Crocidura lea 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 : 52-57

Crocidura lea Miller and Hollister, 1921

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

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

HOLOTYPE: USNM 217553 , an adult male collected by H.C. Raven on 3 August 1916. Prepared as a skin and skull. External measurements from the holotype are 111 mm × 51 mm × 14 mm; ear length and weight were not recorded. TYPE LOCALITY: “Temboan, northeastern Celebes ” (Miller and Hollister, 1921: 102; fig. 25 ). 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 details of our interpretation of Raven’s field notes .

GEOGRAPHIC DISTRIBUTION: Probably endemic to the northern peninsula. We identified specimens of this species from the northwest area of endemism (Mt. Dako, Central Sulawesi Province and Mt. Buliohuto, Gorontalo Province) and the type locality is in the north-east area of endemism (Temboan, North Sulawesi Province). We did not find this species on Mt. Ambang (north-east area of endemism), where its ecological position is apparently held by another tiny, but not closely related shrew, Crocidura tenebrosa ( fig. 25 ). We recorded C. lea at both high and low elevations on both Mts. Dako (512 and 1600 m) and Buliohuto (400– 600 and 1200 m; table 3 ). We did not collect any specimens of this species at our 410 m site on Mt. Dako. The type locality (Temboan) is at roughly 650 m.

120°E 122°E 124°E 126°E

1.5°N

C. lea

0° C. baletei

C. tenebrosa

C. levicula

C. mediocris

C. parva

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

EMENDED DIAGNOSIS: Crocidura lea is a very small shrew ( tables 2 , 8 ) with a brown dorsal pelage, gray-brown ventral pelage, and pale feet. The pinnae are prominent and slightly paler than the surrounding fur, especially at the lobe. The mystacial vibrissae are generally unpigmented, but a few, typically the longer ones, are brown or black proximally. Dorsally, foot color transitions from gray-brown at the wrist and ankle to pale pinkish white on the digits ( fig. 27B ). The claws are small, unpigmented, and sometimes lack the surrounding tuft of white hairs present in many other species. Ventrally, the forefeet mostly lack pigment, but the hind feet are darker. In the hind feet, color transitions from brown posteriorly from the heel, and to a lesser extent laterally, to white at the digits. However, pigment is concentrated in the pads, particularly around the base of the thenar, hypothenar, and in some cases the 4th (lateralmost) interdigital pad ( fig. 27B ). The tail is shorter than head-and-body length, sometimes dorsoventrally bicolored, and thinly covered with very small, dark brown applied hairs. A few sparse bristles are present along the proximal three-fourths of the tail ( fig. 27B ). The skull is short, narrow, and somewhat rounded in overall shape ( fig. 28B ). Relative to body size, the skull is slightly longer than expected, and relative to skull length, the braincase (BB/CIL) is especially narrow, but the interorbital region is not unusual in its relative width (IOW/CIL; fig. 10 ). The maxillary process is weak ( fig. 28B ). The I3

A B 0.5

8.5

BREADTH 8. 2 0 Species C C.. lea baletei

BRAINCASE 7.5

COMP -0.5 C C C C.... parva levicula mediocris tenebrosa

16 17 18 CONDYLOINCISIVE LENGTH

-2 -1 0 1 2 COMP. 1

(U2) is smaller than the C (U3). The parastyle of P4 is modest.

COMPARISONS: Crocidura lea is much smaller than all Sulawesi Crocidura outside of the Small- Bodied Group ( fig. 9 ). Among the Small-Bodied species, only C. baletei and C. tenebrosa are known from the northern peninsula. Crocidura levicula , C. parva , and C. mediocris are apparently restricted to the central core and eastern and southwestern peninsulas ( fig. 25 ). We therefore focus our comparisons on the cooccurring, northern peninsula species. However, first we note that the allopatric C. levicula has a broader skull ( figs. 10 , 26 ; tables 8 , 9), shorter tail, shorter hind feet, and more tail bristles than does C. lea ( figs. 27 , 29 ; table 2 ). Among the Small-Bodied shrews of the northern peninsula, C. lea has a slightly paler and more strongly dorsoventrally bicolored pelage than C. baletei or C. tenebrosa . Both of the latter species are relatively uniform in color, C. baletei being medium brown and C. tenebrosa dark brown. Crocidura lea also has paler skin wherever it is exposed than either C. baletei (somewhat darker) or C. tenebrosa (much darker). Dorsally, the feet of both C. baletei and C. tenebrosa are uniformly dark, whereas the foot color transitions posteriorly from brown at the heel to white or pink at the digits in C. lea ( fig. 27 ). Similarly, the tails of both C. baletei and C. tenebrosa are not obviously bicolored, and both are darker. Tail bristles are present on approximately three-fourths of the tail length in all three species, but they are much more abundant and longer on the tails of C. baletei and C. tenebrosa than in C. lea ( fig. 27 ). Applied hairs on the tail are also much more visible in the two new species than in C. lea . Tail length in C. lea is greater, on average, than in C. baletei , and substantially so compared to C. tenebrosa ( fig. 9 ; table 2 ). The skulls of C. lea are comparable in length, but significantly narrower at the braincase, interorbital region, maxillary process, and to a lesser extent at the rostrum than those of C. baletei and C. tenebrosa ( figs. 10 , 30 ; table 8 ). Crocidura lea occupies distinct morphometric space from the other northern peninsula endemics in bivariate plots of skull length and width and the first two principal components from an analysis of 12 cra-

nial measurements ( fig. 26 ). The C (U3) is larger than I3 (U2) in C. lea , but they are usually subequal in occlusal surface area in C. baletei and C. tenebrosa . The parastyle of P4 is more prominent in C. tenebrosa than in C. lea or C. baletei .

COMMENTS: An 1111 bp cytochrome b sequence from the holotype (USNM 217553) provides strong evidence that the tiny shrews we collected on Mts. Buliohuto and Dako (samples from Mt. Dako were referred to as “ Crocidura pale lea” by Esselstyn et al., 2019) represent this species. Interestingly, we did not find C. lea on Mt. Ambang, our sample site nearest the type locality. Rather, the tiny shrews we collected from Mt. Ambang represent an undescribed spe- cies ( C. tenebrosa ) that does not appear to be a close relative of C. lea . We suspect that C. lea is widespread at relatively low elevations on the northern peninsula, but is displaced by smallerrange, darker-colored endemics in some higherelevation areas ( fig. 13 ; table 3 ). Our only surveys on Mt. Ambang were centered on 1500 m elevation ( fig. 3 ). For BPP species delimitation results, see the C. tenebrosa account below.

Ruedi (1995) reported Crocidura lea from Mt. Rorekatimbo, but we refer those specimens to C. normalis (see below) based on a cytochrome b sequence from Ruedi et al. (1998).

None of our phylogenetic estimates found strong support for the closest relative(s) of Croc- idura lea , but some consistencies are nevertheless apparent. Our mitochondrial analyses placed C. lea as the sister to C. rhoditis and C. pseudorhoditis ( fig. 4 ) or C. elongata ( fig. 5 ), while our UCE species tree placed C. lea as sister to the clade containing C. elongata , C. rhoditis , and C. pseudorhoditis ( fig. 7 ). Other nuclear-based inferences lacked support ( fig. 8 ; supplementary data S6).

SPECIMENS EXAMINED: Mt. Buliohuto ( LSUMZ 38254–38262 , 38271–38274 ; NMV C37692 , C37715 , C37716 , C37720 , C37721 , C37735 , C37744 , C37829 ), Mt. Dako ( LSUMZ 36947– 36950 , 36952 , 36954–36956 , 36958 , 36960 , 36964 , 36968–36972 ), Temboan ( USNM 217553 ).

Figures

FIG. 25. Map of Sulawesi showing localities sampled for shrews. Colored areas enclose localities with known records of members of the Small-Bodied Group of Sulawesi Crocidura.

FIG. 27. 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 three members of the Small-Bodied Group that are from the northern peninsula: A, Crocidura baletei, LSUMZ 36959 (right hind foot); B, C. lea, LSUMZ 38254 (left hind foot); and C, C. tenebrosa, LSUMZ 39268 (right hind foot). Scale bars represent 5 mm. Within each panel, the upper bar applies to the foot and the lower bar corresponds to both tail images.

FIG. 28. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary from the three members of the Small-Bodied Group that are from the northern peninsula:A, Crocidura baletei, LSUMZ 36959; B, C. lea, LSUMZ 38262; and C, C. tenebrosa, LSUMZ 39272.

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. 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. 26. Bivariate plots showing A, variation in the condyloincisive length and braincase breadth and B, the first two axes from a principal components analysis of 12 cranial measurements among all members of the Small-Bodied Group. Loadings and variance explained are given in table 9.

FIG. 29. 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 three members of the Small-Bodied Group that are not from the northern peninsula: A, Crocidura levicula, FMNH 213271; B, C. mediocris, FMNH 210566; and C, C. parva, MVZ 237583. Where two scale bars are present within a panel, the upper applies to the foot and the lower to the tail.

FIG. 30. Box plots showing variation in skull width and tail length from species of the Small-Bodied Group on the northern peninsula of Sulawesi. 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. 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. 3. Plot of the elevational distribution of samples from each of the 12 mountains that comprise the bulk of specimens we examined. Each point represents the median elevation of a specimen we examined. The sample distribution from Mt. Gandang Dewata includes specimens from Salu Tiwo (~200 m). The number of specimens used from each mountain is given above the x-axis and the peak elevation of each mountain is shown on the x-axis.

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 8 Descriptive Statisticsa for Craniodental Measurements (mm) for Species of the Small-Bodied Group of Sulawesi Crocidura

	C. baletei	C. lea	C. levicula	C. mediocris	C. parva	C. tenebrosa
Condyloincisive length	17.68 ± 0.285 (17.25–18.07) 7	17.54 ± 0.293 (17.09–18.02) 21	16.58 ± 0.545 (15.56–17.58) 19	17.31 ± 0.643 (16.11–18.54) 25	16.55 ± 0.372 (15.81–17.34) 26	17.66 ± 0.216 (17.37–17.98) 8
Braincase breadth	8.46 ± 0.152 (8.27–8.65) 7	7.71 ± 0.135 (7.49–7.98) 21	7.98 ± 0.287 (7.51–8.49) 19	7.85 ± 0.246 (7.45–8.34) 25	7.47 ± 0.145 (7.09–7.72) 26	8.36 ± 0.166 (8.09–8.56) 8
Interorbital width	4.08 ± 0.058 (3.98–4.15) 7	3.89 ± 0.123 (3.69–4.14) 21	3.88 ± 0.136 (3.71–4.11) 19	3.88 ± 0.125 (3.68–4.14) 25	3.73 ± 0.109 (3.42–3.89) 28	4.12 ± 0.104 (4.04–4.26) 8
Rostral length	7.05 ± 0.242 (6.78–7.49) 7	6.86 ± 0.208 (6.48–7.27) 22	6.48 ± 0.22 (6.05–6.92) 19	6.91 ± 0.396 (6.37–7.7) 25	6.48 ± 0.182 (6.08–6.86) 28	7.09 ± 0.136 (6.85–7.22) 8
Postpalatal width	3.19 ± 0.088 (3.0–3.26) 7	3.13 ± 0.10 (2.95–3.33) 21	3.01 ± 0.101 (2.86–3.22) 19	3.09 ± 0.106 (2.8–3.3) 25	2.96 ± 0.113 (2.67–3.18) 28	3.2 ± 0.077 (3.12–3.33) 8
Rostral width	2.41 ± 0.162 (2.17–2.61) 7	2.4 ± 0.146 (2.13–2.68) 21	2.28 ± 0.125 (2.07–2.53) 19	2.34 ± 0.169 (2.13–2.67) 25	2.32 ± 0.147 (2.09–2.63) 28	2.55 ± 0.117 (2.44–2.74) 8
Postpalatal length	8.01 ± 0.124 (7.79–8.14) 7	8.08 ± 0.15 (7.81–8.42) 21	7.56 ± 0.265 (7.05–8.1) 19	7.9 ± 0.255 (7.34–8.54) 25	7.62 ± 0.197 (7.12–7.95) 24	8.06 ± 0.13 (7.89–8.26) 8
Condyle to glenoid fossa	7.25 ± 0.156 (7.03–7.43) 7	7.21 ± 0.162 (7.01–7.56) 21	6.83 ± 0.211 (6.5–7.2) 19	7.06 ± 0.22 (6.5–7.45) 25	6.94 ± 0.151 (6.71–7.17) 26	7.24 ± 0.077 (7.11–7.35) 8
Upper toothrow length	7.67 ± 0.118 (7.49–7.82) 7	7.52 ± 0.235 (7.13–7.98) 22	7.15 ± 0.222 (6.73–7.62) 19	7.54 ± 0.369 (6.81–8.28) 25	7.07 ± 0.187 (6.7–7.45) 28	7.62 ± 0.178 (7.34–7.84) 8
P4 to M3 length	4.41 ± 0.077 (4.33–4.52) 7	4.23 ± 0.135 (3.98–4.56) 22	4.09 ± 0.132 (3.87–4.33) 19	4.24 ± 0.201 (3.85–4.58) 25	3.98 ± 0.121 (3.73–4.3) 28	4.36 ± 0.098 (4.23–4.52) 8
M2 to M2 labial width	5.22 ± 0.063 (5.14–5.32) 6	5.03 ± 0.165 (4.61–5.37) 22	4.83 ± 0.174 (4.56–5.23) 19	5.0 ± 0.224 (4.58–5.48) 25	4.66 ± 0.137 (4.41–4.92) 28	5.25 ± 0.128 (5.15–5.49) 8
Palatal width	2.14 ± 0.074 (2.04–2.24) 6	1.98 ± 0.115 (1.8–2.32) 22	2.02 ± 0.105 (1.78–2.24) 19	1.98 ± 0.068 (1.85–2.1) 25	1.89 ± 0.102 (1.73–2.11) 26	2.08 ± 0.115 (1.92–2.24) 8

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

TABLE 9 Results of Principal Components Analysis of Craniodental Measurements of the Small-Bodied Group of Crocidura

	Component 1	Component 2
Variablesa
Condyloincisive length	0.6818	0.2724
Braincase breadth	0.2456	-0.8299
Interorbital width	0.1167	-0.2702
Rostral length	0.3441	0.0190
Postpalatal width	0.1036	-0.0849
Rostral width	0.0779	-0.0082
Postpalatal length	0.2750	0.2500
Condyle to glenoid fossa	0.2073	0.1481
Upper toothrow length	0.3440	0.0510
P4 to M3 length	0.1880	-0.0904
M2 to M2 labial width	0.2256	-0.1674
Palatal width	0.0534	-0.1820
Proportion of variance	0.8056	0.0817
Cumulative proportion	0.8056	0.8873

a Table entries for variables are component loadings.