Crocidura levicula Miller and Hollister, 1921

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 : 62-63

Crocidura levicula Miller and Hollister, 1921

Crocidura levicula Miller and Hollister, 1921: 103 . Original description.

N = 7 N = 21 N = 6

HOLOTYPE: USNM 219450 , an adult female collected by H.C. Raven on 13 February 1918. Specimen prepared as a skin and skull. External measurements from the type are 108 mm × 44 mm × 11 mm; ear length and weight were not recorded. TYPE LOCALITY: “Pinedapa, Middle Celebes” ( fig. 25 ). Pinedapa is located near the north coast of Central Sulawesi Province, in Poso Regency, just west of the town of Mapane. Musser (2014) placed the locality at 1.4167° S, 120.5833° E, 31 m elevation.

2.3

WIDTH 2.2 2.1

PALATAL 1.9 2.0

1.8

N = 6 N = 22 N = 6

WIDTH 4.2 INTERORBITAL 3.8 4.0

GEOGRAPHIC DISTRIBUTION: The type locality is near sea level in the northwestern part of Sulawesi’s west-central area of endemism. We found this species to occur in the northern part of the west-central area of endemism ( Mts. Rorekatimbo and Torompupu , Central Sulawesi Province), in two lowland areas near the boundary between the west-central and south-east areas of endemism ( Wasponda and Tolala , Central Sulawesi Province), and in the east-central area of endemism ( Mts. Katopasa and Tompotika , Central Sulawesi Province; fig. 25 ). These records span a broad elevational range, from approximately 400 m on Mt. Tompotika to 2000 m on Mt. Rorekatimbo ( fig. 13 ; table 3 ).

N = 7 N = 21 N = 6

C. baletei C. lea C. tenebrosa

SPECIES

EMENDED DIAGNOSIS: A very small ( tables 2 , 8 ), medium- to dark-brown shrew, with almost uniformly colored pelage, feet, pinna, and tail. The ventral pelage is only slightly paler than the dorsal pelage. The digits are similarly pigmented as the other foot parts. The tail is unusually short ( table 2 ), with an abundance of bristles (some of which are pigmented) extending along the proximal two-thirds of tail length ( fig. 29A ). The hind foot is short, with darkly pigmented pads. The claws are pale, perhaps lightly pigmented, and surrounded by a small tuft of brown hairs ( fig. 29A ). The skull is small but broad, more so at the braincase than at the interorbital region ( figs. 10 , 31A ). Relative to body size and skull breadth, the skull is quite short, particularly the rostrum ( fig. 10 ). The C (U3) is equal to or larger in occlusal area than the I3 (U2).

COMPARISONS: Crocidura levicula is one of the smallest shrew species on Sulawesi, only being comparable to other members of the Small-Bodied Group ( fig. 9 ). It has a shorter relative tail length than any other shrew species on Sulawesi ( fig. 9 ). Its hind-foot length is shorter than in all Sulawesi shrews except one other member of the Small-Bodied Group, C. parva ( fig. 9 ; table 2 ). Crocidura levicula is also darker in color than both C. lea and C. baletei , but not C. tenebrosa . Absolute tail length is slightly less in C. levicula than in C. parva . Tail bristles are more abundant on specimens of C. levicula than in C. lea , C. tenebrosa , and C. parva . The skull of C. levicula is small, delicate, and broad at the braincase and to a lesser degree at the interorbital region ( fig. 10 ). Its skull width relative to length is greater than in C. lea , C. parva , and C. mediocris , and to a lesser degree, greater compared to C. tenebrosa ( fig. 26 ). Crocidura levicula has a lesser skull length and breadth than C. baletei ( fig. 26 ), but these two species have similar relative skull widths ( fig. 10 ). Samples of Crocidura levicula are nearly nonoverlapping with other members of the Small-Bodied Group in morphometric space in bivariate plots of skull length versus width and along the first two axes from a PCA of 12 cranial measurements ( fig. 26 ). In C. levicula , the C (U3) is equal to or greater in occlusal surface area than is I3 (U2) ( fig. 31 ), which is similar to the conformation in C. lea .

COMMENTS: Miller and Hollister (1921) named this species based solely on the holotype, and unfortunately, we failed to obtain DNA from this specimen. We followed the Tsai et al. (2020) phenol-chloroform extraction protocol and used two separate extractions. The addition of resalting the ethanol supernatants did not yield a quantity of DNA that could be detected with a Qubit 2.0 fluorometer using the dsDNA High Sensitivity Assay Kit (Thermo Fisher Scientific, Waltham, MA). As such, our identification of Crocidura levicula is based on the morphological similarity of the holotype to specimens we collected in areas nearest the type locality.

One specimen (NMV Z63390) from Mt. Torompupu appears to have an introgressed mitochondrion from syntopic Crocidura ordinaria , a member of the Ordinary Group detailed below. Our identification of this specimen is based on morphology alone; we did not sequence any nuclear DNA from this specimen and therefore cannot test our introgression hypothesis.

In our phylogenetic estimates, UCE data confidently placed Crocidura levicula as sister to C. caudipilosa ( figs. 7 , 8 ). However, our nuclearexon and mitochondrial inferences placed this species as a member of a clade of mostly Small- Bodied species that also includes C. caudipilosa ( fig. 5 ; supplementary data S6).

Crocidura levicula was delimited by all BPP analyses. See the C. tenebrosa account above for details.

SPECIMENS EXAMINED: Mt. Katopasa ( LSUMZ 39512–39516 ; NMV C40180 , C40181 , C40200 , C40203 , C40207 , Z55557 ), Pinedapa ( USNM 219450 ), Mt. Rorekatimbo ( FMNH 213192 , 213193 , 213271 ), Tolala ( FMNH 210576 , 210577 ), Mt. Tompotika ( FMNH 213343 – 213365 ), Mt. Torompupu ( LSUMZ 39446–39449 ; NMV C40292 , C40294 , C40306 , C40311 , Z63365 ), Wasponda ( FMNH 210578 , 210579 ).

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. 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).

FIG. 29. Images showing the ventral surface of the left 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 not from the northern peninsula: A, Crocidura levicula, FMNH 213271; B, C. mediocris, FMNH 210566; and C, C. parva, MVZ 237583. Where two scale bars are present within a panel, the upper applies to the foot and the lower to the tail.

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. 31. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary of the three members of the Small- Bodied Group that are not from the northern peninsula: A, Crocidura levicula, FMNH 213362; B, C. mediocris, FMNH 210603; and C, C. parva, MVZ 237577.

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. 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. 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. 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.