 27.XII.01.48 female, MLP-Mz 27.XII.01.49 male, MLP-Mz 27.XII.01.54 female, MLP-Mz 27.XII.01.55 female, MLP-Mz 30.XII.02.17 male, MLP-Mz 2536 male, MLP-Mz 2537 female); three specimens from Sauce Grande lagoon, Monte Hermoso County, Buenos Aires Province, Argentina (38°56 ’51” S; 61°20 ’51” W; MLP-Mz 3.XII.02.14 male, MLP-Mz 2538 male, MLP-Mz 3027 male). See Table S1.

Other referred specimens.

MLP-Mz 3.V.48.4, MLP-Mz 24.IX.69.1, MLP-Mz 18.XI.98.1, MLP-Mz 18.XI.98.2, MLP-Mz 27.XII.01.47, MLP-Mz 27.XII.01.50, MLP-Mz 3028, MLP-Mz 3029, MLP-Mz 3030; MMP-Ma 1776, MMP-Ma 1796, MMP-Ma 1804, MMP-Ma 1806, MMP-Ma 2584; MMH 3.85, MMH 84.2.2, MMH 86.3, MMH 86.3.2, MMH 86.3.3, MMH 86.3.4, MMH 88.2.4, MMH 88.2.5, MMH 89.2.5, MMH 89.2.7, MMH 89.12.2, MMH 89.12.4, MMH 89.12.5, MMH 89.12.7, MMH 89.12.8, MMH 90.1.5, MMH 90.1.10, MMH 90.2.1, MMH 90.2.13, MMH 90.2.14, MMH 91.9.5, MMH 91.9.8, MMH 91.9.10, MMH 92.11.8, MMH 92.11.11, MMH 92.11.18, MMH 92.11.19, MMH 93.11.4, MMH 93.11.5, MMH 94.12.2, MMH 94.12.3, MMH 94.12.5, MMH 94.12.6, MMH 95.11.2, MMH 95.11.4, MMH 95.11.5, MMH 95.11.8, MMH 96.12.5, MMH 96.12.8, MMH 96.12.10, MMH 96.12.11, MMH 97.9.2, MMH 97.9.3, MMH 97.9.6, MMH 97.11.4, MMH 97.11.8, MMH 98.10.2, MMH 98.10.3, MMH 98.10.4, MMH 98.10.5, MMH 98.10.8, MMH 98.12.1, MMH 98.12.2, MMH 98.12.4, MMH 99.10.4, MMH 99.10.6, MMH 99.10.7, MMH 99.10.10, MMH 99.10.11, MMH MH1, MMH MH3, MMH MH5, MMH MH6. See Table S1.

Diagnosis.

A medium-sized species of Ctenomys . Coloration ochraceous with some orange on the dorsum, with a dark patch on the dorsal snout and head, and irregular dark zones along the middle of the back; paler toward the flanks, and buff yellowish ochre on the belly. Cranial rostrum with wide base due to divergent insertion of upper incisors. Incisive foramina short, and premaxillary septum wide. Medial margins of the premaxillaries flattened against the roots of the premaxillary septum. Facial portion of the lacrimal strongly reduced and not protruding; orbital portion of lacrimal interrupted by frontal. Alveolar sheath of M1 protruding into the lacrimal foramen, its anterodorsal portion covered by the maxillary plate posterior to the nasolacrimal canal. Edges of frontals posterior to the orbital constriction subparallel. Ventral spine of the styliform process of the auditory bulla long, especially in the living population. Tube of external auditory meatus long, especially its posterior wall. Bottom of alveolus of dp4 and m1 markedly protruding into the ventral portion of mandibular corpus. Masseteric crest subhorizontal.

Description and comparison.

Ctenomys pulcer sp. nov. is a medium-sized Ctenomys (measurements in Table 1 ), slightly larger in size than its sister species Ctenomys bidaui (see below, Parsimony and Bayesian analyses). Pelage is dense, fine and silky. The dorsal coloration is ochraceous with some orange in most specimens (Fig. 3 ), with individual hairs buff yellowish to ochre at their bases and with dark brown to blackish tips. A more extended blackish section in individual hairs defines a dark patch on the dorsal snout and head, and irregular dark zones along the middle of the back. The coloration is paler toward the flanks, and buff yellowish ochre on the belly where individual hairs lack the dark tips. The coloration of the tail is pale ochre with a brownish dorsal section of variable development. Forelimb hairs and ungual bristles are whitish.

The cranium is similar in general shape to that of the sister species C. bidaui , but with a wider rostrum, smaller orbit, and anteriorly narrower auditory bullae (Figs 4 and 5 ). In the parapatric, similar-sized C. talarum , the rostrum is more expanded anteriorly, the zygomatic arches are more bowed, and the auditory bullae are less inflated (Fig. 4 ). The rostrum of C. pulcer has a wider base than that of C. bidaui because the incisor roots are more divergent. The interpremaxillary foramen is variable, well developed in some specimens and markedly reduced or absent in others (it is absent in the holotype MLP-Mz 8.X.02.17; Fig. 4A ). In C. bidaui and C. talarum this foramen is always present and well developed. The premaxillary septum is wide, and the incisive foramina are slightly shorter and wider than those of C. bidaui , and shorter than those of C. talarum . The premaxillary anterior margins of the incisive foramina are dorso-medially convergent and flattened against the premaxillary septum. The palatal bridge, between the molar series, is wider than in C. bidaui . The major palatine foramina open on the maxillary at the level of M1, as in C. bidaui . The mesopterygoid fossa reaches the level of M2. The zygomatic arches are less bowed than those of C. bidaui . The postglenoid articular region (sensu Verzi and Olivares 2006), between the posterior border of the glenoid fossa and the external auditory meatus, is wider than that of C. bidaui , similar to that of C. talarum (Fig. 4 ). The auditory bullae are more inflated than those of C. talarum ; they have their anterolateral portion less inflated than in C. bidaui . At the anterior end of the bulla, the ectotympanic forms an apophysis where the pterygoid process contacts the bulla (Fig. 6 ). This structure is ventral to the styliform process and here we refer to it as the ventral spine of the styliform process. This ventral spine attains strong development in living C. pulcer , extending markedly forward which is unique among the analyzed Ctenomys (Fig. 6 ). In the fossil † C. pulcer and especially in C. bidaui this apophysis is shorter. The external auditory meatus forms a more protruding tube than that of C. bidaui ; especially the posterior wall of this tube is clearly longer than in C. bidaui (Figs 4 and 7 ). In lateral view, the cranial roof is slightly vaulted (Fig. 5 ), with the nasal bone more noticeably arched in some specimens as MLP 9.XII.02.1 and MLP 9.XI.02.2. The zygomatic arch is dorsoventrally low due to the poor development of the paraorbital process and the ventral jugal process (Fig. 5 ); this is a characteristic shared mainly with species of the Ctenomys mendocinus and Ctenomys magellanicus species groups. The antorbital bar is slightly more oblique, antero-dorsally, than that of C. bidaui , in which it is more vertical. The facial portion of the lacrimal bone is very small (Fig. 8 ), similar to that of C. australis . The orbital portion of this bone is restricted to the dorsal portion of the nasolacrimal canal by the interposition of the frontal bone (Fig. 9 ). Similar to C. bidaui , the first part of the nasolacrimal canal is short because the foramen into the nasolacrimal canal is close to the facial portion of the lacrimal bone (Fig. 9 ). Comprehensive information on lacrimal variability in Ctenomys is not available, but at least in the sample analyzed, the morphology of this bone did not show relevant intraspecific variation. As indicated by the zygomatic index, the orbit of C. pulcer is smaller than that of C. bidaui (Fig. 5 ; ZI in Table 1 ). In the medial wall of the orbit, the maxillary plate delimiting the sphenopalatine fissure covers the anterodorsal portion of the M1 alveolar sheath, as is also the case in species of the Ctenomys mendocinus species group and C. talarum (Fig. 9 ). This M1 alveolar sheath is high in relation to the level of the facial portion of lacrimal bone. In C. bidaui , the anterodorsal portion of the alveolar sheath of M1 is exposed (Fig. 9 ). Similar to C. bidaui , the buccinator and masticatory foramina on the alisphenoid are mostly separated; however, this configuration is variable and in some specimens these foramina are merged into a single foramen. Both the palatine and pterygoid contact the auditory bulla, as in the other species of the Ctenomys magellanicus group and the species of the Ctenomys mendocinus group. The mastoid apophysis is short; its tip does not exceed the ventral margin of the external auditory meatus. Dorsally, the frontal margins of the orbits are subparallel, whereas these are more divergent in C. bidaui (Fig. 4 ). The temporal fossae are shallow as those of C. bidaui . A persistent interfrontal fontanelle is present in the holotype. There is an interparietal in adults discernible as a very short and wide ossification, similar to that of C. bidaui . The petrosal epitympanic recesses are small as in C. bidaui and wider than those of C. talarum . The lambdoid crest is slightly more developed than that of C. bidaui .

As in the other species of the crown group of Ctenomys , C. pulcer has a markedly hystricognathous mandible. In dorsal view, the masseteric crest is more expanded with respect to the mandibular corpus than in C. bidaui . The origin of the masseteric crest is posteroventral to the mandibular notch (for the insertion of the tendon of the infraorbital part of the medial masseter muscle). In lateral view, this origin of the masseteric crest is more separated from the mandibular notch than in C. bidaui . The masseteric crest is subhorizontal in C. pulcer ; in C. bidaui this crest is more ascending and oriented in the same direction as the ventral margin of the mandibular body (Fig. 5 ). Anterolaterally to the origin of the crest, the bottoms of the alveolar sheath of dp4 and m1 form two protuberances on the lower margin of the mandibular corpus in C. pulcer , which are more protruding than those of C. bidaui (Fig. 5 ). The tip of the coronoid process reaches the level of the condylar process or is below it. The chin process is well developed and located at the level of the m1.

The upper incisors have divergent insertion. They are orthodont to slightly proodont as in C. bidaui (see Proc in Table 1 ). The lower incisors are not inserted deeply; the bottom of their alveolar sheath and associated mandibular foramen are located further away from the condyle than in more specialized tooth-digger species such as C. leucodon , C. lewisi , or C. steinbachi ( Verzi and Olivares 2006; Morgan et al. 2017). The DP4-M3/dp4-m3 crowns lack cement.

Sperm morphology.

Simple asymmetric (Fig. S1).

Karyotype.

Massarini et al. (1995) described the karyotype and C-banding pattern of C. talarum recessus from Monte Hermoso. Revision of the vouchers, MMP-Ma 1776, MMP-Ma 1796, MMP-Ma 1804, MMP-Ma 1806, and MMP-Ma 2584 suggests that the 2N = 48 karyotype described by Massarini et al. (1995) corresponds to C. pulcer sp. nov.

Etymology.

From Latin Ctenomys pulcer , in Spanish hermoso (beautiful) in reference to the type locality Monte Hermoso.

Distribution and habitat.

Up to the present, C. pulcer sp. nov. has been found in Monte Hermoso County, in the southeastern Atlantic coast of Buenos Aires Province, in central Argentina. This area corresponds to the southernmost portion of the Pampean phytogeographic province and to the Austral Pampean district ( Cabrera 1971, 1994). The predominant vegetation are grasslands that develop in a subhumid-dry climate, with a mean annual temperature of 15.4°C and mean annual precipitation of 684.9 mm ( Cabrera 1971; Monserrat et al. 2012). In this area, C. pulcer is distributed in parapatry with C. australis and C. talarum (Fig. 2 ). Notably, the distribution pattern of the three species matches the three physiographic units recognized by Monserrat et al. (2012) on the basis of geomorphological characteristics and vegetation units; i.e., from shore to inland, C. australis occupies frontal active dunes, C. pulcer inhabits fixed/semifixed dunes, and C. talarum lives in more compact and humid soils at the edges of cultivated lands. This distribution was checked by conducting a 20 km shore-perpendicular transect (carried out by DHV and Eduardo Etcheverry, at midday in July 1999). C. talarum could be recognized by its vocalizations which are similar to those recorded in populations at the northern end of its distribution (DHV, pers. observ.); three specimens of this species were collected (MLP 2547, MLP 3.XII.02.15, MLP 3028). It is noteworthy that those populations of C. talarum distributed in southern coastal localities where C. pulcer is not present, occupy the fixed/semifixed dunes ( Contreras and Reig 1965; Cutrera et al. 2006). This suggests that the segregation found in Monte Hermoso precludes competition of C. talarum with the larger-sized C. pulcer (see Vassallo 1993).

Natural history.

At the two capture sites in Monte Hermoso area, Estancia Delta (38°56 ’47” S; 61°15 ’22” W) and the vicinity of Sauce Grande lagoon (38°56 ’51” S; 61°20 ’51” W) (Fig. 2 ), the population of C. pulcer sp. nov. was dense. In a sampling conducted on 5 July 1999 between 9.30 a.m. and 1 p.m. at the first station, seven animals were captured on a fixed dune extension of around 20 x 150 m. The dominant plant species in the fixed/semifixed dunes system inhabited by C. pulcer were Poa lanuginosa , Panicum urvilleanum , Hyalis argentea , Sporolobus rigens , and Cortaderia selloana ( Celsi and Monserrat 2008a, 2008b; Monserrat 2010; Monserrat et al. 2012). Unlike C. talarum , the largest-sized individuals of C. pulcer were aggressive when removed from their burrows. Vocalizations were heard in the Sauce Grande lagoon station between 9.30 a.m. and 11 a.m.; these vocalizations are lower-pitched than those of C. talarum , and are composed of a series of tong-tong repeated without change of their frequency. A gravid female was recorded on 7 September 1998.

Fossil record.

A rich fossil record of Ctenomys has been recovered from the current distribution area of C. pulcer sp. nov. (Figs 2 , 10 ). The remains of Ctenomys were recovered during 1984 and 1985 by the late Vicente J. Di Martino at the site Monte Hermoso I (Figs 2 , 10 ; Zavala et al. 1992; Politis and Bayón 1995; Bayón and Politis 1996). This site outcrops on the marine platform near the town of Monte Hermoso (37°57 ’47” S; 61°22 ’48” W). It consists of silty-sand deposits affected by marine abrasion ( Zavala et al. 1992). Two units are recognized, a lower unit informally called "wackes inferiores" (lower wackes) and an upper unit informally called "pelitas grises" (gray pelites; Zavala et al. 1992). More recently, these sediments have been interpreted as part of the Agua Blanca Sequence ( Zavala and Quattrocchio 2001; Zavala 2006). The "wackes inferiores" consist of massive grayish-green and dark olive wackes (see Zavala et al. 1992 for a more detailed description). Different datings have alternatively assigned this unit to the late Pleistocene (14,370 ± 60 BP; Bayón and Politis 1996) and to the early Holocene (8,990 ± 55 BP; based on collagen dating of a Ctenomys mandible; Pardiñas 2001). The upper unit of "pelitas grises" includes several overlying levels with human footprints dating from 7,920 to 6,600 BP ( Bayón et al. 2011).

The fossil sample of † C. pulcer comprises 63 specimens from the "wackes inferiores." This bearing deposit has yielded a rich vertebrate fauna ( Massoia 1988; Pardiñas 2001) including the currently parapatric C. australis and C. talarum (Fig. 10 ; Table S1). The fossil sample of † C. pulcer includes at least two well-preserved crania (MMH 97.11.8 and MMH MH6; Fig. 4C and Fig. 10B, C ) and numerous rostral, palatal, and mandibular remains (Table S1). The cranial and mandibular morphology is in accord with that described for the living population. As an exception, the auditory bullae of fossil specimens present a slightly shorter ventral spine of the styliform process.

Specimens of † C. pulcer from the Monte Hermoso I site were assigned to C. talarum by Massoia (1988) and to Ctenomys cf. talarum by Pardiñas (2001). They were interpreted as an independent lineage belonging to the Ctenomys mendocinus species group by De Santi et al. (2018, 2021), Verzi et al. (2021), and De Santi (2022).

Figures

Figure 2. Geographical distribution of Ctenomys pulcer. A Geographical distribution of the Ctenomys magellanicus, Ctenomys mendocinus and Ctenomys talarum species groups (Bidau 2015; Tammone et al. 2022; Lacey et al. 2022); B distribution of Ctenomys pulcer sp. nov., Ctenomys talarum group and C. australis in central-eastern Argentina (Bidau 2015; Carnovale et al. 2021; this work); C detail of southwestern coastal area of the Buenos Aires province displaying habitats and collecting sites of C. pulcer sp. nov. (blue dots), C. talarum (light orange dots), and C. australis (green dots) and the location of Monte Hermoso 1 site (black rectangle) [map data 2022 (C) Google]; the asterisk denotes Estancia Delta, the type locality of Ctenomys pulcer sp. nov.; white arrow in photographs denotes mounds. Photographs from July 1999.

Figure 3. Skins in dorsal and ventral view of Ctenomys pulcer sp. nov. A MLP-Mz 8. X. 02.17 (holotype, male); B MLP-Mz 3027 (paratype, male); Ctenomys bidaui (C) CFA-MA 11867 (holotype, male). Scale bar 20 mm.

Figure 4. General morphology of the cranium (dorsal and ventral view) and mandible (dorsal view) of Ctenomys pulcer sp. nov. A MLP-Mz 8. X. 02.17 (holotype, male); B MLP-Mz 3027 (paratype, male); C MMH 6; D MMH 3 (C and D fossil specimens); Ctenomys bidaui (E) CFA-MA 11867 (holotype, male); Ctenomys talarum (F) MMP-Ma 4035 (male). Scale bar 10 mm.

Figure 5. General morphology of the cranium and mandible in lateral view of Ctenomys pulcer sp. nov. A MLP-Mz 8. X. 02.17 (holotype, male); B MLP-Mz 3027 (paratype, male); C MMH 6; D MMH 89.2.7 (C and D fossil specimens; D reversed); E Ctenomys bidaui, CFA-MA 11867 (holotype, male); F Ctenomys talarum, MMP-Ma 4035 (male). Scale bar 10 mm.

Figure 6. Anterior portion of auditory bulla in ventral view of Ctenomys pulcer sp. nov. A MLP-Mz 8. X. 02.17 (holotype); B MMH 7 - 11 - 8 (fossil specimen); C Ctenomys bidaui, CFA-MA 11857. Abbreviations: b, auditory bulla (ectotympanic portion); st, styliform process; sp, ventral spine of the styliform process; pt, pterygoid. Scale bar 1 mm.

Figure 7. External auditory meatus (eam) in Ctenomys pulcer sp. nov. A MLP-Mz 3027; B Ctenomys bidaui, CFA-MA 11867 (holotype). Scale bar 1 mm.

Figure 8. Facial portion of lacrimal in Ctenomys pulcer sp. nov. A MLP-Mz 8. X. 02.17 (holotype); B MMH 7 - 11 - 8 (fossil specimen); C Ctenomys bidaui, CFA-MA 11857. Abbreviation: fl facial portion of lacrimal. Scale bar 1 mm.

Figure 9. Orbital region in Ctenomys pulcer sp. nov. A MLP-Mz 27. XII. 01.58; B MMH 6 (fossil specimen); Ctenomys bidaui (C) CFA-MA 11867 (holotype); D MLP 28. V. 01.10. Black arrow indicates the maxillary plate. Abbreviations: f, frontal; m, maxilla; M 1 a, alveolar sheath of M 1; nl, foramen into nasolacrimal canal; ol, orbital portion of lacrimal; sf, sphenopalatine fissure. Scale bar 1 mm.

Figure 10. A Stratigraphical profile of the Monte Hermoso I archaeological site (modified from Zavala et. al 1992). B - E specimens recovered from this site; † C. pulcer sp. nov.: B MMH 94 - 11 - 8, C MH 6 (crania in ventral view); D † C. talarum MMH 88.2.6 (cranium in ventral view); E † C. australis MH 2 (right hemimandible in dorsal view). Scale bar 10 mm.