Sturnira lilium: Dobson 1878: 540

Velazco, Paúl M. & Patterson, Bruce D., 2019, Small Mammals Of The Mayo River Basin In Northern Peru, With The Description Of A New Species Of Sturnira (Chiroptera: Phyllostomidae), Bulletin of the American Museum of Natural History 2019 (429), pp. 1-69 : 26-40

Sturnira lilium: Dobson 1878: 540 (part). Sturnira lilium lilium: Cabrera 1958: 78 (part). S [turnira]. new species 3: Velazco and Patterson

2013: 687.

HOLOTYPE: The holotype ( AMNH 268545 ; fig.

2, table 14), an adult male specimen preserved in

alcohol with the skull removed and cleaned, was collected by Nancy B. Simmons (original field number 846) on 8 October 1994 at Paracou (5°17′N, 53°55′W, 210 m), near Sinnamary, Cayenne, French Guiana. The body and skull are in good condition. Frozen tissues are deposited at the Ambrose Monell Cryo Collection at the American Museum of Natural History ( AMCC 110416).

PARATYPES: An adult female ( FMNH 203582 ) caught by Paúl M. Velazco (original field number PMV 2295 ) collected on 2 May 2007 at the Waqanki locality. An adult female ( MUSM 13260 ) caught by Robert S. Voss (original field number RSV 2365 ) collected on 5 July 1998 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. Frozen tissues are deposited at the Ambrose Monell Cryo Collec- tion of the American Museum of Natural History ( AMCC 109783 ). An adult male ( MUSM 39228 ) caught by Richard Cadenillas (original field number RCO 965 ) collected on 14 May 2007 at El Diamante locality (table 14). Frozen tissues of FMNH 203582 and MUSM 39228 are deposited at the Field Museum of Natural History .

DISTRIBUTION: Eastern slopes of the Andes and adjacent Amazonian lowlands from Colombia to northern Bolivia. Lowlands of southern Venezuela, the Guianas, and Brazilian Amazon ( fig. 3; appendix). One specimen of Sturnira giannae (FMNH 128845) was collected at a locality ( fig. 3: 19) on the western slope of the Andes in the department of Cajamarca, Peru. This record could result from populations of S. giannae using the Huancabamba Depression, which features the lowest montane passes in the Andes between Venezuela and Chile, as a corridor to cross the Andes.

ETYMOLOGY: The epithet giannae , a feminine noun in the genitive case, is proposed in dedication to the daughter of the first author, Gianna C. Velazco Kline.

DIAGNOSIS: Dorsal fur short and bicolored with pale brown bases (80% of length) and dark brown tips. Ventral fur short and monocolored. Shoulder glands (epaulettes) present in both sexes, but variable in the degree of development. Trailing edge of the uropatagium covered by short hairs. Sphenorbital fissure small. Zygomatic arches do not converge anteriorly. Anterior process of glenoid fossa well developed. Upper inner incisor (I1) bicuspidate and slender. First and second lower incisors (i1 and i2) tricuspidate and subequal in height. Paraconid present and well developed in m1 but absent in m2. Metaconids and entoconids of m1, m2, and m3 well defined and separated by a deep notch.

DESCRIPTION: Sturnira giannae is a mediumsized yellow-shouldered bat (FA 43.0–47.0 mm; GLS 21.7–24.2 mm; CIL 20.1–21.8 mm; fig. 4, tables 14–15) with a slender rostrum and a globular braincase ( fig. 2). The dorsal pelage is brown to reddish brown ( fig. 4). Dorsal hairs are bicolored with a long, pale brown base (approximately 80% of the length of each hair), and a short, darkbrown terminal band (approximately 20% of each hair). The ventral pelage is brown to reddish brown ( fig. 4). Ventral hairs are monocolored and vary from gray to pale brown. The fur is short, ~ 5–6 mm long between the shoulders and 4 mm on the chest. Shoulder glands (epaulettes) are present in both sexes with varying degrees of definition: weakly defined in some specimens (e.g., FMNH 203588) and strongly so in others (MUSM

A

B

39228). The trailing edge of the uropatagium is covered by short hairs (5.0 mm) ( fig. 5A). The proximal portion of the forearm (roughly 50% of the shaft just distal to the elbow) is densely furred with short hairs. The dorsal surfaces of the tibia and feet are sparsely covered with long hairs. The III and IV metacarpals are subequal in length, but shorter than the V metacarpal.

The skull of Sturnira giannae has a globular braincase with a slender rostrum and well-developed sagittal crest (smaller in females but still well developed). Postorbital processes moderately developed ( fig. 2). The posterior border of hard palate shows intraspecific variation, some individuals with a U-shaped border while in others it is V-shaped. The basisphenoid pits are divided by a narrow midline septum ( fig. 2). The sphenorbital fissure is oval or circular, but always small. The zygomatic arches do not converge anteriorly. The anterior process of the glenoid fossa is well developed ( fig. 2).

Sturnira giannae has a dental formula of I2/2, C1/1, P2/2, M3/3 = 32 teeth. The upper inner incisor (I1) is bicuspidate, with these cusps noticeable only in younger individuals without pronounced tooth wear ( fig. 6A). The I1 is orthodont, slender, and at least twice the height of I2. P4 is shorter anteroposteriorly than P5, and the crown height of P4 is slightly less than that of P5. P5 has a small distal cusp. The anteroposterior and labiolingual lengths of M1 exceed those of M2. The protocones of P5, M1, and M2 are tall and well developed. The paracones of M1 and M2 are slightly shorter than corresponding metacones on the same teeth. The M3 is ovoid in shape and has one lingual and one or two labial cones (cusps). If two labial cones are present, they are divided by a shallow notch. The first and second lower incisors (i1 and i2) are tricuspidate and subequal in height. The lower canine covers less than 25% of the occlusal area of i2. The lower canine shafts are slightly oriented outward. The lower canine is less than 2× the height of p1. The anteroposterior length of p5 exceeds that of p1. The p1 is slightly higher than p5. The protoconid, hypoconid, metaconid, and entoconid are present on m1 and m2. The paraconid is present and well developed on m1 but absent on m2. The lingual cuspids (metaconid and entoconid) on m1 and m2 are long anteroposteriorly. The metaconids and entoconids of m1, m2, and m3 are well defined and separated by a deep notch ( fig. 7A). In some individuals, the metaconids of m2 is divided into two cusps (e.g., MUSM 5922, 39228). The protoconid is the tallest cuspid on m1 and the entoconid is the lowest. All the four cuspids present on m2 are subequal in height. The m3 is small with only the protoconid, metaconid, and entoconid present. All three cuspids of m3 are subequal in height.

COMPARISONS: Sturnira giannae was compared with all the species of the lilium complex ( S. angeli , S. bakeri , S. lilium , S. luisi , S. parvidens , and S. paulsoni ) ( Velazco and Patterson, 2013) and with other species of the genus that occur in sympatry with it (e.g., S. magna , S. oporaphilum , S. sorianoi , and S. tildae ). External and craniodental measurements for S. giannae and the compared species are provided in tables 14–16 ( S. lilium and S. tildae ); other relevant sources of measurement data are de la Torre (1966: in text— S. angeli and S. magna ), de la Torre and Schwartz (1966: in text— S. paulsoni ), Jones and Phillips (1976: table 1— S. angeli and S. paulsoni ), Molinari et al. (2017: table 3— S. oporaphilum ), Sánchez-Hernández et al. (2005: table 2— S. sorianoi ), Simmons and Voss (1998: table 45— S. tildae ), Tamsitt et al. (1986: table 1— S. magna ), Velazco and Patterson (2014: tables 1–2— S. bakeri , S. luisi , S. oporaphilum , and S. parvidens ), Kwiecinski et al. (2018: table 1— S. paulsoni paulsoni ), and Pedersen et al. (2018: table 1-- S. paulsoni luciae ).

Size serves to distinguish some but not all Sturnira species. Sturnira giannae can be easily distinguished from S. magna by the latter’s longer forearm and longer greatest length of skull ( Tamsitt et al., 1986: table 1) and from S. parvidens by that bat’s shorter forearm and shorter greatest length of skull ( Velazco and Patterson, 2014: table 2). Sturnira giannae , S. angeli , S. bakeri , S. lilium , S. luisi , S. oporaphilum , S. paulsoni , S. sorianoi , and S. tildae overlap somewhat in size but are unambiguously distinguished by pelage and craniodental characteristics (tables 15–17).

Externally, the dorsal fur between the shoulders of S. giannae , S. luisi , and S. parvidens is short (4.0–6.0 mm) whereas it is long (> 8 mm) in S. angeli , S. lilium , S. magna , S. sorianoi , S. oporaphilum , and S. tildae . Individual dorsal hairs are bicolored in S. giannae , S. lilium , S. luisi , and S. parvidens whereas they are 4-colored in S. angeli , S. magna , S. sorianoi , S. oporaphilum , and S. tildae . The overall appearance of the dorsal pelage is brown to reddish brown in S. giannae and S. tildae , whereas it is pale brown in S. angeli , S. lilium , S. luisi , S. magna , and S. oporaphilum , slightly reddish in S. parvidens , and pale gray in S. sorianoi . Ventrally the hairs are short (3–5 mm) and monocolored in S. giannae and S. tildae , whereas they are long (6–8 mm) and monocolored in S. lilium , short (4.0–6.0 mm) and bicolored in S. luisi , short (3–5 mm) and tricolored in S. parvidens , long (6–8 mm) and tricolored in S. angeli , S. sorianoi , and S. oporaphilum , and short (3–5 mm) and 4-colored in S. magna . The ventral fur is pale brown to reddish brown in S. giannae , whereas is pale brown in S. angeli , S. lilium , S. magna , S. sorianoi , S. oporaphilum , and S. tildae , dark gray in S. luisi , and reddish in S. parvidens . Shoulder glands (epaulettes) are weakly to strongly developed in specimens of S. giannae , whereas epaulettes are weakly defined in S. sorianoi and S. oporaphilum and more conspicuous in S. angeli , S. lilium , S. luisi , S. magna , S. parvidens , and S. tildae . The trailing edge of the uropatagium is covered by short hairs (4–6 mm) in S. giannae , S. luisi , S. oporaphilum , S. parvidens , and S. tildae , whereas the uropatagium is covered by long hairs (7–9 mm) in S. angeli , S. lilium , S. magna , and S. sorianoi ( fig. 5). The proximal portion of the forearm (roughly 50% of the shaft just proximal to the elbow) is densely furred with short hairs in S. giannae , S. angeli , S. parvidens , and S. tildae , whereas it is sparsely furred with short hairs in S. luisi and S. oporaphilum and sparsely furred with long hairs in S. lilium , S. magna , and S. sorianoi . The dorsal surfaces of the tibia and feet are sparsely covered with long hairs in S. giannae , S. angeli , S. magna , S. sorianoi , S. oporaphilum , and S. tildae , whereas the tibia and feet are densely covered with long hairs in S. lilium , the tibia is sparsely covered with long hairs and the feet are densely covered with long hairs in S. parvidens , and the tibia is sparsely covered with short hairs and the feet are densely covered with short hairs in S. luisi . Metacarpal IV is subequal to metacarpal III in S. giannae , S. angeli , S. lilium , S. luisi , S. magna , S. sorianoi , and S. oporaphilum , whereas metacarpal IV is shorter than metacarpal III in S. parvidens and longer than metacarpal III in S. tildae .

Cranially, the sagittal crest is well developed in S. giannae , S. lilium , S. magna , S. paulsoni , and S. tildae , whereas it is weakly developed in S. angeli , S. sorianoi , and S. oporaphilum . The postorbital processes are moderately developed in S. giannae , S. oporaphilum , S. paulsoni , and S. tildae , whereas they are well developed in S. angeli , S. magna , and S. sorianoi . The postorbital processes of S. lilium vary from moderately developed to well developed. The basisphenoid pits are divided by a narrow midline septum in S. giannae , S. lilium , S. luisi , S. magna , S. parvidens , and S. tildae , whereas the midline septum is broader in S. angeli , S. oporaphilum , S. paulsoni , and S. sorianoi . The sphenorbital fissure is small in S. giannae and S. magna , whereas it is large in S. angeli , S. lilium , S. oporaphilum , and S. sorianoi . Some specimens of S. tildae and S. paulsoni present a small sphenorbital fissure whereas in others it is large. The zygomatic arches do not converge anteriorly in S. giannae , S. lilium , S. magna , S. oporaphilum , S. sorianoi , and S. tildae , whereas they are bowed outward in S. angeli , S. luisi , S. paulsoni , and S. parvidens . The anterior process of the glenoid fossa is well developed in S. giannae , S. magna , S. luisi , and S. parvidens , whereas it is weakly developed in S. paulsoni , S. sorianoi , and S. tildae , and absent in S. angeli . Some specimens of S. lilium and S. oporaphilum lack the anterior process of the glenoid fossa while in others it is weakly developed.

Dentally, I1 is bicuspidate in S. giannae , S. angeli , S. luisi , S. magna , S. parvidens , S. sorianoi , and S. tildae , whereas it is unicuspidate in S. lilium , S. oporaphilum , and S. paulsoni ( fig. 6). The I1 is orthodont and slender in S. giannae , S. angeli , S. lilium , and S. paulsoni , whereas this tooth is orthodont and broad in S. oporaphilum , S. sorianoi , and S. tildae , and proodont and broad in S. magna . The protocones of P5, M1, and M2 are tall and well developed in S. giannae , S. oporaphilum , and S. sorianoi , whereas they are low and weakly developed in S. angeli and S. magna . These protocones are well developed in some specimens of S. lilium (AMNH 185320), whereas in others they are low and weakly developed (AMNH 205180, 256984). In Sturnira paulsoni and S. tildae , the protocones of M1 and M2 are tall and well developed but on P5, the protocone is low and weakly developed. The i1 and i2 are tricuspidate in S. giannae , S. angeli , S. lilium , S. luisi , S. magna , S. paulsoni , S. parvidens , S. sorianoi , and S. tildae , whereas they are bicuspidate in S. oporaphilum . The metaconids and entoconids of m1 and m2 are well defined and separated by a deep notch in S. giannae , S. lilium , S. luisi , S. paulsoni , and S. parvidens , whereas they are well defined but separated by a shallow notch in S. angeli and S. tildae , and poorly defined and not separated by a notch in S. magna , S. oporaphilum , and S. sorianoi . The metaconids of m1 and m2 are well defined and long mesiodistally in S. giannae and S. angeli , whereas they are well defined and short mesiodistally in S. lilium , S. tildae , and S. paulsoni , and poorly defined in S. magna , S. oporaphilum , and S. sorianoi ( fig. 7). The metaconid and entoconid of m3 are separated by a deep notch in S. giannae , S. lilium , and S. paulsoni (when m3 is present), whereas these cusps are separated by a weak notch in S. angeli and S. magna and not separated in S. oporaphilum ( fig. 7). Some specimens of S. sorianoi and S. tildae present the metaconid and entoconid of m3 separated by a weak notch while in others they are not separated.

NATURAL HISTORY: Natural history information on S. giannae has been previously reported under the name Sturnira lilium , where it is mixed with reports from S. angeli , S. lilium sensu stricto, S. parvidens , and S. paulsoni . We discriminate the information of S. giannae from published records of S. angeli , S. lilium sensu stricto, S. parvidens , and S. paulsoni , all previously considered subspecies of S. lilium sensu lato ( Velazco and Patterson, 2013), by considering only reports from the lower Orinoco and the Amazon basins as belonging to S. giannae . This species may occur in a wide variety of forested habitats, excluding only very dry forests and those above 2000 m elevation ( Handley, 1976). Its documented roosting sites include dense foliage, tree holes, caves, and culverts ( Linares, 1998) as well as buildings ( Goodwin and Greenhall, 1961). S. giannae is a frugivorous bat that has been reported to feed on at least 41 plant species representing 20 genera in 14 families: Cyathula prostrata (Amaranthaceae) ; Rollinia exsucca (Annonaceae) ; Couma utilis (Apocynaceae) ; Anthurium trinerve , Philodendron grandifolium , Ph. squamiferum, Ph. sp. ( Araceae ); Carica papaya , Jacaratia digitata (Caricaceae) ; Cecropia distachya, Ce. ficifolia, Ce.

TABLE 17 Morphological differences among Sturnira giannae , S. lilium , S. oporaphilum , and S. tildae

obtusa ( Cecropiaceae ); Clusia sp. , Vismia guianensis , Vismia sp. (Clusiaceae) ; Muntingia calabura (Elaeocarpaceae) ; Banara guianensis (Flacourtiaceae) ; Poraqueiba sericea (Icacinaceae) ; Byrsonima sp. (Malpiguiaceae) ; Ficus panurensis , F. paraensis (Moraceae) ; Piper aduncum , Pi. bartlingianum , Pi. hostmannianum ; Pi. sp. ( Piperaceae ); Coffea sp. (Rubiaceae) ; Markea longiflora , Solanum asperum , So. caavurana , So. confine , So. coriaceum , So. grandiflorum , So. lanceolatum , So. leucocarpon , So. paniculatum , So. rugosum , So. schlechtendalianum , So. subinerme , So. torvum, So. sp. ( Solanaceae ); Celtis schippii (Ulmaceae) ( dos Reis and Guillaumet, 1983; de Foresta et al., 1984; Charles-Dominique, 1986, 1993; Foster et al., 1986; dos Reis and Peracchi, 1987; Maas et al., 1992; Gorchov et al., 1995; Charles-Dominique and Cockle, 2001; Lobova et al., 2003, 2009; Lobova and Mori, 2004).

Lactating females have been reported in the months of May, June, and November in Peru ( Hice et al., 2004) and pregnant females in the months of March, July, August, October, and November in Peru ( Tuttle, 1970; Hice et al., 2004) and in June, July, and August in French Guiana ( Brosset and Dubost, 1967). Both pregnant and lactating females were reported in December and January in Pará and Amazonas, Brazil ( Marques-Aguiar, 1985).

Wenzel (1976) reported three species of streblid flies occurring on Sturnira giannae in Venezuela ( Aspidoptera falcata , Trichobius lionycteridis , and Trichobius parasparsus ). The dermatophytic fungi Exophiala (Wangiella) dermatitidis was isolated from the lung of one individual collected in a secondary forest in Manaus, Brazil ( Reiss and Mok, 1979). The bacteria Bartonella and Leptospira were found in the single individual tested and in three of 38 individuals tested, respectively ( Matthias et al., 2005; Bai et al., 2012). One of 43 Sturnira giannae near the type locality tested positive for rabies virus ( de Thoisy et al., 2016).

REMARKS: The synonymy of Sturnira lilium sensu lato includes several junior synonyms, one nomen nudum, and unavailable names. The majority of those are undoubtedly assignable to S. lilium sensu stricto (e.g., Phyllostoma spiculatum Lichtenstein, 1823 ; Phyllostoma excisum Wagner, 1842 ; Phyllostoma albescens Wagner, 1847 ; Phyllostoma chrysosema Natterer, 1883 , in Pelzeln, 1883).

A specific type locality was not mentioned in the original description of five junior synonyms of Sturnira lilium . Phyllostoma vampyrus was described by Schinz (1845) from “America tropicali,” but to our knowledge a holotype was not designated. The holotype of Nyctiplanus rotundatus , which was described by Gray (1849) with only “Brazils” as the type locality, is now lost ( Carter and Dolan, 1978). Phyllostoma fumarium Wagner, 1847 was described based on a single specimen. Its label was lost while the specimen was being prepared as a study skin (with partial skull inside) and had been removed from its original fluid condition. Wagner (1847) remembered that the specimen was from Brazil but did not recall a specific locality within Brazil. Photographs of the holotype (ZSM 58) clearly show that the trailing edge of the uropatagium and the tibia and feet are densely covered by long hairs characteristic of S. lilium . For that reason, we recommend continued assignment of Phyllostoma fumarium Wagner, 1847 , as a junior synonym of Sturnira lilium (Geoffoy St.- Hilaire, 1810). Sturnira spectrum Gray, 1842 , was also described based on a specimen from Brazil. The label does not specify sex or a specific locality. Photographs of the holotype (BMNH 42.12.2.4), a dry study skin with a partial skull (only the rostrum is preserved) revealed two diagnostic characteristics of S. lilium : the trailing edge of the uropatagium and the tibia and feet are densely covered by long hairs and the inner upper incisors are unicuspidate. Therefore, we recommend that Sturnira spectrum Gray, 1842 , should likewise be regarded as a junior synonym of Sturnira lilium (Geoffoy St.-Hilaire, 1810). The name Phyllostoma chrysocomos Wagner, 1855 should also be assigned to Sturnira lilium (Geoffoy St.-Hilaire, 1810) as a junior synonym because it is a renaming of Sturnira spectrum Gray, 1842 .