Crocidura quasielongata, 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 : 35-41

Crocidura quasielongata , new species

LSID: urn:lsid:zoobank.org:act:551F4F6E-2983-4C71-923A-047FB0E24B74

Crocidura “pale elongata” Esselstyn et al., 2019: 1715. Informal name.

HOLOTYPE: MZB 43001 (= LSUMZ 36939 ), an adult male, collected on 15 March 2013 by J.L. Patton. The specimen was prepared as a study skin, cleaned skull and skeleton, and frozen tissues. External measurements from the holotype are 215 mm × 126 mm × 22 mm × 11 mm = 16 g. The voucher specimen and a tissue sample will be permanently curated at MZB, with another tissue sample retained at LSUMZ. TYPE LOCALITY: Indonesia, Sulawesi Tengah, Toli Toli, Mt. Dako ; 1.10998° N, 120.90339° E, 410 m.

120°E 122°E 124°E 126°E

1.5°N

0° C. elongata C. quasielongata C. microelongata

1.5°S

Recent sample sites 3°S Miller and Hollister (1921) type localities

100 km 4.5°S

0–1000 m 1000–2000 m 6°S> 2000 m

ETYMOLOGY: We combine “quasi” with “elongata” because this species resembles C. elongata .

GEOGRAPHIC DISTRIBUTION: Widespread on Sulawesi and recorded from all areas of endemism except the north-central and north-east ( fig. 16 ). Populations identified here are from the westcentral (Wasponda and Mts. Balease and Torompupu, Central Sulawesi Province; Salu Tiwo of Mt. Gandang Dewata, West Sulawesi Province; Mt. Latimojong, South Sulawesi Province), south-west (Mt. Bawakaraeng, South Sulawesi Province), south-east (Mt. Mekongga, Southeast Sulawesi Province), east-central (Mts. Katopasa and Tompotika, Central Sulawesi Province), and northwest (Mt. Dako, Central Sulawesi Province) areas of endemism ( fig. 16 ). We found this species from approximately 200 m at Salu Tiwo (low elevation Mt. Gandang Dewata site) to 1700 m on Mts. Mekongga and Katopasa and 1800 m on Mt. Bawakaraeng ( fig. 13 ; table 3 ).

DIAGNOSIS: A long-bodied, somewhat heavily built, moderately bicolored shrew with a long tail and long, pale hind feet ( table 2 ). The dorsal pelage ranges from gray-tan to gray-brown overall, with individual dorsal hairs having a gray base and tan to brown tip. Some specimens also have a narrow, tan band between the gray proximal section and brown tip of each hair. The ventral pelage has silver highlights, the visual effect of individual hairs each with a pale tip. In many specimens, the chest and throat area has a slight red tint due to variation in the color of the hair tips. The ears are large and pale. The mystacial vibrissae are dark proximally, but white distally, with the dark portion occupying 20%–80% of vibrissa length. The hind feet are long absolutely ( table 2 ) and relative to head-and-body length ( fig. 17 ). Dorsally, the feet range from entirely white, to brown at the ankle and wrist, slowly transitioning toward the white digits. Ventrally, the feet show the same transition (except in specimens where they are entirely white), but pigment is concentrated around the base of each foot pad. The claws are translucent ( fig. 14B ). The tail is subtly bicolored, with a brown dorsum and pale brown venter. Tiny applied hairs are present along the entire length of the tail, but they are barely visible to the naked eye along most of the tail. However, these hairs are slightly longer and white near the tip of the tail, creating a very small, sometimes white, distal tuft. Tail bristles are nearly absent ( fig. 14B ). The skull is long, primarily due to elongation of the postpalatal region, but not the rostral region ( figs. 10 , 18C ). Relative to skull length, the braincase is especially narrow (BB/CIL) and the interorbital region somewhat narrow (IOW/CIL; fig. 10 ) and relatively untapered. The lambdoidal crest is prominent. The dentition is robust ( fig. 18C ).

COMPARISONS: This species is easily distinguished by the ratio of tail length to head-andbody length (most specimens>110%; fig. 9 ) from all Crocidura species on Sulawesi except

other members of the Long-Tailed Group. Within this group, C. quasielongata is considerably larger, much stockier, has a much narrower relative braincase breadth (BB/CIL), and has a much less hairy tail than C. caudipilosa . Within the Elongata Subgroup, C. quasielongata is, on average, intermediate in size, tail length, and hind-foot length between the smaller C. microelongata and the slightly larger C. elongata ( fig. 9 ; tables 2 , 5 ). Crocidura quasielongata has long ears, second in length only to C. elongata ( table 2 ). Although these measurements overlap between the species, the averages differ. On the hind foot, the thenar pad is shorter than in C. elongata ( fig. 14 ), despite the similar hind-foot lengths shared by these species. Also, on average, C. quasielongata is paler than either C. elongata or C. microelongata , but there is substantial color variation across the range of the species. The pelage varies in overall color from tan to dark brown. The palest specimens of C. quasielongata are from Mt. Tompotika and Salu Tiwo of Mt. Gandang Dewata, while animals from Mt. Dako are slightly darker, and specimens from Mts. Balease, Katopasa, and Torompupu are darker still. These color differences may reflect a tendency for low-elevation animals to be paler than those sampled at higher elevations, perhaps an elevational version of Gloger’s Rule ( Gloger, 1833). The palest specimens have a middle color band that is light gray on individual hairs. The skull of C. quasielongata is long, with a very narrow braincase and interorbital region. The interorbital region is also rather straight, barely tapering anteriorly. In this regard, the skull is very similar to, but slightly shorter than that of C. elongata , and it is much more elongate than in C. microelongata ( fig. 12 ). In proportion to skull length, rostral length is greater, but postpalatal length is lesser in C. quasielongata than in C. elongata and C. microelongata ( fig. 10 ). The dentition is slightly more robust than in C. microelongata but comparable to that of C. elongata ( fig. 18 ).

COMMENTS: Although Crocidura microelongata is mostly separated in our PCA ( fig. 11 ) and

in univariate measures ( fig. 12 ), C. elongata and C. quasielongata are much more difficult to distinguish, with average differences apparent only from large series of specimens identified with molecular data. Based on current sampling, geography can be a reliable predictor except that we found both species occurring on Mt. Dako and there remains a large sampling gap between Mt. Dako and the west-central area of endemism (i.e., the base of the northern peninsula; fig. 16 ). On Mt. Dako, we trapped C. elongata around 512 and 1600 m, whereas we captured C. quasielongata only around 410 m. We found C. quasielongata at higher elevations in other parts of the island and C. elongata at lower elevations at other localities ( fig. 13 ; table 3 ). Thus, these two species may have a parapatric distribution partitioned by elevation on the one mountain where we found them together. Because these two species are so different morphologically from all the other species on the island, it would not be surprising if they fill similar functional niches and thus one excludes the other wherever they interact.

Despite the morphological similarities of Elongata Subgroup members, genetic evidence is clear that these three species are distinct from each other and do not form a clade. None of our phylogenetic analyses (mtDNA, nuclear exons, or UCEs) even hinted at a sister relationship between any of the three species. Our mitochondrial inferences placed Crocidura quasielongata as sister to C. caudicrassa ( figs. 4 , 5 ), but this seems unlikely because C. caudicrassa is sister to the phenotypically similar C. brevicauda in UCE trees ( figs. 7 , 8 ). In our UCE species tree, C. quasielongata is sister to a mix of Ordinary Group and Rhoditis Group species ( fig. 7 ). Despite these mixed signals, the lack of basal resolution among species in our phylogenetic estimates leaves the door open to possible sister relationships among Elongata Subgroup members. The similarities in cranial proportions (e.g., relative widths; fig. 10 ) between C. elongata and C. quasielongata suggest either inherited similarity, or remarkable convergence. If any of these three species ever show a sister relationship in future analyses, we suspect it will be this pair.

120°E 122°E 124°E 126°E

1.5°N

0° C. rhoditis C. pseudorhoditis C. australis C. pallida 1.5°S

Recent sample sites 3°S Miller and Hollister (1921) type localities

100 km 4.5°S

0–1000 m 1000–2000 m 6°S>2000 m

Our BPP analyses compared the three members of the Elongata Subgroup, even though we did not infer them to form a clade in any of our phylogenetic analyses. The samples of each species were chosen to represent the full extent of our geographic sampling for the range of each species. Samples included comprise Crocidura elongata from three mountains (N = 17), C. microelongata from four mountains (N = 24), and C. quasielongata from eight mountains (N = 28). The matrix is 92% complete and all analyses supported all three species with 1.0 posterior probability.

SPECIMENS EXAMINED: Mt. Balease ( FMNH 210542–210559 , 210596–210601 ), Mt. Bawakaraeng ( NMV Z57377 , Z57061 ), Mt. Dako ( MZB 43001 ; LSUMZ 36935–36938 ), Mt. Katopasa ( LSUMZ 39483 , 39486–39490 , 39492 ; NMV C40177 , C40201 , C40202 , Z62311 , Z61792 ), Mt. Latimojong ( MZB 40936 , MVZ 237573 ), Mt. Mekongga ( MWFB 8091 , 8094 , 8113 , 8114 , 8122 , 8130 , 13507 , 13509 , 13511 ), Salu Tiwo ( FMNH 218548–218557 , 218559–218561 , 218563– 218579 ; MZB 38448 , 38452 ), Mt. Tompotika ( FMNH 213339–213342 ), Mt. Torompupu ( LSUMZ 39418–39422 , 39426–39430 ; MVZ 238107 , 238108 , NMV C40240 , C40241 , C 40243–C40245 , C40247 , C40254 , C 40259– C40262 , C40281 , C40282 , C40288 , C40293 ), Wasponda ( FMNH 210560–210562 ).

Figures

FIG. 16. Map of Sulawesi showing localities sampled for shrews. Colored areas enclose localities with known records of members of the Elongata Subgroup. Although we excluded Pinedapa from the estimated geographic ranges, we suspect the two USNM specimens referred to Crocidura elongata by Miller and Hollister (1921) from this site represent C. microelongata.

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. 14. 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 four members of the Long-Tailed Group: A, Crocidura caudipilosa, LSUMZ 36940; B, C. quasielongata, FMNH 218551; C, C. elongata, LSUMZ 39009; and D, C. microelongata, FMNH 212998. Scale bars represent 5 mm and apply to their nearest images within each panel. The thenar (T) and hypothenar (H) pads are labeled on panel B.

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. 18. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary of the three members of the Elongata Subgroup: A, Crocidura elongata, LSUMZ 39259; B, C. microelongata, FMNH 213426; and C, C. quasielongata, LSUMZ 36939.

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.12. Box plots of skull measurements useful for distinguishing species of the Elongata Subgroup. 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. 11. Bivariate plot of the first two principal components from an analysis of 12 cranial measurements from the Elongata Subgroup. Loadings and variance explained are given in table 4.

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.