Crocidura rhoditis 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 : 42-46

Crocidura rhoditis Miller and Hollister, 1921

Crocidura rhoditis Miller and Hollister, 1921: 102 . Original description.

HOLOTYPE: USNM 217550 , an adult male collected 3 August 1916 by H.C. Raven. Prepared as a skin and skull. External measurements from the type are 153 mm × 70 mm × 17 mm; ear length and weight were not recorded.

TYPE LOCALITY: “Temboan, northeastern Celebes” (Miller and Hollister, 1921: 102; fig. 20 ). Temboan is located at 0.979° N, 124.605° E, 650 m elevation in the Southeast Minahasa Regency , North Sulawesi Province, 6 km south of Kalait. See the gazetteer (appendix) for a detailed explanation of our interpretation of Raven’s type locality.

GEOGRAPHIC DISTRIBUTION: Known only from the north-east area of endemism (Temboan and Mt. Ambang, North Sulawesi Province; fig. 20 ). Ruedi (1995) reported specimens from Mt. Rorekatimbo, but mitochondrially ( Ruedi et al., 1998), these match the sister taxon, Crocidura pseudorhoditis . Musser (1987) reported C. rhoditis from southwestern and central Sulawesi, but those records likely represent other taxa. We recorded this species between 1400 and 1700 m on Mt. Ambang ( fig. 13 ; table 3 ). Specimens from Temboan are from low elevation habitat, probably around 650 m.

EMENDED DIAGNOSIS: Crocidura rhoditis is one of the larger shrews on Sulawesi ( tables 2 , 7 ), with a stocky build ( fig. 17 ). Its overall color is paler than most species on the island, with a medium gray dorsal pelage and slightly paler venter, often with cinnamon highlights. The feet are pale, especially the forefeet. The digits of the hand are nearly white or pale pink colored, but those of the hind feet are off-white. The tail is slightly shorter than head-and-body length, thick at the base, and similar in color to the pelage. Tail bristles are present, but sparse along the proximal half of the tail ( fig. 21D ). The lips are paler than the surrounding pelage and the rhinarium is also generally pale, but the upper margins of each nostril have a dark rim. The skull of C. rhoditis is large, with the rostral length making up an unusually large proportion of skull length (RL/CIL; fig. 10 ). The braincase is wider than expected for a shrew of this size, but the interorbital region is narrow relative to the braincase breadth ( figs. 10 , 22A ). The lambdoidal ridge is fairly prominent and the squamosalparietal suture also forms a ridge that extends horizontally from above the internal ear to above the glenoid fossa. This ridge is visible from a dorsal aspect and highlights the tapering shape of the anterior portion of the braincase margin. The angle at which the braincase narrows anteriorly is similar to the tapered shape of the interorbital region. The dentition is robust, occupying a large portion of the palate ( fig. 22A ).

COMPARISONS: Crocidura rhoditis is larger than all Sulawesi Crocidura except C. elongata , C. quasielongata , C. nigripes , and the two Thick- Tailed Group members, C. brevicauda and C. caudicrassa . Its mass-to-HBL ratio is greater than in all other species except C. caudicrassa ( fig. 17 ) and its relative rostral length (RL/CIL) is greater than in all other species ( fig. 10 ). The tail of C. rhoditis is much shorter absolutely and relative to body length than in members of the Long-Tailed Group, but longer absolutely than in all other species except C. pseudorhoditis ( fig. 9 ). The dorsal pelage of C. rhoditis is similar in color to C. elongata , darker than C. quasielongata , and paler than C. nigripes . The feet of C. rhoditis are paler than those of most other species, with the excep- tions of C. lea (much smaller), C. pallida (smaller), C. elongata (longer tail), and C. quasielongata (longer tail). Within the Rhoditis Group, C. rhoditis is easily confused with C. pseudorhoditis , its apparent sister species, but it is larger in all dimensions than the other two members of the Rhoditis Group, C. australis and C. pallida . Both C. rhoditis and C. pseudorhoditis have a pale integument, but C. rhoditis is larger, slightly paler, and has a narrower thenar pad on the hind foot ( fig. 21 ). Although differences in body length are modest ( fig. 23 ), C. rhoditis is stockier than C. pseudorhoditis ( fig. 17 ) and size differences are apparent in condyloincisive length and braincase breadth ( fig. 23 ; table 7 ). In addition to the greater relative rostral length mentioned above, C. rhoditis also has a lesser relative interorbital width (IOW/CIL) than all other members of the Rhoditis Group ( fig. 10 ). The narrowness of the interorbital region is also reflected in that it is lesser relative to braincase breadth (IOW/BB) in C. rhoditis compared to C. pseudorhoditis , whereas braincase breadth relative to skull length (BB/CIL) does not differ appreciably between the two species ( figs. 10 , 22 ). The skull of C. rhoditis has a prominent ridge at the suture of the squamosal and parietal bones. This ridge is present, but less conspicuous in C. pseudorhoditis . A PCA of cranial measurements largely separates these two taxa along the first axis, which represents size ( fig. 19 ; table 6 ). The differences in size measurements between C. rhoditis and its sister species are somewhat more pronounced when only syntopically sampled specimens from Mt. Ambang are considered ( fig. 23 ), perhaps indicating a role for character displacement in these species.

COMMENTS: Mitochondrial sequences from the type series ( USNM 217550 , 217552 , and 217554, and FMNH 43858 ) are all very similar to cytochrome b sequences from our Mt. Ambang specimens, with maximum intraspecific Jukes-Cantor distances ≤0.011 ( fig. 4 ; supplementary data S5). Parapatrically distributed, phenotypically similar specimens with distinct mitochondrial sequences (mean Jukes-Cantor

distance = 0.08) and smaller skulls are described below as Crocidura pseudorhoditis . Although the morphological differences between these two species are slight, the fairly large mitochondrial divergence, corroborating inferences from nuclear exons and UCEs ( figs. 7 , 8 ; supplementary data S6), and their syntopy on Mt. Ambang ( fig. 20 ) strongly support their recognition as distinct taxa. See the account of C. pseudorhoditis for results of BPP analyses.

LENGTH 100

HEAD-AND-BODY 80

90 70 N = 5 N = 74 N = 49 N = 94 N = 18 N = 27

SPECIMENS EXAMINED: Mt. Ambang ( LSUMZ 39032 , 39033 , 39037 , 39038 , 39050 , 39053– 39055 , 39062 , 39064 , 39065 , 39068 , 39284 , 39296 , 39319 , 39321 ; NMV C38022 , C38031 ), Temboan ( USNM 217550 , 217552 , 217554 , FMNH 43858 ).

Figures

FIG. 20. Map of Sulawesi showing localities sampled for shrews. Colored areas enclose localities with known records of members of the Rhoditis 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. 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. 21. 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 four members of the Rhoditis Group: A, Crocidura australis, MVZ 237610 (right hind foot); B, C. pallida, FMNH 210582 (left hind foot); C, C. pseudorhoditis, LSUMZ 39040 (right hind foot); and D, C. rhoditis, LSUMZ 39296 (left hind foot). Scale bars represent 5 mm. When two scale bars are present in 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. 22. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary from two members of the Rhoditis Group: A, Crocidura rhoditis, LSUMZ 39050 and B, C. pseudorhoditis, LSUMZ 39310.

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. 23. Box plots summarizing head-and-body length, condyloincisive length, and braincase breadth measurements for members of the Rhoditis Group. Data from Crocidura rhoditis and C. pseudorhoditis are divided into two boxes. Dark gray boxes show all available measurements from across the species range while light gray boxes show only samples taken on Mt. Ambang, where the two species occur in syntopy. Note that the differences between these two species are greater on Mt. Ambang than they are for the islandwide sample. 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. 19. Bivariate plots showing the first two principal components from analyses of 12 cranial variables in the Rhoditis Group. Panel A shows analysis of individuals sampled syntopically on Mt. Ambang (C. pseudorhoditis and C. rhoditis) and panel B shows individuals sampled across the island. Loadings and variance explained by component axes are presented in table 6.

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. 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.