Crocidura pseudorhoditis, 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 : 46-48

Crocidura pseudorhoditis , new species

LSID: urn:lsid:zoobank.org:act:980DF37A-D8F0-4DBF-877C-A11C04F55FC1

Crocidura rhoditis Ruedi, 1995: 255 . Misidentification.

11.5

Mt. Ambang

Crocidura rhoditis Esselstyn et al., 2019: 1716 . Misidentification.

BREADTH 10.5

11 Sulawesi-wide

HOLOTYPE: MZB 43002 (= LSUMZ 39310), an adult female, collected on 22 February 2016 by H. Handika. The specimen was prepared as a cleaned skull and skeleton, study skin, stomach, intestine, and frozen tissues. External measurements from the type are 148 mm × 70 mm × 16 mm × 11 mm = 11 g. The voucher specimen and a tissue sample will be permanently curated at MZB, with another tissue sample retained at LSUMZ.

BRAINCASE 9.5 10

9 N = 5 N = 27 N =

35

N = 76 N = 10 N = 20 ralis

aust C.

pallida

C.

rhoditis

C.

pseudorhoditis

C.

SPECIES

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: We combine “pseudo” with “rhoditis” because this species looks very similar to C. rhoditis .

GEOGRAPHIC DISTRIBUTION: We recorded this species from the northwestern portion of the west-central area of endemism (Mts. Torompupu and Rorekatimbo, Central Sulawesi Province), and the north-west and north-east areas of endemism of the northern peninsula ( fig. 20 ; Mt. Dako, Central Sulawesi Province; Mt. Buliohuto, Gorontalo Province; and Mt. Ambang, North Sulawesi Province). The absence of records from the north-central area of endemism is almost certainly due to the lack of general mammal surveys and specimens from this region. Both specimens we report from Mt. Rorekatimbo were trapped by Ruedi (1995); we did not collect any Crocidura pseudorhoditis on Mt. Rorekatimbo, despite working at similar elevations. We found this species at a range of elevations ( fig. 13 ), the low on Mt. Buliohuto (500 m) and the high on Mt. Rorekatimbo (2200 m; table 3 ).

DIAGNOSIS: Crocidura pseudorhoditis is a moderately large shrew ( tables 2 , 7 ) with a somewhat stocky build, medium gray, moderately bicolored pelage, a tail that is shorter than headand-body length, and dorsal foot surfaces that range from light gray-brown to pinkish white. The forefeet are paler than the hind feet and the claws are unpigmented and accompanied by a small tuft of white hairs on the hands, but on the hind feet, some of these hairs are dark. The tail is barely dorsoventrally bicolored proximally, but this transitions to a uniformly colored tail for the distal half of tail length. The tail has only sparse bristles over the proximal half of its length ( fig. 21C ). The lips are gray-brown, but the nose is distinctly paler. The palmar surface ranges from gray-brown to white, being palest on the digits. The color of the plantar surface also transitions from darker to paler colors toward the digits ( fig. 21C ), but all aspects are darker than on the forefeet. The skull is long ( table 7 ) and broader at the braincase and interorbital region than expected given its length ( figs. 10 , 22B ). The rostrum is long relative to the postpalatal portion of skull length, reflected in the RL/CIL ( fig. 10 ). The suture between the squamosal and parietal bones is often open and in the shape of a sickle blade just below the opening of the sinus canal ( fig. 22B ). The maxillary bridge is wide.

COMPARISONS: Crocidura pseudorhoditis is smaller than C. rhoditis , C. elongata , and C. quasielongata , but larger than C. caudipilosa, Rhoditis Group members C. australis and C. pallida , all members of the Small-Bodied Group, and all members of the Ordinary Group except C. nigripes , which is similarly sized ( fig. 19 ; tables 2 , 7 ). The body of C. pseudorhoditis is more robust than those of C. microelongata , C. australis , and C. pallida , but less stocky than in C. rhoditis and C. caudicrassa ( fig. 17 ). Crocidura pseudorhoditis is slightly darker (both pelage and feet) than C. rhoditis and tail bristles, though not abundant, are still more prevalent than in C. rhoditis ( fig. 21 ). The thenar and hypothenar pads on the hind foot are both more rounded than the oblong pads of C. rhoditis ( fig. 21 ). Crocidura pseudorhoditis is similar in pelage color to C. australis and C. pallida . Braincase breadth relative to skull length is greater than in many of the species with somewhat similar body sizes, including C. rhoditis , and all Elongata Subgroup and Thick-Tailed Group species. However, C. pallida is comparable in this regard, and C. australis has an even greater relative skull breadth no matter where it is measured ( fig. 10 ). The braincase is a bit more angular in C. pseudorhoditis than in C. rhoditis , with the widest part of the cranium in C. pseudorhoditis forming an obtuse point ( fig. 22 ). However, the angularity of the braincase does not reach the degree seen in C. nigripes . The ratio of rostral length to skull length is large in C. pseudorhoditis and exceeded only by that of C. rhoditis ; the other Rhoditis Group members have comparatively short relative rostral lengths (RL/CIL) and outside the Rhoditis Group, C. nigripes and the two Thick- Tailed species (defined below) are comparable ( fig. 10 ). Crocidura pseudorhoditis is larger in head-and-body length, foot length, and all cranial dimensions than C. australis and C. pallida ( fig. 19 ; tables 2 , 7 ). The slight difference in size between C. pseudorhoditis and C. rhoditis appears to be enhanced where the two species cooccur (Mt. Ambang; fig. 20 ), especially condyloincisive length ( fig. 23 ). A principal components analysis of 12 cranial measurements that only included these two species readily separated them on the first axis, which represents size ( fig. 19 ; table 6 ).

COMMENTS: While Crocidura pseudorhoditis is on average smaller than C. rhoditis , the two species are easily confused phenotypically and they occur in sympatry in the north-east area of endemism ( fig. 20 ; table 3 ). The large mitochondrial distances between C. rhoditis and C. pseudorhoditis , along with the slight but consistent differences in size, which appear to be enhanced where they are syntopic ( fig. 23 ), strongly suggest these are independently evolving populations. Our BPP analyses tested species limits with an alignment that contains 15 C. rhoditis and 58 C. pseudorhoditis and is 96% complete. The analyses supported these species’ distinction with 1.0 posterior probability with all prior combinations in all runs.

One of the few cases of clarity from our phylogenetic analyses is the consistent and well-supported sister relationship between Crocidura rhoditis and C. pseudorhoditis ( figs. 4 , 5 , 7 , 8 ; supplementary data S6). Given their phenotypic similarity, this makes sense from a morphological perspective. In our UCE species tree, we found these two species sister to C. elongata ( fig. 7 ).

SPECIMENS EXAMINED: Mt. Ambang ( LSUMZ 39030 , 39031 , 39034–39036 , 39039–39043 , 39045 , 39048 , 39049 , 39051 , 39052 , 39056 , 39059 , 39060 , 39063 , 39066 , 39067 , 39278 , 39280–39283 , 39293 , 39297 , 39298 , 39300– 39309 , 39311–39314 , 39316 , 39317 , 39322 ; MZB 43002 ; NMV C37985 , C37992 , C37996 , C38017 ), Mt. Buliohuto ( LSUMZ 38275–38278 , 38284 ; NMV C37793 ), Mt. Dako ( LSUMZ 36973 , 36978 , 36979 , 36986 , 36990 , 36991 , 36993 , 36995 , 36998 , 37000 , 37002 , 37005 , 37007 , 37008 , 37011–37016 , 37033 , 37034 ; MZB 38564–38566 ; NMV C37252 , C37254 , C37264 , C37268 , C37292 , C37297 , 37308 , 37315 , C37328 , 37329 , C37363 , C37367 ), Mt. Torompupu (NMV C40308), Mt. Rorekatimbo ( RMNH 38409 (= IZEA 4406 ), IZEA 4407 ) .

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. 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. 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. 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. 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. 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. 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.