Hsunycteris dashe, Velazco & Soto-Centeno & Fleck & Voss & Simmons, 2017

Velazco, Paúl M., Soto-Centeno, J. Angel, Fleck, David W., Voss, Robert S. & Simmons, Nancy B., 2017, A New Species of Nectar-feeding Bat of the Genus Hsunycteris (Phyllostomidae: Lonchophyllinae) from Northeastern Peru, American Museum Novitates 2017 (3881), pp. 1-28 : 7-18

Hsunycteris dashe , new species

Dashe’s nectar-feeding bat

Lonchophylla mordax: Fleck et al., 2002: 96 .

Hsunycteris sp. nov.: Voss et al., 2016: 11.

HOLOTYPE: The holotype ( MUSM 15206 ; figs. 1 , 3A , 4A ), an adult female specimen preserved in alcohol with the skull removed and cleaned, was collected by David W. Fleck (original number: DWF 380 ) on 2 September 1999 at Nuevo San Juan (73°9′ 50″W, 5°14′ 50″S; 150 m above sea level), a Matses village on the right ( SE) bank of the Río Gálvez in the Peruvian department of Loreto ( fig. 2 ). Frozen tissues are deposited at the Ambrose Monell Cryo Collection of the American Museum of Natural History ( AMCC 109488 ).

PARATYPES: Two additional specimens, a lactating adult female ( AMNH 273165 [ DWF 662 ]) and her female pup ( MUSM 15211 [ DWF 663 ]), were collected at the type locality by David W. Fleck on 21 October 1999. The adult paratype ( AMNH 273165 ), preserved in alcohol with the skull removed and cleaned, is accompanied by frozen tissues deposited at the Ambrose Monell Cryo Collection of the American Museum of Natural History ( AMCC 109608 ). The juvenile paratype ( MUSM 15211 ) is preserved in alcohol .

DISTRIBUTION: Hsunycteris dashe is known only from the vicinity of the type locality in the Yavarí-Ucayali interfluvial region of the Peruvian Amazon ( fig. 2 ).

DIAGNOSIS AND DESCRIPTION: Hsunycteris dashe is the largest species in the genus (FA 35–36 mm; tables 2–3). Dorsal pelage 9–10 mm long, fur distinctly bicolored with pale pinkish bases (20% of length) and pale brown tips; ventral pelage 7 mm long, similar in color to the dorsal pelage, bicolored with pale pinkish bases (30% of length) and pale brown tips. Two interramal vibrissae present; genal vibrissae absent. Central rib of noseleaf weakly defined from lateral portions, extending from apex to edge of upper lip. Chin with several small dermal papillae arranged in a V shape and separated by a wide cleft ( fig. 3A ). Antero-internal surface of pinna sparsely covered with long hairs. Dorsal surface of the forearm naked. Metacarpal formula III> V> IV. Dorsal surface of uropatagium naked. Dorsal surface of foot sparsely covered by short hairs.

Skull with broad rostrum; postorbital region not inflated and lacking lateral projections ( fig. 1 ). Lateral margin of infraorbital foramen not projecting beyond rostral outline in dorsal view. Sphenoidal crest ( Giannini et al., 2006: fig. 10) well developed. Posterior border of hard palate V-shaped. Left and right basisphenoid pits separated by narrow septum. Dentary deep, coronoid process low (slightly above level of articular condyle), and angular process broad.

Dental formula I2/2, C1/1, P2/3, M3/3 × 2 = 34 or I2/2, C1/1, P3/3, M3/3 × 2 = 36 .3 Inner and outer upper incisors not in contact. Outer upper incisors relatively large. P4 lingual cusp absent; P5 lingual cusp weakly developed; small gap present between P5 and M1 ( fig. 4A ). M1 parastyle well developed and labially oriented; M1 and M2 with broad protocone basin; M3 large; palate posterior to M3 shorter than the length of M3 ( figs. 1 , 4A ). 3 The former dental formula characterizes the adult paratype, and it is the usual formula in other congeneric species, whereas the holotype has an additional pair of small upper premolars ( figs. 1 , 4A ). With only two adult specimens in hand, it is obviously impossible to determine which formula predominates in the species, although we suspect that the small anterior premolars of the holotype are supernumerary teeth, which commonly occur in other lonchophyllines ( Phillips, 1971; Nogueira et al., 2014).

Lower incisors large and broad. Distal cusp weakly developed on p1. Anterior cusp of p4 oriented horizontally. Protoconid labially oriented on m1; m1 paracristid notch strongly developed. Hypoconid wide on m2.

COMPARISONS: External and craniodental measurements for Hsunycteris dashe and other congeneric species are provided in tables 2 and 3. Hsunycteris dashe can be easily distinguished from all other species of Hsunycteris by its longer forearm. However, there is substantial overlap among all Hsunycteris species in craniodental measurements, with H. dashe falling at the larger end of the spectrum for most variables.

Externally, Hsunycteris dashe is distinguished from all other species in the genus by having longer hairs between the shoulders (9–10 mm, versus 7–8 mm in H. cadenai , H. pattoni , and H. thomasi ). The central rib of the noseleaf extends from the tip of the spear to the edge of the upper lip in H. dashe and H. thomasi , and it is weakly defined from the lateral portions of the noseleaf. In contrast, the central rib of the noseleaf is well defined but does not reach the edge of the upper lip in H. pattoni , and a distinct central rib is absent in H. cadenai . The chin has several small dermal papillae arranged in a V and separated by a wide basal cleft in H. dashe ( fig. 3A ), whereas the dermal papillae are larger and not separated by a basal cleft in H. cadenai , H. pattoni , and H. thomasi ( fig. 3B ). The antero-internal surface of each pinna is sparsely covered with long hairs in H. dashe , H. cadenai , and H. thomasi , whereas these hairs are more abundant in H. pattoni . Lastly, metacarpal V is longer than metacarpal IV in H. dashe , whereas metacarpal V is shorter than IV in H. cadenai and H. pattoni , and these metacarpals are subequal in length in H. thomasi .

The skull of Hsunycteris dashe is distinguished from those of all other species in the genus by having a relatively broader rostrum and lacking inflation of the postorbital region (versus rostrum narrower and postorbital region inflated in H. cadenai , H. pattoni , and H. thomasi ). The postorbital region lacks a lateral projection in H. dashe , H. pattoni , and H. thomasi , whereas a lateral projection is present in H. cadenai (see Woodman and Timm, 2006: fig. 11A). The lateral margin of the infraorbital foramen does not project beyond rostral outline in dorsal view in H. dashe , whereas the infraorbital foramen is wider with a lateral margin that projects beyond rostral outline in dorsal view in H. cadenai , H. pattoni , and H. thomasi . The sphenoidal crest is well developed in H. dashe , whereas this crest is weakly developed in H. cadenai , H. pattoni , and H. thomasi . The septum separating the left and right basisphenoid pits is narrow in H. dashe and H. pattoni , whereas the septum is broader in H. cadenai . 4 The maxilla imme-

4 Hsunycteris thomasi exhibits considerable intraspecific variation in this feature, with some specimens having a relatively narrow septum (e.g., AMNH 267940) and others having a broader septum (e.g., AMNH 16120). diately posterior to M3 is less than the length of M 3 in H. dashe , H. cadenai , and H. pattoni ; in contrast, the maxilla posterior to M3 is longer than the length of M 3 in H. thomasi .

The body of the dentary is deep in Hsunycteris dashe , H. cadenai , and H. thomasi , whereas it is shallow and the entire dentary appears more slender in H. pattoni . The coronoid process is low (extending dorsally slightly above the level of the articular condyle) in H. dashe and H. thomasi , whereas the coronoid process is significantly higher in H. cadenai and H. pattoni . The angular process is broad in H. dashe , H. cadenai , and H. thomasi , whereas it is narrower in H. pattoni .

In lateral view, the inner and outer upper incisors are not in contact in Hsunycteris dashe , whereas these teeth are in contact in H. cadenai and H. pattoni ( Hsunycteris thomasi exhibits variation in this character: the inner and outer upper incisors are in contact in some specimens [e.g., AMNH 16120] but not in others [e.g., AMNH 267940, 267943]). The outer upper incisors are large (slightly smaller than inner upper incisors) in H. dashe whereas they are proportionally smaller (less than half the size of the inner upper incisors) in H. cadenai , H. thomasi , and H. pattoni . Whereas P4 lacks a lingual cusp in H. dashe ( fig. 4A ), H. cadenai , and H. pattoni ( fig. 4B ), this cusp is present in H. thomasi ( fig. 4C ). The lingual cusp of P5 is weakly developed in H. dashe ( fig. 4A ), whereas this cusp is well developed and narrow in H. pattoni ( fig. 4B ) and well developed and broad in H. cadenai and H. thomasi ( fig. 4C ). There is a small gap present between P5 and M 1 in H. dashe , H. cadenai , and H. pattoni , whereas this gap is variable H. thomasi (e.g., present and wide in AMNH 16120, but absent in AMNH 267940 and 267943). The parastyle on M1 is well developed and labially oriented in H. dashe . In contrast, the parastyle is weakly developed and directed anteriorly in H. cadenai , while it is well developed and directed anteriorly in H. pattoni and H. thomasi . The protocone basins of M1 and M2 are broad in H. dashe and H. thomasi , whereas they are reduced in H. cadenai and H. pattoni . The third upper molar is large in H. dashe , H. cadenai , H. pattoni , and some specimens of H. thomasi (e.g., AMNH 267940, 267943), whereas other specimens of H. thomasi have smaller M3s (e.g., AMNH 16120).

The lower incisors are large and mesiodistally broad in Hsunycteris dashe and H. cadenai , whereas these teeth are proportionally smaller and narrower in H. thomasi and H. pattoni . The distal cusp on p1 is weakly developed in H. dashe , whereas it is well developed in H. cadenai , H. pattoni , and H. thomasi . The anterior cusp of p4 is oriented horizontally in H. dashe , whereas this cusp in H. cadenai and H. pattoni is inclined upwards. Hsunycteris thomasi exhibits intraspecific variation in this feature, with some individuals having the cusp oriented horizontally (e.g., AMNH 267940, 267943) while it is inclined upwards in others (e.g., AMNH 16120). The paracristid notch of m1 is strongly developed in H. dashe and H. cadenai , but this notch is weakly developed or absent in H. pattoni and H. thomasi . The hypoconid of m2 is wide in H. dashe and H. cadenai , whereas it is narrow in H. thomasi and H. pattoni .

MORPHOMETRIC ANALYSES: Our multivariate statistical analysis included only female specimens because males are unknown for Hsunycteris dashe . We compared three specimens of H. cadenai , 14 of H. pattoni , 18 of H. thomasi , and two of H. dashe (appendix 1), using a principal components analysis (PCA) based on one external measurement (FA) and the 11 craniodental measurements described above. The first three principal components accounted for 82.4% of the

-0.20 -0.15 -0.10 -0.05 0.00 0.05 0.10 0.15 PC 1 (56.3%)

total variance in the log-transformed measurements of this material (appendix 3). PC 1 accounted for the highest percentage (56.3%), and this vector has uniformly positive loadings, suggesting that it is a size factor (with a notably high loading for coronoid height). Although all four species show overlapping scores on PC1 and PC2 ( fig. 5A ), H. dashe specimens are widely separately from the other three species on PC3 ( fig. 5B ). Factor loadings on PC3 suggest that this separation is attributable primarily to differences in forearm length, width at canines, and width at M2.

MOLECULAR ANALYSES: Molecular analysis of mitochondrial Cyt-b sequences from selected specimens ( table 1) recovered well-supported clades consistent with the divergence of Hsunycteris from other lonchophyllines ( fig. 6 ). The mono-

phyly of Hsunycteris is strongly supported by these data, and H. dashe was recovered as the sister lineage of a robustly supported clade comprised of

H. cadenai , H. pattoni , and H. thomasi in both

Bayesian inference and ML analyses. Pairwise genetic comparisons between H. dashe and other congeneric species averaged at least 11% and 15%

for uncorrected-p and K2P distances, respectively

(appendix 4).

NATURAL HISTORY: Our three specimens of

Hsunycteris dashe were all collected at diurnal roosts discovered by Matses hunters near Nuevo

San Juan. The first to be collected (MUSM 15206,

an adult female) was found roosting alone beneath the undercut bank of a small stream in dense val-

ley-bottom primary forest on 2 September 1999. FIGURE 7. Dashe, the Matses hero who led his D.W.F. collected this bat after having been led to the people to victory in their struggle for survival during the mid-20th century. (Photographed by Steroost by the hunters who found it. According to his

ven Romanoff on the upper Chobayacu, ca. 1975.) field notes, “the roof of the [undercut] bank was held together by the root mass of a nearby tree,” and the bat was hanging from this root-stabilized surface, about 1 m above the water’s edge. The other two specimens ( AMNH 273165 , MUSM 15211 ; mother and young, respectively) were found roosting together with a third individual (which escaped capture) beneath the undercut bank of another stream, in primary upland forest on 21 October 1999. No additional details were provided by the Matses hunters who collected these two specimens and described their roost to

D.W.F.

Except for the narrow floodplain of the Río Gálvez, the landscape surrounding Nuevo San

Juan consists of low hills and terraces (nowhere more than 200 m above sea level) eroded from

Miocene lake sediments; there are no caves or rock outcrops anywhere in the region. As described elsewhere, the average annual rainfall is probably close to 3000 mm. Except where cleared for Matses horticulture or regenerating from their slash-and-burn clearings, the local vegetation consists of a variety of primary formations determined by drainage and seasonal flooding ( Fleck and Harder, 2000; Voss and Fleck, 2011). All our specimens of Hsunycteris dashe were taken in tall, undisturbed forest on hilly interfluvial terrain far from the palm swamps and seasonally flooded formations of the Gálvez floodplain.

ETYMOLOGY: For Dashe (ca. 1910–1980, fig. 7), also known as Quioshash, a hero of the Matses people. Dashe grew up during the rubber boom, when mercenaries were sent to Matses territory to exterminate the indigenous inhabitants. Dashe grew up fleeing from attackers who killed his kinsmen and carried off women and children to be prostituted or sold as slaves. After he had grown to manhood, Dashe rallied the Matses to fight back, leading multiple successful raids on rubber camps and settlements, eventually expelling all outsiders ( Jiménez Huanán et al., 2014). Without his courage and military cunning the Matses would no longer exist as an intact culture with legally recognized title to their tribal land.

Figures

FIGURE 1. Dorsal and ventral views of the cranium and lateral view of the cranium and mandible of Hsunycteris dashe (MUSM 15206, holotype). Scale bar = 5 mm.

FIGURE 2. Map showing collecting localities of Hsunycteris species within the Yavarí-Ucayali interfluvial region (boundaries highlighted in gray). See appendix 2 for locality names and geographic coordinates. The arrow indicates the type locality of H. dashe.

FIGURE 3. Anterior views of the chins of Hsunycteris dashe (A, AMNH 273165) and H. pattoni (B, MUSM 13205) illustrating taxonomic differences in the arrangement of the dermal papillae. In H. dashe the chin has several small dermal papillae arranged in a V and separated by a wide basal cleft. In H. pattoni, however the dermal papillae on the chin are larger and are not separated by a basal cleft.

FIGURE 4. Occlusal views of partial upper toothrows in Hsunycteris dashe (A, MUSM 15206), H. pattoni (B, MUSM 13205), and H. thomasi (C, AMNH 16120) illustrating taxonomic differences in the morphology of the premolars and first molar (see text). Abbreviations: p, parastyle of M1; P4, first upper premolar; P5, second upper premolar; M1, first upper molar.

FIGURE 5. Results of principal components analysis, illustrating the dispersion of specimen scores for female Hsunycteris cadenai (open triangles), H. dashe (asterisk), H. pattoni (filled circles), and H. thomasi (open circles). See text for explanation and appendix 3 for factor loadings and other results.

FIGURE 6. Cytochrome-b maximum likelihood (ML) phylogram for the subfamily Lonchophyllinae. Support statistics from ML analysis and Bayesian inference (BI) are indicated at each resolved node. For the ML analysis, gray shading indicates bootstrap frequencies between 50% and 75% and black indicates bootstrap frequencies>75%. For the BA, gray indicates posterior probabilities <0.95, whereas black indicates posterior probabilities>0.95.