Institutions and Specimens:

The definitions of species documented here are determined from examination of specimens stored in the following institutions: the American Museum of Natural History, New York (AMNH); Natural History Museum (formerly British Museum of Natural History), London (BMNH); Field Museum of Natural History, Chicago (FMNH); Museum Zoologicum Bogoriense, Cibinong, Java (MZB; now the Indonesian National Museum of Natural History, also known as the Research Center in Biology–Lembaga Ilmu Pengetahuan Indonesia); Naturhistorisches Museum Basel, Switzerland (NMB); Nationaal Museum of Natural History Naturalis (formerly the Rijksmuseum van Natuurlijke Historie), Leiden (RMNH); National Museum of Natural History, Smithsonian Institution, Washington, D.C. (USNM). Specimens referenced by catalog number in gazetteers, tables, text, and figure legends are preceded by one of these acronyms. Some specimens are also cited by Archbold Sulawesi Expedition field numbers (ASE).

Many of the generic and specific traits described here are those associated with a dry skin (usually stuffed as a museum study specimen) and an associated skull—one type of standard museum preparations. Color descriptions of fur, ears, feet, and tail of E. leucura are derived from those museum specimens—Musser's field work did not take him to the geographic regions where that species resides. Color descriptions of E. centrosa come primarily from his field journals (stored in Mammalogy Archives, AMNH) where he recorded coloration and other details of freshly caught rats. His collection also includes fluid-preserved whole specimens or skinned carcasses that were initially fixed in 10% formalin, soaked for several days in water, and finally stored in 70% ethanol. From this material comes descriptions of stomach morphology and topography of palmar and plantar regions.

Measurements:

Values for external dimensions are from two groups of specimens. One consists of samples Musser collected in central Sulawesi. For each of these specimens he measured total length; length of tail (LT); length of the dorsal distal white tail segment (taken from the distal border of the basal brown portion to tip of the tail along the dorsal surface); length of hind foot, including claw (LHF); and length of ear, from notch to crown (LE). He took these measurements soon after the rat was caught, and also obtained a value for body weight (WT, in grams).

The second group contains specimens in museums caught and prepared by other collectors. They recorded total length, lengths of tail and hind foot, sometimes length of ear, but not weight. Musser used their value for length of tail, and measured length of the distal white tail segment on the dry study skin; value for ear length, when available, was sometimes ignored because it was unclear how preparators measured that dimension. Values for length of hind foot were usually ignored and instead Musser measured those distances on the dry skins. He also did not use total length from either group in any analyses, but subtracted length of tail from it to obtain a value for length of head and body, which is a more useful metric.

In the laboratory, several measurements were made on specimens from both groups. The number of scale rings per centimeter on the tail was counted about one-third the distance from its base. To measure lengths of overfur and guard hairs on the dorsum, Musser placed a ruler at a right angle to the skin surface on the back near the rump and recorded the approximate mark where ends of the bunched hairs rested; the technique is unsophisticated and the results imprecise, but provides a descriptive estimate of lengths for those pelage constituents.

Using handheld dial calipers, Musser measured the following cranial and dental dimensions to the nearest 0.1 mm; shorter dimensions (BBP, LIF, BIF, BMF, LB, and dimensions of toothrows and individual molars) were measured under a dissecting microscope. Dimensional limits are illustrated in figure 1; abbreviations are used in the tables.

Fig. 1.

An adult Bunomys chrysocomus illustrating limits of cranial and dental dimensions measured. Additional definitions are provided in the text.

In the multivariate analyses used to generate principal-components and discriminant-function graphs, values for alveolar length of the maxillary molar row (ALM1–3) instead of crown length of the molar row (CLM1–3) were used. The molars are very small, particularly the third molar, and some were lost when skulls were cleaned. By using alveolar length, a complete set of variables for the analyses could be employed, even when teeth were missing, and the largest possible sample sizes assembled.

Age and Sex:

Specimens could consistently be placed into one of the following age groups: old adult (body size usually among the largest in a sample; clothed in adult pelage; occlusal surfaces of molars worn nearly to tops of roots so cusp patterns are obliterated, the crowns worn into shallow basins with either intact or eroded margins); adult (body size among the largest in a sample; covered in adult pelage; molars worn; occlusal surfaces retain outlines of major cusps, but their enamel margins are worn low so that dentine is broadly exposed forming shallow basins; labial cusplets obliterated); young adult (body size usually smaller than older adults; covered in fresh adult fur; molars slightly worn; enamel borders of cusps much higher than the enclosed dentine, which has a restricted exposure; laminae, cusps, and labial cusplets are discrete; juvenile (body size among smallest in a sample; covered in juvenile pelage, which is easily recognizable compared to the adult coat; upper and lower third molars unerupted or if erupted usually unworn).

These roughly defined age groups are unequally represented among samples: old adults and juveniles are scarce, adults and young adults are most common. Old adults, adults, and young adults were combined into samples from which cranial and dental measurement values were obtained for multivariate analyses and univariate descriptive statistics. Recognition of relative age classes was important for identifying relative age of holotypes and gauging the position of particular specimens showing incongruous distributions in principal-components and canonical-variate ordinations.

Males and females were not separated in any of the statistical analyses. Examined side by side, size differences in adult skulls of males and females within a single species collected from the same area appeared negligible. This observation was reinforced by results from determining significance of differences between means for cranial and dental variables of each sex (t-test) in samples of Echiothrix centrosa and E. leucura (table 1). Within each of the species, differences between means were not significant across all variables—sex is a trivial contribution to intrasample nongeographic variation of cranial and dental variables.

Table 1

Differences in Means of Cranial and Dental Variables between Sexes in Samples of Echiothrix centrosa and E. leucura

Mean ± 1 SD are listed; probability values (P) are derived from t-tests. Samples (consisting of young-to-old adults) from different localities had to be combined to obtain a sufficiently large number of specimens for testing the significance of sexual differences.

Results of principal-components analysis of each species (not illustrated here) did not reveal a different pattern in variation among the cranial and dental variables due to sex. The distribution of specimen scores projected onto first and second components for each species produced a single cloud of thoroughly intermixed points for males and females—polygons enclosing maximum dispersion of scores representing each sex, and ellipses outlining 95% confidence limits for cluster centroids broadly overlapped.

Weak sexual dimorphism in cranial and dental variables generally characterizes nongeographic sexual variation among muroid rodents. For examples of sigmodontines, see Carleton and Musser (1989, 1995 [Microryzomys and Oligoryzomys], Carleton et al. (1999 [Sigmodon]; 2009 [Oecomys]), Voss (1991 [Zygodontomys]), and Emmons and Patton (2012 [Juscelinomys]); for murine examples, see Carleton and Robbins (1985 [Hybomys]), Carleton and Martinez (1991 [Dasymys]), Carleton and Van der Straeten (1997 [Lemniscomys], Maryanto (2003 [Rattus argentiventer]), Carleton and Byrne (2006 [Otomys]), Carleton and Stanley, 2005, 2012 [Hylomyscus and Praomys]), Helgen and Helgen (2009 [Pseudohydromys]), Musser (unpublished data [Bunomys, Margaretamys, Rattus facetus, and Coccymys]), Heaney et al. (2006 [Apomys, Batomys, and Limnomys]), and Balete et al. (2012 [Soricomys and Archboldomys]). A striking exception is the sigmodontine Oryzomys couesi (Carleton and Arroyo-Cabrales, 2009).

Statistical Analyses:

Standard univariate descriptive statistics (mean, standard deviation, and observed range) were calculated for population samples (identified in table 2) as well as for each species and are listed in tables throughout the text. Principal-component and discriminant-function analyses were computed using original cranial and dental measurements transformed to natural logarithms. Principal components were extracted from a variance-covariance matrix, and canonical variates were extracted from the discriminant-function analyses; loadings (correlations) of the variables are given as Pearson product-moment correlation coefficients between the extracted principal components or canonical variates and the log-transformed input variables. Probability levels denoting the significance of the correlations in both kinds of analyses are unadjusted. Analyses are based on 16 cranial and two dental measurements from intact skulls of adults (young to old). The statistical packages in SYSTAT 11 for Windows, Version 11 (2005), were used for all analytical procedures.

Table 2

Population Samples Employed in Univariate and Multivariate Analyses of Cranial and Dental Variables for Species of Echiothrix

Localities, along with elevations and geographic coordinates, are referenced in the gazetteers and marked on the distribution map. Brackets enclose total number of specimens for each species. Specimens measured are identified in footnote.

Anatomy:

Terminology follows Brown (1971) and Brown and Yalden (1973) for particular external features of the head and limbs; Bugge (1970) for cephalic arteries; Wahlert (1985) for cranial foranima; Carleton (1980), Musser and Newcomb (1983), Carleton and Musser (1984), Musser and Heaney (1992), and Voss (1988) for cranial morphology; and Rinker (1954), Turnbull (1970), and Satoh and Iwaku (2006, 2008) for cranial musculature. Names of cusps and cusplets of maxillary (upper) and mandibular (lower) molars are indicated in figure 9 where sources of the terminology are explained in the legend.

Stomach Contents:

Musser recorded in his field journal the contents found in stomachs of some freshly caught rats. Some samples were preserved in ethanol, which he examined later in the laboratory under a dissecting microscope. He supplemented this material by extracting stomachs from fluid-preserved animals. Stomachs were removed by severing the posterior end of the esophagus and the anterior section of the duodenum. The isolated stomach was bisected along the midfrontal plane; contents were transferred to a white ceramic dish and examined with a dissecting microscope. In addition to remains of ingested foods, stomachs contained soft and spinous hairs, most likely ingested during grooming. Stomachs emptied in the field are still attached to the gasterointestinal tract of carcasses preserved in fluid at AMNH. Those stomachs extracted in the laboratory are stored, with their contents, in leakproof vials in the fluid collection at AMNH. The stomachs illustrated in figure 11 were fully distended and dissected from adults.

One captive Echiothrix centrosa was supplied with a range of forest foods to determine what would be accepted or rejected.

Geography:

The island of Sulawesi consists of a central region from which four arms, or peninsulas radiate (see distribution map in fig. 2): the northern peninsula, which ends in a northeastern jog; the eastern peninsula; the southeastern peninsula; the southwestern peninsula. We use these informal labels when describing distributions of the two species of Echiothrix over the island, and refer to the central portion as Sulawesi's core, or simply “core.”

Fig. 2.

(above) The island of Sulawesi and environs, showing Sulawesi's four peninsulas and its “core” or central portion. Boundaries separating regions of endemism discussed here are indicated by dashed lines: SM-D  =  lowland reaches of the Sungai Onggak Mongondaw and Sungai Onggak Dumoga; SB-DL  =  lowlands of the Sungai Bone and Danau Limboto; TD  =  Tempe Depression. (opposite page) Collection localities for samples of Echiothrix leucura and E. centrosa. Numbers key to localities described in the gazetteer. Note the range of E. leucura, which is east of SM-D.

Fig. 2.

Continued.

In the text we refer to the west-central highlands or west-central mountain block, which forms the western portion of Sulawesi's core. It is the region of foothills, peaks, and interior valleys situated above 100 m and lying roughly west of Danau Poso and extending from the Palu area in the north to Pegunungan Latimojong in the south. For our purposes here it excludes the coastal strip along the shores of the Makassar Strait simply because no nonvolant mammals have been collected there. A suite of mammals, from shrews to rats, have been collected only in the west-central region: a few species are found in tropical lowland evergreen rain forest covering lower altitudes on foothills and in valleys, but most occur at higher altitudes in montane forests (Musser et al., 2010).

Another area of endemicity of relevance to distributions of Echiothrix is the northeastern tip of the northern peninsula east of Gorontalo (see the distribution map in fig. 2).

We use the Indonesian terms sungai (stream or small river), kuala (stream discharging directly into the sea), danau (lake), gunung (mountain), pegunungan (mountain range), pulau (island), kepulauan (archipelago), selat (strait), tanjung (cape) and teluk (bay).

Localities from which samples were collected, along with the institutional acronyms and catalog number of each specimen examined, are listed in a gazetteer of collection localities for each species. No specimen of Echiothrix is listed that Mussser did not personally examine. Descriptions of locality and elevations (given here in meters but may have been originally recorded in either meters or feet) were taken from labels attached to skins. These basic data were enhanced where necessary by relevant information from field journals, other archival material, and published expeditionary accounts and gazetteers; sources are cited in the locality entry.

Spelling of locality names are those approved by the United States Board on Geographic Names in the Gazetteer of Indonesia, Third Edition, volumes 1 and 2, published by the Defense Mapping Agency, Washington, D.C., in 1982 (referenced as USBGN Indonesia, 1982). Some localities could not be located in that gazetteer but were found on the topographic map sheets described below; other spellings come from Musser's field notes.

Coordinates for some collection localities were found in USBGN Indonesia (1982) or the Gazetteer of Celebes published in 1944 through the Hydrographic Office of the United States Navy Department (HOUSND Celebes, 1944). Coordinates for most of Harry C. Raven's collection localities were estimated from his personal copy of a Dutch map of Celebes on which he had marked his camp sites and travel routes (Overzichtskaart van het eiland Celebes, Schaal 1∶1,250,000, “met aanduiding van de politieke indeeling, de organisatie van het bestuur, de bestaande en nog aan te leggen verkeerswegen en van de groote cultuur- en industrieele centra” (“indicating the political divisions, the organization of the administration, the existing and the still to be built road system, and the large cultural and industrial centers”). Samengesteld op last van de N.I. Regeering (“Created at the request of the N.I. [ =  Nederlands Indië  = Dutch East Indies] Government”). Published in 1909), and referred to in the text as “Raven's map.” Coordinates for Musser's collection localities, as well as height above sea level for places for which altitudes were not recorded by collectors, were estimated from “JOINT OPERATIONS GRAPHIC-GROUND” topographic maps, scale 1∶250,000, compiled by Mapping and Charting Establishment RE, 1969, and published by the Director of Military Survey, Ministry of Defence, United Kingdom, 1970, or by the Army Map Service, Washington, D.C. (sheets NA 51-9 [1967], NA 51-12 [1967], NA 51-14 [1967], SA 50-8 [1971], SA 51-1 [1970], SA 51-5 [1967], and SA 51-14 [1967], SB 50-8 [1966], SB 51-1 [1970]).

Forests:

The tropical rain forests embracing the habitats of Sulawesi's species of Echiothrix will be described broadly in the accounts of species by applying three of the forest formations categorized by Whitmore (1984): tropical lowland evergreen rain forest, tropical lower montane rain forest, and tropical upper montane rain forest. Whitmore's descriptions of these different forest landscapes are illuminating and, as he notes, an extension and elaboration of P.W. Richards (1952) classic work The Tropical Rain Forest, which readers will also find informative (a second edition was published in 1996).

Institutions:

Paratypes of the new species of Polyplax are deposited in the collections of the American Museum of Natural History, New York (AMNH); the Natural History Museum, London (BMNH); private collection of L.A. Durden (LAD), the Museum Zoologicum Bogoriense, Cibinong, Java (MZB); and the National Museum of Natural History, Smithsonian Institution, Washington, D.C. (USNM). The holotype and allotype are deposited in the USNM.

Procedures and Abbreviations:

Host shrew rats were collected by G.G. Musser. Lice were removed from pelts by L.A. Durden. Description of the new species of louse presented in this paper follows the format and terminology of morphological structures and setae used by Musser et al. (2010). Drawings of entire lice conventionally illustrate dorsal structures to the left of the midline and ventral features to the right. Measurements were made using a calibrated micrometer inserted into the eyepiece of a high-power phase-contrast Olympus BH2 microscope. Drawings and measurements of lice were made by L.A. Durden.

Abbreviations for anatomical structures used in the description of the new species of louse are as follows:

Type Species:

Echiothrix leucura Gray, 1867: 600 (fixation by monotypy; see ICZN, 1999: 71, article 68.3).

Emended Diagnosis:

A genus in Murinae within Muridae (as delimited by Musser and Carleton, 2005) that is distinguished from all other described murine genera by the following combination of traits: (1) species terrestrial in habitus; (2) dorsal pelage covering head and body dark gray or bluish gray, coarse and bristly, overhair coat composed mostly of wide flexible, and channeled spines intermixed with slender soft hairs; (3) ventral coat white (some individuals with russet stain), coarse but softer than dorsal pelage, demarcation between upperparts and underparts sharp and conspicuous; (4) muzzle elongate, mask encircling each eye, ears gray and large relative to body size; (5) tail typically longer than combined length of head and body (ranges of mean values for LT/LHB are 103.8%–116.0% for E. leucura, and 112.8%–126.0% for E. centrosa), tail scales moderately large (7–8 rows per cm), the rings of scales slightly overlapping, with one, two, or three hairs associated with each scale (tail appears scantily haired), basal one-fourth to one-half dark gray to brownish gray on dorsal surface and sides, rest of tail white (ranges for dorsal white length–tail length is 47%–67% for E. leucura and 44%–73% for E. centrosa); (6) forearms short and slender, front feet moderately large but delicately built, claws sturdy but not elongate, digits white, dorsal surfaces of carpal regions white or speckled with patches of gray, three central digits of front foot longer than lateral digit, palmar surface adorned with three interdigital pads, a thenar, and a hypothenar; (7) hind foot elongate, digits white, dorsal surfaces of metacarpal regions white or speckled with patches of gray, three middle digits very long compared with much shorter lateral digits, plantar surface with full complement of plantar pads (four interdigitals, a thenar, and a hypothenar), but thenar and hypothenar very small relative to plantar surface; (8) two pairs of teats, both inguinal in position; (9) testes large relative to body size (16%–23%); (10) symphysis of mandible flexible, so tips of lower incisors can be spread apart up to 7 mm; (11) rostrum long and slender, interorbital and postorbital margins bounded by moderately high ridges, zygomatic arches moderately sturdy and flare from sides of skull, posterior zygomatic root situated low on braincase, braincase boxlike (wide and deep), occiput deep, no cranial flexion; (12) zygomatic plate moderately wide, its anterior margin projecting beyond dorsal maxillary root of zygomatic arch, its posterior edge even with the anterior margin of the first upper molar; (13) squamosal intact, not perforated by a subsquamosal foramen; (14) alisphenoid struts typically absent; (15) incisive foramina long and wide, set in middle of diastemal region; (16) molar rows parallel or bowed toward midline, bony palate long with its posterior margin projecting well beyond the molar rows to form a bony shelf, palatal surface with moderately deep palatine grooves, posterior palatine foramina at level of either second or third upper molars; (17) moderately long and wide sphenopalatine vacuities; (18) pterygoid plates appear absent but are reduced to slim and inconspicuous ridgelike vestiges, narrow platforms undefined by discrete margins, and apparently transformed into a vertical component in the outer wall of the mesopterygoid fossa in some specimens; (19) auditory bulla moderately large relative to skull size, the ectotympanic (bullar) capsule covering all but a narrow wedge of periotic, posterodorsal wall of carotid canal formed by bullar capsule; (20) large stapedial foramen, no sphenofrontal foramen or squamosal-alisphenoid groove, indicating a carotid arterial pattern widespread within Murinae (character state 2 of Carleton, 1980; pattern 2 described by Voss, 1988); (21) dentary elongate, long and narrow ramus (diastema) between incisor and molar row, very small coronoid process, large condyloid (articular) process, end of alveolar capsule forming large labial bulge just posterior to coronoid proces; (22) upper incisors typically white (dentine and enamel unpigmented), small and short relative to skull size, emerging from rostrum at a right angle (orthodont), each anterior face with two shallow grooves; (23) each lower incisor long and awl shaped with elongate wear facets, anterior faces smooth, dentine white and enamel either white or tinted pale yellow; (24) maxillary molars with three roots, mandibular molars with two; (25) molars brachydont, cusp rows forming cuspidate occlusal patterns that transform into basins with only moderate wear, third molar very small relative to others in toothrow; (26) no cusp t7 on upper molars, and no other occlusal embellishments (such as an enamel ridge projecting from anterolingual surface of cusp t8 anteriorly to posterior margin of lingual cusp t4, a labial enamel ridge connecting anterolabial margin of cusp t9 with posterolabial margin of cusp t6, or a comparable but shorter ridge projecting from the anterior surface of cusp t5 to meet the posterior margin of cusp t3 near the cingulum, all typical of some other murines with more complicated enamel occlusal patterns—the New Guinea Coccymys is an example [Musser and Lunde, 2009]), posterior cingulum present in one species but absent in the other; (27) anteroconid formed of large anterolingual and anterolabial cusps, anterocentral cusp absent, anterolabial cusp present at low frequency or missing from second and third lower molars depending upon the species, anterior labial cusplets not present on any lower molars, but posterior labial cusplet present at a low frequency on most teeth, posterior cingulum present on first and second lower molars in one species, missing from those molars in another; (28) stomach unilocular-pouched, glandular epithelium confined to a pouch situated on the greater curvature within the lumen of the stomach; (29) sperm head long and sickle shaped, with single apical hook that lacks ventral processes, spermatozoal tail long; (30) karyotype, 2N  =  40, FNa  =  72 (total of autosomal arms) and FNt  =  75 (total number of arms, including XY), for E. centrosa.

Contents:

Two species are currently recognized, Echiothrix leucura and E. centrosa, both endemic to Sulawesi.

Between 1867 and 1920, Echiothrix was regarded as monotypic with E. leucura, the type species, occurring east of Gorontalo in the northeastern end of the northern peninsula (Alston, 1876; Jentink, 1883; Thomas, 1896b; Trouessart, 1897; Meyer, 1899). In 1921, Miller and Hollister (1921: 67) described two additional species, both from the central part of Sulawesi. Echiothrix centrosa was based on samples from “the interior of Middle Celebes,” the Besoa region, Gimpu, Tuare, and Winatu. Echiothrix brevicula was applied to a sample from Pinedapa, “about 5 miles inland from the Gulf of Tomini, near Mapane, Middle Celebes.” Tate (1936), in his treatise covering some Indo-Australian Murinae, discussed E. leucura and referred to the two taxa described by Miller and Hollister as species. Subsequent rodent compendia and regional lists of species, however, demoted centrosa and brevicula to either subspecies of E. leucura (Ellerman, 1941; Laurie and Hill, 1954) or synonyms (Corbet and Hill, 1992; Musser and Carleton, 1993). By 2005, Musser and Carleton had recognized two species, E. leucura and E. centrosa, which are the two we define here. Geography, morphometric differences in cranial and dental variables, and different cusp patterns of maxillary and mandibular molars comprise the anatomical distinctions between the two species. The outlines of geographic range and phenetic interpretation of species diversity in Echiothrix sketched here is a hypothesis that should be tested by analyses of DNA sequences.

The first of the two accounts of species that follow consists of a description of Echiothrix leucura, the type species of the genus. Musser has not worked in the region where this species occurs and knows it only from his study of material held in museum collections. The geographic and morphological traits characteristics of E. leucura form the standard to which comparable characteristics of E. centrosa will be compared.

Musser did encounter E. centrosa in his fieldwork and the report on that species derives from material he collected (skins, skulls, rats preserved in fluid, and chromosomal preparations), descriptions of freshly trapped animals recorded in his field journals, and specimens obtained by other collectors now stored in collections of museums (skins and skulls). Information on spermatozoal and stomach morphologies, karyotype, and external characteristics of juveniles will be included—this kind of information is not available for E. leucura.

The accounts cover the following information: (1) description of the holotype and type locality; (2) emended diagnosis; (3) reference to the gazetteer where specimens are identified; (4) etymology of the scientific name (5) summary of geographic and elevational distributions; (6) description; (7) comparisons with other species; (8) geographic variation in phenetic characters; (9) allocation of a synonym (relevant to E. centrosa).

Holotype:

“No. 1499,” which is Gray's catalog number. To learn more about this specimen, Musser queried Paula Jenkins at the Natural History Museum in London, who wrote (in litt., 1999) that the “specimen has apparently never been registered using the four-digit system, however, these Gray catalogue numbers are also traditionally accepted as register numbers.” “It is,” she continued, “listed in one of Gray's catalogues … as: ‘1499 Skull a. the specimen fig. [the skull was illustrated in Gray, 1867: 599] Skin in a bottle in the Colln.’ There is no locality given here.” Paula also checked Thomas' catalog and noted that “no number is given; the entry reads: ‘a. Sk. ad. male Australia. Type of genus and species.’” The identity of the collector was not recorded. Musser examined the holotype but at the time he took no measurements. The holotype is an adult male and consists of a dry skin and skull. Except for the damaged head, the skin is whole. The skull is incomplete (fig. 3): anterior portion of the nasals, nearly all of the skull behind the orbit, and posterior half of each zygomatic arch are missing. The mandible is intact; upper and lower incisors and molars are present. The few measurements that could be made on the holotype are listed in table 3.

Table 3

Age, Sex, and Measurements (mm) for Holotypes Associated with Species of Echiothrix^a

Type Locality:

Manado (01° 30′ N, 124° 50′ E; locality 1 in gazetteer and fig. 2), coastal plain near sea level, the northeastern tip of the northern peninsula of Sulawesi, Propinsi Sulawesi Utara, Indonesia.

Gray (1867) indicated the specimen he described to have come from “Australia.” No other reference to the actual provenance of the specimen exists. Paula Jenkins could not locate any additional information in the archives of the Natural History Museum (London). Subsequent researchers recognized that the holotype was not collected in Australia. Sixteen years after Gray's description was published, Jentink (1883: 177) reported two additional specimens:

Tate (1936: 585–586) discussed specimens in the American Museum of Natural History that had been collected by G. Heinrich at Rurukan and noted that this locality is “at the extreme northeast of the Celebes and within a few miles of Menado, whence came the specimen in the Dresden Museum alluded to by Jentink,” and wrote that “In absence of evidence to the contrary the type locality of E. leucura may be restricted to Menado, north Celebes, making our series practically topotypical.”

Emended Diagnosis:

Traits associated with external and cranial morphology as enumerated in the generic diagnosis also characterize Echiothrix leucura. The species differs from E. centrosa in possessing (1) a longer body and hind foot, but a shorter tail in relation to length of head and body; (2) a larger skull (as indexed by the greater mean values for occipitonasal and rostral lengths; interorbital breadth; height and breadth of braincase; and lengths of diastema, bony palate, and postpalatal region), but shorter incisive foramina and narrower rostrum, bony palate, and mesopterygoid fossa; (3) larger molars and slightly more complex cusp patterns; (4) cusp t3 occurring at a higher frequency on second upper molar, a posterior cingulum typically present on first and second upper molars, (5) an anterolabial cusp present at a low frequency on second and third lower molars, posterior labial cusplets on all lower molars in some specimens, and a posterior cingulum present on first and second lower molars in most individuals surveyed.

Specimens Examined:

Total 25 (see Gazetteer and Specimens).

Etymology:

The species name leucura is derived from the Greek leukos meaning “white.” Whether Gray meant to highlight the white ventral coat of Echiothrix or its white incisors (“cutting-teeth white,” as Gray, 1867: 300, described them) is unknown, although we suspect the latter. Many species of murines have white underparts but not many possess incisors with white enamel layers.

Geographic and Elevational Distributions:

Voucher specimens indicate Echiothrix leucura is endemic to the northeastern end of the northern peninsula east of the Gorontalo region (00° 31′ N, 123° 03′ E; see the map in fig. 2). All specimens come from the mainland between coastal lowlands and approximately 1000 m (see gazetteer), an elevational interval that would be covered by tropical lowland evergreen rain forest.

The geographic range of E. leucura is concordant with the distributions of several other mammalian species: the macaque Macaca nigra (Fooden, 1969; Groves, 1980, 2005); and the murids, Bunomys fratrorum, Taeromys taerae, Rattus xanthurus, and R. marmosurus (Musser and Carleton, 2005, unpublished ms.).

Description:

Gray (1867: 600) provided a short description of E. leucura:

His account does not do justice to the species. Echiothrix leucura is moderately large (table 4) with a lean body, long head, bristly dark gray or bluish gray upperparts, white underparts, mostly white tail that is longer than head and body, delicate front legs and small feet but robust hind legs with large and elongate hind feet, and very large ears (fig. 4; Musser, 1990: fig. 3). The skull shows specializations such as a long and slender rostrum and a lack of pterygoid plates; the incisors are white or cream, and the molars are very small relative to skull size. The following description is drawn from adults; we have not seen examples of juvenile E. leucura, but their external characteristics are likely similar to juvenile E. centrosa, which are described in the account of that species.

Fig. 4.

Reproduction of Meyer's (1899) color plate of “Craurothrix leucura” ( =  Echiothrix leucura) rendered from animals collected at Tomohon (locality 5 in gazetteer and on map in fig. 2).

Table 4

Descriptive Statistics for Measurements (mm) of Lengths of Head and Body, Tail, Hind Foot, and Ear, and for Weight (g) Derived From Samples of Adult Echiothrix leucura and E. centrosa^a

Mean ± 1 SD, observed range (in parentheses), and size of sample are provided. Mean values were used to compute LT/LHB. Specimens measured are listed in footnotes.

Fur: The glossy dorsal coat of adults is harsh and bristly to the touch (not rigidly spiny as in hedgehog fur) and 15–20 mm long. It is composed of underhairs (or “wool” hairs; Voss, 1988) that form a thin underfur layer, and longer overhairs (also called “awns”; Voss, 1988) comprising the overfur. The underhairs are soft, fine, wavy, and unpigmented along their entire lengths. The overfur layer consists mostly of wide and flat flexible spines, each with a channel extending along the dorsal surface, and a sharp tip. The base of each spine is unpigmented but the remainder is gray, which ranges in tone from pale gray near the unpigmented base to dark gray distally to the tip. In adults showing molt from old to new fur, the old spines have faded to straw brown, but those in the new layer proliferating through the skin are dark bluish gray. Scattered among the spines are softer thin hairs, each unpigmented except for a gray subterminal band. Guard hairs are inconspicuous because they are scattered throughout the coat and barely extend beyond the overfur layer; each is thin and round with an unpigmented base, long blackish subterminal band, and silvery tip. Overall, the fresh dorsal fur is dark gray or dark bluish gray frosted with white along the back but lightens to gray on sides of the head and body; old, worn pelage fades to pale straw brown.

The ventral coat of adults is 8–10 mm long on animals from low elevations but 10–13 mm thick over rats from higher places and consists of underhairs and overhairs but no guard hairs. Hairs forming the underfur are soft, fine, and wavy; those constituting the overfur are narrow, flat, and soft spines, each with a dorsal channel from base to near the tip. Texture of the coat is soft to slightly harsh to the touch but not spinous. Underhairs and overhairs are unpigmented in most specimens, so the ventral pelage, from tip of the muzzle to base of the tail, is overall white and sharply demarked from the gray dorsal coat. A few animals from Temboan show buffy or buffy orange patches on the chest and abdomen.

The white ventral coat is best appreciated in living rats or freshly prepared specimens. Some museum preparations, especially study skins stored since the early 1900s, appear pale yellow because the yellow dry skin shows through the fur or the hairs are stained with fatty oils (some of the skins from Temboan, for example, are obviously stained with yellowish deposits, so the entire animal appears to have a yellowish tint) and the underparts are yellow-orange (oily debris adheres to the hairs, and some skins are greasy yellow because subcutaneous fat was either not or incompletely removed before the skin was stuffed).

Fur covering the head of adults is pigmented like that clothing the body; throat and cheeks are white, chromatically indistinguishable from chest and abdomen. Rhinarium and lips are pink. Behind each ear is a crescent-shaped pale gray patch of soft, fine and short hairs that provides a whitish-gray crescent-shaped tuft around the base of each ear. The only obvious facial pattern is formed by blackish-brown eyelids and a circle of darker hairs around each eye, which on some individuals are more expansive and form a mask. All species have an array of mystacial, submental, superciliary, subocular, genal, and interramal vibrissae adorning the head; the longest mystacial extend beyond the ears when laid back over the head (see Brown, 1971, for descriptions of these sensory hairs and terminology). Some of the hairs lack pigment (appearing silvery), the rest are black or dark brown, and all have glossy surfaces.

Ears: Pinnae are very large relative to size of head and body (table 4). We have not seen living E. leucura, but the pinnae appear and feel rubbery in freshly caught E. centrosa, and while they seem naked, they are covered on inner and outer surfaces by short, fine, dark hairs that form a short and inconspicuous fringe along the dorsal internal rim of each pinna. Color of the ears is glossy dark gray with a pinkish tinge in living E. centrosa. We suspect texture and coloration to be similar in live E. leucura. Dried ears of stuffed museum skins lack the rubbery texture of the live animal and have dried to dark brown.

Tail: In samples of adults, average length of tail exceeds combined head and body length (LT/LHB  =  103.8%–116.0%; table 4). The tail is squarish in cross section and bicolored: in living animals, dorsal and lateral surfaces of the basal one-third to one-half range from dark gray to blackish gray, the rest of the tail, including the entire ventral surface, is glistening white (dorsal white length/tail length  =  47%–67%; table 5). In some material collected in the late 1800s and early 1900s, the pigmented basal portion of the tail has darkened to black and the white region altered to pale yellow, reflecting stain from the subcutaneous fat in the tail. Gray (1867: 600), for example, wrote of the holotype, “tail yellow, black at base.” White tail segments are yellowish in all of H.C. Raven's material (stored at USNM), which was collected in the early 1900s. Slightly overlapping rings of moderately large scales (7–8 scale rings per cm, counted on the basal third of the tail) cover the tail. One, two, or three fine hairs (as long as one or two scales) emerge from beneath each scale. The tail appears to be scantily haired because the hairs are fine, inconspicuous, and vary in number per scale (instead of three at each scale, the usual pattern in murines), and the scutellation is exposed. Scale hairs are brown in the pigmented basal portion of the tail but unpigmented (silvery) in the white region.

Table 5

Absolute Lengths (mm) of Dorsal White Tail Segment and Length of Tail, and Length of Dorsal White Segment Relative to Length of Tail (%) In Samples of Echiothrix

Mean ± 1 SD and observed range in parentheses are listed.

Legs and feet: The front legs are short and slender, particularly the forearms. Each front foot has four slender digits ending in unpigmented stout claws and a tiny stubby thumb (pollex) bearing a nail (fig. 4). The middle digits are the longest, the medial second digit shorter, and the lateral fifth digit extending about to the base of the adjacent digit. Dorsal surface of the metacarpal region and digits are white, covered with silvery hairs. Ungual tufts are sparse, consisting of one or two short hairs confined to the end of each digit, leaving the claws uncovered. Three interdigital pads along with a moderately large thenar and small hypothenar mounds form most of the naked palmar surface (fig. 4), which ranges from unpigmented to dark gray (palmar surfaces of live E. centrosa have a rosy tinge reflecting the subcutaneous arterial circulation).

While the front claws are stout, moderately long, gently arched, and sharp, they are not excessively large relative to length of digits and size of the front foot (fig. 4). By contrast, the montane Sulawesian shrew rats Melasmothrix naso, Tateomys rhinogradoides, and Paucidentomys vermidax, all consumers of earthworms, bear elongate curved claws that are very long relative to size of the foot (Musser, 1982; Esselstyn et al., 2012).

The hind legs are large and robust. Hind feet are long and very narrow; the first (hallux) and fifth digits are much shorter than the three much longer middle digits, which are all about the same length (fig. 4). The claw of the hallux barely reaches the base of the second digit, and the claw of the fifth digit extends to about middle of the second digit. Dorsal surfaces of the metatarsal region are either white (covered with unpigmented hairs), or white with small patches of gray speckling; digits are typically white. Conspicuous silvery ungual tufts cover bases of the ivory-colored stout claws. Each naked, dark gray plantar surface is adorned by six moderately fleshy pads: four interdigital mounds (forming a cluster at the bases of the digits), a tiny pimplelike hypothenar, and a short and narrow ridgelike thenar (both are very small and inconspicuous relative to plantar surface). The hind claws are curved and sharp tipped and moderately long relative to the length of the digits and hind foot, proportionally similar to the configuration seen in Sundaic Berylmys bowersii and Sundamys muelleri (Musser and Newcomb, 1983: 15: fig. 15).

Teats: Two pairs of inguinal teats are characteristic of all female shrew rats surveyed (12 E. leucura, 15 E. centrosa). Tate (1936) and Ellerman (1941) reported three pairs, which is incorrect.

General cranial features: The cranial configuration of E. leucura is illustrated in the portrait of a skull from Rurukan (fig. 5; the skull of E. centrosa from Sungai Sadaunta is portrayed in fig. 6). A long (about 40% of occipitonasal length) and narrow (about 38% of braincase breadth; table 6) rostrum is typical; from a lateral view, the rostrum tapers from its highest point level with the zygomatic plates distally to the incisors. The smooth sides are broken near the base of the rostrum by low nasolacrimal capsules that barely bulge beyond the rostral walls (and are hardly evident in dorsal or ventral views). Pointed tips of the nasals overhang the external nares and are either even with or project slightly beyond anterior edges of the premaxillaries; posterior borders of the nasals extend well beyond the premaxillary-frontal suture (by 14% of nasal length). The zygomatic plate is moderately wide, its maxillary root originating posterior to the nasolacrimal bulge and above and in front of the first molar; its anterior margin is typically convex, is usually also inclined, and joins the dorsal maxillary root to form a conspicuous notch between the anterior edge of the plate and lateral side of the skull (as seen from dorsal perspective). The posterior edge of the zygomatic plate sits above the anterior one-third of the first molar. A tall and narrow infraorbital foramen is the usual configuration. The tendon of the superficial masseter muscle attaches to a small bony swelling or roughened raised area on the anteroventral corner of the zygomatic plate. Robust zygomatic arches bow appreciably outward; the maxillary and squamosal roots of each arch are united by a short jugal. The squamosal root of each zygomatic arch originates low on the outer braincase wall and its posterior margin extends as an indistinct ridge along the braincase to disappear well before the occiput.

Fig. 5.

Cranium and left dentary of Echiothrix leucura (AMNH 101246; ONL  =  56.6 mm, CLM1–3  =  6.6 mm), an adult female from Rurukan. X2.

Fig. 6.

Cranium and left dentary of Echiothrix centrosa (AMNH 225043; ONL  =  52.5 mm, CLM1–3  =  6.0 mm), an adult female from Sungai Sadaunta. X2.

Table 6

Descriptive Statistics for Cranial and Dental Measurements (mm) Derived from Population Samples for Echiothrix leucura and E. centrosa

Mean ± 1 SD and observed range in parentheses are listed.

Table 6

(Continued)

A moderately wide interorbital region is usual. Its dorsolateral borders are defined by conspicuous ridges that extend along dorsolateral margins of the postorbital region (but never wide enough to form narrow shelves) and to the braincase where they form low but prominent temporal ridges that disappear anterior to the occiput (just before the lamboidal ridges). The otherwise smooth braincase is squarish (as seen from dorsal perspective) and deep (as viewed from the side) with a domed roof. A rectangular portion of the parietal drops below the dorsolateral margin of the braincase almost to the top of the zygomatic root; this projection and the squamosal form the wall of the braincase. The inner sidewalls of the braincase are smooth, without squamosal-alisphenoid grooves. Sides of the braincase are vertical from the temporal beading to squamosal roots of the zygomatic arches. The occipital region is moderately deep and roofed by the interparietal in the middle and dorsal segment of the exoccipital on either side. The boundary between squamosal and exoccipital is marked by prominent lamboidal ridges. The posterior wall of the occiput is vertical (in lateral view) and even with the posterior boundaries of the occipital condyles. The squamosal above each auditory (ectotympanic or bullar) capsule and just anterior to the lamboidal ridge is complete (not penetrated by a subsquamosal foramen).

As seen from the ventral perspective, the moderately long incisive foramina (about 50% of diastemal length; table 6) are located in the center of the diastema and form an elongate teardrop in outline. Just behind the upper incisors is a slitlike interpremaxillary foramen. Except for a pair of grooves that increase in depth from front to back, the bony palate is smooth, its posterior margin projects well past the third molars to form a bony shelf. A pair of large posterior palatine foramina penetrate the palate at the maxillopalatine suture opposite either first or second upper molars. Maxillary molar rows are either parallel or bow medially toward the back of the bony palate. The mesopterygoid fossa is narrow and its dorsolateral walls are perforated by two wide and moderately long sphenopalatine vacuities that expose the medial borders of the presphenoid and basisphenoid.

Each ectotympanic bulla ( =  bullar capsule) is moderate in size (about 11% of the occipitonasal length) and bears a wide and long bony eustachian tube. The medial sagittal plane of each bullar capsule is oriented ventromedially, so the capsules appear to rest on the basicranium and project toward the midline rather than more nearly vertical (an orientation similar to that seen in the Philippine Tarsomys apoensis [Musser and Heaney, 1992: 23, fig. 9]). The bullar capsule does not cover the entire surface of the enclosed periotic bone, leaving exposed a thick posteromedial wedge and a narrow flange extending forward between the ectotympanic and basioccipital. The carotid canal is bounded by part of the periotic, adjacent ectotympanic, and lateral border of the basioccipital (pattern is closely similar to that illustrated for Philippine Chrotomys [Musser and Heaney, 1992: 78, fig. 43]). All specimens possess a large stapedial foramen penetrating the crevice (the petromastoid fissure) between the bullar capsule and the periotic. A middle lacerate foramen, either spacious or narrow, separates the bullar capsule from the posterior margin of the alisphenoid.

In lateral view, a narrow flange of periotic is exposed along the anterodorsal margin of the bullar capsule. The capsule and periotic are separated from most of the squamosal by a broad postglenoid foramen that is confluent with a ventral middle lacerate foramen. The mastoid portion of the periotic is slightly inflated, its outer surface without perforations.

Within the orbit, the ethmoid foramen is small and the optic foramen large, a typical murine pattern. Orbitosphenoid, alisphenoid, and frontal bones join to form a solid section of the braincase wall, unbroken by a sphenofrontal foramen. Sphenopalatine and dorsal palatine foramina are separate, a pattern similar to that found in species of Rattus (Musser, 1982: 22).

Pterygoid region: Osseous structure of the pterygoid region of Echiothrix is extremely simplified: the pterygoid plates have regressed and are represented only by diminutive remnants. Among murines, this osteological design of the pterygoid-alisphenoid region is repeated only in the Philippine shrew rat Rhynchomys (see the cranial illustrations in Musser and Heaney [1992: 78] and Balete et al. [2007: 293]) and the Sulawesian shrew rat Paucidentomys (Esselstyn, et al., 2012). The best way to appreciate this severe modification is to first describe the pterygoid region in the Sulawesian Maxomys dollmani, which expresses a pattern common to nearly all other murines, especially those from the Indomalayan region, Sulawesi, Philippines, New Guinea, and Australia (see the cranial illustrations in Musser, 1982, 1991; Musser and Newcomb, 1983; Musser and Holden, 1991; Musser and Heaney, 1992; Flannery, 1995; Musser et al., 2008; Musser and Lunde, 2009; Heaney et al., 2012; Balete et al., 2012), as well as species in Europe and Africa (see the cranial drawings in Happold, 2013).

In Maxomys dollmani, each pterygoid plate forms a long and wide shelf bounded on the medial side by a hamular process and defined laterally by a smooth margin; the palatine bone forms the plate's anterior half and the pterygoid bone its posterior section (fig. 7D). Nearly all of the ventral surface of the pterygoid plate anterior to the foramen ovale is shallowly excavated and forms the pterygoid fossa. The posterolateral and posterior edges of the plate converge behind the foramen ovale to form a wide and smoothly rounded ridge, which defines the anterolateral border of the spacious medial lacerate foramen separating the pterygoid plate and posterior margin of the alisphenoid from the ectotympanic bullar capsule. Just medial to this pterygoid ridge is a deep groove for the infraorbital branch of the stapedial artery. The spot where the artery leaves the groove and passes to the dorsal surface of the pterygoid plate defines the posterior opening of the alisphenoid canal. Medial to the foramen ovale is the sizeable opening of the transverse canal.

Fig. 7.

Ventral views of crania showing variation in the specialized configuration of the alisphenoid region in Echiothrix as represented by E. centrosa (A, AMNH 225043; B, AMNH 225683; C, AMNH 225679), contrasted with the usual conformation found in nearly all other murines as represented by Maxomys dollmani (D, AMNH 224862). Abbreviations: aalc, anterior opening of alisphenoid canal (see fig. 8); ab, auditory bulla; al, alisphenoid; als, alisphenoid strut; bs, basisphenoid; fo, foramen ovale; hp, hamular process; iag, groove in which the infraorbital artery courses; mbt, trough for masticatory and buccinator divisions of maxillary nerve; mlf, middle lacerate foramen; mpf, mesopterygoid fossa; mpp, margin of pterygoid plate; palc, posterior opening of alisphenoid canal; pp, pterygoid plate; ps, presphenoid; rpp, platformlike remnant of pterygoid plate; sq, squamosal; tc, transverse canal.

As seen from lateral perspective (fig. 8D), a bony alisphenoid strut is not present in Maxomys dollmani, a loss resulting in the coalescence of the foramen ovale accessorius and masticatory-buccinator foramina (see fig. 48 in Musser and Newcomb, 1983: 457, showing the configuration when an alisphenoid strut is present). Exposed to view is the anterior opening of the alisphenoid canal, the open canal itself, the foramen ovale and the defining lateral margin of the pterygoid plate. Emerging from the foramen ovale is a shallow trough for the masticatory and buccinator divisions of the maxillary nerve.

Fig. 8.

Lateral views of the same specimens diagrammed in figure 7 showing variation in the specialized configuration of the alisphenoid region in Echiothrix as represented by E. centrosa (A, AMNH 225043; B, AMNH 225683; C, AMNH 225679) contrasted with the usual conformation found in nearly all other murines as represented by Maxomys dollmani (D, AMNH 224862). Abbreviations are the same as in figure 7, except for the following: mx, maxillary; vrpp, vertical remnant of the pterygoid plate.

In Echiothrix, the pterygoid plates have disappeared as major horizontal structural entities and only remnants remain, as seen from ventral perspective of skulls (fig. 7A–C). In all three views of E. centrosa, most of the alisphenoid bone extends to the base of the hamular process without meeting a generous horizontal pterygoid plate (panel A) and the entire outer surface of the alisphenoid is exposed. Aside from tiny scattered nutrient foramina, only two major openings are present in the alisphenoid: the anterior opening of the alisphenoid canal forms a small round or irregular aperture anterior to the much larger and spacious foramen ovale. Emerging from the latter is a shallow trough for the masticatory and buccinator divisions of the maxillary nerve. Between the foramen ovale and the large middle lacerate foramen is a shallow groove in which the infraorbital artery courses. In some specimens, a continuation of the groove can be detected between the anterior rim of the foramen ovale and the anterior opening of the alisphenoid canal (fig. 7C) but in others the groove exists only between the middle lacerate foramen and the foramen ovale (fig. 7A–B). Apparently the infraorbital artery courses along the surface of the alisphenoid in Echiothrix but in Maxomys is concealed by the pterygoid plate and is exposed only between the middle lacerate foramen and foramen ovale, the latter marking the posterior opening of the alisphenoid canal.

Variation in vestiges of the pterygoid plate is also shown in figure 7. The skull in panel A retains an alisphenoid strut to which a sliver of pterygoid plate margin is attached; forward of the strut is a slight ridgelike remnant of the anterior margin of the plate. Panel B reflects the configuration of the alisphenoid region in many examples of Echiothrix where a short sliver of the anterior plate margin is the only sign of the pterygoid plate from ventral perspective. The skull depicted in panel C preserves a narrow ridgelike relic of the anterior plate margin and a slim crescent of bone representing the posterolateral margin of the pterygoid plate; stippling that connects the anterior part of the bony crescent with the relict anterior plate margin outlines a narrow ledge (remnant of the pterygoid plate) undefined by a discrete lateral margin; a comparable narrow ledge or platform is found in many examples of Echiothrix.

The alisphenoid region, as seen from lateral perspective, of the same three specimens of E. centrosa that are illustrated in figure 7 is shown on panels A–C in figure 8. In panel A, a bit of the pterygoid plate margin is evident as is an alisphenoid strut, which is typically absent in most examples of Echiothrix). The anterior opening of the alisphenoid canal is small (also seen in panels B and C), in contrast to the comparable spacious opening in Maxomys (panel D). Vestiges of the pterygoid plate margin are also evident in panels B and C. So is the encroachment of what appears to be a low vertical remnant of the pterygoid plate into the alisphenoid. This vertical remnant apparently represents the transformation of a horizontal pterygoid ridge—the usual murine conformation—into a vertical surface that, along with the lower portion of the alisphenoid, forms the outer wall of the mesopterygoid fossa (mpf in fig. 7); this vertical remnant varies in extent among specimens of Echiothrix, ranging from the expanse illustrated in panels B and C to a thin sliver just above the ridgelike pterygoid margin. In most species of murines, such as Maxomys dollmani (panel D), the alisphenoid extends from its suture with the squamosal ventrally to the base of the pterygoid plate and anteriorly to the maxillary (mx) just behind the molar row. The outer wall of the mesopterygoid fossa is formed only by the alisphenoid.

Cephalic arterial pattern: All specimens of Echiothrix leucura (and E. centrosa) surveyed possess a carotid arterial plan that is primitive for members of the subfamily Murinae (character state 2 of Carleton, 1980; pattern 2 described by Voss, 1988; conformation diagrammed for Oligoryzomys by Carleton and Musser, 1989), but derived for muroid rodents in general. The pattern is reflected in certain cranial foramina and osseous landmarks seen in cleaned skulls. No sphenofrontal foramen penetrates the bony junction of orbitosphenoid, alisphenoid, and frontal bones; no squamosal-alisphenoid groove scores the inner surface of each wall of the braincase; and the stapedial foramina is neither minute nor absent. Instead, there is a large stapedial foramen in the petromastoid fissure, and a shallow groove (iag in fig. 7B–C) extending from the middle lacerate foramen (mlf in fig. 7D) to the foramen ovale (fo in fig. 7B–D). This disposition of foramina and grooves indicates that the stapedial artery branches from the common carotid and enters the periotic region through a large stapedial foramen. The infraorbital branch of the stapedial artery exits the pteriotic through the middle lacerate foramen, courses in a short groove (between middle lacerate foramen and foramen ovale), and continues on the outside of the skull at the base of the hamular process to disappear into the braincase through the anterior opening of the alisphenoid canal from which it emerges to course through the anterior alar fissure into the orbit. The supraorbital branch of the stapedial is absent; the arterial supply to the orbit is furnished by the distal part of the infraorbital branch. This circulatory plan is common among murines (Musser and Newcomb, 1983; Musser and Heaney, 1992) and is also found in some North and South American cricetids (Carleton, 1980; Voss, 1988). The derived murine version of the carotid arterial supply is contrasted with the primitive configuration and another more derived pattern, both of which are found within other muroid rodents as documented by Bugge (1970), Carleton (1980), Carleton and Musser (1989), and Voss (1988).

Mandible: Each gracile dentary is elongate, particularly the diastemal portion between the incisor and anterior margin of the first molar (fig. 5). On the dorsal rim of the ramus behind the molar row, the coronoid process is a minute triangular projection, and the long rim between it and the large and long condyloid (articular) process is either straight or slightly concave (very shallow sigmoid notch). The posterior margin of the dentary between the large condyloid and angular processes is deeply concave (outlining a half circle). A large bulge on the side of the dentary behind the coronoid process and even with the dorsal rim marks the posterior termination of the incisor sheath (alveolus). Masseteric ridges on the lateral surface of each dentary are pronounced.

Dentition: Upper incisors are small, short, and narrow, and emerge from the rostrum at a right angle (orthodont in form; see Thomas [1919] and Hershkovitz [1962: 103] for definitions of incisor configurations). The anterior face of each incisor is scored by two shallow grooves (fig. 3). Dentine is white (unpigmented) as is the enamel in most specimens, but a few show a pale yellow tinge in the enamel layers. In live E. centrosa, the teeth appear ivory and emit a translucent quality; we suspect the teeth appear similar in live E. leucura. Enamel layers form the face and anterolateral third of each incisor, and dentine the remainder, a configuration similar to that found in most murines (as illustrated for Rattus in Musser and Heaney, 1992: 79).

Beyond their emergence from the anterior body of the dentary, the lower incisors are awl shaped—each is long, slim, gently curved, and with a sharp tip and elongate wear (occlusal) facet; enamel layers are smooth, without grooves. While the dentine is white, the enamel layers range from white to a pale yellow tinge—usually the distal portion of each incisor is unpigmented but the basal portion pale yellow. The extent of the enamel layer is similar to the pattern seen in most murines, Rattus, for example (Musser and Heaney, 1992: 79, fig. 46). The full length of each long incisor is slender and although gracile in form the tooth is not weak. Two-thirds of the incisor is contained in a sheath within the body of the dentary where it ends between coronoid and condyloid processes in an elongate bulge on the lateral surface of the dentary. This bony enclosure provides the incisor with foundational strength for stabbing prey (see Natural History Particulars of E. centrosa).

Every maxillary molar is secured by three roots. The alveolar patterns illustrated for Maxomys wattsi (Musser, 1991: 32, fig. 18) are also usual for Echiothrix. Each first and second molar is anchored by large anterior and lingual roots along with a smaller posterior holdfast; each third molar is held in place by three roots of about the same size. There are two large roots beneath each of the mandibular molars.

The brachydont molars are small and molar rows are short relative to size of skull (13% of occipitonasal length; table 8); the rows are either parallel or curve gently posteriorly toward the midline of the bony palate. Molars grade in size within each row: the first is the largest, the third the smallest, which is the usual configuration observed in most species of murine rodents (Carleton and Musser, 1984). Like many murines, the cusp rows incline caudad, so that within each maxillary row the first molar overlaps the second and that tooth leans slightly against the third; the third molar in each mandibular row inclines against the second, which slightly overlaps the first molar. The rows of cusps on each tooth are moderately close to one another, a condition usually associated with inclined rows of cusps; in murines with widely separated rows, the cusps are typically erect.

Occlusal surfaces of maxillary molars are formed by simple rows of low cusps and lack the complexities found in more complicated patterns that characterize some other murines (fig. 10, upper row). For example, there is no cusp t7, which is a prominent feature on the occlusal surface in certain murine genera (Lenothrix, for example; fig. 9); cusp rows stand free, unconnected by labial or lingual enamel bridges (stephanodont crests as described by Misonne, 1969: 55); although close to one another, cusps t4 and t8 do not coalesce along their lingual margins until they are worn to the cingulum; the anterior cingular face on each first molar is smooth, without a shelflike ridge or small cusp (a cingular ridge, often bearing a small cusp, is a usual element on the first molar in Rattus hoffmanni, for example; Musser and Holden, 1991: 348). An occasional specimen of E. leucura shows an auxiliary cusp behind cusp t1 on the first molar (fig. 10A).

Fig. 9.

Nomenclature of dental structures using right maxillary (upper) and mandibular (lower) molars of Lenothrix canus. Maxillary molars (right toothrow): cusps are numbered according to Miller's (1912) scheme and referred to in the text with the prefix “t”; pc  =  posterior cingulum. Mandibular molars (left toothrow): the anterocentral cusp (acen), anterolabial cusp (alab), and anterolingual cusp (aling) form the anteroconid; an anterior labial cusplet (alc) is present on the first lower molar, and posterior labial cusplets (plc) occur on the first and second lower molars; primary cusp rows are formed by the protoconid (pd) and metaconid (md), and the hypoconid (hd) and entoconid (ed); a posterior cingulum (pc) sits at the back of each molar (adapted from van de Weerd, 1976: 44).

Fig. 10.

Occlusal views of left maxillary (top row) and mandibular (bottom row) molar rows in four specimens of Echiothrix (lingual margin of each row is on the left, labial on the right). A, young adult E. leucura (USNM 217807, Temboan; CLM1–3 and clm1–3  =  7.5 mm). The next three drawings portray wear stages in E. centrosa: B, juvenile (USNM 219719, Tuare; CLM1–3  =  6.4 mm, clm1–3  =  6.6 mm); C, young adult (AMNH 225680, Kuala Navusu; CLM1–3 and clm1–3  =  6.5 mm); D, adult (AMNH 225683, Kuala Navusu; CLM1–3  =  6.5 mm, clm1–3  =  6.4 mm).

On the first upper molar, the labial and central cusps in each row are transversely aligned; the lingual cusps t1 and t4 are situated well back of the first and second rows, respectively. A posterior cingulum occurs on nine of the 10 specimens surveyed (sample size is small because teeth are missing from some specimens or in others the occlusal surfaces are too worn to identify a posterior cingulum). The posterior cingulum extends from the back of cusp t8 in the form of a ridge, a triangular projection, or a large cusp projecting labially to form a portion of the occlusal surface (as exemplified by Lenothrix; fig. 9).

On the second molar, the first row of cusps is represented by cusp t1, which is always present, and cusp t3, which is present in only about half the sample surveyed. A posterior cingulum was located on nine of 10 specimens.

Cusp t1 is present on the small third molar, but cusp t3 is not. Cusps 4, 5, and 6 form a structure that is usually chevron shaped. Cusps 8 and 9 form a posterior lamina in some specimens, but in others only a single structure is present, representing either cusp t8 only or completely merged cusps t8 and t9; the third molar lacks a posterior cingulum.

Occlusal topography of each mandibular molar consists primarily of chunky transverse rows, each representing the fusion of two cusps (fig. 10, lower row). A large posterior cingulum, generally elliptical in cross section, occurs on the first lower molar in 11 of the 12 specimens surveyed, and a much smaller posterior cingulum could be identified on the second molar in seven of 10 specimens. Located at the front of the first molar is a chunky anteroconid composed of large anterolabial and anterolingual cusps (no anterocentral cusp was found on any of the specimens) that have merged to form a large oblong lamina (without discernable cusp boundaries in some specimens, but clearly formed from two cusps in others) either slightly or much narrower than the lamina behind it. None of the molars bear anterior labial cusplets; various frequencies of occurrence of posterior labial cusplets on all molars along with anterolabial cusps on the first and second molars comprise minor components of the occlusal surface.

Comparisons:

Cranial and dental morphometrics as well as qualitative cusp differences and geographic distributions between E. leucura and E. centrosa will be offered in the account of the latter species.

Geographic Variation:

The samples of E. leucura used in analyses of morphometric traits come from four places and each analytical sample is small. There is insufficient material and geographic coverage for any serious analysis of geographic variation in external, cranial, and dental traits. We can report that features of fur coloration along with lengths of head and body, tail, hind foot, and ear among adults show hardly any differences from place to place other than that ascribed to individual, age, and sexual variation. Nor do definable groups emerge when cranial and dental measurements are subjected to principal-components analysis. The distribution of specimen scores for the samples from Rurukan, Gunung Masarang, Tondano, and Temboan projected on the first and second principal components (not illustrated here) intermix to form a single large cluster. If significant geographic variation exists within the range of E. leucura, it will have to be demonstrated in the future by obtaining larger samples from more places and adding analyses of DNA sequences to results derived from morphometric inquiry.

Echiothrix brevicula Miller and Hollister, 1921:67.

Holotype:

USNM 218706, the skin and skull of an adult male (original number 3077) collected January 9, 1917, by H.C. Raven. The skin was prepared as a conventional stuffed museum preparation; the skull and mandible are complete; all teeth are present. External, cranial, and dental measurements along with other data are listed in table 2.

Type Locality:

Winatu (01° 34′ S, 119° 59′ E; locality 7 in gazetteer and on the map in fig. 2), 762 m, in the core of the island, Propinsi Sulawesi Tengah, Indonesia.

Emended Diagnosis:

Echiothrix centrosa is similar to E. leucura in aspects of physical size as well as coloration and texture of fur but differs in other traits: (1) a shorter body and hind foot, but a longer tail in relation to length of head and body; (2) a smaller skull (as indexed by the lesser mean values for occipitonasal and rostral lengths; interorbital breadth; height and breadth of braincase; and lengths of diastema, bony palate, and postpalatal region), but longer incisive foramina, narrower rostrum, and wider bony palate and mesopterygoid fossa; (3) smaller molars with less complex cusp patterns: (4) cusp t3 occurs at a lower frequency on the first upper molar, a posterior cingulum is rarely present on the first and second upper molars: (5) an anterolabial cusp is absent from the second and third lower molars, posterior labial cusplets occur at low frequencies on the first and second lower molars but are absent from the third lower molar, and neither the first or second lower molar bears a posterior cingulum.

Specimens Examined:

Total 39 (see Gazetteer and Specimens).

Etymology:

Miller and Hollister used centrosa to reference the provenances of their samples (Gimpu, Winatu, Besoa, and Tuare) from the central region of Sulawesi.

Geographic and Elevational Distributions:

Voucher specimens are from two localities on the northern peninsula and several places in the core of the island (see gazetteer and the map in fig. 2). Although collection sites are spotty, and expansive landscapes of Sulawesi are without records, the specimens at hand indicate that E. centrosa ranges throughout the northern peninsula west of the Gorontalo region (00° 31′ N, 123° 03′ E) and into the core of the island. All specimens come from the mainland between coastal lowlands and approximately 1000 m (see gazetteer), an interval that would be covered by tropical lowland evergreen rain forest.

The actual distribution of E. centrosa south of the northern peninsula is unknown. There are no records from the eastern, southeastern, or southwestern peninsulas. However, there are no reasons to think the species does not occur in tropical lowland evergreen rain forest on at least the eastern and southeastern peninsulas. Whether it also occurred on the southwestern peninsula before most of the lowland forest was removed and the landscape converted to agriculture (see Fraser and Henson, 1996; Whitten et al., 1987) or is present in remnant tracts of lowland forest (as described by Froehlich and Supriatna, 1996) is not known. Samples of subfossil murines excavated from caves in the southern part of the southwestern peninsula include species of Bunomys, Maxomys, Paruromys, Taeromys, Lenomys, and Rattus, but no Echiothrix (Musser, 1984, also unpublished mss.).

Description:

Physical size and external features (color and texture of fur; lengths of head and body, hind foot, and ear; length of tail and its pigmentation pattern; and number of teats) of E. centrosa closely resemble those attributes shown by E. leucura (see description of that species). Descriptions of the skull, mandible, incisors, and molars for E. leucura also describe the basic shapes in these structures for E. centrosa except for the differences in cranial measurements and proportions along with size differences in molars and contrasts in their occlusal topographies, which are described below in the section covering comparisons.

Here we provide descriptions of a few characteristics of E. centrosa, primarily derived from material Musser collected, which are not currently available for E. leucura.

Testes and spermatozoal morphology: The testes are large relative to body size (16%–23% of head and body length; table 14), the scrotal sac is densely haired, and the hairs behind the penis are stained by a brownish-yellow exudate. There is no gross external sign of a midventral gland.

Gross morphology of the spermatozoa of Echiothrix centrosa has been described by Breed and Musser (1991; reported as E. leucura). Basically, the asymmetrical sperm head is long and sickle shaped, the apical hook is short, ventral hooks are not present, and the tail is long (see the table of measurements and micrograph of the spermatozoa in Breed and Musser, 1991: 4 and 8, respectively).

Stomach morphology: Echiothrix centrosa has a unilocular-pouched stomach, that is, it combines aspects of what Carleton (1973) regards as the two basic morphological designs within muroid rodents—unilocular-hemiglandular or bilocular-discoglandular. Carleton (1973: 10) described a unilocular-hemiglandular stomach as:

This single-chambered hemiglandular morphology, in which the glandular zones are separated by a smooth bordering fold and the incisura angularis is shallow, forms the gastric conformation that Carleton (1973, 1980) suggested represents the primitive evolutionary state among muroid rodents. The general unilocular-hemiglandular design is common to Sulawesian species in which the diets are composed of insects and fruit (Margaretamys); fruit, small seeds (Haeromys); fruit, vegetative and flowering plant parts, insects (Lenomys and Eropeplus); small vertebrates, arthropods, snails, earthworms (oligochaetes), fruit, fungi (Bunomys); primarily fruit, some insects (Taeromys); and mostly fruit (Rattus). In these species, the extent of glandular epithelium lining the antrum relative to the area of cornified epithelium of the corpus resembles the pattern exemplified by Rattus hoffmanni as illustrated in figure 11, with a range of variation in which the glandular portion does not extend beyond the level of the esophageal orifice to a configuration where the glandular lining penetrates the corpus well past the esophageal opening.

Fig. 11.

Ventral views of the unilocular-hemiglandular stomach (in midfrontal section) of Rattus hoffmanni (AMNH 226041) and the bilocular-discoglandular stomach of Maxomys hellwaldii (AMNH 224939) contrasted with the unilocular-pouched stomach of Echiothrix centrosa (AMNH 225043). Abbreviations: a, antrum; bf, bordering fold; c, corpus; ce, cornified squamous epithelium; d, anterior end of duodenum; e, posterior end of esophagus; fv, fornix ventricularis; ge, glandular epithelium; gp, glandular pouch; ia, incisura angularis; mc, muscular walls of the corpus; p, pylorus; ps, pyloric sphincter. Scale lines  =  10 mm.

In Carleton's view (1973: 10), a bilocular-discoglandular stomach has:

A bilocular-discoglandular pattern is the stomach morphology common to Maxomys hellwaldii (fig. 11) and other Sulawesian species in that genus. A spacious fornix ventricularis inclines toward the esophagus and projects craniad beyond the esophageal opening, the incisura angularis is deep, and the walls of the antrum are muscular. The corpus and most of the antrum is lined with muscular cornified squamous epithelium. Glandular epithelium is restricted to a small patch in the antrum on the ascending portion of the greater curvature; the glandular zone is bounded by a bordering fold. Fruit, arthropods, snails, earthworms, and small vertebrates are consumed by M. hellwaldii.

The stomach of Echiothrix centrosa (fig. 11) is unilocular and pouched. “Unilocular” because the corpus and antrum are not separated by a bordering fold, which transforms the bulk of the stomach into a single chamber, and the incisura angularis is shallow (either even with the esophageal orifice or barely extending beyond it). “Pouched” because the entire corpus and antrum is lined with cornified squamous epithelium, and glandular epithelium occurs only in a pouch situated on the greater curvature within the lumen of the stomach opposite the esophageal orifice. This pouch is lined with thick glandular epithelium and connects with the main chamber of the stomach through a small aperture at the end of a funnel-shaped or tubular neck. (We are indebted to Michael Carleton [in litt., 2013] for identifying Echiothrix's stomach conformation as unilocular-pouched.)

The possible correlation of stomach design and diet will be explored below in the section covering natural history aspects of E. centrosa.

Karyotype: The chromosomal composition has been recorded for a male E. centrosa (AMNH 225682) collected at Kuala Navusu: 2N  =  40, FNa  =  72 (total of autosomal arms) and FNt  =  75 (total number of arms, including XY). Autosomes comprise 14 pairs of submetacentrics with the first pair the largest and the others ranging in size from moderately large to small, two pairs of small acrocentrics, and three pairs of small metacentrics; the presumed X chromosome is a small submetacentric, the Y a small acrocentric (Musser, 1990: fig. 10; documented as E. leucura).

Juveniles: All the information provided in the preceding descriptions of E. centrosa and E. leucura is derived from adults. We have seen only two juveniles, both E. centrosa: a skin and skull from Pinedapa (USNM 219737) and skull only from Tuare (USNM 219714). All molars are erupted and exhibit a degree of wear similar to the juvenile molars of USNM 219714 illustrated in figure 10. The dorsal pelage is brown and the ventral coat off-white in the juvenile from Pinedapa; although we have not seen live or freshly caught juveniles, we suspect the skin is discolored and colors in the live rat were likely grayish brown and pure white. The feet and most of the tail are white (with slight greasy discoloration). Fur covering upperparts from shoulders to rump is spinous but softer, without the rigid texture of the adult coat. The spines are long, and about half the width of adult spines (but still flat, flexible, and grooved), so the curly and soft underfur layer forms more of the coat than it does in adults, which is why the fur feels less bristly to the touch. Legs and sides of the body are covered with softer fur, composed mainly of soft and curly underhairs through which are scattered flattened, long spines. Mask on the face (around each eye) and pigmentation pattern of the tail is like that of adults. Ears are dry and brown, but were probably rubbery and dark gray in life. The ventral fur is soft to the touch and composed of both thin hairs and thicker flat hairs; the latter are much narrower than those in the adult coat.

Comparisons:

Miller and Hollister (1921: 67) diagnosed Echiothrix centrosa as:

Farther along in the description, Miller and Hollister remarked that the new species

In the following contrast between E. leucura and E. centrosa, the taxon brevicula, also described by Miller and Hollister and also from the central part of Sulawesi, is included as a synonym of E. centrosa. Reasons for doing so are set forth below in the section explaining allocation of the synonym.

In the samples at hand of E. centrosa and E. leucura, which includes the material examined by Miller and Hollister, and contrary to their observations, we see differences in size and proportions of external measurements. Mean values for length of head and body (206.0 mm for E. centrosa, 215.8 mm for E. leucura; P  =  0.013) and length of hind foot (51.5 mm and 53.5; P  =  0.003) are significantly different—E. centrosa averages smaller. Means for length of tail (240.9 mm for E. centrosa, 240.2 mm for E. leucura; P  =  0.877), however, are statistically identical—therefore, E. centrosa has on average a shorter body and hind foot but a longer tail relative to length of head and body (sample sizes are N  =  30 for E. centrosa and N  =  13 for E. leucura for all three variables).

Other external differences between E. centrosa and E. leucura that were described by Miller and Hollister are not apparent to us. Both species have dark gray to bluish-gray dorsal coats; both have underparts that are either all white (in live animals) or white with patches or streaks of buff, orange, or pale rust (the rust may be a stain because the hairs in these colored places have pigmented debris adhering to them while hairs in the white region are clean); both show a similar color pattern on the tail, including length of the dorsal white portion (means of dorsal white length/tail length are 59.1% for E. centrosa and 58.5% for E. leucura; table 5); and both possess two pairs of inguinal teats.

To Miller and Hollister, the smaller ears of centrosa—as well as brevicula, the other taxon they described from central Sulawesi—were diagnostic in relation to E. leucura. But their descriptions of the new taxa and comparisons were based on material obtained by H.C. Raven, who did not measure length of ear on freshly caught rats. Miller and Hollister simply measured ears (from the notch) on the dry museum skins; because such ears are shriveled and their lengths contracted, they recorded smaller values than would be obtained from freshly caught animals. They reported, for example, 29.4 mm for the holotype of centrosa and 28.1 mm for the holotype of brevicula. Musser also measured the ear (from notch to crown of pinna) on specimens he collected within the geographic ranges of centrosa and brevicula and did not encounter any ear length less than 32 mm, a value within the range of measurements obtained by G. Heinrich for a sample of E. leucura from Rurukan (table 4).

Except for its smaller ears and teeth, E. centrosa was considered by Miller and Hollister to be similar to E. leucura in cranial size and proportions. In addition to the contrast in molar size, (see below), there are—contrary to the perceptions of Miller and Hollister—impressive distinctions between the two species in certain cranial dimensions and proportions. Univariate mean differences in cranial variables show that, compared with E. leucura, the central Sulawesian E. centrosa has a shorter skull and narrower interorbit, a shorter but wider rostrum, smaller braincase, shorter diastema and postpalatal region, shorter but wider bony palate, wider mesopterygoid fossa, and longer incisive foramina (table 6).

The univariate mensural cranial and dental differences are also summarized by results from multivariate analyses (fig. 12). There the top scatterplot contains the distribution of specimen scores for all population samples of E. centrosa and E. leucura projected on the first and second principal components. Scores for specimens in population samples from regions west of Gorontalo in the northern peninsula (Molinggapoto, Bumbulan) and from the core of the island (Sadaunta-Besoa, and Kuala Navusu–Pinedapa) with small skulls and molars are scattered in the left half of the plot: these are samples of E. centrosa. Specimen scores for samples from the northeastern portion of the northern peninsula east of the Gorontalo region, animals with larger skulls and molars, fall in the right half of the ordination: these scores identify E. leucura. Covariation among most variables indicates size to be the primary influence for dispersion of the scores along the first component, as indicated by the many positive and high correlations on that axis (r  =  0.57–0.94). Four variables yielded moderate to high negative correlations (r  =  −0.19 to −0.72; table 7), which point to the broader rostrum, bony palatal bridge, and mesopterygoid fossa along with a longer incisive foramina relative to skull size (indexed by occipitonasal length) in E. centrosa compared with E. leucura. The patterns of significant loadings of cranial and dental measurements are generally mirrored by the univariate mean contrasts (table 6).

Fig. 12.

Scatterplots of specimen scores representing the sample of Echiothrix leucura (filled circle; N  =  16) and the four population samples of E. centrosa (N  =  30; Molinggapoto  =  asterisk, Bumbulan  =  cross, Kuala Navusu–Pinedapa  =  square, Sadaunta-Besoa  =  triangle) projected on first and second principal components extracted from principal-components analysis (upper), and on first and second canonical variates extracted from discriminant-function analysis (lower) of 16 cranial and two dental log-transformed variables. Scores for holotypes: Echiothrix centrosa (filled triangle, Winatu in Sadaunta-Besoa sample) and Echiothrix brevicula (filled square, Pinedapa in Kuala Navusu–Pinedapa sample). See table 7 for correlations (loadings) of variables with extracted components or canonical variates and for percent variance explained in both ordinations.

Table 7

Results of Principal-Components and Discriminant-Function Analyses Comparing Samples of Echiothrix leucura and E. centrosa

Correlations (loadings) of 16 cranial and 2 dental log-transformed variables are based on 16 E. leucura and 30 E. centrosa. See figure 12.

Results of discriminant-function analysis (which identifies the variables most strongly separating the centroids of predefined population samples) provide a sharper resolution of morphometric affinity among samples, but the pattern is generally similar to that illuminated by results of the principal-components analysis. Individual specimen scores projected on first and second canonical variates form two nonoverlapping constellations (fig. 12, bottom): scores for E. leucura, with the larger skulls and molars, fall in the left half; points representing E. centrosa, with smaller skulls and molars, are contained in the right half. Size is the force separating scores along the first variate as indicated by covariation among most of the same variables that proved significant in the principal-components analysis (table 7). Here, the analysis again shows that E. centrosa has a shorter skull and rostrum, narrower interorbit, smaller braincase, shorter bony palate, and smaller molars (as measured by alveolar length of maxillary molar row and breadth of first upper molar) (r  =  −0.51 to −0.91), but a wider rostrum, bony palate, and mesopterygoid fossa, coupled with a longer incisive foramina (r  =  0.28–0.62) compared with E. leucura.

Miller and Hollister noted the contrast in molar size between E. centrosa and E. leucura, and the difference is striking as shown by the univariate means for lengths of maxillary molar rows: 6.4 mm for E. centrosa and 7.0 mm for E. leucura (table 8). Furthermore, there is no overlap in the observed range of values. Mean differences in lengths of the mandibular molar rows is comparable (6.4 mm for E. centrosa and 7.1 mm for E. leucura), although there is slight overlap in the observed range of measurements. The shorter maxillary and mandibular molar rows in E. centrosa are related to its smaller molars compared with those of E. leucura, as estimated by means for breadth of first upper molars (table 8).

Table 8

Descriptive Statistics for Measurements (mm) of Maxillary and Mandibular Molar and Alveolar Rows Derived from Samples of Echiothrix leucura and E. centrosa

Mean ± 1 SD, observed range in parentheses, and size of sample are listed.

Contrast in molar size is not the only dental distinction between the two species. The molars of E. centrosa also have less complex occlusal surfaces, as indicated by the difference between the two species in frequency of occurrence of particular cusps and cusplets (table 9, fig. 10). In the maxillary molars, cusp t3 occurs at a lower frequency on the second molar in E. centrosa (25%) compared with E. leucura (45%), and a posterior cingulum is present on the first and second molars in only 1% of the sample of E. centrosa but present in 90% of the sample of E. leucura. In the mandibular molars, an anterolabial cusp is not present on either the second or third molars in E. centrosa (occurs in 30% of the sample of E. leucura); none of the specimens of E. centrosa surveyed showed a posterior cingulum on the first and second molars (frequency is 92% on the first molar and 70% on the second molar in E. leucura); and a posterior labial cusplet is present on the first molar in 46% of the sample, on the second molar in 19%, and not present on the third molar in the sample of E. centrosa (92% on the first molar, 40% on the second, and 20% on the third molar are the frequencies for E. leucura).

Table 9

Presence or Absence of Particular Cusps and Cusplets on Maxillary and Mandibular Molars in Samples from Echiothrix leucura and E. centrosa^a

Table 9

(Continued)

Geographic Variation:

Except for the 19 specimens in the Kuala Navusu–Pinedapa sample, the other population samples are small. Three from Molinggapoto and one from Bumbulan are the only specimens we have examined from the northern peninsula west of the Gorontalo area, and the seven in Sadaunta-Besoa are the only specimens from middle elevations in central Sulawesi west of the lowlands in which Kuala Navusu and Pinedapa are located. Without larger samples from more places, especially from transects that would connect the current collection localities, we cannot provide a definitive pattern of geographic variation using external traits and measurements from cranial and dental variables. For now only a few comments covering the different population samples is possible.

The specimens from Molinggapoto and Bumbulan have white underparts without patches of pigmentation. Both all-white underparts and white ventral coats with patches or streaks of buff or rust occur in the samples from the core of Sulawesi. More specimens from the northern peninsula both east and west of Gorontalo are needed to determine the frequency of occurrence of all-white versus partially pigmented underparts in the population there.

The pattern of covariation among cranial and dental variables as revealed by principal-components and discriminant-function analyses places the specimen from Bumbulan within or close to the cluster of specimen scores representing the Sadaunta-Besoa sample (fig. 12). Its physical size and fur color are indistinguishable from specimens of comparable age in the Sadaunta-Besoa sample, at least those individuals with all-white underparts.

In the ordinations generated by multivariate analyses, scores for the Sadaunta-Besoa sample cluster close to those representing the Kuala Navusu–Pinedapa sample, both in principal components and canonical variate scatter plots (fig. 12). There are some perceptible differences between the two samples. Animals from the lowlands at Kuala Navusu and Pinedapa have slightly shorter ventral coats and slightly smaller skulls than do those in the Sadaunta-Besoa sample, differences that will be elaborated upon in the section below where the reasons are given for treating brevicula as a synonym of E. centrosa. Again, the significance of these observations within the context of revealing geographic variation in external and cranial traits is elusive without samples from intervening regions between the two population samples and without samples from elsewhere in the core of the island and the various peninsulas.

The specimens from Molinggapoto are geographically closest to the range of E. leucura, but their cranial and dental morphometric attributes, along with molar occlusal cusp patterns, link them with the specimen from Bumbulan and those collected in the core of Sulawesi. However, there are a few morphometric differences, which are graphically summarized in the canonical variate scatterplot in figure 12. There, along the first axis, the specimen scores for Molinggapoto are aligned in the right half of the ordination along with scores for the samples from Bumbulan and central Sulawesi, all of which we identify as E. centrosa; scores for E. leucura, with larger skulls and molars, fall into the left half of the graph. But along the second axis, the points for Molinggapoto are separated from those representing the other examples of E. centrosa. Compared with that material, the Molinggapoto sample has a relatively wider interorbital region and zygomatic plate, narrower mesopterygoid fossa, and smaller bullae, as indicated by the high positive and negative correlations for these variables (table 7).

Future attempts to recover any patterns of geographic variation within what is identified as E. centrosa here will depend on study of additional material collected from a greater expanse of Sulawesi and analyses of molecular as well as morphometric data.

Allocation of Synonym:

Echiothrix brevicula Miller and Hollister, 1921: 67. The holotype is USNM 219744, the skin and skull (measurements are listed in table 3) of an adult male collected January 29, 1918, by H.C. Raven. The type locality is Central Sulawesi, Pinedapa (01° 25′ S, 120° 35′ E; locality 4 in gazetteer and on the map in fig. 2), Propinsi Sulawesi Tengah, Indonesia.

The Latin brevis means “short” (also connotes “small” and “narrow”), and Miller and Hollister used brevicula to reflect what they perceived to be the smaller size of the specimens in the sample from Pinedapa as compared with their sample of E. leucura from Temboan in the northeastern end of the northern peninsula and E. centrosa from the west-central highlands. Miller and Hollister (1921: 68) diagnosed Echiothrix brevicula as follows:

The authors remarked that the new species “is easily separated from E. leucura and E. centrosa by its small size, peculiar coloration, and the less narrowed skull. It has small ears and small teeth as in E. centrosa.”

Our sample of brevicula includes the type series Raven obtained at Pinedapa and the sample Musser collected from Kuala Navusu; both localities are in the coastal lowland region east of the west-central highlands (see gazetteer and the map in fig. 2). Specimens from each place are inseparable in physical size, color of fur, morphometric traits associated with the skull and molars, and molar occlusal patterns formed by cusps and cusplets. We subjected cranial and dental measurements from all the samples identified here as E. centrosa to principal-components analysis and on the resulting scatterplot (not illustrated here) the scores representing specimens from Pinedapa and Kuala Navusu intermingle to form a tight cluster. The two geographic samples were combined to form a single population sample (Kuala Navusu–Pinedapa) used to generate the multivariate analytical results illustrated in figure 12.

Specimens that can be assigned to what Miller and Hollister would have identified as centrosa consist of the holotype from Winatu and collections from Tuare, Besoa, Gimpu, Kulawi, and Sungai Sadaunta, all localities in the west-central highlands west of the eastern coastal lowlands containing Kuala Navusu and Pinedapa (see the maps in Musser et al., 2010: 16, 81).

The type series of brevicula from Pinedapa does differ in magnitude of two external measurements from the series collected by Raven at Temboan, which is the sample Miller and Hollister used as their representative of leucura. Means for length of head and body (197.0 mm for brevicula, 215.4 mm for leucura; P  =  0.003) and length of hind foot (50.3 mm and 54.7 mm; P  =  0.0001) are significantly different, but means for length of tail are not (239.6 mm and 250.0 mm; P  =  0.082). (Sample sizes are N  =  12 for brevicula from Pinedapa and N  =  7 for N. leucura from Temboan.) The Temboan sample has a larger body and longer hind foot than the series from Pinedapa, and the tail is shorter relative to length of head and body; this is the same pattern of differences seen between all samples of E. leucura and all samples of E. centrosa (including brevicula) that we presented previously (see comparisons in the account of E. centrosa).

In contrast, the distinction between brevicula and centrosa as noted by Miller and Hollister cannot be corroborated by us. We compared external measurements from the type series of brevicula (Pinedapa; N  =  12) with the specimens Miller and Hollister assigned to centrosa (Gimpu, Winatu, and Besoa; N  =  3). Means for length of head and body (197.0 mm for brevicula, 206.7 mm for centrosa; P  =  0.37), length of tail (239.6 mm and 233.3 mm; P  =  0.80) and length of hind foot (50.3 mm and 51.7 mm; P  =  0.25) are not significantly different.

Specimens (all adults) that Musser collected from Sadaunta (representing centrosa; N  =  6) and those he obtained from Kuala Navusu (representing brevicula; N  =  7) are closely similar in physical size as indexed by means for length of head and body (215.3 mm for brevicula, 213.8 mm for centrosa; P  =  0.70), length of tail (249.9 mm and 241.2 mm; P  =  0.25), and length of hind foot (52.3 mm and 53.2 mm; P  =  0.29), but the Sadaunta sample has slightly larger ears (33.3 mm and 34.8 mm), although the difference is not statistically significant (P  =  0.23); see also table 4. The sample from Kuala Navusu has a larger mean weight (267.3 g) than that from Sadaunta (237.6 g), just the opposite of expectation if brevicula were physically smaller as Miller and Hollister claimed.

Coloration and texture of the fur is similar in the samples of centrosa and brevicula. Both contain specimens with dark gray or dark bluish-gray dorsal coats and white ventral coats, with some individuals showing buffy or rusty streaks on the chest and abdomen. One difference is the shorter ventral fur on the specimens from Kuala Navusu and Pinedapa; all were taken between 31 and 122 m, specimens representing centrosa, with slightly softer and longer fur, are from 400–985 m. Another difference is that the dorsal coat is somewhat softer in the specimens comprising the Sadaunta-Besoa sample compared with the slightly harsher and stiffer fur typical of animals in the Kuala Navusu–Pinedapa series.

It is unclear what Miller and Hollister saw when they described brevicula as having a “less narrowed skull” than either leucura or centrosa—perhaps they meant a skull less narrow, with the implication that it was wider than those in the samples of leucura and centrosa. Specimens in the samples from Pinedapa and Kuala Navusu, as well as those from landscapes to the west at higher elevations (the Sadaunta-Besoa population sample), do have appreciably smaller skulls compared with the northeastern peninsular E. leucura, as does all the material at hand from places west of the Gorontalo region (figs. 5, 6; table 6).

Restricting the focus to the core of Sulawesi, there are significant differences in univariate means between the Kuala Navusu–Pinedapa (brevicula) and Sadaunta-Besoa (centrosa) samples for eight cranial dimensions. Most means for the Kuala Navusu–Pinedapa sample average smaller, including interorbital breadth as well as breadth and height of braincase, three variables that could be used conceivably to index degree of cranial narrowness—in this case brevicula actually has a more narrowed skull, not a “less narrowed skull,” as contrasted with centrosa. Significant differences between means for other variables highlight the average longer skull in centrosa, its longer diastema and bony palate, wider incisive foramina, but narrower mesopterygoid fossa (table 6). For the other cranial measurements, as well as the dental variables, there are no significant differences in mean values between the Kuala Navusu–Pinedapa and Sadaunta-Besoa samples. Keep in mind the dissimilar sample sizes involved (N  =  19 for Kuala Navusu–Pinedapa, N  =  7 for Sadaunta-Besoa), each containing a range in age from young-to-old adults.

The mensural differences noted here are reflected in a principal-components ordination where most of the scores for Sadaunta-Besoa congregate to the right along the first axis of the scatter plot but overlap those signifying the Kuala Navusu–Pinedapa sample to the left (fig. 13), a pattern influenced by the moderate to large positive correlations for 13 of the 18 variables (r  =  0.39–0.83; table 10) a measure of the average larger means for some measurements in the Sadaunta-Besoa series. Whether these univariate mean distinctions seen in samples at hand measure real geographic variation in the two populations will have to be determined by study of larger samples equal in number of specimens and equal in age classes. Nevertheless, present evidence from phenetic traits associated with skins, skulls, and teeth persuades us that the sample from Kuala Navusu and Pinedapa, corresponding to what Miller and Hollister described as E. brevicula (originally based on the sample from Pinedapa), represents a coastal lowland population of E. centrosa with slightly shorter ventral fur, harsher dorsal coat, and some cranial dimensions that average smaller. This specific homogeneity is reinforced by sucking lice (Anoplura): hosts in the Kuala Navusu–Pinedapa sample as well as those in the west-central highlands (Sadaunta-Besoa sample) are parasitized by the same species of louse, Polyplax beaucournui, n. sp. (see the section describing ectoparasites of Echiothrix).

Fig. 13.

Scatterplot of specimen scores representing the sample of Echiothrix “centrosa” (Sadaunta-Besoa; asterisk; N  =  7) and the two population samples of E. “brevicula” (Kuala Navusu–Pinedapa; filled circle  =  Kuala Navusu, empty square  =  Pinedapa; N  =  19) projected on first and second principal components extracted from principal-components analysis of 16 cranial and two dental log-transformed variables. See table 10 for correlations (loadings) of variables with extracted components and for percent variance explained.

Table 10

Results of Principal-Components Analyses Comparing Samples of Echiothrix “centrosa” (Sadaunta–Besoa) and E. “brevicula” (Kuala Navusu–Pinedapa)

Correlations (loadings) of 16 cranial and 2 dental log-transformed variables are based on 16 E. leucura and 30 E. centrosa. See figure 13.

Habitat:

All specimens of E. centrosa obtained by Musser were trapped in primary tropical lowland evergreen rain forests in the watershed of Sungai Sadaunta and lowlands containing Kuala Navusu. Summaries of ambient air temperatures, relative humidity, and days of rainfall compared with days of trapping for Sungai Sadaunta and Kuala Navusu are listed in table 11. Ten to 12 consecutive wet months and up to two consecutive dry months dry months are the rainfall patterns for the drainage basin of Sungai Sadaunta, which places it in a “permanently humid” zone. Five to six consecutive wet months and three or fewer consecutive dry months are usual for Kuala Navusu on the eastern coastal plain, a “slightly seasonal” region (see Whitten et al., 1987: 22). Mean annual rainfall in both areas is about 3000 mm (Whitten et al., 1987: 25).

Table 11

Ambient Air Temperatures, Relative Humidity, and Rainfall Patterns at Sungai Sadaunta and Kuala Navusu^a

Examples of the forest habitats occupied by the shrew rats around Kuala Navusu are depicted in figures 14 and 15; images of streamside habitats along Sungai Sadaunta can be found in Musser (1982: 26–29).

Fig. 14.

Tropical lowland evergreen rain forest on terrace behind camp at Kuala Navusu, 38 m, the habitat of Echiothrix centrosa. A tall canopy pohon benoa (Octomeles sumatrana) on the right and subcanopy Neolamarckia macrophylla on the left bracket a dense understory of shrubs, tree saplings, ferns, young palms—mostly Licuala celebica, Livistona rotundifolia, and rattan rosettes of Calamus and Daemonorops—and a small clearing formed when a subcanopy ebony (Diospyros macrophylla) was uprooted during a storm. Photographed in 1975.

Fig. 15.

Tropical lowland evergreen rain forest on hillsides above rocky stream bed, Kuala Navusu, 38 m. During the night, Echiothrix centrosa (AMNH 225678; see table 12) and Rattus hoffmanni were caught upstream where a decaying tree trunk spanned the rocky creek bed; the squirrels Prosciurillus alstoni and Rubrisciurus rubriventer were taken during the day on the same spot. The rats Maxomys hellwaldii and Paruromys dominator were frequently trapped on this hillside forest as well as six other species of murines (see table 12). Photographed in 1975.

Along Sungai Sadaunta and at Kuala Navusu, traps were placed on the ground, on top of decaying tree trunks lying on the forest floor, and above ground at different levels in the understory. Cage-type live traps, Sherman live traps (10 inch), Victor snap traps, Museum Special snap traps, and Conibear (single spring #110) body gripping traps were employed. In both areas, all E. centrosa were taken only with the Conibear traps set at ground level, two in runways along decaying tree trunks resting in hillside forest near a stream or wet ravine, 12 on decaying tree or palm trunks spanning streams in dense streamside forest. Summaries of habitats at trapping sites are provided in table 12.

Table 12

Summary of Microhabitats in Primary Tropical Lowland Evergreen Rain Forest and Stomach Contents for Specimens of Echiothrix centrosa Collected in Central Sulawesi, 1974–1975

Table 12

(Continued)

Diet:

Echiothrix centrosa is an aggressive earthworm (oligochaete) predator. Earthworms form the primary component of its diet, but a variety of insects along with geophilomorph centipedes are also eaten (table 12). Musser determined the foods eaten by examining contents of stomachs (table 12) and offering different foods to a captive young adult male (AMNH 225682/ASE 3448) caught by the tail in a Conibear trap at Kuala Navusu on October 15, 1975 (table 13). The following descriptions of feeding behavior of the male are summarized from Musser's observations recorded at camp.

Table 13

Earthworms and Insects eaten by a Captive Echiothrix centrosa^a

Earthworms: Echiothrix sports a unique set of adaptations for handling earthworms. The upper incisors are short, their anterior surfaces scored by shallow grooves, the cutting edges chisel shaped; the lower incisors are long and slender, with smooth faces and sharp tips. The connection between mandible and cranium is loose, and the dentary symphysis is flexible, which allows tips of the lower incisors to be spread apart up to 5–7 mm. When the mouth is open, the lower incisors curve upward from the lips, and resemble two long, slender, and sharp-tipped miniature white tusks. Held close together (adducted), they form a stabbing lance; with the tips separated (abducted), they are transformed into either a two-pronged spear or a forcepslike gripping instrument. When the mouth is closed and the molars are occluded, tips of the lower incisors rest against the palate just behind the upper incisors. The loose articulation between mandible and cranium allows the rat to open its flexible mouth (gape is about 25 mm) and pull the mandible back and down, so lower incisor tips are 4 mm behind the uppers—it is the mandible that is retracted, not the lower lip, which remains in place. The rat can also launch the lower incisors forward beyond the lips; during all the times Musser watched the rat feeding, the lower lips appeared stationary and the lower incisors were propelled beyond the lips and then retracted into a sheathlike lip receptacle. This behavior and the feeding action described below were observed by Musser who offered the rat individual earthworms or arthropods by hand.

When the rat reaches for an earthworm, it thrusts the lower incisors beyond the lips and separates the tips (this is a purposeful action, as the incisors do not automatically separate as the mouth opens); the two incisor tips form a V. A thick earthworm is immobilized by the rat driving each sharp incisor tip into each side of the worm; a thin worm is held between the incisors in a forcepslike clamp. Whether impaled by the incisor spear or gripped by the incisor forceps, the earthworm is held against the upper incisors, with the uppers pressing down into the earthworm and against the lowers as the rat draws the earthworm up through its paws.

When offered an earthworm the rat quickly seizes it with its incisors and then clasps it between the front feet, pressing it against claws and digital pads of each foot. While clasping the worm between the digits and simultaneously holding it by the lower incisors, the rat jerks its own head upward in a series of rapid thrusts. The worm is hauled up through the digits, which are usually held stationary, and clasped so tightly that with each upward heave of the rat's head the earthworm is stretched and its gastrointestinal contents squeezed out and ejected onto the ground. Sometimes the front feet are wrenched downward to squeeze the earthworm. In this manner the apparently distasteful gastrointestinal contents are removed and the earthworm, now a hollow tube of muscle and other tissue, is pulled up through the front feet and into the mouth. When a small worm was drawn toward the mouth, the lower incisors were opened and then closed lower on the worm's body; a larger worm required the rat to retract its incisors and then thrust them into the worm lower down on its body. Sometimes when very hungry, the rat seems to jab, pull, and suck the earthworm up quickly, then jab and tug again. Usually the bulk of the worm is pulled and swallowed this way and only when the worm tore apart did the rat stop to chew the last part that went into his mouth. Similarly, if the entire earthworm is sucked in without breaking, the rat chews only the last bit; when chewing, it retracts the lower incisors, so they either do not or barely project beyond the lips and upper incisors.

The rat seems to mostly swallow earthworms without chewing, especially the smaller ones; some medium-sized earthworms (8–10 cm long) were pulled apart and others were bitten into segments and then swallowed. There was minimal chewing. Smaller earthworms (4–6 cm) were grasped by the forcepslike clamp of the lower incisors and virtually inhaled without holding them between the front feet. The rat is so quick in acquiring an earthworm, and so swift in consuming it, that several feeding sessions in afternoon light were required before Musser was able to appreciate the process. Medium-sized and smaller earthworms were usually consumed in 1–9 seconds, 15 or 17 seconds at the most (see table 13).

The observed feeding action explains why earthworm segments found in stomachs are empty tubes, and why the front feet become covered with slime while the mouth remains relatively clean. In addition to remains of earthworms, contents of stomachs revealed a muddy fluid smelling of earthworms, partly resulting from the gastrointestinal residue of small earthworms that were swallowed intact and partly from the mucous and muddy liquid cleaned from the front feet after consuming a larger earthworm. Echiothrix does not wipe its front feet on the ground or on leaves (the cleaning behavior typical of the Sulawesian shrew rat Melasmothrix naso) but cleans them with its tongue, swallowing the slime and muddy fluid. During one particular session, the rat was fed about 25 grams of medium-sized and small earthworms, and only after all were offered and eaten did he clean himself, shaking each front foot in the air several times, then licking one paw by holding the forearm with its opposite paw, and repeating the process on the other foot.

The behavior described above was observed when the rat was provided with medium-sized (8–10 cm long) and small (4–6 cm long) earthworms. Below are two examples of the rat's behavior when given larger worms. When Musser fed the rat an earthworm 15 cm long and 6 mm thick, the rat grabbed the worm, extended the lower incisors 4–5 mm beyond the lips and separated the tips for about the same distance. He speared the worm from below while at the same time sinking his upper incisors in from above. He then manipulated the worm until one end was up and in the mouth. He proceeded as he usually did with smaller worms, but thrust the lower incisors deeper into the earthworm and held the tips farther apart so each tip penetrated a side of the worm; Musser could see the lower incisors penetrate the worm and the gut contents spurt out with each thrust. At times, the earthworm broke into segments as it was pulled up through the paws. The rat finished with a piece in his mouth and then quickly stabbed segments that had fallen to the cage floor, transferring each to his mouth. The lower incisors were actually thrust forward from the lip sheath, the tips separated and driven into the body of the worm, like a two-pronged spear.

The second example shows the rat's reaction to an earthworm 23 cm long and 1 cm thick, which was consumed in 3.5 minutes; during the first 2 minutes he stopped eating at intervals and cleaned his front feet of sticky slime that was hindering manipulation and ingestion of the worm. The rat started at the head end by thrusting the separated lower incisors forward and spearing the worm, which was so thick that he had to spear it about three times, nearly severing the earthworm, and he separated the segment from the remaining body and ate it. Because the worm was long and thick bodied, the rat had to eat slowly and take in short segments, about 5 mm long. He seemed to have difficulty swallowing some of these segments, spitting them out onto the ground and breaking them apart with the incisors before picking up and ingesting the resultant fragments. Eventually he worked down the worm, gradually taking larger segments after he got past the thick middle; nearly all thrusts of the separated incisors (spread about 4 mm) through this thick part of the worm penetrated the body about 2 mm and either held the worm against the upper incisors while the rat pulled its head back and up, or were instantly retracted and thrust forward again until the worm was almost severed again and the segment pulled off the main body. Several times the rat moved the incisors up, retracted, thrust again, moved the worm up a bit, then thrust again and held the worm tight while the rat pulled its head back and up in rapid sequence. After the anterior third of the earthworm was consumed, the rest was eaten more quickly with the rat pulling and then cutting 5-cm segments; finally he slurped in the last 7 cm, leaving his front feet covered with muddy fluid and slime. A cord of gastrointestinal contents mimicking the shape of the worm was left lying on the leaf litter. By licking and shaking his front feet, he cleaned them of worm fluid and slime; this was followed by cleaning his lips, rhinarium, and finally face. The earthworm slime was viscous and thick, and the rat had to forcefully pull apart his feet several times because they kept sticking together.

We lack data about size of earthworms selected by the shrew rat during a night's foraging, but suspect that very large earthworms would be avoided, unless perhaps very hungry. Only remains of medium-sized (8–10 cm long) and small earthworms (4–6 cm long) were found in the stomachs surveyed, and those smaller worms are consumed more quickly (usually between 1 and 9 seconds) than very large worms that take minutes to eat, which would leave the rat exposed for a longer time to potential nocturnal predators.

Bunomys chrysocomus, B. andrewsi, and Maxomys hellwaldii, which occur in the same habitat as Echiothrix centrosa in the west-central highlands as well as the eastern coastal plain (see tables 15 and 16) include earthworms in their diets, but they are less efficient consumers. All three grab an earthworm with the incisors and quickly transfer it to the front feet where it is held in the same way as Echiothrix does. Bunomys and Maxomys do not pull the earthworm up through the front paws but bite and pull apart a segment (usually 1 cm long), chew it, then bite and pull off another segment until the earthworm is consumed. None of these rats squeeze the gastrointestinal contents out, but eat everything—the worm is writhing right up to the last few millimeters and the rat's front feet and muzzle are covered with the worm's stomach and intestinal contents (basically a thick muddy liquid) along with sticky mucous. Because Echiothrix squeezes the gastrointestinal contents out of the medium-sized earthworm, nothing is left but the hollow body—the last third or fourth of the earthworm appears lifeless, and only the rat's paws are covered with muddy fluid and slime.

Compared with Echiothrix, the two species of Bunomys and Maxomys hellwaldii take longer to consume earthworms. Earthworms averaging 5 cm long were consumed in 3 to 14 sec by captive Bunomys chrysocomus; earthworms 10 cm long were completely ingested after 57 to 145 sec. One B. chrysocomus took 5 min to eat a 15 cm long annelid that it first had to bite into several pieces. Medium-sized and small earthworms are consumed in 16–54 sec by Bunomys andrewsi, and in 17–42 sec by Maxomys hellwaldii. Earthworms of comparable size are usually eaten in 9 sec or less by Echiothix centrosa (table 13; data summarized from Musser's field journals). None of the Bunomys or Maxomys individuals observed swallowed the earthworm whole as Echiothrix centrosa did with small and some medium-sized earthworms, but bit off segments that were generally chewed and then ingested.

Beetle (Coleoptera) larvae: The shrew rat was offered a large beetle larva (12 cm × 1 cm), which he attacked quickly, thrusting the spread lower incisors into the thorax behind the head capsule and penetrating the tough skin. The rat then withdrew the incisors and ignored the grub. Musser retrieved it and found three places where the exoskeleton had been split by the splayed incisor tips. When the rat attacked a medium-sized earthworm he spread the lower incisor tips 2–4 mm apart but for something like the large grub, or very large earthworm, he opened the incisors wider and lunged with incisors thrust out and spread, moving very quickly.

A huge beetle larva (10 cm × 2 cm) was offered, which the rat tried to eat; he opened his mouth wide and got purchase on the larva but could not penetrate the tough skin, and after several attempts abandoned the grub. Musser retrieved the larva, cut it open and offered it to the rat. This time the rat used his lower incisors to scoop out the soft insides of the abdomen and left the head capsule, thorax, and tough abdominal skin on the cage floor.

All smaller beetle larvae (5 cm × 5 mm) offered were readily accepted and entirely consumed. Larvae of this size are not sucked up like the earthworms; rather the rat holds the larva between its front digits, bites into one end and pulls up, then chews, bites again, pulls its head up again and chews. He took longer to consume a beetle larva than to consume several medium-sized or large earthworms.

A large adult beetle was offered and the shrew rat attacked it as he had other adult insects, biting at the head and thorax; however, after several attempts he shied away from the beetle. His incisors made shallow dents in the sclerites of the thorax but nowhere else. Musser retrieved the insect and sliced open its thorax and abdomen and again offered it to the shrew rat; this time he eagerly consumed the soft insides. Apparently the thickly sclerotized exoskeleton of large adult beetles is too hard to penetrate, and no such remains were found in stomachs of other Echiothrix examined.

Other insects: The rat was offered a small green cicada (Hemiptera: Cicadidae), which he first seized with the incisors and then transferred to his front feet, manipulating it until the head was up. He then bit the insect's head and proceeded to consume head, thorax, and abdomen—wings and legs were discarded (a behavior common to Sulawesi murines that prey on winged stages of insects). Two katydids (Orthoptera: Tettigoniidae) and two adult cockroaches (Blattodea) were attacked, handled and eaten in the same manner (table 13).

A mole cricket (Orthoptera: Gryllotalpidae) was offered to the rat, which he chased around the cage and eventually pinned to the cage floor with his front feet. He began eating the posterior end but the cricket easily crawled away. The shrew rat did not seem to know how to dispatch this particular cricket. However, later another mole cricket was offered, this one 6 cm long, which was attacked and finally eaten in 6.5 minutes.

Snails: Snails are consumed but probably infrequently and likely only small ones. Musser offered the shrew rat a snail 2.5 cm in diameter. He tried to break the shell by biting it but could only flake off a few pieces of the outer layer; then he attempted to bite off pieces near the opening but was unsuccessful and dropped the snail. After extracting the soft snail body, Musser offered it to the shrew rat but this was also ignored. The shrew rat did accept a small snail 10 mm in diameter and consumed the soft body extracted by Musser in 106 seconds. Of the other shrew rats Musser collected, none had remains of snails in their stomachs.

Rejected foods: Fruits from a variety of trees, shrubs, woody and herbaceous vines, palms, other plant parts, ferns, and several kinds of fungi were offered to the captive shrew rat but were always ignored; no evidence of these kinds of foods was found in the contents of stomachs.

Yearly dietary regimen: An aspect of understanding the complete range of foods consumed by a species is any seasonal variation in dietary composition during a yearly cycle. Stomach contents from Musser's collection of E. centrosa, consisting of adult males and females, obtained during a period of seven months (September to March) suggests that throughout most of a year, and probably the full 12-month cycle, earthworms form the predominant prey as compared with insects and other invertebrates. This is a reasonable hypothesis springing from available data, but requires testing by study of food preferences during an entire year derived from larger samples of shrew rats living throughout a more expansive geographic region of Sulawesi. Such an inquiry should also determine the dietary composition of postweaning juvenile shrew rats to determine the relative percentages of earthworms versus insects or other invertebrates in their diets, along with size of the prey.

Earthworms should be accessible to shrew rats year-round in the Sungai Sadaunta watershed and along the coastal plain that encompasses Kuala Navusu. Neither region is typified by strongly seasonal rainfall patterns (Whitten et al., 1987: 21 note that the “climate of Sulawesi is best described with reference to rainfall since temperature is relatively constant [table 11], and other climatic variables such as wind velocity, evaporation and humidity change within even small areas”). Ten to 12 consecutive wet months and up to two dry months are the rainfall patterns for the drainage basin of Sungai Sadaunta, which places it in a “permanently humid” zone (Whitten et al., 1987: 22). Kuala Navusu is located in a “slightly seasonal” region where generally five or six consecutive months are wet and three consecutive months or less are dry (Whitten et al., 1987: 22). During the 57-day period in which the rats were captured along Sungai Sadaunta, there were 23 days without rain or with only sprinkles; rainfall during 34 of the days averaged 35.2 mm with a range of 1–175 mm. At Kuala Navusu where examples of E. centrosa were caught during a 45-day period, there were 19 days with no rain or sprinkles only; rainfall during 26 of the days averaged 38.2 mm with a range of 1–230 mm. October is usually the driest month in both areas (Musser's experience, and assertions by the local people). Even during the relatively driest interval, earthworms were available as prey for E. centrosa for they were found in stomachs of rats trapped during that period, and Musser collected samples of earthworms from different parts of the forest (see below).

Prey distribution in the forest: Although Echiothrix centrosa (and presumably E. leucura) preys primarily on earthworms, soft-bodied coleopteran larvae are also taken, as well as other kinds of insects (mole crickets, katydids, cockroaches, and rhinotermitid termites were either found in contents of stomachs or accepted and consumed by the captive shrew rat), and geophilomorph centipedes. Near camp on the Kuala Navusu (August 28–November 30, 1975), Musser searched for places on the forest floor where Echiothrix centrosa might find invertebrates, particularly earthworms, and during the night after a rain located earthworms scattered on the clear ground surface, beneath leaf litter, or in pools of water near the stream. During the day he found them in rotting sections of tree trunks and limbs or in the underlying soil. He also found burrows, each marked by a pile of processed soil, some as tall as 5 cm. Several small worms occupied a single burrow and were found 5–15 cm below the ground surface. Burrows were always on well-drained slopes or stream terraces. Because the earthworms are spotty in their distribution, it is difficult to provide any meaningful estimate of worms available to E. centrosa per unit area. Musser did find one place on a steep hillside above a wet ravine where a piece of wood had decayed into slivers. The soil was stable. He collected 21 earthworms (8 grams total) within a square meter; all occurred throughout the soil from near the surface to a depth of 15 cm.

The most common site for both large and small earthworms was within and beneath rotting trunks and limbs from old tree falls. At a certain stage of decomposition the wood becomes soft and is mixed at soil level with a dense gray or bluish-gray claylike layer; the worms are in this layer, and in passages within the damp and rotting pulpy wood.

In addition to earthworms, decaying sections of old tree falls lying on the forest floor also provide habitat for a variety of other invertebrates, some of which are eaten by E. centrosa. Musser tore apart a long section of rotting trunk (5 m long, 30 cm in diameter) lying on a terrace about 3 m above a stream. The pulpy wood was saturated with water and the underlying claylike layer nearly liquefied. Pigs had ripped open the trunk in places. Musser extracted 30 grams of invertebrates (excluding termites—the terrestrial rhinotermitid termites, which infested the entire trunk and were too numerous to collect and weigh): 21 earthworms (some large, up to 13 cm long, most were smaller, 5–8 cm), three mole crickets, and six adult and nymphal cockroaches.

Prey procurement: Musser observed only captive Echiothrix held in a cage. While he did not see shrew rats at night searching for food in the forest, some inferences regarding behavior in procuring prey can be made based on the physique of the shrew rat. Echiothrix has a long muzzle, very large ears, a tail that is longer than combined head and body, delicate front legs with small feet and moderately large and stout claws, and strong hind legs with elongate and robust hind feet (fig. 4). The long muzzle reflects the underlying long and narrow bony rostrum containing extended turbinals, likely well suited for probing in loose leaf litter and sniffing out earthworms. Large ears may also help detect scraping movement of prey as they move through and beneath decaying leaves on the forest floor. The front claws are not as large relative to body size and don't seem to be as adapted for digging as those seen in species of either Melasmothrix and Tateomys (Musser, 1982) or Paucidentomys (Esselstyn et al., 2012), the other Sulawesian shrew rats; the claws of Echiothrix are stout and appear sufficiently robust to excavate earthworms from moist subsurface soil layers and to dig into old tree falls lying on the forest floor where the wet wood has decayed to a soft and spongy texture. One female E. centrosa, caught in a Conibear trap set on a decaying limb bridging the Sungai Sadaunta, had soil and debris matted on the fur beneath the chin and on parts of the front legs. In addition to excavating earthworms, we can imagine the rat separating loose leaf litter and other debris on the forest floor with its muzzle and front feet, and pouncing on the uncovered earthworms and small arthropods, sometimes inadvertently ingesting small pebbles and woody fragments (found in some stomachs). Should a predator approach, its presence might be picked up by the large ears and escape accomplished by the rat instantly leaping away in unpredicted directions.

Miscellaneous Behavior:

When the shrew rat sits, resting or during feeding, its body rests on the entire lengths of the hind feet, the rump about 5 mm off the ground and the tail lying stretched out behind, so the weight is on the hind feet and an appreciable length of the tail. It stands and moves about only on its digits and interdigital pads.

The captive rat was quiet most of the time. When he vocalized he never squealed or screamed but emitted a rusty eh-eh-eh-eh-eh with a slight warbling quality.

Spinous Fur:

Function of the spinous dorsal pelage of E. centrosa (and E. leucura) is unknown. It is unlikely that predators are deterred by the spines because the long and broad spines are flexible, and the dorsal coat is unlike the bristly and rigid spiny fur of porcupines and hedgehogs. Furthermore, Musser never saw the captive shrew rat erect the hairs of the dorsal coat, even when disturbed. Avian predators, presumably owls because the shrew rats are nocturnal, would simply use their talons to seize the shrew rats, then fly to their roosts and pick the rats apart with their sharp beak, avoiding the spinous hairs. The endemic Sulawesi palm civet, Macrogalidia musschenbroekii, which Musser encountered on his transects, is an agile and aggressive predator and could stalk and capture a shrew rat, crunching it between the jaws without hindrance from the spinous fur (the other viverrid occurring on Sulawesi, the nonnative Viverricula indica, is a bumbling and inept rodent predator judged from Musser's observations). Nocturnal snakes are the other kind of predators, and by manipulating the shrew rat so the head is swallowed first and the fur laid back against the skin they can swallow a rat without any resistance from the flexible spines in the coat.

One possible function of spinous fur was suggested to Musser by Joe T. Marshall, who trapped rodents throughout Thailand. He thought the spinous hairs would trap drops of water coming off wet vegetation, misty air, or rain and suspend them long enough for the rat to shake the drops from the fur before they wet the skin. In tropical lowland habitats where ambient temperatures and relative humidity are high (table 11), drying fur would be problematic for nonamphibious species if the fur became soaked to the skin. At the prompting of David Johnson, formerly a curator in the Mammal Division at USNM, Marshall sprinkled two Thai spinous-furred Maxomys surifer and two soft-furred Rattus rattus. The broad and flat flexible spines in the dorsal coat of M. surifer are channeled with the concave surface facing dorsally on the back. Marshall's (1988: 402) observations are worth repeating:

To test Marshall's observations, Musser sprinkled a caged Echiothrix centrosa and a Margaretamys beccarii; the latter is a small-bodied arboreal rat with spinous dorsal pelage very similar in texture to the fur of Echiothrix (Musser, 1981). The shrew rat did not shake its fur but simply ran from the water source and cowered in a corner of the cage. The Margaretamys shook its body in a fashion similar to the motion described by Marshall for Maxomys surifer. As the water hit the fur of both the Echiothrix and Margaretamys, it collected into drops held by surface tension to tips and channeled surfaces of the broad spines and tips of the soft overhairs and guard hairs. The drops remained attached for a minute or so before breaking up and running down the hairs to wet the underfur and skin. The drops were flung off the fur when the Margaretamys shook its body, and had the shrew rat not been so timid it would have shaken off the drops in a similar manner.

When Musser sprinkled soft fur, such as that covering species of Bunomys held in cages, the water also collected as drops at the tips of the hairs. Droplets quickly coalesced into large drops, which sank deeper into the fur, still adhering to the hairs without falling to the skin, but soon flowed downward to wet the skin; none of the Bunomys shook themselves and their fur would have become soaked had Musser continued sprinkling them. So, with both small and large drops, the rat can remain relatively dry by shaking the drops off shortly after they hit the fur; if the rat waits too long the water sinks to the skin.

It is important that rats keep their fur dry. Droplets from mist and dripping vegetation that fall on the fur can be shaken off with the fur retaining its insulation qualities. The fur would become soaked should rats fall into a stream or have to run through shallow pools. In the ambient environments along the Sungai Sadaunta and at Kuala Navusu where temperatures and relative humidity are high (table 11), it would be difficult for the animals to dry their pelage, thus impairing the insulative quality of the coat and possibly producing deleterious changes in body temperature; also time required to dry and groom the fur would impose on time necessary for foraging. Some soft-furred rats that Musser trapped in cage live traps, such as Bunomys chrysocomus were soaked because the trap had been placed too close to the spray from waterfalls, or the rat had knocked the trap into a stream, or the trap was unprotected from a night's rain. Back at camp, the animals made no attempt to dry their fur; by day's end, the coat was partially dry from evaporation and despite the rat's attempts to fluff out the fur, it remained matted and difficult to groom; some animals did not recover their health. This was the typical reaction observed for most of the soaked soft-furred species trapped alive.

Whether one function of a dorsal spinous coat is to deter accumulation of water is an aspect that requires more rigorous inquiry. However, the reaction of the rats to being sprinkled or soaked bears on results from setting traps on decaying tree trunks and limbs spanning streams and ravines, highlighting the importance of these pathways over natural bridges for rats. In the regions where Musser worked, heavy rains cause streams and rivers to rise, often to the level of flooding their banks, and filling hillside ravines that are normally dry. Tree and palm trunks or tree limbs extending from one stream terrace to the other that are resting on terraces high enough to escape inundation from runoff provide reliable crossing points for rats, woody connections allowing them quick access to the forest on the other side without becoming soaked. At times of low water, rats may use crossing places where they can scramble across on exposed stones or decaying pieces of a tree fall scattered on the stream bed, but during flood the higher links formed by downed trunks and limbs are safer. All six of the shrew rats caught along the Sungai Sadaunta were taken on tree or palm trunks or limbs connecting opposite stream terraces; six of the eight E. centrosa caught at Kuala Navusu were also trapped on similar kinds of bridges over streams and wet ravines (table 12). Examples of the majority of the species of murines caught along Sungai Sadaunta and at Kuala Navusu (tables 15, 16) were also trapped on decaying sections of tree falls spanning streams and ravines (Musser's field journals).

Reproductive Insights:

The six examples of E. centrosa from Sungai Sadaunta and the eight from Kuala Navusu that Musser collected consist of old adults, adults, and young adults; most were obtained during September, October, and November. The old adults and adults were sexually mature (females with large teats, either lactating or not, and containing embryos; males with large scrotal testes and sperm in the epidydimis), and the young adults sexually immature (females with tiny teats, vagina sealed; males with small abdominal testes). All the specimens from Sungai Sadaunta and Kuala Navusu are listed in table 14 and provide examples of general reproductive status in relation to body size, pelage condition, and date of collection.

Table 14

Dates of Collection, Sex and Age, Physical Size, Reproductive Aspects and Pelage Condition of Adult Echiothrix centrosa Collected at Sungai Sadaunta and Kuala Navusu

Measurements are in millimeters, weight in grams. Measurements of testes (T) include the epididymis and are from the fluid-preserved carcasses and intact specimens. All females have two pairs of inguinal teats. Information is extracted from specimens and Musser's field journals (stored in Mammalogy Archives, AMNH).

Table 14

(Continued)

Presumed litter size is documented by only one female (AMNH 225683) caught September 12, 1975, at Kuala Navusu, which had three embryos (each 10 mm long) in the left horn of the uterus (table 13); gestation period is unknown.

Although the period of time during which the rats were collected is short (September to November, one record in March) and the sample size of animals small (14), the data indicate that adults are reproductively active from September to November and likely through to March.

Whether mating activity and birth is year-round or seasonal cannot be determined with the present information, but possibly shrew rats become sexually mature and bear young throughout the year. Neither the west-central highlands containing the watershed of Sungai Sadaunta nor the coastal plain to the east at Kuala Navusu are typified by strongly seasonal rainfall patterns (see preceding section); it is unlikely that nesting sites and prey resources are available during the entire year.

Nests:

Unfortunately, Musser was unable to locate nesting sites in the forest. Observations on nest construction are based on a captive young adult male collected at Kuala Navusu. The rat was provided with a fresh pile of dry leaves into which he burrowed and slept. Eventually as the leaves compressed, the rat arranged them about him in a loosely constructed partial sphere; after the leaves were compressed even more, he slept on top of the mound in a shallow round depression and did not attempt to build a high enclosure even though there were plenty of leaves scattered on the cage floor. Only when Musser gathered all the leaves and piled them in a corner did the rat burrow into them rather than sleeping on top.

Sympatry:

Echiothrix centrosa shares its forest habitat with other species of murines that are also endemic to Sulawesi. Along with E. centrosa, samples of 15 other species were collected in streamside and hillside forests along Sungai Sadaunta (table 15); samples of nine species were collected in addition to E. centrosa in the Kuala Navusu area (table 16). Many were taken in the same traplines that yielded E. centrosa.

Table 15

Echiothrix centrosa and 15 Sympatric Species of Murines Collected in Primary Lowland Tropical Evergreen Rain Forest at Sungai Sadaunta in the West-Central Highlands (1973–1976)

Information was gathered during 1973–1976 and is summarized from Musser's field journals (stored in Mammalogy Archives, AMNH).

Table 16

Echiothrix centrosa and the Nine Sympatric Species of Murines Collected in Primary Lowland Tropical Evergreen Rain Forest at Kuala Navusu in the Coastal Lowlands East of The West-Central Highlands

Information was gathered during 1975 and is summarized from Musser's field journals (stored in Mammalogy Archives, AMNH).

Our understanding of the ecological interactions between E. centrosa and the other species is limited to the observational data listed in the categories (elevation, terrestrial or arboreal, number of teats, litter size, and diet) presented in tables 15 and 16. One interactive aspect that is of special interest is the possible resource competition between E. centrosa and the other murines that also include earthworms in their diet. In the forests along the Sungai Sadaunta, the terrestrial and nocturnal Bunomys chrysocomus, Bunomys andrewsi, Maxomys hellwaldii, and Maxomys dollmani devour earthworms, although they comprise only one element in each of their diets (table 15). Of these species, B. chrysocomus was the most frequently collected (43% of the total specimens representing all species), samples of the four species combined make up 52% of the murines trapped (table 15). At Kuala Navusu, Maxomys hellwaldii and Bunomys andrewsi are the only potential vemivorous competitors with E. centrosa; the former was common and easily caught (69% of the total sample of all species), the latter less so (5%). At both Sungai Sadaunta and Kuala Navusu, E. centrosa constituted less than 2% of all specimens collected.

Judged by relative numbers of each species trapped, the anecdotal evidence suggests that along the Sungai Sadaunta, Bunomys chrysocomus would be the most important earthworm competitor with Echiothrix centrosa. This potential competition is strengthened because both species were trapped in environments that remain wet and humid—streamside habitats and at the bottom of hillsides adjacent to streams—and not on steep slopes and ridgetops that tend to dry out sooner than streamside environs.

Maxomys hellwaldii is the obvious competitor with Echiothrix centrosa for earthworms at Kuala Navusu. Here the competition may not be as potentially intense. Maxomys hellwaldii was trapped in a range of habitats, from streamside to ridgetops; E. leucura was taken only in streamside environments.

At both places, these observations need to be bolstered by more rigorous study of relative dietary composition over the course of a 12-month cycle or longer that incorporates both dry and wet periods before any significant conclusions regarding competition among these earthworm-eating rodents can be drawn. Some questions that require answers come to mind. What percent of the diet of B. chrysocomus and M. hellwaldii consists of earthworms compared with the dietary components of E. centrosa? Are earthworms taken during both wet and dry periods throughout a year by M. hellwaldii and B. chrysocomus or do other foods comprise the bulk of their diets during certain months? Are there certain times of the year when E. centrosa consumes fewer earthworms and more insects and other invertebrates? What is the availability of earthworms and other invertebrates, and their respective mass for consumption, in streamside habitats during a 12-month cycle or longer? Do postweaning juveniles have the same dietary range as adults during a given surveyed period of months (the data we discuss are obtained from adults)?

Another aspect requiring investigation is the abundance of Echiothrix centrosa relative to the other earthworm consumers along Sungai Sadaunta and at Kuala Navusu, especially the more abundant Bunomys chrysocomus and Maxomys hellwaldii. Examples of those two species were readily caught by live traps and kill traps (a cage-type live trap, 10 inch Sherman live traps, Victor and Museum Special snap traps, and Conibear traps), but only the Conibears took E. centrosa. Musser baited all the traps with a mixture of oatmeal, raisins, bacon, and peanut butter. Earthworms were used as bait for a few nights, but they attracted more B. chrysocomus and M. hellwaldii and, during the early morning, birds. Whether the relatively low densities we record for E. centrosa at both localities is real or an artifact of trapping technique is unknown. Any future study of competition between E. centrosa and other syntopic murine earthworm consumers will have to include firm data on relative densities of these vermivore predators.

Skull:

General conformation of the cranium behind the rostrum is not unlike other murines: the interorbital region is moderately wide, the zygomatic arches are robust and flare out from the sides of the cranium, the zygomatic plate is moderately wide with a narrow anterior spine (shallow zygomatic notch), and the boxy braincase is wide and deep (see figs. 5 and 6 and cranial portrayals of various species in Musser and Newcomb, 1983) showing expansive surfaces for origin of the temporal musculature.

The notable specializations in the skull involve the rostrum and pterygoid region. The very long, slim, and tapered rostrum is distinctive and encloses long sets of turbinals covered in nasal mucosa. This extended surface of epithelium likely enhances olfactory sensitivity that may be required to distinguish the scent of earthworms from ambient background odors redolent in the strong vegetative and earthy fragrances emanating from wet and decaying leaves, rotting tree falls, wet moss, and soil. Also, Samuels (2009: 880) has suggested that rostral elongation “increases the velocity of closing the mouth, which facilitates the capture of prey.”

Morphology of the pterygoid region of Echiothrix is extremely simplified. As we have described previously (see description of E. leucura), the pterygoid plates no longer exist as significant structures and are represented by only inconspicuous vestiges (see figs. 7 and 8). This transformation from the common design likely includes modification of the pterygoid musculature.

We have not dissected musculature in the pterygoid region and do not know whether those muscle groups would show changes from the usual murine condition that might be correlated with loss of the typical horizontal and wide pterygoid plates. Still, it is productive to conjecture on possible modifications of the relevant muscle groups, speculations that can be tested by actual dissection. Two primary muscles, the external and internal pterygoids, originate from the pterygoid-alisphenoid region of muroid rodents (Greene, 1935; Rinker and Hooper, 1950; Rinker, 1954; Turnbull, 1970; Voss, 1988; Satoh, 1997; Satoh and Iwaku, 2004, 2006, 2008).

The external pterygoid muscle (M. pterygoideus externus) originates from the lateral surface of the anterior third of the pterygoid plate, from the adjacent surface of the alisphenoid bone anterior to the groove for the masticatory-buccinator nerves, and from the segment of the maxillary just behind the molar row; it inserts on the medial surface of the articular (condyloid) process of the dentary (origin and insertion is nicely visualized in fig. 6 in Thorington and Darrow [1996, as the “lateral pterygoid”] and in figs. 10 and 11 in Satoh and Iwaku [2004]; also see Turnbull, 1970: 231). Acting together, the external pterygoids protract the mandible—depressing the lower jaw in the case of Echiothrix, and launching the incisors forward to either spear an earthworm or grip it in the forcepslike V of the incisor tips. In the shrew rat, the bulk of this muscle may originate mostly on the broad alisphenoid and bit of maxillary just behind the third molar because the anterior lateral margins of a pteryoid plate are represented only by vestigial ridgelike bony slivers; between origin on the alisphenoid and portion of the maxillary, possibly with some fibers on the vestigial pterygoid margins, and insertion on the robust condyloid process, the muscle's action may be only moderately suppressed over what it would be in a murine showing the usual pterygoid configuration, such as seen in Maxomys (figs 7D, 8D), Onychomys, (Satoh and Iwaku, 2006), or Rattus (Turnbull, 1970), for example. Retaining substantial external pterygoid muscles would be critical for Echiothrix's ability to depress the mandible and extend it forward so the long, slender, and sharp-tipped incisors can be thrust beyond the tips of the upper incisors. The mylohyoid group of muscles, especially the digastric complex, would join the external pterygoids in depressing the mandible (open the jaw) and would also act to retract it.

The internal pterygoid muscle (M. pterygoideus internus) originates from the pterygoid fossa (which is the ventral surface of the pterygoid plate, usually excavated to some degree) and inserts on the medial surface of the angular process and dorsal surface of its inflected ventral border (see fig. 6 in Thorington and Darrow [1996, identified as “medial pterygoid”], figs. 10 and 11 in Satoh and Iwaku [2004], fig. 12 in Satoh and Iwaku [2006], and p. 231 in Turnbull [1970] where origin and insertion is diagrammed). Acting together and in concert with the temporal and masseter muscles, the internal pterygoids elevate the mandible (close the jaw); acting alternately they pull the mandible from side to side; and overall assist in mastication.

Landry (1970: 363) has coined the name “mandibular sling”

While the large angular process on the dentary of Echiothrix provides expansive surface for insertion of the internal pterygoid on its medial surface (as well as the superficial masseter), the site of origin is problematic because there is no pterygoid fossa. Possibly origin is on the cramped posterior portion of the alisphenoid or on the ventral surface of the narrow shelf that represents a remnant of a pterygoid plate in some specimens (see fig. 7C). Likely the muscle is smaller and the force capable of being exerted weaker than its counterpart in a murine like Maxomys or in those muroids in which dissection has revealed large and substantial internal pterygoids, the usual configuration (examples are the murines Rattus and Apodemus [Turnbull, 1970; Satoh, 1997; Satoh and Iwaku, 2008]; the sigmodontine ichthyomyines, Oryzomys, and Sigmodon [Rinker, 1954; Voss, 1988], the neotomines Onychomys, Peromyscus, and Reithrodontomys [Rinker and Hooper, 1950; Rinker, 1954; Satoh and Iwaku, 2006]; cricetines [Satoh and Iwaku, 2004]; and arvicolines [Kesner, 1980; Satoh, 1997]).

The internal pterygoid muscles, noted Rinker and Hooper (1950: 9) “should be important in crushing and grinding actions of the molar teeth and in gnawing actions of the incisors,” an observation based on dissection of two species of Reithrodontomys. But Echiothrix's molars are very small relative to size of the skull and the cusps low in relief; there is little crushing and grinding of prey. Watching the shrew rat feed (see above), Musser noticed periodic bouts of chewing, only seconds in duration, but typically earthworms, the primary dietary constituent, were either cut into segments and swallowed without mastication or swallowed intact. And there is no functional gnawing—the earthworm is seized using the incisors, either by stabbing or gripping it with the lower incisors and held against the uppers in the process already described (see discussion of diet). Elevating the mandible to close the jaws may rest mainly with the temporal and masseter muscles rather than with the internal pterygoids. Judging from osteological landmarks, the temporal and masseter complex are well developed in Echiothrix. In most muroids, the temporalis (which usually consists of separate parts) originates on the side of the cranium at the back of the orbit, and the squamosal and ventral projection of the parietal; it is bounded anteriorly by the frontal forming the posterior rim of the orbit, dorsally by the temporal ridge and posteriorly by the lamboidal crest. Insertion is on the tip of the coronoid process and anteromedial surface of the dentary between the coronoid process and the end of the molar row (Rinker, 1954; Turnbull, 1970; Satoh and Iwaku, 2006, 2008). Echiothrix's spacious postorbital region, high braincase, and patent temporal and lambdoidal ridges provide expansive surface area for the origin of the temporalis. Although the tip of the coronoid is small, the anteromedial margin of the dentary between the coronoid tip and the end of the molar row (the retromolar fossa) is extensive. Origins for the different parts of the masseter complex involve the side of the rostrum forming the medial boundary of the infraorbital canal, the zygomatic plate, and the zygomatic arch; insertion is on various portions of the lateral surface of the dentary (Rinker, 1954; Turnbull, 1970; Satoh and Iwaku, 2006, 2008). These bony surfaces are also ample in area, including the robust zygomatic plate and arch. Without the necessity to gnaw, and need for only minimal mastication of food, substantial internal pterygoid musculature and an elongate surface on which it can originate are no longer indispensible, especially when the temporal and masseter muscle complexes remain sufficiently sizeable to take over action of closing the jaw.

Michael Carleton (in litt., 2014) provided us with another possible function of the internal pterygoid muscles in Echiothrix. He wonders

Mandible:

The dentary is long and low but not structurally delicate (figs. 5, 6). Compared to most murine species, it is stretched from front to back, especially the body of the dentary posterior to the molar row and the ramus anterior to the tooth row. The long body of the dentary forms a strong bony casing in which two-thirds of the slender, gently curved, and sharp-tipped incisor is tightly held, a strong handle absorbing the force when the dentary and free end of the incisor is thrust forward to impale the target prey (see Natural History Particulars of Echiothrix centrosa).

Dentition:

Molars and incisors of Echiothrix contrast sharply with the dentition of most murines, designs that are thought typical for gnawing and processing food by rigorous crushing and grinding actions. Echiothrix has small and delicate molars relative to the size of the skull. Length of the molar row is 12–13% of the occipitonasal length; percentages are 15%–18% for murines of about the same body size in Rattus, Maxomys, and Bunomys, for example, and many other Indo-Australian genera (compiled from Musser's records). Although occlusal surfaces are tuberculate, the cusps are low and wear rapidly to form series of dentine basins outlined by enamel rims (fig. 10). With a diet consisting of soft-bodied arthropods, primarily earthworms in the case of Echiothrix, that are swallowed whole or cut into segments and swallowed without mastication or only minimal chewing, molar occlusal surfaces play a minimal triturating function as invertebrate segments pass through the buccal cavity to the esophagus.

Form of the incisors and degree of enamel pigmentation also reflect adaptations to a vermivorous diet. The upper incisors emerge from the rostrum at a 90° angle to the ventral surface of the rostrum and the occlusal surface of the molar row (orthodont in configuration), and that exposed segment is short, as well as narrow; the enamel layers either lack pigment or are tinged with pale yellow or orange, usually near their exit from the premaxillaries; the anterior margins are scored with shallow grooves. Overall configuration of the upper incisors suggests a short chisellike instrument, suited to chop earthworms or other soft-bodied invertebrates such as coleopteran and other insect larvae into segments before they are ingested, an action aided by the grooved enamel faces, which facilitate penetration of the incisor tips into pliant earthworm and larval tissues.

The segments of the lower incisors emerging from the dentaries curve slightly upward as long and slim tusklike structures with sharp tips. Enamel layers are either unpigmented or tinged with pale yellow or orange near their exit from the bony incisor sheath. Because the madibular symphysis is flexible, the incisor tips can be splayed into a V. We previously described how the incisors can be used to procure prey, by either stabbing it or gripping it between the incisor tips. And when the jaw is closed, the prey is held against tips of the upper incisors. The entire complex is geared toward efficiently procuring earthworms and processing them into the mouth, either as cut segments or as whole worms.

The reduction of enamel pigmentation in the incisor's enamel layers of Echiothrix is significant. Most rodents possess incisors in which the enamel layers are densely orange due to the deposition of iron (Møinichen et al., 1996; Wen and Paine, 2013). It is generally accepted that “the primary function of the pigmentation is to harden the enamel and maximize the differential wear between the enamel and the [softer] dentine to produce a sharp chisellike tooth” (Strait and Smith, 2006: 703). The deposition of iron forming the red enamel on the teeth of soricine shrews is also thought to make the enamel harder and more resistant to wear (Strait and Smith, 2006). The mostly unpigmented enamel on the incisors of Echiothrix is obviously strong enough to process soft-bodied invertebrates, and at some point in the evolutionary history of the genus, natural selection has eliminated much of the iron as necessary to the functional integrity of the incisor actions—basically the energy demands related to iron deposition has been minimized. Echiothrix uses its incisors to procure soft-bodied invertebrates, not for cropping vegetation, digging, removing bark, or felling trees, all activities requiring strong biting forces that would be enhanced by iron in the enamel layers.

Upper and lower incisors in which the enamel is either unpigmented or only tinged with pale yellow are also typical of the other vermivorous Sulawesian shrew rats Melasmothrix naso, the two species of Tateomys (Musser, 1982) and Paucidentomys vermidax (Esselstyn et al., 2012) as well as the Philippine species of Rhynchomys (Musser and Heaney, 1992; Balete et al., 2007).

Stomach Morphology:

As described previously, the stomach of Echiothrix centrosa (fig. 11) generally corresponds to the unilocular and pouched configuration discussed by Carleton (1973: 28)—we have not examined stomachs of E. leucura but assume the anatomy to be similar to that of E. centrosa. The bulk of the stomach (the combined corpus and antrum) forms a single chamber lined with cornified squamous epithelium that is thickened and muscular in places; thick glandular epithelium is restricted to a pouch within the lumen of the stomach that connects with the main stomach chamber through a small aperture at the tip of a funnel-shaped or tubular neck. This configuration obtained in all 13 stomachs examined.

Among muroid rodents surveyed for their stomach morphology, the gastric structure of E. centrosa most closely resembles the unilocular-pouched stomachs of the South American sigmodontine Oxymycterus rufus (Carleton, 1973, reported as O. rutilans; Vorontsov, 1979) and the deomyine Lophuromys sikapusi (Genest-Villard, 1968), but in both of those species the glandular epithelium is entirely confined to a diverticulum or pouch (“glandular diverticulum” or “isolated blind chamber” in Vorontsov's description, 1979: 184) located on the outside of the greater curvature; a minute opening connects this glandular pouch with the main lumen of the stomach (Carleton, 1973: 16, fig. 5; Vorontsov, 1979: 185, fig. 100). Gross conformation of the stomach in many other species of Lophuromys is similar to that of L. sikapusi (Dieterlen, 1976: fig. 29).

The gastric configuration is different in E. centrosa because the glandular pouch is contained within the lumen of the stomach—not along its outside border—and connects with the lumen by an aperture at the end of a funnel-shaped neck (fig. 11).

The relationship of this specialized gastric morphology (glandular diverticulum either outside or inside the stomach lumen) to diet is obscure. While some dietary components of Oxymycterus and Lophuromys overlap with those of Echiothrix, the former two enjoy a broader range of foods than the latter. Oxymycterus rufus (Suarez, 1994, reported as O. rutilans; Musser and Carleton [2005] explain why the name rufus should be used in place of rutilans) and O. nasutus (Barlow, 1969), for example, consume mainly insects—earthworms, snails, centipedes, plant tissues, and seeds are taken but comprise minor components of the diet. Lophuromys sikapusi, as reported by Dieterlen (2013b: 256) is:

Dieterlen also summarized reports of other researchers who recorded foods consumed by L. sikapusi in Central African Republic, Uganda, Nigeria, DR Congo, Rwanda, and Côte d'Ivoire; insects, earthworms, and plant material in different combinations were the primary dietary constituents, and there is sufficient data from some regions to show seasonal changes in the diet. But omnivory is not special to L. sikapusi, for most species of Lophuromys “are omnivorous, and include a large proportion of insects and other invertebrates in the diet” (Dieterlen, 2013a: 239). By contrast with Oxymycterus and Lophuromys, Echiothrix centrosa can be labeled as a vermivore that supplements its primary diet with arthropods (chiefly soft bodied, such as coleopteran larvae and rhinotermitid termites; and geophilomorph centipedes; see tables 12 and 13).

These dietary comparisons are derived from examining stomach contents and offering captive rats different food items, and while informative at one level are a long way from meeting Carleton's (1973: 37) observation that:

The significance of a glandular diverticulum or pouch located within the stomach lumen, as in Echiothrix centrosa, but outside the lumen along the greater curvature, as in Oxymycterus and Lophuromys, is unclear, but its role in digestion is likely similar. Insects, Carleton (1973) noted, are biochemically heterogeneous, a statement that could also be applied to earthworms and other kinds of invertebrates consumed by these rats. The digestive process in all three genera may conform to Carleton's (1973: 39) suggestion that

Finally, we note that not all Sulawesi murines that include worms and insects in their diet possess the same gastric morphology seen in Echiothrix. For example, Bunomys chrysocomus, Bunomys andrewsi, and Maxomys hellwaldii, all sympatric with E. centrosa, consume earthworms, a variety of insects and other arthropods, snails, small vertebrates, and fruit. Bunomys has a unilocular-hemiglandular stomach morphology very similar to that of Rattus hoffmanni illustrated in figure 11. Bilocular-discoglandular is the design common to samples of Maxomys hellwaldii (fig. 11). Is digestion of the carbohydrate and protein components of earthworms and soft-bodied insects more efficient in the stomach of Echiothrix as compared with the processes breaking down these fractions in stomachs of the other genera? We don't know and can only apply Carleton's (1973: 39) conclusion, derived from a survey of stomach morphology among certain groups of muroid rodents, to the variation in gastric design and diet noted above:

Types:

Holotype male, allotype female, and 18 paratypes (4 males, 12 females, 1 second instar Nymph, 1 third instar Nymph) ex Echiothrix centrosa (AMNH 225044, adult male; Rodentia, Muridae, Murinae) collected by G.G. Musser at Sungai Sadaunta (1°23′S, 119°58′E; see gazetteer and fig. 2), 985 m, Propinsi Sulawesi Tengah, Indonesia, on 7 November 1974.

Two paratypes (1 female, 1 first instar Nymph) ex E. centrosa (AMNH 225045, adult female), collected by G.G. Musser at Sungai Sadaunta, 884 m, Propinsi Sulawesi Tengah, Indonesia, on 30 November 1974. One female ex Echiothrix centrosa (AMNH 225681, adult male), collected by G.G. Musser at Malakosa, Kuala Navusu (0°58′S, 120°27′E), 350 m, Propinsi Sulawesi Tengah, Indonesia, on 7 November 1975.

Distribution:

Known only from the collections itemized above, all from Echiothrix centrosa. Polyplax beaucournui may parasitize E. centrosa throughout its geographic and altitudinal ranges.

Deposition of Specimens:

Holotype, allotype, and six paratypes (1 male, 2 females, 1 first instar nymph, 1 second instar nymph, 1 third instar nymph) deposited in USNM. Other paratypes deposited in AMNH, BMNH, MZB, and private collection of L.A.D.

Etymology:

This species is named for Jean-Claude Beaucournu (Université de Rennes, France) in recognition of his exemplary studies of ectoparasites, especially fleas, his enduring friendship, and his collaborative studies with us on ectoparasites of mammals in southeast Asia, including Sulawesi.

Diagnosis:

Polyplax beaucournui is a fairly typical member of its genus. It does not have extreme morphological adaptations that are present, for example, in the congeneric P. melasmothrixi, which parasitizes the endemic Sulawesi shrew rat, Melasmothrix naso (see Durden and Musser, 1992), or in Hoplopleura musseri, which parasitizes another endemic Sulawesi rat, Maxomys musschenbroekii (see Durden, 1990). Nevertheless, P. beaucournui is unique and adults can be distinguished from all other described species of Polyplax based on a combination of the following characters.

In the male, the genitalia differ from those of all other known Polyplax, especially the very small, subcircular parameres and the small protuberance borne on each of them. The shape of the posterior arms of the basal apodeme is also distinctive. Other diagnostic characters are: (1) the shape of the thoracic sternal plate; (2) the shape of the paratergal plates and the lengths of the paratergal setae borne on them; (3) the presence of 2 DAcHS next to the DPHS with all 3 of these setae aligned in a row and borne on distinct protuberances; (4) the narrow dorsal abdominal tergites, especially the very narrow plates 5 and 6.

The female of P. beaucournui can be identified using a combination of the following characters: (1) the morphology of the genitalia, including the shapes and associated setae of the subtriangular subgenital plate and gonopods VIII; (2) the shape of the thoracic sternal plate; (3) the shape of the paratergal plates and the lengths of the paratergal setae; (4) the presence of two DAcHS next to the DPHS with all three of these setae aligned in a row and borne on distinct protuberances.

Nymphal stages of P. beaucournui are presumably also unique, but immature stages of very few species of Polyplax have been described (Kim, 1987) and none have previously been described that were collected from mammal species native to Sulawesi. The immature stages of the spiny rat louse, Polyplax spinulosa (Burmeister) have been described (Kim, 1987) and this louse parasitizes commensal Rattus throughout most of the world including nonnative Rattus species on Sulawesi (Durden, 1987). The three dorsal setae inserted in a row in the posterior head region (1 DPHS and 2 DAcHS) that are also present in adult males and females are unusual and are probably diagnostic for all three nymphal stages of P. beaucournui. As in adults of both sexes, these setae are borne on distinct small protuberances in the third instar nymph of P. beaucournui, which is even more unusual for the genus. These characters can be further assessed when the immature stages of other species of Polyplax, particularly native species from Sulawesi, are described.

Description:

Male (fig. 16A–D): Length of holotype, 1.05 mm; mean for series (N  =  5), 1.00 mm; range, 0.95–1.05 mm. Head and thorax well sclerotized.

Fig. 16.

Polyplax beaucournui, n. sp., male. A, dorsoventral view of entire male (dorsal morphology is shown to the left of the midline, ventral morphology to the right); B, thoracic sternal plate; C, paratergal plates; D, genitalia.

Head: Broad, about as broad as long, with squarish but distinctly crenulated anterior margin; lateral margins somewhat curved, broadening toward thorax. Two SHS, 2 DMHS, 1 DPoCHS, 1 DPHS, 2 DAcHS, 1 SpAtHS, 1 SpAtCHS, 2 DAHS, 2 ApHS, 1 VPHS, and 1 VPaHS on each side. DPHS and both DAcHS each borne on small protuberance and aligned in a row. Antennae: Five segmented with basal segment much larger than other segments.

Thorax: About as broad as long. Thoracic sternal plate (fig. 16B), shield shaped with rounded apical projection, rounded anterolateral margins and acute, elongate posterior margin. Mesothoracic spiracle moderate in size (0.023 mm in diameter) with 1 small DMsS and 1 fairly long DPTS (0.11 mm in length) medial to spiracle. Legs: Forelegs small with small tibiotarsal claw; midlegs and hindlegs larger with progressively larger tibiotarsal claws; all coxae subtriangular.

Abdomen: Wider than thorax. Eight dorsal plates; plates 4–8 narrow, especially plates 5 and 6 which are extremely reduced; 1 DCAS anteriorly, followed by 2 TeAS on plate 1, 8 TeAS on each of plates 2–4, 10–12 TeAS on each of plates 5–6, 8 TeAS on plate 7 and 4 TeAS on plate 8; TeAS on plates 2–4 alternating in length between long and short; other TeAS long; 5 long DLAS present on each side. Eight fairly broad ventral plates anterior to subgenital plate; 5 StAS on plate 1, followed by 4 StAS on each of plates 2–3, 6 StAS on plate 4, 6–7 StAS on each of plates 5–7, and 4 StAS on plate 8; all StAS long except lateral seta on each side on plate 4.

Paratergal plates (fig. 16C): Present on segments 2–8; plates I–VI all subtriangular with lateral posteroapical angles acuminate; plates II–VII each with spiracle; plates I–IV each with 1 apical seta slightly longer than other apical seta on same plate; plates VI–VII each with 2 long apical setae; 4 small setae also present on plate I; all plates differentially sclerotized as shown (fig. 16C).

Genitalia (fig. 16D): Subgenital plate broader anteriorly with two lacunae; anterior lacuna with acuminate lateral margins and two long setae inserted anteriorly; posterior lacuna smaller without associated setae and lacking acuminate lateral margins; aedeagal basal apodeme much longer than parameres with small extension at tip of each posterior arm; parameres, small, subcircular but with lateral extension and small posterior protuberance; pseudopenis long, extending well beyond parameres and extruding from tip of abdomen.

Female (fig. 17A–D): Length of allotype, 1.28 mm; mean for series (N  =  14), 1.25 mm; range, 1.13–1.47 mm.

Fig. 17.

Polyplax beaucournui, n. sp., female. A, dorsoventral view of entire female (dorsal morphology is shown to the left of the midline, ventral morphology to the right); B, thoracic sternal plate; C, paratergal plates; D, genitalia.

Head, thorax, and legs: As in male unless noted otherwise. Thoracic sternal plate (fig. 17B) with anterolateral margins projecting slightly more anteriorly than in male. Mesothoracic spiracle diameter, 0.12 mm.

Abdomen: Dorsally, with 2 rows of 2 DCAS anteriorly followed by 11 fairly broad dorsal plates; plates 1 and 2 each with 6 TeAS, plates 3–9 each with 6–9 TeAS, plate 10 with 5 TeAS, plate 11 with 3 TeAS; lateral TeAS on plates 1 and 2 distinctly shorter than medial TeAS on same plate; 5 DLAS present on each side. 12 fairly broad pregenital plates ventrally; plates 1–3 each with 4 StAS, plate 4 with 5 StAS, plates 5–11 each with 6–8 StAS; lateral StAS on plate 2 distinctly shorter than medial StAS on same plate. 5 VLAS present on each side.

Paratergal plates (fig. 17C): More or less as in male but with both apical setae on plates III–V about equal in length.

Genitalia (fig. 17D): Subgenital plate subtriangular with smoothly convex anterior margin, slightly concave posterolateral margins and broadly rounded posterior apex; 4 small medial setae immediately anterior to anterior margin. Gonopods XIII subtriangular each with 3 long setae, with lateral seta extending beyond apex of abdomen. Gonopods XI each with robust apical seta; 3 long setae inserted laterally and 3–4 long setae inserted anteriorly to gonopods XI; 2 tiny setae medial to gonopod XI on each side; vulvar fimbriae distinct.

First instar nymph (fig. 18A): Length (1 specimen): 0.48 mm.

Fig. 18.

Polyplax beaucournui, n. sp., nymphal stages—dorsoventral views of entire nymphs (dorsal morphology is shown to the left of the midline, ventral morphology to the right). A, first instar nymph; B, second instar nymph; C, third instar nymph.

Head: Broadly rounded anteriorly and laterally. Two SHS, 1 DPTS, 2 DAcHS, 1 DPaHS, 2 ApHS, 1 VPHS, and 1 VPaHS on each side; insertions of DPTS and both DAcHS aligned in a row. Antennae: Five segmented with basal segment larger than other segments.

Thorax: Broader than head with distinct mesothoracic spiracle and DPTS; thoracic sternal plate absent. Legs: All legs about equal in size, but tibiotarsal claws progressively increasing in size from forelegs to hind legs; coxae subtriangular.

Abdomen: Wider than thorax; paratergal plates lacking but paired, long lateral setae present on segment 8 borne on small protuberance; no other lateral abdominal setae; no abdominal tergites or sternites present; 8 long DCAS present on each side; 1 long VCAS located posteriorly on each side.

Second instar nymph (fig. 18B): Length (1 specimen): 0.82 mm

Head and thorax: As in first instar nymph unless stated otherwise. Anterior margin of head slightly crenulated; lateral margins of head less rounded than in first instar; 2 DMHS present on each side (in addition to other head setae listed for first instar); midlegs and hind legs distinctly larger than forelegs; subcircular thoracic sternal plate present; small DMsS present next to DPTS and borne on small protuberance.

Abdomen: Wider than thorax; 9 long DCAS, 6 long VCAS, and 1 small DLAS present on each side. Two pairs of long posterolateral setae present, the anterior pair borne on the most posterior paratergal plate. Paratergal plates: Seven partially formed plates present on segments II–VIII; plates I–VI subtriangular; plates II–VII each with distinct spiracle.

Third instar nymph (fig. 18C): Length (1 specimen): 0.64 mm (note: the third instar nymph specimen is shorter than the second instar nymph specimen; normally, the opposite would be expected; however, the second instar specimen had an extended, blood-engorged abdomen and the third instar specimen had not fed resulting in a compressed abdomen).

Head and thorax: As in first instar nymph unless stated otherwise. Anterior margin of head distinctly crenulated. Two DMHS and 1 DPoCHS present on each side (in addition to other head setae listed for first instar). DPHS and both DACHS each borne on small protuberance; midlegs and hind legs (except coxae) missing on both sides; subcircular thoracic sternal plate present; small DMsS present next to DPTS and borne on small protuberance.

Abdomen: Wider than thorax; 9 long DCAS, 7 long VCAS, and 1 small DLAS present on each side. Two pairs of long posterolateral setae present, the anterior pair borne on the most posterior paratergal plate, the posterior pair borne on small protuberance. Paratergal plates: Seven well-formed plates present on segments II–VIII; plates I–VI subtriangular; plates II–VII each with distinct spiracle.

Host and Parasite Relationships:

Eggs (nits) of P. beaucournui were attached only to the guard hairs or thin overhairs of the dorsal pelage (fig. 19) and never on the spines that characterize E. centrosa or on the underfur hairs. The eggs shown in figure 19 had hatched previously because the operculum (“cap”) is absent on each of them. Nevertheless, as with other species of Anoplura, many hatched eggs remain cemented to the host hairs. Cement egg bases of P. beaucournui with partial remains of hatched eggs are also visible in figure 19.

Fig. 19.

Polyplax beaucournui, n. sp., ova (nits) attached to guard hairs in the dorsal coat of Echiothrix centrosa. All ova shown had hatched previously; cement and egg bases where other ova were previously attached are also visible.

The diameters of different hair types of P. beaucournui at their maximum width and at the hair base where P. beaucournui lice would typically be present (at the skin surface where they feed on host blood) are listed in table 17. Also listed in that table are the tibiotarsal claw gap sizes for different sexes and nymphal stages of P. beaucournui. Although each louse specimen has six legs in life, some legs or leg segments were broken in some of the desiccated (i.e., brittle) specimens that were removed from study skins of E. centrosa. Also, if tibiotarsal claws were not slide mounted in a completely flat plane, their gap widths could not be reliably measured. For these reasons, the sample sizes for tibiotarsal claws listed in table 17 are lower than would initially be expected from the total number of louse specimens available.

Table 17

Hair Diameter Measurements (mm) for Echiothrix centrosa and Claw-Opening Diameters for Its Louse, Polyplax beaucournui

Dorsal spines, guard hairs, thin hairs of the overfur and underfur hairs are components of the fur covering upperparts of head and body; ventral overhairs and underfur hairs form the coat covering the underparts.

Regardless, the data in table 17 highlight some important findings with respect to the host-parasite relationships between Echiothrix centrosa and Polyplax beaucournui. Firstly, the claw gap sizes of males, females, and all nymphal stages of P. beaucournui are not large enough to be able to grasp the dorsal spines, guard hairs, or thin overhairs of the dorsal coat of E. centrosa or the overhairs of its ventral pelage at their maximum diameter. Similarly, only the largest claws of a few male and female lice could grasp the smallest host spines at their base. This, combined with the fact that louse eggs were never recorded on host spines, strongly suggests that, even though these spines are characteristic of E. centrosa, they are almost certainly avoided by P. beaucournui. The measurements listed in table 17 show that adults of P. beaucournui can, however, adequately grasp any of the other hair types of E. centrosa at or near their bases. Conversely, although few samples were available for analysis, claws of nymphal P. beaucournui are clearly not large enough to grasp some of these hairs at their bases. Therefore, nymphs must mainly grasp the smaller underfur hairs that have sufficiently small diameters for all measured nymphal claws to be able to grasp. These data suggest there could be a partial microhabitat segregation between adults and nymphs of P. beaucournui in the pelage of E. centrosa, with adults frequenting the bases of the larger hairs (but avoiding the spines) and nymphs occurring near the bases of the underfur hairs.

Polyplax beaucournui could be host-specific to E. centrosa in Central Sulawesi or it could infest both this murid and the congeneric E. leucura in the northeastern arm of the northern peninsula. This question can be answered when lice are collected and examined from E. leucura. Although study skins of two specimens of E. leucura (BMNH 97.1.2.45 and 97.1.2.46) were carefully examined, no lice were found on them.

Order Siphonaptera (fleas), Family Pygiopsyllidae:

Farhangia quattuordecimdentata Mardon and Durden, 2003. Allotype ♀ and 1 paratype ♀ ex Echiothrix centrosa (AMNH 225043; listed in original description as Echiothrix leucura), collected by G.G. Musser at Sungai Sadaunta, 884 m, Propinsi Sulawesi Tengah, Indonesia, on 5 October 1974. Central Sulawesi.

The principal hosts of fleas belonging to the genus Farhangia are considered to be tree squirrels, and most other specimens of F. quattuordecimdentata have been collected from the endemic Sulawesi pygmy tree squirrel Prosciurillus murinus (see Musser et al., 2010). However, in addition to E. centrosa, this flea has been recorded from another endemic Sulawesi rodent, the murid Margaretamys beccarii. Mardon and Durden (2003) provide collection data including host information for all known specimens of this flea. The genus Farhangia is only known from Sulawesi (3 species) and Borneo (1 species) and some morphological traits suggest that members of this genus are inefficient jumpers and therefore are probably nest-associated fleas (Traub, 1980). The specimens of F. quattuordecimdentata from E. centrosa and M. beccarii may represent atypical host associations or they could indicate reduced host specificity or less reliance on squirrels as hosts for this flea species. To date, no flea species that are host-specific to either species of Echiothrix have been collected.

Subclass Acari, Order Ixodida, Family Ixodidae (hard ticks):

In this section, some tick collections have HH (Harry Hoogstraal) accession numbers whereas others have RML (U.S. National Tick Collection) accession numbers. The HH collection is now incorporated into the U.S. National Tick Collection on the campus of Georgia Southern University, Statesboro, Georgia.

Amblyomma sp.: Two larvae (RML 122184) ex AMNH 225044, 6 nymphs, 4 larvae (RML 122185) ex AMNH 225045, 4 larvae ex AMNH 225046, all from E. centrosa, Central Sulawesi, Sungai Sadaunta, Nov. 1974, G.G. Musser.

These nymphs do not match known nymphal stages of any of the other species of Amblyomma known to occur on Sulawesi (Durden et al., 2008).

In addition to E. centrosa, ticks of this genus have been collected from a suite of other mammal hosts living in Sulawesi: shrews (the commensal Suncus murinus), pigs (Sus celebensis and the domestic Sus scrofa), water buffalo (Bubalus bubalis, nonnative), humans, domestic dog (nonnative), two endemic squirrels (Rubrisciurus rubriventer and Hyosciurus heinrichi), nine other species of endemic murid rodents (Bunomys fratrorum and B. andrewsi; Margaretamys beccari; Maxomys hellwaldii and M. musschenbroekii; Paruromys dominator; Rattus hoffmanni, R. xanthurus, and R. facetus [recorded as R. marmosurus]); and two nonnative murines (Rattus tanezumi [recorded as R. rattus] and R. exulans) (Durden et al., 2008).

Haemaphysalis (Ornithophysalis) kadarsani Hoogstraal and Wassef, 1977: One paratype nymph (MZB 1525, HH 45,046) ex E. centrosa (listed in original description as E. leucura), Central Sulawesi, Malakosa, Kuala Navusu, Coll.: G.G. Musser.

New specimen: 1 male (RML 121405) ex E. centrosa (AMNH 225682), Central Sulawesi, Malakosa, Kuala Navusu, elevation 122 m, 15 Oct. 1975, G.G. Musser (tick removed from host study skin by L.A.D. on 12 April 1994).

This tiny tick (the smallest known species of Haemaphysalis, a genus that comprises 166 known species worldwide) is known only from Central Sulawesi (Durden et al., 2008), with most adult specimens reported by Hoogstraal and Wassef (1977) collected (by Musser) from another endemic murid, Paruromys dominator, which is sympatric with Echiothrix centrosa. Morphologically, Hoogstraal and Wassef (1977) considered H. kadarsani to be closest to H. (O.) sciuri, which parasitizes tree squirrels in the Philippines (Mindanao). No molecular phylogenetic analyses have been undertaken to further investigate the evolutionary relationships among species in the genus Haemaphysalis, including H. kadarsani and H. sciuri.

Haemaphysalis (Kaiseriana) hystricis Supino, 1897: Two nymphs, 3 larvae (RML 122187) ex E. centrosa (AMNH 225046), Central Sulawesi, Sungai Sadaunta, Nov. 1974, G.G. Musser.

In addition to Sulawesi, this tick is known from Vietnam, Laos, Taiwan, the Ryuku Islands, northeastern India, northern Myanmar, Thailand, and Sumatra (Durden et al., 2008). Adults mainly parasitize ungulates (especially suids and cervids) whereas immature stages parasitize rodents (Durden et al., 2008). Besides E. centrosa, Durden (1986a) recorded H. hystricis from samples of three murid species collected in the northeastern end of the northern peninsula of Sulawesi; Bunomys fratrorum, Maxomys hellwaldii, and Maxomys musschenbroekii—all are Sulawesi endemics, and B. fratrorum occurs only in forests of the northeastern arm.

Haemaphysalis sp.: Five nymphs (RML 122186) ex E. centrosa (AMNH 225045), Central Sulawesi, Sungai Sadaunta, Nov. 1974, G.G. Musser. These nymphs do not match H. kadarsani or any of the other Sulawesi species of this genus for which nymphs have been described (Durden et al., 2008).

In addition to E. centrosa, unidentified immature stages belonging to the genus Haemaphysalis have been collected from other mammal hosts living in Sulawesi: shrews (the endemic Crocidura elongata, and the commensal Suncus murinus), rusa (Rusa timorensis, nonnative), three endemic squirrels (Rubrisciurus rubriventer, Hyosciurus heinrichi, and H. ileile), 10 other species of endemic murid rodents (Bunomys fratrorum, B. andrewsi, and B. chrysocomus); Maxomys hellwaldii, M. musschenbroekii, and M. wattsi; Paruromys dominator; Taeromys sp.; Rattus hoffmanni, R. facetus [recorded as R. marmosurus]), and three nonnative murines (Rattus tanezumi [recorded as R. rattus], R. argentiventer, and R. exulans) (Durden et al., 2008).

Subclass Acari, Order Mesostigmata, Family Laelapidae:

The following specimens were collected from E. centrosa from Central Sulawesi: Five female specimens ex AMNH 225044; 1 female ex AMNH 225045, 2 females ex AMNH 225046 (all from Sungai Sadaunta, Oct–Nov. 1974, G.G. Musser); 2 females ex USNM 219738 (Pinedapa, 21 Jan. 1918, H.C. Raven); 1 female ex BMNH 40.385 (Koelawi, 29 Dec. 1938, W.J.C. Frost).

Musser's field notes reveal that laelapid mites are common on E. centrosa. Virtually all endemic Sulawesi rodents examined in the field by Durden were heavily infested with laelapid mites; often there were more than 100 of these mites on a single host individual (Durden, 1986b). These mites, including the specimens from E. centrosa, were forwarded to D. Gettinger (University of Central Arkansas) in 2006 but have not yet been identified.

Subclass Acari, Order Sarcoptiformes, Family Atopomelidae (fur mites):

Listrophoroides (Marquesania) echiothrix Bochkov et al., 2004: Holotype male plus 20 male and 20 female paratypes ex E. centrosa (FMNH 43409), Central Sulawesi, Pinedapa, 7 Feb. 1918, H.C. Raven.

New specimens ex E. centrosa from Central Sulawesi as follows: Two specimens ex AMNH 225044, 1 specimen ex AMNH 225047 (both from Sungai Sadaunta, Nov. 1974, G.G. Musser); 1 specimen ex AMNH 225681, 3 specimens ex AMNH 225682 (both from Kuala Navusu, Oct. 1975, G.G. Musser). These specimens were forwarded to A.A. Bochkov (Russian Academy of Sciences, St. Petersburg) in 2009.

This tiny fur mite appears to be host-specific to E. centrosa; however, as with the louse Polyplax beaucournui, it could also parasitize E. leucura. The male and female of L. echiothrix were described and illustrated by Bochkov et al. (2004).

Subclass Acari, Order Trombidiformes, Family Trombiculidae (chiggers):

Eighteen specimens ex E. centrosa (AMNH 225047, Central Sulawesi, Sungai Sadaunta, Nov. 1974, G.G. Musser).

These specimens were removed from the host study skin by L.A.D. in April 1994 and forwarded to M.L. Goff (Chaminade University, Hawaii) later that year but have not yet been identified or described. Based on these specimens and on Musser's field notes, chiggers also appear to be common on E. centrosa.