Crocidura tenebrosa, Esselstyn & Achmadi & Handika & Swanson & Giarla & Rowe, 2021

Esselstyn, Jacob A., Achmadi, Anang S., Handika, Heru, Swanson, Mark T., Giarla, Thomas C. & Rowe, Kevin C., 2021, Fourteen New, Endemic Species Of Shrew (Genus Crocidura) From Sulawesi Reveal A Spectacular Island Radiation, Bulletin of the American Museum of Natural History 2021 (454), pp. 1-109 : 60-62

Crocidura tenebrosa , new species

LSID: urn:lsid:zoobank.org:act:856C039C-7F2E-4E38-8F16-02E4376F8B11

HOLOTYPE: MZB 43006 (= LSUMZ 39272 ), an adult male collected by H. Handika on 21 February 2016. The specimen comprises a study skin, cleaned skull and skeleton, and frozen tissues. External measurements from the holotype are 100 mm × 37 mm × 11 mm × 8 mm = 6.28 g. The voucher specimen and a tissue sample will be permanently curated at MZB, with additional tissues retained by LSUMZ. TYPE LOCALITY: Indonesia, Sulawesi Utara, Bolaang Mondgondow, Passi Timur, Insil , Mt. Ambang , near Lake Aliyah; 0.76385° N, 124.41188° E, 1481 m elevation.

ETYMOLOGY: Tenebrosa is Latin for “dark,” describing the overall color of this animal.

GEOGRAPHIC DISTRIBUTION: Recorded only on Mt. Ambang in the north-east area of endemism (North Sulawesi Province) between 1400 and 1500 m elevation ( fig. 25 ; table 3 ). Future surveys of other mountains in the north-central area of endemism and at the eastern extreme of the north-east area of endemism may extend the known range of this species.

DIAGNOSIS: Crocidura tenebrosa is a very small ( fig. 9 ; tables 2 , 8 ), very dark shrew. The pelage and all areas of exposed skin (feet, tail, pinna, lips, and nose) are uniformly dark brown ( fig. 27C ). The overall dark pelage of this animal appears to be primarily from a darker proximal base of individual hairs. The mystacial vibrissae are black for most of their length, but unpigmented at the tips. The soles of the feet are mostly dark brown, but the areas that tend to accumulate pigment (base of the foot pads) are black ( fig. 27C ). The claws are translucent. The tail is short, with a notable density of applied hairs and a comparative abundance of bristles extending for three-fourths of the tail length. The skull is short, particularly the postpalatal portion, relative to its width ( figs. 10 , 28C ) and to overall body size. Posteriorly, the skull is rounded, with a smoothly inflated and broad braincase ( fig. 28C ). The lambdoidal ridge is thin, but relatively high for such a delicate skull. The interorbital region is smoothly tapered, and the maxillary process is relatively inconspicuous, a consequence of the broad interorbital region. The palate is narrow, with a somewhat prominent dentition. The C (U3) and I3 (U2) are sub- equal in occlusal surface area. The parastyle of P4 is prominent.

COMPARISONS: Crocidura tenebrosa is smaller than all Sulawesi shrews except the other members of the Small-Bodied Group, which are all comparable in body size. Among these, only C. lea and C. baletei are found on the northern peninsula, near the range of C. tenebrosa . Crocidura tenebrosa is readily distinguished from C. lea by its more dark and uniform color, shorter tail ( fig. 9 ), and wider skull ( figs. 10 , 26 ). Crocidura tenebrosa is distinguished from its sister species, C. baletei , by its shorter tail ( fig. 30 ; table 2 ), darker integument, shorter relative hind-foot length ( fig. 17 ), and slightly narrower braincase, but wider interorbital region and rostrum ( fig. 30 ; table 8 ). The ratio of the braincase breadth to interorbital width is slightly lower for C. tenebrosa than C. baletei ( fig. 10 ). For additional details, see comparisons sections of C. lea and C. baletei , above.

COMMENTS: We tested species limits with BPP between Crocidura baletei and C. tenebrosa , among these two species and C. lea , and among these three species and C. levicula . The alignments we analyzed contain: 6 and 13; 6, 13, and 12; and 6, 13, 12, and 34 individuals per species, respectively. Alignments are 91%, 87%, and 93% complete. All analyses supported all species with a posterior probability of 1.

Crocidura baletei and C. tenebrosa are probable sister species ( figs. 7 , 8 ) and phenotypically similar. We define them as distinct species because they have modest differences in color and skull shape, they are divergent in their mitochondrial DNA (mean 0.076 Jukes-Cantor distance; supplementary data S4), they are reciprocally monophyletic in our UCE, mitochondrial, and nuclear exon trees ( figs. 4 , 5 , 7 , 8 ; supplementary data S6), and finally since both species have been recorded only above 1000 m elevation ( fig. 13 ), they are likely isolated from each other by the low, dry habitat of the Gorontalo Divide. These two small-bodied highland endemics may be replaced across the northern peninsula lowlands by the similarly sized but paler colored and distantly related C. lea .

SPECIMENS EXAMINED: Mt. Ambang ( LSUMZ 39019–39023 , 39025 , 39267–39271 , 39273 , 39274 ; MZB 43006 ) .

Figures

FIG. 25. Map of Sulawesi showing localities sampled for shrews. Colored areas enclose localities with known records of members of the Small-Bodied Group of Sulawesi Crocidura.

FIG. 9. Box plots showing variation in external measurements from all species of Sulawesi shrew. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. Species are grouped according to the species groups used in the text (Thick = Thick- Tailed Group). All measurements in mm. HBL = head-and-body length.

FIG. 27. Images showing the ventral surface of the hind foot and dorsal surfaces of the tail base (approximately 1 cm from rump) and tail tip from the three members of the Small-Bodied Group that are from the northern peninsula: A, Crocidura baletei, LSUMZ 36959 (right hind foot); B, C. lea, LSUMZ 38254 (left hind foot); and C, C. tenebrosa, LSUMZ 39268 (right hind foot). Scale bars represent 5 mm. Within each panel, the upper bar applies to the foot and the lower bar corresponds to both tail images.

FIG. 10. Box plots of relative skull measures showing braincase breadth (BB), interorbital width (IOW), and rostral length (RL) divided by condyloincisive length (CIL) and BB divided by IOW for all species of Sulawesi shrew. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. Species are ordered according to the species groups used in the text (Thick = Thick-Tailed Group).

FIG. 28. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary from the three members of the Small-Bodied Group that are from the northern peninsula:A, Crocidura baletei, LSUMZ 36959; B, C. lea, LSUMZ 38262; and C, C. tenebrosa, LSUMZ 39272.

FIG. 26. Bivariate plots showing A, variation in the condyloincisive length and braincase breadth and B, the first two axes from a principal components analysis of 12 cranial measurements among all members of the Small-Bodied Group. Loadings and variance explained are given in table 9.

FIG. 30. Box plots showing variation in skull width and tail length from species of the Small-Bodied Group on the northern peninsula of Sulawesi. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. All measurements in mm.

FIG. 17. Box plots showing the length of the hind foot (HF) relative to the head-and-body length (HBL) and the ratio of mass to HBL. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. Species are ordered along the x-axis according to the species groups used in the text (Thick = Thick-Tailed Group). Lengths are in mm and mass is in grams.

FIG. 7. Estimated species tree from analysis of 3940 ultraconserved element loci in ASTRAL. Samples from Sulawesi are labeled with the species name, locality, and catalog number. Asterisks indicate type specimens from Miller and Hollister (1921). Local posterior probabilities <0.95 are shown. Tip branch lengths are arbitrary.

FIG. 8. Estimated phylogenetic relationships from a maximum likelihood analysis of 983 concatenated ultraconserved elements. Samples from Sulawesi are labeled with the species name, locality, and catalog number. Asterisks indicate type specimens from Miller and Hollister (1921). Ultrafast bootstrap values <95 are shown.

FIG. 4. Maximum-likelihood estimate of the gene tree of Sulawesi Crocidura derived from an alignment of 851 individuals and 1111 characters from the mitochondrial gene cytochrome b. Bootstrap support is shown along branches. Clades corresponding to species are collapsed for ease of presentation. Tips are labeled with the species name, the number of tips (T), and number of localities (L), as labeled in figure 1, and the maximum intraspecific (MI) Jukes-Cantor distance calculated from a reduced alignment. Two species are paraphyletic and their respective, within-clade MI values are shown separately. For species described by Miller and Hollister (1921), the holotype or paratypes are included for C. elongata, C. lea, and C. rhoditis. Branch lengths between C. nigripes and other taxa are shortened for presentation. See supplementary data S2 for the full tree.

FIG. 5. Maximum likelihood estimate of the mitochondrial gene tree derived from an analysis of 14,007 characters (representing protein-coding and rRNA genes) from 83 samples. Bootstrap support values <95 are shown at nodes. Tips are labeled with the species, locality, and voucher number.

FIG. 13. Elevational records of all species of Crocidura known from Sulawesi. Each point represents a specimen. For specimens associated with a minimum and maximum elevation, we used the center of the given elevational range. Sample sizes are given above the x-axis. Species are grouped according to the species groups used in the text (Thick = Thick-Tailed Group).