Lichonycteris obscura O. Thomas, 1895

Zamora-Gutierrez, Veronica & Ortega, Jorge, 2020, Lichonycterisobscura (Chiroptera: Phyllostomidae), Mammalian Species 52 (999), pp. 165-172 : 165-170

Lichonycteris obscura O. Thomas, 1895

Dark Long-tongued Bat

Lichonycteris obscura O. Thomas, 1895:56 . Type locality “ Managua,” Nicaragua.

Lichonycteris obscurus: Miller, 1900:156 . Incorrect subsequent spelling of L. obscura Thomas, 1895 .

Lichonycteris degener Miller, 1931:411 . Type locality “Para,” Pará, Brazil.

Lichonycteris deneger dos Reis, 1984:248 . Incorrect subsequent spelling of Lichonycteris degener Miller, 1931 .

CONTEXT AND CONTENT. Context as for genus. Lichonycteris degener has been considered either a subspecies ( Simmons 2005) or a synonym of L. obscura ( Hill 1985) . Gardner (1976) argued that the characters used to distinguished degener were also found in obscura , and thus suggested the two names corresponded to the same species. Hill (1985) examining a female from Belize, Central America, noted that the specimen matched Miller’s (1931) definition of degener , and proposed the latter to be considered a synonym of L. obscura (Taddei and Pedro 1993) . Simmons and Voss (1998) define two color morphs of L. obscura , a dark brown that resembles the original description of L. obscura presented by Thomas (1895), and a lighter brown that was described as L. degener by Miller (1931). Further comparisons with the holotype of L. obscura and the analysis of additional specimens from different countries revealed that the original description of L. degener is almost identical to L. obscura ( Hill 1985) . Simmons (2005) followed Hill (1985) and also considered Lichonycteris as monotypic. Later, Griffiths and Gardner (2008) considered L. degener as a valid species because the anteroposterior length of the first lower molar is shorter (≤ 1.3 mm in L. degener versus> 1.3 mm in L. obscura ) and the anteroposterior length of the lower canine is equal to or longer than anteroposterior length of the adjacent premolar in L. degener , compared to L. obscura . The taxonomic status of L. degener is problematic due to confusion regarding patterns of variation in both craniodental and pelage characters ( Gardner 1976; Hill 1985; Ochoa-G. et al. 1993). Pending a thorough revision of the genus, we follow Gardner (1976), Hill (1985), Ochoa-G. et al. (1993), and Koopman (1993, 1994), in regarding degener as a junior synonym of obscura , contra Griffiths and Gardner (2008).

The origin of the name Lichonycteris is from the Greek word lichas, hanging on the cliff; and bat from the Greek word nycteris. The species name comes from the Latin word obscura , meaning of dark color (Álvarez-Castañeda and Álvarez 1996).

DIAGNOSIS

Lichonycteris obscura ( Fig. 1 ) can be distinguished from other members of the tribe Glossophagini ( Glossophaga , Leptonycteris , and Monophyllus ) by the absence of lower incisors (a characteristic it shares with all members of the tribe Choeronycterini — Hall 1981; Carstens et al. 2002). L. obscura might be confused in the field with the lesser long-tailed bat ( Choeroniscus minor ), Godman’s long-tailed bat ( C. godmani ), and Ega long-tongued bat ( Scleronycteris ega ), but L. obscura has a distinct combination of features that distinguishes it from these species and other members of the tribe Choeronycterini (genus Anoura , Choeroniscus , Choeronycteris, Dryadonycteri , Hylonycteris , Musonycteris , Scleronycteris ): two upper molars, tricolored dorsal pelage that has a dark basal band, well-furred elbow region on the forearms, wing membrane that attaches to the foot at about mid-length of the metatarsals (Griffiths and Gardner 2008).

Members of Anoura have three upper molars, and a reduced uropatagium with or without tail, which differ from the welldeveloped uropatagium and two upper molars of L. obscura ( Thomas 1895; Husson 1962; Griffiths and Gardner 2008). The hog-nosed bat ( Choeronycteris mexicana ) differs from L. obscura by its dorsal pelage that varies from buffy brown to relatively dark grayish-brown; the venter is paler than the dorsum, compared to the dark brown dorsal pelage and darker ventral pelage of L. obscura (Griffiths and Gardner 2008) . Underwood’s long-tongued bat ( Hylonycteris underwoodi ), it is one of the smaller choeronycterines and it has three upper molars (length of forearm = 32.7 mm, compared to 33 mm in L. obscura and two upper molars), with a moderately long muzzle and small, rounded ears (Jones and Homan 1974). L. obscura is very similar in external characters to the Capixaba nectar-feeding bat ( Dryadonycteris capixaba ) but differs from it in the following: a) the shape of the rostrum in L. obscura is not anteriorly inflated but it is in the Capixaba nectar-feeding bat; b) the premaxillae are not well-developed in L. obscura but they are in the Capixaba nectar-feeding bat; c) the position of the upper incisors are evenly separated in a straight-line shape in L. obscura , and convergently positioned in the Capixaba nectar-feeding bat; d) L. obscura has two upper molars versus three in the Capixaba nectar-feeding bat ( Thomas 1895; Tschapka 2004; Nogueira et al. 2012).

GENERAL CHARACTERS

Lichonycteris obscura is a small-sized Neotropical bat. The hair is tricolored, with a narrow dark basal band providing a dark brown pattern in the dorsal pelage, and a slightly darker dorsum ( Thomas 1895; Goodwin 1942; Emmons 1999; Wetterer et al. 2000; Nogueira et al. 2007). The wing membrane is attached to the feet at about mid-length of the metatarsals; the elbow and the metacarpal region of the thumb are densely covered with fur ( Thomas 1895; Elliot 1904). Representatives of the genus Lichonycteris have a small nose-leaf in the shape of an equilateral triangle, prominent whiskers, and ears that are short and rounded; the tragus is one-third the length of the ear ( Elliot 1904; Husson 1962; Eisenberg and Redford 1999; Tirira 2007). It has a tail that extends to the knees and the tip can be seen pointing upwards from the well-developed uropatagium that attaches to the ankles ( Thomas 1895; Husson 1962). L. obscura also has a distinctively long calcar (5.8–9.0 mm) almost as long as the foot ( Thomas 1895; Reid et al. 2000). The muzzle is elongated, robust, but not narrow and tube-like ( Fig. 2 ). The lower jaw is longer than upper, the lower lip extends as a slit, and the lower incisors are absent ( Sanborn 1943; Aguirre 2007).

External measurements (mm) from the holotype (female) were: total length, 46; tail length, 6.7; ear length, 10; forearm length, 33; calcar, 5.8; length of hind foot without claws, 7.5; length of interfemoral membrane, 17 ( Thomas 1895). Cranial measurements (mm) of the holotype were: basal length, 16.8; greatest length of skull, 19.7; breadth of braincase, 8.1; interorbital breadth, 4; length of palate, 11; breadth outside last

Ranges of cranial measurements (mm, mean ± SD) for adult L. obscura (sexes combined) were: greatest length of skull, 17.7–19.9 (18.8 ± 0.7); basal length, 15.4–16.8 (16.3 ± 0.6); condylobasal length, 17–18.9 (18.0 ± 0.6); condylo-incisive length, 17.5 ( Reid et al. 2000); braincase breadth, 8.0–9.2 (8.2 ± 0.3); interorbital breadth, 3.3–4.5 (4.1 ± 0.3); palatal length, 9.3–11 (10.5 ± 0.8); mastoidal breadth, 7.9–8.4 (8.2 ± 0.2); breadth across M2–M2, 4.1–4.5 (4.3 ± 0.2); breadth across M3– M3, 4.2–4.8 (4.4 ± 0.2); length of maxillary toothrow, 5.4–6.5 (6.0 ± 0.3); length of mandibular toothrow, 5.8–6.8 (6.3 ± 0.3); zygomatic breadth, 8.1–9 (8.5 ± 0.3); breadth across canines, 3.9–4.4 (4.0 ± 0.1— Thomas 1895; Elliot 1904; Sanborn 1936, 1943; Goodwin 1942, 1946; Davis et al. 1964; Carter et al. 1966; Gardner et al. 1970; Jones et al. 1971; Gardner 1976; LaVal and Fitch 1977; Hall 1981; Brosset and Charles-Dominique 1990; Álvarez-Castañeda and Álvarez 1991; Ochoa-G. et al. 1993; Simmons and Voss 1998; Zortea et al. 1998; Albuja 1999; Reid et al. 2000; Lim and Engstrom 2001; Soriano et al. 2005). Additional measurements (mm) in the literature were: length of the third digit of the first phalanx, 11.5; length of the third digit of the second phalanx, 16; length of metacarpal III, 30.5; length of rostrum, 2.22 ± 0.04 ( Davis et al. 1964). The first phalanx of fifth finger is more than one-fourth the length of the metacarpal ( Goodwin 1942; Sanborn 1943). molar, 4.4; length from front of upper canine to back of last molar, 6.4 ( Thomas 1895).

Ranges of external measurements (mm or g, mean ± SD) for adult L. obscura (sexes combined) were: total length, 46–63 (54.7 ± 5.4); length of forearm, 29.8–35.5 (32.9 ± 1.7); length of hind foot, 7.5–12 (8.6 ± 1.2); length of ear, 10–13 (10.7 ± 1.1); length of tragus, 4–7 (5.3 ± 1.5); length of tail, 6–11 (8.3 ± 1.8); weight, 6–11 (7.4 ± 2.1— Thomas 1895; Sanborn 1936, 1943; Goodwin 1942, 1946; Davis et al. 1964; Carter et al. 1966; Gardner et al. 1970; Jones et al. 1971; Gardner 1976; LaVal and Fitch 1977; Hall 1981; Brosset and Charles-Dominique 1990; Álvarez-Castañeda and Álvarez 1991; Ochoa-G. et al. 1993; Simmons and Voss 1998; Zortea et al. 1998; Albuja 1999; Reid et al. 2000; Lim and Engstrom 2001; Soriano et al. 2005).

DISTRIBUTION

Lichonycteris obscura is distributed from southern Chiapas, Mexico through Central America and into South America where the distribution follows the Andean region in the Amazonian versant across Venezuela, Guyana, Surinam, and French Guiana until the Amazon basin of Brazil ( Hall 1981; Eisenberg and Redford 1999; Fig. 3 ; for additional locality information, see Table 1). It has been recorded in western Venezuela, northwestern and central Colombia, and there are some records from Colombian Amazon ( Montenegro and Romero-Ruiz 1999; Mantilla-Meluk et al. 2009), western Colombia, and western Ecuador on the Pacific slope, whereas in Peru and Bolivia it occurs on the Amazonia slope (eastern). L. obscura occurs on an elevation range from 0 to 1,000 m ( Castaño et al. 2003; Genoways and Timm 2005; Griffiths and Gardner 2008; Reid 2009; SaavedraRodríguez and Rojas-Díaz 2011). No fossils are known.

FORM AND FUNCTION

Dental formula of Lichonycteris obscura is i 2/0, c 1/1, p 2/3, m 2/2, total 26 ( Thomas 1895; Goodwin 1942; Sanborn 1943; Phillips 1971; Eisenberg and Redford 1999). The frontal dental gap is calculated as 1.25 mm 2 ( Freeman 1995); upper incisors are small, spaced apart, laterally dislocated, and evenly distributed between canines ( Carstens et al. 2002). The inner incisors have flat crowns; the outer incisors have pointed crowns. Upper canines are simple and recurved; the base of each canine is long and narrow with a trace of posterior cingular vestige ( Carstens et al. 2002).

First upper premolar is smaller than the second; the main cone of the first upper premolar is prominent and has a small postero-lingual shelf. The second upper molar is twice as long as it is broad; it has a cingular shelf that begins at the anterior upper end of the tooth and extends along the lingual side forming a postero-lingual shelf ( Phillips 1971). Upper molars do not touch each other.The W-shaped ectoloph is usually present, and in some individuals, the paracone is lacking or reduced. The second upper molar shows similar topology as the first upper molar but it is slightly smaller. The mesostyle is lacking or it can be found on the posterior element of the ectoloph, and the metacone is lower than the labial margin of the tooth (second upper molar) but is the same size of the metastyle. The protocone is a low, ridge-like cusp, and the hypoconal basin is absent. Lower canines are simple with a reduced cingular shelf ( Phillips 1971).

The three lower premolars are not in contact; the first one is the smallest and the third is the largest. All premolars are short and broad; the first lower premolar is low and lacks anterior and posterior cingular styles. Whereas, the second and third are higher and lack anterior and posterior cingular styles. The two lower molars are separated by a small space. The metaconid of the first lower molar m1 is large, in a vertical cone, and the protoconid is reduced. The paraconid of the first lower molar is broad and rounded; the entoconid is low with a ridge-like cusp separated from the labial margin of the talonid by a shallow U-shaped valley. The hypoconid is reduced with none distinct cusp. The second lower molar differs from the first in having a larger protoconid and a narrow paraconid ( Phillips 1971).

The upper molars in L. obscura are extremely variable in structure compared to other Glossophaginae . In a review of the dental abnormalities of Lichonycteris , some specimens showed supernumerary upper molars ( Phillips 1971). In an adult male from Panama, an extra tooth was present anterior to the first molar. It differs from the first upper premolar in having a single root that is set in its own alveolus; it resembles the first upper premolar in coronal configuration ( Phillips 1971). In an adult female from Brazil, an extra tooth was located posterior to the upper canine. The tooth was separated from the first upper premolar by a small gap and it was relatively lower-crowned ( Phillips 1971).

Lichonycteris obscura has an incomplete zygomatic arch. The superficial fibers of the genio-hyoideus muscle pass ventrally to the basihyal to form a weak insertion into fibers of the hyoglossus and sternohyoideus, via the former bashyal raphe. The stylohyoideus is present ( Griffiths 1982; Wetterer et al. 2000).

Lichonycteris obscura has basketlike medial-posterior mechanical papillae in the tongue. Three small papillae are anterior to the four larger papillae, and the central two are largest ( Griffiths 1982). Winter and Von Helversen (2003) investigated operational tongue length, as an adaptation associated with nectar-feeding, by measuring how far down from the upper rim to the bottom of two test tubes (inner diameters of 9 and 15 mm) a bat could drain the level of sugar water. The range of operational tongue length for the nine species of glossophagine bats included in the study was 38–66 mm ( L. obscura = 46 mm) for the 9-mm tube, and 55–77 mm ( L. obscura = 55 mm) for the 15-mm tube (Winter and Von Helversen 2003). The species presents Brunner’s glands at the gastroduodenal juncture ( Forman et al. 1979).

The brain of L. obscura shares some external characteristics with members of Hylonycteris and Choeroniscus . These include a small and simple cerebellum with a smooth surface, small olfactory bulbs, and shallow pseudocentral sulci; however, the brain of L. obscura differs by its ventrally angular pseudotemporal lobes, compared to the ventrally rounded ones in the aforementioned genera. Brain characters of L. obscura differ from other Glossophaginae in that members of Glossophaga and Leptonycteris have smaller sulci; Choeronycteris and Monophyllus have shallower pseudotemporal lobes with a cerebellum containing only primary foliations. Species of Anoura have larger olfactory bulbs, shallower pseudotemporal lobes, and larger cerebral hemispheres ( McDaniel 1976).

The wings of L. obscura are more similar to those of the Carolliinae and diverge from the rest of the Glossophaginae species in their longer forearms and third metacarpals but are closely similar to those of Underwood’s long-tongued bat (Smith and Starrett 1979). The calculated wing loading for L. obscura is 2 Nm 2, the aspect ratio index mean (± SD) is 2.2 ± 0.05, with a wing tip index of 2 ± 0.05 ( Tschapka 2004; White 2009). Species presenting similar measurements (i.e., Pallas’s longtongued bat Glossophaga soricina ) have good maneuverability and fast flight, and can be an inference for L. obscura ( White 2009) . L. obscura wing indices are significantly different from those of Commissaris’s long-tongued bat ( G. commissarisi ) and the orange nectar bat ( Lonchophylla robusta — White 2009).

ONTOGENY AND REPRODUCTION

The reproductive period of Lichonycteris obscura occurs during the dry season in the Neotropics ( Wilson 1979). One pregnant female with a 16-mm embryo was reported from Mexico in May (Álvarez-Castañeda and Álvarez 1991); pregnant females from Guatemala with 17-mm and 14-mm embryos were recorded in February ( Carter et al. 1966). One lactating female and one pregnant female with one embryo of 14 mm were captured from Costa Rica in January and March, respectively ( Gardner et al. 1970). One pregnant female from Venezuela was reported in March ( Soriano et al. 2005); one pregnant female, from Brazil, had a 13.0-mm embryo in August (Taddei and Pedro 1993). Reports from Ecuador include two pregnant females, one with a 20-mm embryo and one with a 10-mm embryo, and a lactating one in October ( Albuja 1999; Reid et al. 2000). It is estimated that the embryo can add up to an additional 30% of the female’s body weight ( Tschapka 2004). Male testes range from 1 to 3 mm by about 2 mm ( Jones et al. 1971; Reid et al. 2000).

Figures

Fig. 1.—An adult male Lichonycteris obscura from the Ecological Reserve Michelin, State of Bahía, northeastern Brazil. Specimen caught April 2009 in the Atlantic forest. Used with permission of the photographer M. Mello.

Fig. 2.—Dorsal, ventral, and lateral views of skull and lateral view of mandible of a female of Lichonycteris obscura ([Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional] 4242) from 15 km E of Pichucalco, Chiapas, México. Greatest length of the skull is 19.42 mm.

Fig. 3.—Geographic distribution of Lichonycteris obscura. Map redrawn from Hall (1981), and Eisenberg and Redford (1999) with modifications.