Crocidura nigripes 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 : 71-75

Crocidura nigripes Miller and Hollister, 1921

Crocidura nigripes Miller and Hollister, 1921: 101 . Original description.

Crocidura nigripes lipara Miller and Hollister, 1921: 101 . Original subspecies description.

HOLOTYPE: USNM 217545 , an adult male collected by H.C. Raven on 4 August 1916 and prepared as a skin and skull. External measurements from the holotype are 131 mm × 51 mm × 14 mm; ear length and weight were not recorded.

TYPE LOCALITY: “Temboan (southwest from Tondano Lake), northeastern Celebes ” (Miller and Hollister, 1921: 101; fig. 1 ). We estimate Temboan is in the Southeast Minahasa Regency of North Sulawesi Province, 6 km south of Kalait , at 0.979° N, 124.605° E, 650 m. See the gazetteer (appendix) for a full justification of our interpretation of Raven’s notes .

GEOGRAPHIC DISTRIBUTION: Crocidura nigripes is generally regarded as a Sulawesi endemic that occurs broadly across lowland areas of the island ( fig. 1 ), but the species was tenta- tively reported from Obi Island by Fabre et al. (2018). This latter record is based solely on the similarity of cytochrome b sequences between C. nigripes and a single specimen from Obi; we have not examined the Obi specimen. On Sulawesi, we recorded this species from the north-east (Mt. Ambang, Temboan, and Lembeh, North Sulawesi Province), north-central (Toraut, North Sulawesi Province), north-west (Mt. Buliohuto, Gorontalo Province and Mt. Dako, Central Sulawesi Province), west-central (Mts. Balease, Rorekatimbo, and Torompupu, Toare, Tolai, and Sungai Miu, Central Sulawesi Province; Mt. Gandang Dewata (including our lowland sample area at Salu Tiwo), West Sulawesi Province), and east-central areas of endemism (Mt. Katopasa and Peleng Island, Central Sulawesi Province). Notably, we did not record the species from the south-west or southeast areas of endemism. Similarly, Musser (1987) reported the species only from the west-central area of endemism and northern peninsula. The full elevational extent of C. nigripes records across these areas extends from near sea level to just over 2000 m ( fig. 13 ; table 3 ).

EMENDED DIAGNOSIS: A medium-sized shrew ( tables 2 , 14 ) with a medium build and uniformly dark pelage, feet, and tail (light chocolate to black; fig. 36 ). The tail is shorter than head-andbody length. The hind foot is somewhat short relative to head-and-body length ( fig. 17 ), and usually dark brown to black. The skull is broad, and quite angular, with a prominent maxillary process, broad palate, and dentition with a large occlusal area relative to palatal area ( fig. 37B ). The interorbital region is unusually narrow, which enhances the prominence of the braincase breadth and maxillary process ( fig. 10 ). Rostral length makes up a large proportion of skull length ( fig. 10 ).

COMPARISONS: Crocidura nigripes is generally very dark in color with a short tail and moderate body size, but there is substantial variation in size

and color. The feet are often nearly black, which will, in most cases, distinguish this species from all Sulawesi shrews except the darkest members of the Small-Bodied Group, which are much smaller. Typically, C. nigripes is smaller than C. elongata , C. quasielongata , C. caudicrassa , and C. rhoditis , comparable in size to C. microelongata , C. pseudorhoditis , C. brevicauda , and C. australis , and larger than the remaining species known from Sulawesi. It is the largest species in the Ordinary Group. These size differences can be observed using measures of skull length, head-and-body length, mass, or hind foot length ( figs. 9 , 17 ). Tail length is shorter than head-and-body length, which will distinguish C. nigripes from all similarly sized shrews (as judged by HBL, CIL, etc.) except the two Thick-Tailed species, which have greater relative hind-foot lengths (HF/HBL) and stockier bodies ( figs. 9 , 17 ). The skull of C. nigripes has a more angular braincase, more prominent maxillary process (enhanced by the narrow interorbital region), and more robust dentition (larger occlusal surface area) than all other Sulawesi shrews. The relative interorbital width (IOW/CIL) is substantially less than in all other species except C. elongata and C. quasielongata ( fig. 10 ), two species with much longer skulls, tails, hind feet, and bodies.

COMMENTS: Phylogenetically, Crocidura nigripes is more closely related to shrew species endemic to Sundaland than to any others that live on Sulawesi ( Ruedi et al., 1998; Esselstyn et al., 2009, 2019; Hinckley et al. 2021). Our phylogenetic analyses conducted on far more species than previous studies reinforce this conclusion. We placed C. nigripes as sister to C. palawanensis , a species endemic to the Palawan Island group in the southwestern Philippines ( figs. 7 , 8 ). Hinckley et al. (2021) estimated C. nigripes as a close relative of C. foetida , a Bornean endemic that was not included in our analyses.

Miller and Hollister (1921) described two subspecies, Crocidura nigripes nigripes from Temboan and C. n. lipara from Gimpoe, in Central Sulawesi Province. Ruedi (1995) treated northern peninsula populations as C. n. nigripes and specimens from other parts of the island as C. n. lipara. He noted size differences with this geographic division, but also highlighted the limited sample of available specimens. We treat C. n. lipara as a synonym of C. nigripes because we have not identified any geographically partitioned morphological

( fig. 38 ; tables 15, 16) or genetic diversity with our improved sampling. Jukes-Cantor cytochrome b distances between specimens sampled from across Sulawesi are <0.01 ( fig. 4 ; supplementary data S3). As such, we see no reason to maintain the subspecific distinction between C. n. nigripes and C. n. lipara.

SPECIMENS EXAMINED: Mt. Ambang ( LSUMZ 39044 , 39279 , 39320 ), Mt. Balease ( MZB 38491 ; FMNH 210593 , 210595 , 210611 ), Mt. Buliohuto ( LSUMZ 38279–38281 , 38283 , 38286 , 38287 , 38292–38295 , 38297 ; NMV C37778 ) , Mt. Dako ( LSUMZ 37017–37019 , 37022 , 37025–37029 , 37032 , 37035–37049 ; NMV C37257 , C37265 , C37307 , C37318 , C37368 , C37369 ) , Mt. Gandang Dewata ( FMNH 218708 ), Gimpoe (= Gimpu ) ( USNM 219444 , 219446 ), Lake Lindu ( USNM 218668 , 501223 ), Mt. Katopasa ( LSUMZ 40925 ; NMV C40227 , C40229 , C40230 ), Koelawi (= Kulawi ) ( FMNH 47361 ), Kuala Navusu ( AMNH 226105 , 226106 , 226108 , 226109 , 226110 , 226112 ), Peleng Island ( AMNH 109215 ), Pinedapa ( USNM 219435 ), Mt. Rorekatimbo ( FMNH 213190 , 213191 , 213252 ), Salu Tiwo ( FMNH 218703 , 218704 , MZB 38488 , 38489 ), Toraut ( RMNH 38389 [= IZEA 4413 ], 38390 [= IZEA 4415 ]) , Lembeh ( FMNH 31844 ), Sungai Miu ( AMNH 223989 ), Sungai Tolewonu, Tolai ( AMNH 226537–226539 ), Temboan ( FMNH 43859 ; USNM 217536 , 217541– 217545 ), Toare (= Tuare or Toware ) ( FMNH 47362 , USNM 219434 , 219437–219440 , 219443 , 219447 ), Mt. Torompupu ( LSUMZ 39469–39474 ).

Figures

FIG. 1. Maps of A, Southeast Asia and B, Sulawesi showing topographical relief and the approximate boundaries (thick black lines) between areas of endemism (sensu Evans et al., 2003). Two-letter abbreviations in dark gray typeface identify the north-east (NE), north-central (NC), north-west (NW), west-central (WC), eastcentral (EC), south-west (SW), and south-east (SE) areas of endemism. Diamonds label localities where we, or others, have collected shrew specimens since 2010 with the mountain (or locality) name. Stars indicate type localities (Temboan and Pinedapa) from Miller and Hollister (1921). The type localities for the only two Crocidura described from the island since 1921 are Mt. Rorekatimbo (west-central area of endemism) for C. musseri Ruedi (1995) and Mt. Dako (north-west area of endemism) for C. caudipilosa Esselstyn et al. (2019).

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. 36. Images showing the ventral surface of the right hind foot and dorsal surface of the tail base (approximately 1 cm from rump) and tail tip from two darkly pigmented members of the Ordinary Group: A, Crocidura musseri, FMNH 213267; and B, C. nigripes, LSUMZ 37018. Scale bars apply to all images in panel A and to foot (upper) and tail (lower) in panel B.

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. 37. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary of two darkly pigmented members of the Ordinary Group: A, Crocidura musseri, FMNH 213255; and B, C. nigripes, FMNH 210611.

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. 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. 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. 38. Bivariate plot of the first two principal components from an analysis of A, five external measurements and B, 12 cranial variables from across the geographic distribution of Crocidura nigripes on Sulawesi. Specimens coded as C. n. nigripes are those from the northern peninsula and specimens from all other areas were designated as C. n. lipara, per the designations of Miller and Hollister (1921) and Ruedi (1995). Loadings and variance explained are given in tables 15 and 16.

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.