Crocidura pallida, 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 : 49-52

Crocidura pallida , new species

LSID: urn:lsid:zoobank.org:act:1249AC44-0D01-4060-B5FD-3000D9C4D29D

HOLOTYPE: MZB 43004 (= FMNH 210607 ), an adult female collected by J.A. Esselstyn on 18 October 2010. The specimen consists of a

dried skin, cleaned skull ( fig. 24B ) and skeleton, and tissue sample. It carried one embryo measuring 18 mm in crown-rump length. External measurements from the holotype are: 140 mm × 62 mm × 15 mm × 8 mm = 11 g. The voucher specimen and a tissue sample will be permanently curated at MZB, with another tissue sample retained at FMNH.

TYPE LOCALITY: Indonesia, Sulawesi Selatan, Luwu Utara, Sukamaju, Mt. Balease ; 2.4995° S, 120.4874° E, 900 m elevation.

ETYMOLOGY: We use the Latin pallida to highlight the pale color of the feet of this species.

GEOGRAPHIC DISTRIBUTION: Recorded from the west-central (Mt. Gandang Dewata, West Sulawesi Province; Mts.Torompupu and Balease, Central Sulawesi Province; Mt. Latimojong and Rindingallo, South Sulawesi Province), east-central (Mts. Katopasa and Tompotika, Central Sulawesi Province), and south-east areas of endemism (Mt. Mekongga, Southeast Sulawesi Province; fig. 20 ). Across these areas, we found this species over a broad elevational range, from approximately 100 to over 2500 m ( fig. 13 ; table 3 ).

DIAGNOSIS: Crocidura pallida is a moderately sized shrew ( figs. 9 , 23 ; tables 2 , 7 ) with very pale feet ( fig. 21B ) and a somewhat pale ventral side of the tail. The tail is shorter than the head-andbody length ( fig. 9 ; table 2 ). The dorsal pelage is gray to gray-brown while the ventral pelage is pale gray. The pinna and the dorsal side of the tail match the dorsal pelage, but the dorsal side of the feet are distinctly paler. The dorsal surface of the hand is nearly white, but some pigment is present near the wrist. The hind feet show a similar pattern but are modestly darker. Ventrally, the feet are also pale, especially on the digits, which are usually white. The darkest parts of the hind foot are usually the thenar and hypothenar pads ( fig. 21B ). The pads of the forefeet are rarely pigmented. Tail bristles are sparse to nearly absent ( fig. 21B ), extending along no more than the proximal third of the tail length. The tail varies from uniformly colored to moderately bicolored with a paler ventral side. The skull is typical of Crocidura of this size. The braincase is generally rounded, but a subtle lateral point is evident at the mastoid region when viewed from a dorsal aspect ( fig. 24B ). The braincase is somewhat inflated dorsoventrally, and it is wide relative to skull length ( fig. 24B ), as are the interorbital region and rostrum ( fig. 10 ; table 7 ). The wide interorbital region gives the maxillary process a relatively weak appearance. In some individuals, the nasal passage is particularly inflated and laterally bulging, further obscuring the maxillary process. The rostrum is somewhat long, relative to skull length ( fig. 10 ). The maxillary bridge is usually narrow, with an anteriorly placed lacrimal foramen. The posterior portion of the hard palate is narrow, sandwiched between broad molars.

COMPARISONS: Crocidura pallida is smaller than C. rhoditis , C. pseudorhoditis , C. nigripes , and members of the Elongata Subgroup and Thick-Tailed Group. It is considerably larger than all members of the Small-Bodied Group and somewhat larger than all members the Ordinary Group except C. nigripes . In absolute terms and relative to head-and-body length, the tail length is comparable to members of the Ordinary, Thick-Tailed, and Rhoditis groups, but substantially shorter than in all members of the Long- Tailed Group and considerably longer than in any member of the Small-Bodied Group ( fig. 9 ). Outside of the Rhoditis Group, most species have much darker feet than C. pallida . These include C. caudipilosa and C. microelongata of the Long-Tailed Group, C. normalis , C. musseri , and C. nigripes of the Ordinary Group, both Thick-Tailed Group members, and all members of the Small-Bodied Group except C. lea . Within the Rhoditis Group, C. pallida is smaller in absolute measurements ( fig. 9 ) and more delicately built than C. rhoditis and C. pseudorhoditis ( fig. 17 ); it is paler with a relatively narrower braincase and interorbital region than the otherwise similarly proportioned C. australis . Rostral length makes up a smaller proportion of skull length (RL/CIL) in C. pallida than in either C. rhoditis or C. pseudorhoditis , but this trait is comparable in C. australis ( fig. 10 ).

COMMENTS: Substantial mitochondrial genetic divergence is evident between populations from Mt. Katopasa, Mt. Tompotika, and the remaining sites (up to 0.089 Jukes-Cantor distance; fig. 4 ; supplementary data S3). However, these populations form a cohesive set of morphological specimens, form a clade in our phylogenetic analyses of nuclear genes ( figs. 7 , 8 ; supplementary data S6), and all of the mitochondrial variation is partitioned geographically (i.e., no sympatry between divergent mitochondrial clades). We therefore did not divide them further.

We identified a single specimen of Crocidura pallida from Mt. Latimojong (MVZ 237618), a locality where C. solita is abundant. Although C. pallida is slightly larger, these two can be difficult to distinguish. As such, it is possible that this specimen is a slightly large individual of C. solita with mtDNA introgressed from C. pallida . Unfortunately, we did not obtain nuclear loci (exons or UCEs) from this specimen and there- fore cannot test for introgression. Contamination of this cytochrome b sequence is unlikely because it is unique in our alignment. We favor the hypothesis that MVZ 237618 is C. pallida because its cytochrome b sequence differs slightly from C. pallida sequences from nearby localities (i.e., Mts. Gandang Dewata and Balease) and phenotypically, it is nearer the averages for C. pallida than C. solita .

Phylogenetic estimates were not consistent regarding the relationships of Crocidura pallida . Our mitochondrial gene trees put it as sister to a clade of Small-Bodied species, C. caudipilosa , and C. normalis ( figs. 4 , 5 ). However, our nuclearbased inferences placed C. pallida as part of the large basal polytomy ( figs. 7 , 8 ; supplementary data S6).

SPECIMENS EXAMINED: Mt. Balease ( FMNH 210580–210592 , 210608 , 210609 , MZB 43004 ), Mt. Gandang Dewata ( FMNH 218687–218702 , 218989 ; MZB 34872 , 34886 , 34888 , 34889 ), Mt. Katopasa ( LSUMZ 39527 , 39529–39538 ; MVZ 238115–238118 ; NMV C40187 , C40192 , C40199 , C40206 , C40214 , C40217 , C40307 , Z56723 , Z62366 , Z61754 , Z62414 ), Mt. Latimojong ( MVZ 237618 ), Mt. Mekongga ( MWFB 8059 , 8115 , 8125 , 8139 , 8150 , 8161 , 8162 , 8195 , 8196 , 8438 , 8439 ), Rindingallo , Tana Toraja ( MSB 93256 ), Mt. Tompotika ( FMNH 213366–213369 ), Mt. Torompupu ( NMV C40307 ) .

Figures

FIG. 24. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary of two members of the Rhoditis Group: A, Crocidura australis, MVZ 237610 and B, C. pallida, FMNH 210607.

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. 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. 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. 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. 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.

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.