Anoura javieri, Pacheco & Sánchez-Vendizú & Solari, 2018

Pacheco, Víctor, Sánchez-Vendizú, Pamela & Solari, Sergio, 2018, A new species of Anoura Gray, 1838 (Chiroptera: Phyllostomidae) from Peru, with taxonomic and biogeographic comments on species of the Anoura caudifer complex, Acta Chiropterologica 20 (1), pp. 31-50 : 33-42

Anoura javieri , sp. nov.

Figs. 1 and 2

Anoura sp. nov. Pacheco et al. (1993).

Anoura sp. Pacheco et al. (1995).

Holotype

A male adult specimen catalogued in the Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos ( MUSM 6736 ). The holotype is a skin and skull in good condition, collected by Víctor Pacheco (field number VPT 887 ) on 5 September 1990. External and craniodental measurements for the holotype and paratypes are provided in Table 1 .

Type locality

Trocha Ericcson (13°11’47’’S, 71°37’11’’W), District of Challabamba, Province of Paucartambo, Department of Cusco, Peru, 3350–3450 m a.s.l. This locality is on the southern border of the Manu National Park at km 110 on the Paucartambo-Pillcopata road, in the headwaters of Río Cosñipata, a tributary of the Río Alto Madre de Dios ( Fig. 3 ).

Paratypes

Two adult males from the same locality: MUSM 6734 , collected on 3 September 1990 ; and MUSM 8749 , collected on 19 July 1991. Other designated paratypes are from nearby localities: adult male, MUSM 19602 (= FMNH 174510 ), from La Esperanza, 2880 m ; adult female, MUSM 11753 , from Pillahuata, 2600 m ; and adult male, MUSM 16559 (= FMNH 169821 ) from Suecia, 1900 m. All the type specimens were collected along the Paucartambo-Pillcopata road in the Río Cosñipata valley . Vouchers are preserved in good condition. All are skins and skulls except MUSM 16559 , which is an alcoholic specimen (fixed in formalin, and then transferred to ethanol) with skull removed, and MUSM 19602 that consists of a dry skin, skull and carcass in ethanol .

Distribution

Anoura javieri is known only from the upper montane forests of Manu Biosphere Reserve (1900– 3450 m a.s.l.), Department of Cusco, Peru ( Fig. 3 ).

Diagnosis

A small-sized Anoura that can be distinguished from other congeners by the following combination of characters: pelage dark brown overall with no distinct demarcation between dorsum and venter; tail present in two of six specimens; uropatagium narrow (<four mm at femur level) and densely furred with long hairs; and whitish claws on the hindfeet. Skull small with a long and narrow rostrum (GSL 23.7–24.8 mm); zygomatic arch complete; and lambdoid crest poorly developed. Upper incisors small and peg-like; first upper premolar (P 2) also peg-like and separated from the upper canine by a wide gap; second upper premolar (P 3) with anterobasal cusp absent; third upper premolar (P 4) without a posterolingual shelf; and paracone and metacone well developed in M 1. Mandible with long, thin, and delicate ramus; mandibular symphysis larger than canine width; and infra-angular process ventral to the middle part of the sigmoid notch.

Description

Anoura javieri is a small-size bat (HBL 61.0– 69.0 mm). Dorsal pelage is long (about 6–7 mm), dark brown, and woolly throughout; individual hairs are white at the base (80%) contrasting with dark brownish tips (20%). The ventral fur is dark brown and not contrasting with the dorsal coloration; chin is dark brown as well, but the hairs have two bands, white in the base and dark brown in the tips. The mystacial vibrissae are dark brown, robust and comparatively long. The supra and infralabial vibrissae are present and long. The genal and interramal vibrissae are present and relatively long. The tragus is long (5–6 mm) with a rounded tip. The forearm is moderately long (37–38 mm) and densely haired. The interfemoral membrane is reduced to a narrow band (1.1–1.9 mm, measured in dry skins) with its edge densely furred with long hairs (4.3 mm average, some reaching up to 5.4 mm). The femur is barely haired or naked on the proximal half, becoming densely furred on the distal half. The tibia is densely haired. The tail is present in two of six specimens (absence could be an artifact of preparation). The feet are long and have whitish claws.

The skull has comparatively short and smoothly rounded braincase, and a long and comparatively narrow rostrum (GSL, 23.7–24.8 mm). The zygomatic arch is complete, straight and slender. The palate is moderately depressed, with posterolateral margins shallow and without palatal processes. The lambdoid crest is weakly developed. The paraoccipital processes are conspicuous, slender, and medially oriented. The upper incisors are notably weak, peglike, and subequal. The surface of the upper canines is smooth, without a conspicuous sulcus. P 2 is peglike, without the anterobasal cusp, but has a low posterobasal cusp. P 2 is separated from the upper canine by a wide gap, which is almost twice the length of P 2. P 3 lacks the anterobasal cusp, and is separated from P 4 by a distinct gap. The postero-lingual cingulum on P 4 is absent or notably reduced, lacking a shelf. The molars have well developed paracones and metacones. The first upper molars are rectangular and have a weakly developed hypoconal basin; and the postprotocrista does not make an angle with the metacone. The lower premolars and molars are narrow, laterally compressed, and have well developed cusps. The paraconid on M 1 is comparatively elongated. The trigonid and talonid of lower molars are separated by a narrow constriction, and the trigonid is longer than the talonid. The mandibular ramus is long, thin, delicate, straight, and markedly low; and the mental foramen is comparatively small. The mandibular symphysis is large, usually subequal to the length of the lower canine or larger. The coronoid process is low, almost in line with the condylar process. A posterior process on the ventral surface of the mandible is well developed, and just ventral or postero-ventral to the sigmoid notch ( Fig. 1 ).

Comparisons

Anoura javieri is a small bat that differs external, cranial and dentally from any other known species of Anoura . It is easily separated from the larger species A. carishina , A. geoffroyi , A. latidens , A. peruana or A. cultrata by smaller size (forearm length <40 mm), zygomatic arches always present, paracone and metacones well developed, tail sometimes present (see below), rostrum unusually long, canines small and without sulcus, and P 1 not bladelike ( Tamsitt and Nagorsen, 1982; Mantilla-Meluk and Baker, 2010).

The new species can be confused with species of the A. caudifer complex, especially with A. caudifer and A. aequatoris , and with A. fistulata , present also in the Cosñipata valley ( Tables 2 and 3 ; and Figs. 4 , 5 , 6 , and 7). Anoura javieri and A. caudifer are similar in cranial and dental features; however, A. javieri can be distinguished by its larger body size (FA = 37.4 versus 35.27 mm on average), a longer and narrow rostrum (GSL = 24.3 vs. 22.0 mm on average), a depressed or smoothly rounded brain- case, a zygomatic arch mostly horizontal in lateral view, and absence of a palatal process. In A. javieri , the outer incisors are barely longer than the inner, whereas in A. caudifer they are longer. Anoura javieri lacks a sulcus in the upper canine, which is distinctly present in A. caudifer . The anterior cusp of P 3 is reduced or absent in A. javieri , but is always conspicuous in A. caudifer . In A. javieri , there are large gaps between C and P 2, and between P 3 and P 4, whereas in A. caudifer the gaps are small. In A. javieri , the ventral margin of the mandible is straight vs. slightly or markedly bowed in A. caudifer . In A. javieri , the mandibular symphysis is larger than the length of the lower canine, whereas in A. caudifer it is shorter. The first lower molar of A. javieri has a large, conspicuous paraconid, the trigonid is larger than the talonid, and both structures are well separated by a narrow constriction, whereas in A. caudifer the paraconid is smaller, the trigonid and talonid are subequal, and the constriction between them is not as narrow. Additionally, A. javieri has darker coloration, paler hindfeet claws, shorter calcar, and a densely furred uropatagium reduced to a narrow band in comparison to A. caudifer , which has paler brown pelage, darker hindfeet claws, longer calcar, and wider and sparsely haired uropatagium. In A. javieri , the upper and lower labial vibrissae are longer.

Anoura javieri and A. cadenai are of similar size (FA = 37.0–38.0 mm vs. 36.1–37.0 mm; GSL = 23.7–24.8 mm vs. 23.1–23.8 mm), but the skull and rostrum is much slender and delicate in the former species. In A. javieri , the upper canines are small without trace of a sulcus, whereas in A. cadenai , they is a moderate deep sulcus. In A. javieri , the upper incisors are separated when viewed from below ( Fig. 6 ), whereas in A. cadenai , they are in contact. In addition, A. javieri exhibits a distinct keel at the mandibular symphysis whereas A. cadenai has a reduced or absent keel. At present, A. cadenai is known only from western Colombia.

Compared to A. luismanueli , A. javieri is larger (FA = 37.0–38.0 mm vs. 33.6–36.9 mm; GSL = 23.7–24.8 mm vs. 20.4–21.6 mm), with longer rostrum and a longer palatal length (PAL = 12.6–13.5 mm vs. 9.6–11.0 mm). Other measurements that show no overlap between these two species are condylobasal length, maxillary toothrow length, dentary length, dentary height, and mandibular toothrow length. P2 is very small and widely separated from the canine in A. javieri . Hairs on the margin of the uropatagium of A. javieri are longer and denser than those found in A. luismanueli . In ventral view of the skull, toothrows converge anteriorly in A. javieri , in contrast to the more parallel toothrows of A. luismanueli . At present, A. luismanueli is known to occur only in Venezuela and Colombia.

Anoura aequatoris and A. javieri are more similar and could be confused because both have dark pelage and hairy uropatagia. However, A. javieri is on average larger (GSL = 24.3 mm vs. 22.0 mm; FA = 37.4 mm vs. 35.8 mm), has a longer slen- der rostrum, and a smoothly rounded braincase. Additionally, A. javieri is characterized by a small P 2 that is widely separated from the canine, a M 1 with well-reduced hypoconal basin, and a shallow angle between the postprotocrista and metacone. Other differential characters of A. javieri are absence of palatal process, smooth anterior surface of upper canines, lower molars laterally compressed, m1 larger than the other molars, well developed paraconid, and lower molars with a deep constriction between the trigonid and the talonid. The mandibular symphysis in A. javieri is also larger than in most specimens of A. aequatoris , and the uropatagium is more densely haired.

Compared to A. fistulata , A. javieri has a much narrower and densely haired uropatagium, usually less than two mm in width vs. a broader, not as well haired membrane (4.0– 7.5 mm). Foot claws are pale brown to whitish in A. javieri vs. dark brown in A. fistulata . Anoura javieri and A. fistulata average about the same size (GSL = 24.3 vs. 24.0 mm; FA = 37.4 vs. 37.5 mm), but the higher range of measurements shows that A. fistulata can attain larger size ( Table 3 ). Anoura javieri has a narrow and slender rostrum and a smoothly and rounded braincase, whereas A. fistulata has a rectangular and broader rostrum and a more globular braincase with more distinct lambdoid crests. The palate in A. javieri is slightly domed in the midline and post-molar palatal processes are absent; in contrast to the flatter palate and distinctive palatal processes in A. fistulata . In A. javieri , the upper incisors are sub-equal in length vs. a distinctly larger outer incisor in A. fistulata . In A. javieri , the upper canines lack a posterior cusp on the cingulum and a sulcus on the anterior surface, which are distinct in A. fistulata . The lower molars of A. javieri are narrow and the trigonid is larger than the talonid; in contrast, the molars are comparatively broader, and the trigonid and talonid are subequal in A. fistulata . The mental foramen is small in A. javieri , vs. large in A. fistulata .

Etymology

It is a pleasure to dedicate this species to Javier Ortiz de la Puente Denegri (1928–1952), one of the first Peruvian mammalogists ( Fig. 8 ). Javier had been highly interested in the natural sciences since childhood, and became a professor at Universidad Nacional Mayor de San Marcos at an early age. Unfortunately, he died young at the age of 24 in a tragic automobile accident, thus was unable to complete several planned publications and could not have the opportunity to prepare students in mammalogy. However, his legacy continues among Peruvian biologists because of his charisma, talent and his few, but significant contributions. Surviving contemporaneous colleagues recall him as an enthusiastic, talented and devoted student of the natural sciences. The late professors Luz Sarmiento and Hernando de Macedo often talked about Javier as a talented young scientist. Javier Ortiz de la Puente inspired the senior author to follow him in the study of mammals. Both, the late Philip Hershkovitz and Karl K. Koopman personally knew Ortiz de la Puente and also expressed their admiration for him to the senior author. His monograph ‘Estudio Monográfico de los Quirópteros de Lima y Alrededores’ ( Ortiz de la Puente, 1951) is still a benchmark for anybody interested in the study of the Peruvian bat fauna. Additional notes, with photographs, on Javier’s life have been published by Aguilar-Fernández (2009) and Franke (2007, 2012).

Ecology and habitat

Anoura javieri has been collected in upper montane forest habitat, but only from July to September during the typical dry season; none has been collected during the rainy season expeditions in spite of similar mist-netting efforts at the same sites. Anoura javieri has been collected in sympatry with the following bat species: A. caudifer , A. cultrata , A. peruana , Chiroderma salvini , Artibeus glaucus , Enchisthenes hartii , Micronycteris megalotis , Sturnira erythromos , S. magna , Platyrrhinus albericoi , P. masu , Tadarida brasiliensis , Eptesicus brasiliensis , Lasiurus blossevillii , Myotis keaysi , and M. oxyotus ( Pacheco et al., 1993; Solari et al., 2006).

The analysis of one stomach of A. javieri revealed an abundance of pollen of diverse forms, and vegetative remains that appears to be anthers. Neither arthropods nor endoparasites were found. No ectoparasites have been collected on any of the reported specimens.

Morphometric analysis

The 13 craniodental and forearm length variables exhibited a normal distribution with the Shapiro- Wilk test. Multivariate tests of MANOVA showed an overall significant difference among species (P = 0.000 for Pillai’s Trace and Wilks’ Lambda). Bonferroni post-hoc test identified the variables that significantly differentiated species in multiple comparisons ( Table 4 ). Anoura javieri differed significantly from A. aequatoris in six variables, from A. caudifer in 11 variables, and from A. fistulata in six of 14 variables. A Principal Component Analysis (PCA) of the measurements of A. caudifer , A. aequatoris , A. fistulata , and A. javieri , found two components with eigenvalues larger than 1.0. These two components (PC1 and PC2) accounted for 79.1% of total variance (56.3% and 22.8%, respectively — Table 5 ). The third component had an eigenvalue of 0.79 (5.7%), and therefore was ignored. In the plot of PC 1, usually considered to be a ‘size’ component, vs. PC 2, A. javieri is clearly separated in morphospace. This plot shows that A. javieri is larger than A. aequatoris and A. caudifer , and suggests that ‘shape’ is an important factor to differentiate A. javieri from A. fistulata . Anoura caudifer and A. aequatoris show some degree of mutual overlap, but A. fistulata is also clearly separated from the other species ( Fig. 9 ). The variables that accounted for the greatest proportion of variance are CBL, GSL, MANDL, DENL, MXTRL, BRW, and PALTL, for the first component; and C 1 C 1, ZYGW, and DENT for the second component.

Figures

FIG. 1. Dorsal, ventral and lateral views of cranium and mandible of A. javieri sp. nov. (MUSM 6736, holotype). The scale represents 10 mm

FIG. 2. Live photograph of the holotype of A. javieri sp. nov. (MUSM 6736). Photograph by V. Pacheco

FIG. 3. Map showing the collecting localities of: A. aequatoris (™), A. caudifer (l), and A. javieri sp. nov. (p) from Peru. Numbers are cross-referenced in Appendix

FIG. 4. Dorsal view of the uropatagia of: A — A. caudifer (MUSM 11754), B — A. aequatoris (MUSM 14916), and C — A. javieri sp. nov. (MUSM 19602). The uropatagium of A. javieri sp. nov. is narrower and hairy than the other species, but most similar to A. aequatoris. Not at scale

FIG. 5. Dorsal view of the skull of: A. caudifer (MUSM 16560), A. aequatoris (MUSM 37880), and A. javieri sp. nov. (MUSM 6736, holotype). Note the larger size of A. javieri sp. nov.

FIG. 6. Ventral view of the skull of: A. caudifer (MUSM 16560), A. aequatoris (MUSM 37880), and A. javieri sp. nov. (MUSM 6736, holotype)

FIG. 8. A photograph of Javier Ortiz de la Puente Denegri, taken from Franke (2012) with permission of the author

FIG. 9. Projection of specimen scores for axes 1 and 2 of PCA, applied to 13 craniodental variables and forearm length of adult males of A. aequatoris (n = 16), A. caudifer (n = 18), A. fistulata (n = 11), and A. javieri sp. nov. (n = 5). See Table 5 for variable correlations and explanation of percent variance