Crocidura elongata 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 : 23-33

Crocidura elongata Miller and Hollister, 1921

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

.

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

HOLOTYPE: USNM 217534 , an adult male obtained by H.C. Raven on 1 August 1916. The specimen comprises a skin and skull. External measurements recorded from the type are 214 mm × 120 mm × 22 mm; no ear length or weight was recorded. TYPE LOCALITY: “Temboan (southwest from Tondano Lake), northeastern Celebes” (Miller and Hollister, 1921: 101; fig. 1 ). We estimate that the type locality is at 0.979° N, 124.605° E, 650 m elevation, which differs from other interpretations (e.g., Musser, 2014). See the gazetteer for a full explanation (appendix).

GEOGRAPHIC DISTRIBUTION: Apparently restricted to the northern peninsula of Sulawesi, where clear records are known from the northeast (the type locality, Temboan and Mt. Ambang, North Sulawesi Province) and north-west (Mt. Dako, Central Sulawesi Province, and Mt. Buliohuto, Gorontalo Province) areas of endemism ( fig. 16 ). The absence of records from the north-central area of endemism are almost certainly due to the general lack of mammal collecting from this region. Miller and Hollister’s (1921) paratypes from “Pinedapa, eastern Middle Celebes ” and the two specimens from Mt. Rorekatimbo reported by Ruedi (1995) almost certainly represent Crocidura microelongata (see below). Crocidura elongata is known from a moderately broad range of elevations, with the low elevation records between 500 and 600 m from Mts. Buliohuto and Dako and high-elevation records reaching 1600 m on Mt. Dako ( table 3 ). The type locality at Temboan is around 650 m elevation.

Long-Tailed Ordinary Rhoditis Small-Bodied Thick ● ●● ● ● ● ●● ● 54 43 34 ● 40 17 78 27 15 43 5 27 75 20 7 21 20 26 27 6 5 11 = = = = = = = = = N = = = = N = = = = = N = N = = N N N N N N N N N N N N N N N N N ● ● ● ● ● ● ● ●● ● ● ● ● ● ● = 54 = 44 = 33 = 40 = 17 = 81 = 27 = 15 = 43 = 5 = 27 = 75 = 22 = 7 = 21 = 20 = 26 = 27 = 6 = 5 = 11 N N N N N N N N N N N N N N N N N N N N N ● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● = 54 = 43 = 32 = 40 = 18 = 78 = 27 = 15 = 43 = 5 = 27 = 76 = 20 = 7 = 21 = 20 = 26 = 27 = 6 = 5 = 11 N N N N N N N N N N N N N N N N N N N N N ● ● ● ● ● ● ●● ● 54 44 34 40 17 81 27 15 ● 43 5 27 75 22 7 21 20 26 27 6 5 11 = = = = = = = = = N = = = = N = = = = = N = N = = N N N N N N N N N N N N N N N N N

EMENDED DIAGNOSIS: A long-bodied, somewhat heavily built, moderately bicolored shrew with a very long tail and unusually long, pale hind feet ( figs. 9 , 14C , 17 ; tables 2 , 5 ). The dorsal pelage is gray-brown overall; individual dorsal hairs are gray at the base and brown at the tip. The ventral pelage is paler, with individual hairs gray-based like those on the dorsum, except that the hair tips are silvery. The silvery appearance of the venter is most pronounced on the throat and chest area. In some specimens, however, this area has a reddish tint, due to variation in the color of the tips of some hairs. The mystacial vibrissae are dark proximally but white distally. The ears are prominent and pale. Dorsally, the feet are pale, transitioning from light brown near the wrist and ankle to nearly white on the digits. Ventrally, the feet show the same transition, but pigment is concentrated around the base of the pads ( fig. 14C ). The claws are translucent. The hind feet are long, even relative to head-and-body length ( fig. 17 ). The long 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 ( fig. 14C ). However, these hairs are slightly longer and white near the tip of the tail, creating a very small white distal tuft. The long bristle hairs that are common at the base of the tail of many Crocidura are nearly absent in this species. The skull is long and slender, with a notably narrow braincase, interorbital region, and palate ( figs. 10 , 18A ). Although the interorbital region is narrow relative to skull length, it is less constricted than the braincase. The long skull of C. elongata is attributable primarily to elongation of the postpalatal region; the rostral length is short relative to skull length ( fig. 10 ). The lambdoidal ridge is prominent for a shrew of this size. The interorbital region is relatively straight (i.e., not strongly tapered) when viewed from the dorsal aspect. The dentition is prominent relative to the palatal breadth ( fig. 18A ).

NMKR

BobAaTe NM

=

BoAfkCApb VKR V

COMPARISONS: Crocidura elongata is readily distinguished from most shrew species on Sulawesi by its long body and even longer tail, relatively pale color, and long and narrow hind feet and skull ( tables 2 , 5 ). Its head-and-body length is considerably longer than all species except C. rhoditis and C. quasielongata . Absolute hind-foot and ear lengths are on average greater in C. elongata than in any other shrew on Sulawesi ( fig. 9 ; table 2 ). However, the other members of the Elongata Subgroup, first described below, can be difficult to distinguish ( fig. 11 ; table 4 ). Compared to C. elongata , C. microelongata is smaller bodied, with a darker pelage and shorter average tail length. The thenar pad on the hind foot of C. elongata ( fig. 14C ) is considerably longer than in either C. microelongata ( fig. 14D ) or C. quasielongata ( fig. 14B ). The skull of C. microelongata is also shorter but

jO

=

AT T

=

tfaTe SKR

=

Coltk S

elongata C. microelongataC. quasielongata C. pmbCfbp

nearly as wide at the braincase and interorbital region, hence its relative width (BB/CIL and IOW/CIL) is greater than that of C. elongata ( figs. 10 , 12 ). Compared to C. elongata , C. quasielongata has a similar head-and-body length, but, on average, a shorter tail and paler pelage ( fig. 12 , table 2 ). The skull of C. elongata is very similar in length to that of C. quasielongata ( figs. 12 , 18 ). However, in C. elongata the rostrum makes up a smaller proportion and the postpalatal region makes up a greater proportion of skull length than in C. quasielongata ( figs. 10 , 12 ). In addition, relative braincase breadth (BB/ CIL and BB/IOW) is, on average, slightly less in C. elongata than in C. quasielongata . A principal components analysis of 12 cranial measurements shows that these two species have broad, though not complete, overlap in multivariate morphometric space ( fig. 11 ).

COMMENTS: A nearly complete cytochrome b sequence (1109 bp) from a topotypical paratype (USNM 217535) is nearly identical to those from specimens we collected on Mt. Ambang ( fig. 4 ), which is approximately 32 km to the southwest. Our inference based on mitogenomes also place USNM 217535 as a close relative to specimens from Mt. Ambang ( fig. 5 ). These animals’ mitochondrial sequences are also closely related to a series from Mt. Buliohuto and to specimens from Mt. Dako referred to as “dark elongata” by Esselstyn et al. (2019). Maximum Jukes-Cantor distances between these sample localities is 0.05 ( fig. 4 ; supplementary data S5). Samples of this species from Temboan and Mts. Ambang, Buliohuto, and Dako formed a well-supported clade in our analyses of UCEs ( figs. 7 , 8 ) and concatenated nuclear exons (supplementary data S6).

The phylogeographic study of Eldridge et al. (2018), which examined the correspondence of genetic diversity in Elongata Subgroup shrews to the area of endemism paradigm expectations, conflated the three species of this subgroup with Crocidura elongata . More recently, specimens of C. elongata from Mt. Dako were referred to as “dark elongata” by Esselstyn et al. (2019) because the authors were unable to determine if either of two long-tailed species on Mt. Dako represented true C. elongata . Mt. Dako is the only area where we found C. elongata occurring in syntopy with another member of the Elongata Subgroup ( C. quasielongata ). Despite the confusing history of specimens in this subgroup, none of our analyses suggested a sister relationship between any two of these species. In our UCE species-tree inference, C. elongata was moderately supported as the sister to C. rhoditis and C. pseudorhoditis ( fig. 7 ), but in our mitogenome estimate it was placed as sister to C. lea , although without statistical support ( fig. 5 ).

Ruedi (1995) suggested a scansorial lifestyle for this species based on its long, naked-appearing tail and long hind feet. While this is certainly possible, direct evidence for a scansorial lifestyle is lacking, and these traits could be linked alternatively to a saltatorial locomotory style ( Brosset, 1988). Some very limited evidence indicates that Crocidura caudipilosa , which has a long, but less extreme tail combined with a more typical hind-foot length, is a skilled climber ( Esselstyn et al., 2019).

For coalescent species delimitation results, see the Crocidura quasielongata account below.

SPECIMENS EXAMINED: Mt. Ambang ( LSUMZ 39008–39013 , 39015–39018 , 39057 , 39058 , 39061 , 39248–39251 , 39257–39264 , 39318 ; NMV C38009 , C38032 ) , Mt. Buliohuto ( LSUMZ 38238 , 38240 , 38243–38247 , 38251–38253 ; NMV C37742 , C37752 , C37760 ), Mt. Dako ( LSUMZ 36905–36907 , 36909 , 36916 , 36919 , 36921 , 36923 , 36924 , 36932 ; NMV C37248 , C37249 , C37303 ), Temboan ( USNM 217534 , 217535 ).

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. 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. 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. 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. 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. 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. 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.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. 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.

Tables

TABLE 3 Elevational Ranges (m) and Species Richness of Crocidura on Mountains of Sulawesia

	North Peninsula				West-Central				SW	East-Central		SE
	Amb	Bulio	Dako	Gand	Lati	Bal	Rore	Torom	Bawa	Kato	Tomp	Mek
Long-tailed group:
caudipilosa	1460– 1655	480– 1390	512– 1630	1535– 2640	1697– 2500	—	2020– 2250	793– 862	1660– 2550	1352– 1610	—	1710– 2536
elongata	1460– 1592	580– 1390	512– 1630	—	—	—	—	—	—	—	—	—
microelongata	—	—	—	1535– 2640	683– 2535	—	2020– 2250	1584– 2218	—	—	—	—
quasielongata	—	—	410	170	683	830– 1140	—	663– 1727	1660– 2040	365– 1700	350	1366– 1717
Ordinary group:
musseri	—	—	—	—	—	—	2020– 2250	—	—	—	—	—
nigripes	1460– 1481	480– 1390	410– 1630	170	—	900– 1140	2020	790– 1371	—	414– 875	—	—
normalis	—	—	—	1535– 2640	1770– 2500	—	2020– 2250	—	—	1380– 1610	—	1366
ordinaria	—	—	—	170– 2640	—	—	—	724– 790	—	—	—	—
solita	—	—	—	1535– 2640	683– 2518	—	2020– 2250	—	—	—	—	—
Rhoditis group:
australis	—	—	—	—	—	—	—	—	1660– 2550	—	—	—
pallida	—	—	—	1535– 1620	1376	860– 1244	—	1584– 1727	—	450– 1610	350– 600	120– 2578
pseudorhoditis	1460– 1655	480– 1210	512– 1630	—	—	—	2230	1584– 1727	—	—	—	—
rhoditis	1460– 1655	—	—	—	—	—	—	—	—	—	—	—
Small-bodied group:
mediocris	—	—	—	170	1697	817– 1107	—	663– 859	—	—	—	1471– 1936
balete	—	1375– 1390	1560– 1630	—	—	—	—	—	—	—	—	—
lea	—	400– 1210	512– 1600	—	—	—	—	—	—	—	—	—
levicula	—	—	—	—	—	—	2020	1371– 1890	—	1365– 1700	350– 600	—
parva	—	—	—	—	—	—	—	—	1660– 2550	—	—	—

TABLE 2 Descriptive Statisticsa for External Measurements (mm) and Mass (g) for Species of Sulawesi Crocidura

	Total	Tail	Hind foot	Ear	Mass
C. australis	142 ± 4.3 (136–148) 5	63 ± 3.3 (59–67) 5	16 ± 0.4 (16–17) 5	11 ± 0.5 (10–11) 5	10.9 ± 1.83 (8.5–12.7) 5
C. baletei	112 ± 5.24 (102–121) 17	47 ± 3.1 (42–53) 17	12 ± 0.6 (10–12) 17	8 ± 0.6 (7–9) 17	5.3 ± 0.58 (4.3–6.4) 17
C. brevicauda	141 ± 6.1 (130–150) 8	58 ± 3.1 (54–64) 8	16 ± 0.8 (15–17) 8	9 ± 0.7 (8–10) 8	12.4 ± 1.63 (10.6–15.2) 8
C. caudicrassa	141 ± 5.5 (130–150) 15	59 ± 4.3 (50–64) 15	16 ± 0.5 (16–17) 16	10 ± 0.5 (9–10) 16	15.5 ± 1.34 (13.5–18.5) 16
C. caudipilosa	164 ± 7.7 (145–183) 75	86 ± 4.6 (79–98) 74	17 ± 0.9 (15–19) 76	10 ± 1.0 (8–13) 77	8.8 ± 1.27 (5.8–12) 75
C. elongata	213 ± 8.6 (192–229) 54	118 ± 6.9 (102–137) 57	22 ± 0.9 (21–24) 57	13 ± 1.2 (10–15) 53	14.5 ± 1.57 (9.5–17.7) 55
C. lea	115 ± 51 (100–124) 37	50 ± 2.5 (44–55) 37	12 ± 0.8 (10–14) 38	8 ± 0.7 (7–9) 37	5.0 ± 0.73 (3.4–6.6) 34
C. levicula	99 ± 5.3 (85–109) 51	36 ± 2.9 (27–44) 51	11 ± 0.5 (10–12) 51	8 ± 0.8 (6–10) 49	4.4 ± 0.77 (3–7) 49
C. mediocris	106 ± 5.0 (89–117) 93	44 ± 2.9 (37–50) 93	11 ± 0.6 (10–13) 97	8 ± 0.7 (6–9) 97	4.4 ± 0.72 (2.9–5.9) 97
C. microelongata	188 ± 9.7 (165–209) 98	106 ± 6.4 (94–121) 93	19 ± 0.9 (17–21) 98	10 ± 0.8 (8–13) 96	11.1 ± 1.59 (7.5–14.25) 93
C. musseri	131 ± 6.8 (112–144) 27	57 ± 3.6 (51–67) 28	15 ± 0.7 (14–17) 30	9 ± 0.7 (8–11) 30	9.1 ± 1.27 (6.2–12.0) 27
C. nigripes	140 ± 9.2 (106–156) 95	57 ± 5.7 (42–71) 97	15 ± 1.1 (13–18) 97	10 ± 1.4 (7–15) 79	11.2 ± 1.86 (7.9–16.0) 74
C. normalis	122 ± 5.1 (110–140) 58	54 ± 4.6 (46–65) 58	14 ± 0.8 (12–16) 56	8 ± 0.7 (7–10) 58	6.1 ± 0.86 (4.3–8.2) 58
C. ordinaria	137 ± 7.8 (122–163) 44	63 ± 4.8 (52–76) 44	15 ± 0.6 (14–17) 44	9 ± 0.6 (8–10) 44	9.7 ± 1.35 (5–12.8) 43
C. pallida	140 ± 7.7 (122–160) 74	62 ± 4.7 (49–73) 74	16 ± 0.7 (14–17) 82	10 ± 1.0 (7.5–13) 77	10.4 ± 1.50 (7.4–16) 75
C. parva	104 ± 5.36 (88–112) 33	41 ± 3.0 (29–47) 34	11 ± 0.5 (10–12) 34	8.0 ± 0.46 (7–9) 34	4.3 ± 0.62 (3.2–5.9) 34
C. pseudorhoditis	158 ± 8.7 (135–180) 98	73 ± 6.0 (59–84) 93	17 ± 0.8 (15–19) 96	10.7 ± 1.1 (8–13) 97	13.2 ± 1.72 (10.3–18.5) 93
C. quasielongata	205 ± 13.9 (171–240) 112	114 ± 10.5 (86–144) 115	21 ± 1.2 (18–24) 115	12 ± 1.2 (9–14) 112	13.6 ± 2.20 (8.6–19.5) 110
C. rhoditis	158 ± 11.0 (131–182) 26	70 ± 5.2 (57–77) 26	18 ± 1.1 (16–20) 26	11 ± 1.1 (10–13) 18	16.9 ± 2.64 (11.5–21.9) 18
C. solita	135 ± 7.1 (118–154) 152	62 ± 4.1 (50–75) 152	15 ± 0.8 (14–19) 154	9 ± 0.9 (7–11) 155	8.5 ± 1.34 (5.4–12.5) 154
C. tenebrosa	104 ± 4.2 (96–111) 14	41 ± 2.4 (36–44) 14	12 ± 0.7 (11–13) 13	10 ± 1.0 (8–11) 14	5.6 ± 0.67 (4.3–6.6) 14

a The sample mean ± one standard deviation, the observed range in parentheses, and the sample size.

TABLE 4 Results of Principal Components Analysis of Craniodental Measurements of the Elongata Subgroup of Crocidura

	Component 1	Component 2
Variablesa
Condyloincisive length	0.7310	0.0787
Braincase breadth	0.0950	0.3000
Interorbital width	0.0345	0.2089
Rostral length	0.3256	-0.5244
Postpalatal width	0.0533	0.0238
Rostral width	0.0654	-0.0098
Postpalatal length	0.3520	0.3492
Condyle to glenoid fossa	0.2238	0.5233
Upper toothrow length	0.3401	-0.3828
P4 to M3 length	0.1675	-0.1932
M2 to M2 labial width	0.1531	-0.0187
Palatal width	0.0336	0.0667
Proportion of variance	0.9089	0.0261
Cumulative variance	0.9089	0.9350

a Table entries for variables are component loadings.