Sturnira hondurensis Goodwin, 1940

Hernández-Canchola, Giovani, Ortega, Jorge & León-Paniagua, Livia, 2021, Sturnira hondurensis (Chiroptera: Phyllostomidae), Mammalian Species 53 (1001), pp. 23-34 : 23-28

Sturnira hondurensis Goodwin, 1940

Honduran Yellow-shouldered Bat

Sturnira hondurensis Goodwin, 1940:1 . Type locality “La Cruze Grande [= La Cruz Grande], near San Jose; elevation about 3000 feet; Department La Paz, Honduras ” (see “Nomenclatural Notes”).

Sturnira ludovici: Hershkovitz, 1949:441 . Name combination (see “Nomenclatural Notes”).

Sturnira oporaphilum: de la Torre, 1961:113 . Name combination.

Sturnira ludovici occidentalis Jones and Phillips, 1964:477 . Type locality “Plumosas, 2500 feet elevation, Sinaloa,” Mexico.

Sturnira ludovici ludovici: Jones and Phillips, 1964:477 . Name combination.

Sturnira ludovici hondurensis: Koopman, 1994:86 . Name combination.

Sturnira hondurensis hondurensis: Ramírez-Pulido et al., 2014:13 . First use of current name combination.

Sturnira hondurensis occidentalis: Ramírez-Pulido et al., 2014:13 . First use of current name combination.

Sturnira hondurensis ludovici: Téllez-Girón, 2014:737 . Name combination.

CONTEXT AND CONTENT. Order Chiroptera , suborder Yangochiroptera , family Phyllostomidae , subfamily Stenodermatinae , tribe Sturnirini , genus Sturnira . S. hondurensis is one of 24 described species (Velazco and Patterson 2019). The following two subspecies are currently recognized (RamírezPulido et al. 2014):

S. h. hondurensis Goodwin, 1940:1 . See above.

S. h. occidentalis Jones and Phillips, 1964:477. See above.

NOMENCLATURAL NOTES. In our examination of the type specimen of Sturnira hondurensis we noticed that the spelling of the type locality on the original specimen tag was “La Cruz Grande” as opposed to “La Cruze Grande” as it appears in Goodwin (1940). Sturnira hondurensis was described in 1940 by Goodwin as a smaller species of Sturnira , distinct from S. ludovici , because the lower incisors were deeply bilobed instead of simple, as seen in S. ludovici . Nevertheless, S. hondurensis was synonymized to S. ludovici by Hershkovitz (1949), because he noted that some specimens of Colombian S. ludovici with bilobate lower incisors wear down these teeth and thus lose this characteristic with age. Nevertheless, subsequent molecular and morphological reviews of the genus Sturnira have supported recognizing S. hondurensis as an independent Mesoamerican species ( Iudica 2000; Velazco and Patterson 2013).

Sturnira comes from the Latin sturnirus or sturnus (starling), possibly in reference to the “H. M. S. Starling,” an escort vessel on which the type specimen of the genus was collected. The specific epithet hondurensis was coined to indicate that the type specimen is from Honduras ( Gannon et al. 1989; SánchezHernández et al. 2016).

One common name of S. hondurensis is highland yellowshouldered bat (Téllez-Girón 2014; Álvarez-Castañeda and Gonzalez-Ruiz 2018); however, it is the same common name currently used for S. ludovici ( Burgin et al. 2018) . S. hondurensis has also been called Honduran yellow-shouldered bat (SánchezHernández et al. 2016), and in Spanish murciélago de charreteras mayor (Álvarez-Castañeda and Gonzalez-Ruiz 2018).

DIAGNOSIS

For positive identification purposes, Sturnira hondurensis

( Figs. 1 and 2 ) needs to be compared with other species of the municipality, Veracruz, Mexico, February 2007. Photograph by Antonio Guille genus, especially species that are more closely related, or with which it can be sympatric ( S. parvidens ). S. hondurensis has four well-developed lower incisors, whereas S. bidens (bidentate yellow-shouldered bat) and S. nana (lesser yellow-shouldered bat) have only two functional inferior incisors (Molinari and Soriano 1987). In S. hondurensis the metaconoid and entoconoid in m1–2 are poorly defined, whereas in many other species of Sturnira ( S. angeli [ Dominica yellow-shouldered bat], S. aratathomasi [Arata-Thomas yellow-shouldered bat], S. bakeri [Baker’s yellow-shouldered bat], S. giannae [Gianna’s yellow-shouldered bat], S. lilium [little yellow-shouldered bat], S. luisi [Luisi’s yellow-shouldered bat], S. cf. mistratensis [Mistratoan yellow-shouldered bat], S. parvidens [little yellow-shouldered Mesoamerican bat], S. paulsoni [Paulson’s yellow-shouldered bat], S. perla [Perla yellow-shouldered bat], and S. tildae [Tilda’s yellow-shouldered bat]), they are well separated by a deep notch ( Iudica 2000).

Sturnira hondurensis can be easily distinguished from S. magna (greater yellow-shouldered bat) by its smaller size. The forearm and greatest skull lengths of S. hondurensis are 38.58–46.9 mm and 21.7–25.6 mm, respectively, whereas those of S. magna are 56.3–59.6 mm and 27.9–29.1 mm ( de la Torre 1966). The fourth metacarpal is shorter than the third metacarpal in S. hondurensis , whereas they are of similar length in S. adrianae (Adriana’s yellow-shouldered bat— Molinari et al. 2017). The basisphenoid pits are deep and divided by a high septum in S. hondurensis , whereas they are shallow and divided by a low midline septum in S. burtonlimi (Burton’s yellow-shouldered bat), S. ludovici (highland yellow-shouldered bat), S. mordax (Talamancan yellow-shouldered bat), and S. oporaphilum (Tschudi’s yellow-shouldered bat—Velazco and Patterson 2014). The sphenorbital fissure is subcircular in S. hondurensis , whereas it is oval in S. adrianae , S. ludovici , and S. parvidens (Velazco and Patterson 2014; Molinari et al. 2017). The proximal end of the stylohyoid is narrow in S. hondurensis , whereas it is expanded in S. burtonlimi , S. ludovici , S. oporaphilum , and S. parvidens (Velazco and Patterson 2014) . The palate of S. hondurensis is depressed but it is flat in S. bogotensis (Bogota yellow-shouldered bat) and S. erythromos (hairy yellow-shouldered bat—Pacheco and Patterson 1991). In S. hondurensis all teeth are close together, but in S. koopmanhilli (Choco yellow-shouldered bat) there are diastemas among premolars and molars ( McCarthy et al. 2006). The upper central incisors in S. hondurensis have a single cusp, in contrast, they are bilobed in S. adrianae , S. ludovici , S. mordax , S. oporaphilum , and S. parvidens (Velazco and Patterson 2014; Molinari et al. 2017). S. hondurensis lacks the small distal cusp on P3 that is present in S. burtonlimi and S. oporaphilum (Velazco and Patterson 2014) . The direction of the premetacrista of M1 is oblique to the upper alveolar plane in S. hondurensis , whereas it is perpendicular in S. burtonlimi . One labial cusp is present on M 3 in S. hondurensis , whereas there are two in S. parvidens (Velazco and Patterson 2014) . The lower incisors are bilobed in S. hondurensis but they are trilobed in S. parvidens and S. cf. sorianoi (Soriano’s yellow-shouldered bat— Sánchez-Hernández et al. 2005; Velazco and Patterson 2014). The lower canines are not laterally divergent in S. hondurensis , whereas they are laterally divergent with shafts slanted outward in S. burtonlimi , S. ludovici , and S. parvidens (Velazco and Patterson 2014) .

Average measurements (external and cranial) were smaller for Sturnira h. occidentalis than S. h. hondurensis . Also S. h. occidentalis is paler (both ventrally and dorsally) than S. h. hondurensis and it has a relatively broader skull with a shorter and more abruptly elevated rostrum ( Fig. 3 ; Jones and Phillips 1964).

GENERAL CHARACTERS

Sturnira hondurensis is a medium-sized stenodermatine bat. As in other stenodermatines, the eyes are large and have eyelashes ( de la Torre 1961). The ears are sharp-pointed, and the tragus is long, falcate, curved, and tapers to a point. A large antitragus forms a thickened horizontal ledge at the base of the ear. Two glandular ridges originate laterally to the anterior base of the noseleaf and continue dorsally to the level of the eyes. The nares are directed anteriorly, and are located at the basal part of the well-developed triangular noseleaf. The upper lip is simple and has small and variable warty growths. The lower lip has wart-like cutaneous pads that occur as a semicircular row of small pads surrounding a large central pad ( Fig. 1 ; Goodwin 1940; de la Torre 1961; Sánchez-Hernández et al. 2016).

The propatagium originates medially at the level of the shoulder. The plagiopatagium extends laterally down to the ankles and is sparsely covered with short hairs. The fourth metacarpal is shorter than the third. There is a vestigial uropatagium, and the trailing edge of the uropatagium is furred with long hairs (7.0–9.0 mm); there is no tail and the calcar is short ( de la Torre 1961; Velazco and Patterson 2014).

Fur color ranges from dark gray to dark brown, and the venter is paler than dorsum.Young are paler than adults, and most individuals, especially adult males, have reddish or yellowish patches on the shoulders. Dorsal (between the shoulders) and ventral pelage is long (7.0– 10 mm). The proximal portion of the forearm, the dorsal surfaces of the femur, tibia, feet, and digits of the feet are densely covered with long hairs ( Fig. 2 ; Téllez-Girón 2014; Velazco and Patterson 2014; Sánchez-Hernández et al. 2016).

Ranges of external measurements (mm or g) in S. h. hondurensis from eastern Mexico, Guatemala, El Salvador, Honduras, and Nicaragua ( Goodwin 1940; Lukens and Davis 1957; de la Torre 1961; Jones et al. 1971; Swanepoel and Genoways 1979; Velazco and Patterson 2014), and S. h. occidentalis from Colima, Jalisco, and Sinaloa ( Mexico —Jones and Phillips 1964; Sánchez-Hernández et al. 2002, 2016), respectively, were: head–body length, 65.0–77.0 and 52.0–77.0; length of hind foot, 12.0–15.0 and 11.0– 16.0; ear length, 12.9–19.0 and 12.0–19.0; forearm length, 43.0–46.9 and 38.58–44.93; and weight, 26.8 and 12.0–22.5. Ranges of cranial measurements (mm) in S. h. hondurensis and S. h. occidentalis, from previous references in addition to those from the Mexican states of Durango and Jalisco (S. h. occidentalis —Jones and Phillips 1964) were: greatest length of skull, 21.8–25.6 and 21.7–24.23; condyle–canine length, 20.1–22.2 and 19.0–20.79; zygomatic breadth, 12.5– 14.2 and 12.49–14.3; mastoid breadth, 11.5–12.4 and 10.8– 12.48; braincase breadth, 10.1–10.6 and 9.58–10.70; length of maxillary toothrow, 6.3–7.2 and 5.8–7.36; length of mandibular toothrow, 7.2–8.0 and 6.7–8.17; and interorbital width, 6.0–6.3 and 5.3–7.71 ( Fig. 3 ). In S. hondurensis from Oaxaca, Mexico it has been suggested that males average slightly larger than females (Swanepoel and Genoways 1979).

DISTRIBUTION

After Sturnira hondurensis was recognized as an independent species ( Iudica 2000; Velazco and Patterson 2013), there was no consensus concerning its southern geographic boundary (Téllez-Girón 2014; Sánchez-Hernández et al. 2016; Torres-Morales 2019); however, a phylogeographic analysis of S. hondurensis populations confirmed that the southern boundary is located in northern Nicaragua (HernándezCanchola 2018). S. h. hondurensis occurs on mountain ranges in eastern Mexico, from Nuevo León and Tamaulipas southward to northern Nicaragua. On the other hand, S. h. occidentalis occurs in western and central Mexico. Jones and Phillips (1964) described this subspecies from western Mexico, occurring from southern Sinaloa and Durango to Jalisco (Sierra Madre Oriental), but analyses with mitochondrial DNA showed that S. h. occidentalis occurs as far east as the state of Estado de Mexico, through the eastern and central portions of the Trans-Volcanic Belt ( Fig. 4 ; HernándezCanchola 2018). S. hondurensis has been found from sea level up to 2,900 m ( Lavariega et al. 2012; Molinari et al. 2017; Verde Arregoitia et al. 2018). No fossils of S. hondurensis are known.

FORM AND FUNCTION

The skull of Sturnira hondurensis is relatively long and narrow, and the braincase is moderately high with a moderately well-developed sagittal crest ( Goodwin 1940). The rostrum is slender, the basisphenoid pits are deep and divided by a high septum, the sphenorbital fissure is subcircular, the anterior process of the glenoid fossa is well developed, and the proximal end of the stylohyoid is narrow (Velazco and Patterson 2014). The brain of S. hondurensis closely resembles that of S. parvidens . It has deep and extremely smooth cerebral hemispheres. The pseudocentral sulci and sulci anterior to the pseudocentral sulci are poorly developed compared to other stenodermatine bats. The pseudotemporal lobes are angular and project ventrally. The inferior colliculi are completely covered, and the cerebellum is simple and has a medial crest ( McDaniel 1973). Phillips et al. (1977) described in detail the gross anatomy and histology of the parotid, submandibular, and sublingual glands. The parotid gland is large and is posterior to the masseter, on the midline of the throat. It is a compound acinar gland that is densely packed with elongate secretory acini comprised of typical serous cells, and is characterized by an extensive system of ducts. Stenson’s duct arises from the anterior edge of the parotid to the oral cavity at the level of the posterior side of the canines. The submandibular gland is large and triangular, filling the cervical fossa. It is a compound tubuloacinar gland with large and densely packed secretory acini. The duct system of the submandibular is relatively simple; Wharton’s duct arises from the center of the inferior surfaces and is joined to the main duct from the sublingual gland, and together they open near the first lower premolar. The sublingual gland is moderately sized, triangular, and soft. It is unilobular but has numerous fine subdivisions that can be seen clearly. The sublingual gland is a compound tubuloacinar gland comprised of mucous cells with a relatively simple duct system ( Phillips et al. 1977).

The dental formula is i 2/2, c 1/1, p 2/2, m 3/3, total = 32 (Téllez-Girón 2014). I1 is unicuspidate and larger than I2 (Jones and Phillips 1964). The direction of the premetacrista of M1 is oblique to the upper alveolar plane, and there is one labial cusp in M3 (Velazco and Patterson 2014). P3–4 and M1 occur in straight, slightly diverging lines, but M2–3 are at an inwarddirected angle. The lower incisors are deeply bilobate, though these teeth wear with the age as in other member of the genus Sturnira ( Goodwin 1940; Hershkovitz 1949). The lower canines are not laterally divergent (Velazco and Patterson 2014). The paraconid and metaconid of m1–2 are poorly defined and the entoconid suppressed, with no division between them and the metaconid ( Hershkovitz 1949). The coronal portion of the dentin in the teeth of S. hondurensis is characterized by distinct, highly arborized dentinal tubes that follow a general S-shaped path from the pulpal chamber to the dentino–enamel junction. The pulpal cavity is filled with a complex soft tissue that is continuous with the periapical tissue through the apical foramen of the roots. In S. hondurensis , the pulp is most often healthy and odontoblastic cells are essentially normal. Nonetheless, extensive hyperemia (dilation of capillaries) is commonly found in S. hondurensis . This condition has been shown to be either transitory or an indication of early pulpitis ( Phillips et al. 1977).

Sturnira hondurensis has a simple stomach with a welldeveloped, elongated and tapered cardiac vestibule ( Rouk 1973; Forman et al. 1979). The fundic cecum is saccular and thin-walled, forming a spacious chamber with an apex ( Forman et al. 1979). The pyloric valve is vestigial ( Rouk 1973). The gastroesophageal junction lies well superior to the gastroduodenal junction ( Forman et al. 1979), and the latter is clearly marked by a decreased thickness of the muscularis ( Rouk 1973). The corpovestibular and vestibulocecal junctions are marked by distinct sulci that anastomose near the midregion of the stomach ( Rouk 1973). The tunica muscularis is bilaminate, and the tunica submucosa forms the rugae, which in general are longitudinally oriented; there are numerous branches forming transverse secondary folds, but there are not many elastic fibers ( Rouk 1973). In the tunica mucosa, cardiac glands surround the gastroesophageal junction ( Rouk 1973; Forman et al. 1979), and they are weakly reactive or nonreactive to procedures intended to demonstrate the presence of acid mucopolysaccharides ( Forman et al. 1979). Oxyntic glands occupy the cardiac vestibule, the cardiac cecum, and a portion of the corpus ( Rouk 1973). In the basal one-third of these glands, there are numerous alpha chief cells and only a few mucous gland cells ( Rouk 1973). As oxyntic glands disappear, transitional glands (mainly mucous cell glands) become increasingly apparent ( Rouk 1973). There are cells within the bases of the pyloric glands which are histologically identical to the submucosal glands of Brunner located in the uppermost duodenum ( Forman et al. 1979). The morphology of the stomach of S. hondurensis resembles that of S. parvidens , though there are some differences between the two species. In S. hondurensis , the stomach is more robust, the pyloric tube is shorter, the pyloric sphincter is only a short projection on the lesser curvature, the musculature of the terminal portion is relatively thinner, and mucous neck cells in the lower portion of the fundic glands are more abundant ( Forman 1973). S. hondurensis has a mean gut area of 4.34 cm 2 ( Saldaña-Vázquez et al. 2015).

The hairs of S. hondurensis do not have a medulla, and the scales are coronal and unequally hastate (Baca-Ibarra and Sánchez-Cordero 2004). In Hidalgo ( Mexico), one of 16 individuals of S. hondurensis showed partial leucism in both wings ( García-Morales et al. 2012b). In the same Mexican state, another individual of S. hondurensis had a white spot extending from above the left eye to the mouth (SánchezHernández et al. 2012). In both of the previous mentioned cases, the individuals were pregnant females, supporting the idea that chromatic disorders are not detrimental for bats (Lucati and López-Baucells 2017; Hernández-Canchola et al. 2019). In Nicaragua, the stable-hydrogen isotope (δD) in claws was −78.8% and in hair was −80.7%, similar values were reported in other frugivorous bats from the same region ( Fraser et al. 2010).

In Oaxaca ( Mexico) the wing aspect ratio [wing span in m 2 / wing area in m 2] of S. hondurensis was 11.11, and the relative wing loading [(mass in g) (gravitational acceleration in m/s 2)/ wing area in m 2] was 5.97 (García-García et al. 2014).

ONTOGENY AND REPRODUCTION

Pregnant females were found in January–February ( Mexico: Guerrero), March ( El Salvador: Santa Ana; Mexico: Puebla), April ( El Salvador: Santa Ana; Mexico: Jalisco), May ( El Salvador: Santa Ana), June ( El Salvador: Santa Ana; Mexico: Guerrero, Jalisco), July ( El Salvador: Santa Ana; Mexico: Jalisco), August ( El Salvador: Santa Ana; Mexico: Chiapas, Puebla), September–October ( El Salvador: Santa Ana), November ( Mexico: Jalisco), and December ( Mexico: Guerrero). In all cases, females had a single embryo (Jones and Phillips 1964; Villa-R 1966; Watkins et al. 1972; Hellebuyck et al. 1985; Iñiguez-Dávalos 2005; Jiménez-Salmerón 2008; Cabrera-Garrido 2016; Morales-Rivas 2016).

As in most bats, there are two axillary mammary glands ( de la Torre 1961). Lactating females were found in March ( Mexico: Puebla), April ( El Salvador: Santa Ana; Mexico: Colima, Guerrero, Jalisco), May–June ( El Salvador: Santa Ana; Mexico: Jalisco), July ( El Salvador: Santa Ana; Mexico: Colima, Guerrero, Jalisco), August ( El Salvador: Santa Ana; Mexico: Colima, Jalisco, Puebla), September ( El Salvador: Santa Ana; Mexico: Jalisco), October ( Mexico: Jalisco, Puebla), November ( El Salvador: Santa Ana), December ( Guatemala — de la Torre 1961; Baker and Phillips 1965; Watkins et al. 1972; Hellebuyck et al. 1985; Sánchez-Hernández et al. 2002; Iñiguez-Dávalos 2005; Jímenez-Salmerón 2008; Cabrera-Garrido 2016; MoralesRivas 2016). Post-lactating females were reported during April ( El Salvador: Santa Ana; Mexico: Guerrero), May ( El Salvador: Santa Ana), June ( El Salvador: Santa Ana; Mexico: Guerrero, Jalisco), July ( El Salvador: Santa Ana; Mexico: Guerrero), August–September ( El Salvador: Santa Ana — Iñiguez-Dávalos 2005; Jímenez-Salmerón 2008; Morales-Rivas 2016). One juvenile was recorded in August ( Mexico: Colima), and sub-adults during August ( Mexico: Colima) and December ( Guatemala — de la Torre 1961; Sánchez-Hernández et al. 2002).

Males with scrotal testes were reported in January ( Mexico: Colima, Guerrero), February ( Mexico: Guerrero), March ( Guatemala; Mexico: Puebla), April ( Mexico: Guerrero, Jalisco), May–June ( Mexico: Jalisco), July ( Mexico: Guerrero), September ( Mexico: Guerrero, Jalisco), October ( El Salvador: Santa Ana), November ( Mexico: Guerrero), and December ( Mexico: Colima, Guerrero — de la Torre 1961; Villa-R 1966; Sánchez-Hernández et al. 2002; Iñiguez-Dávalos 2005; JímenezSalmerón 2008; Cabrera-Garrido 2016; Morales-Rivas 2016).

In the Mexican state of Guerrero a bimodal, polyestrous reproductive pattern has been suggested (Jiménez-Salmerón 2008), but a continuous, polyestrous reproductive pattern interrupted by periods of inactivity was suggested in El Salvador, possibly due to severe climate during autumn and winter ( Morales-Rivas 2016). On the other hand, in western Mexico the maximum frequency of pregnant and lactating females and juveniles of S. hondurensis is observed between May and July, coinciding with the greatest seasonal abundance of the primary fruit ( Solanum nigricans ) consumed locally by S. hondurensis ( Iñiguez-Dávalos 2005) .

Figures

Fig. 1.—An adult female Sturnira hondurensis from Ahuatepec, Zongolica municipality,Veracruz, Mexico, November 2015.Photograph by Alfredo Andre

Fig. 2.—An adult male Sturnira hondurensis from Santuario de Bosque de Niebla, A

Fig. 3.—Dorsal, ventral, and lateral views of skulls and lateral view of mandibles of two adult males of Sturnira hondurensis. Left, Sturnira hondurensis occidentalis (MZFC-M [Museo de Zoologi Mexico. Greatest length of skull, excluding incisor is 21.79 mm. Right, Sturnira hondurensis hondurensis (MZFC-M 10015) from 1.3 km al NNW de Chiquihuites, Unio Lucero-Verdugo used with permission.

Fig. 4.—Geographic distribution of Sturnira hondurensis. Subspecies: 1, S. h. hondurensis (blue shading); 2, S. h. occidentalis (green shading); distribution according to Hernández-Canchola (2018). Black dots indicate the type locality of each subspecies.