Nyctiellus lepidus ( Gervais, 1837 )

Tejedor, Adrian, 2011, Systematics Of Funnel-Eared Bats (Chiroptera: Natalidae), Bulletin of the American Museum of Natural History 2011 (353), pp. 1-140 : 15-23

Nyctiellus lepidus ( Gervais, 1837)

Figure 10

Vespertilio lepidus Gervais, 1837: 253 . No holotype bearing this name exists. The original specimen appears to have been relabeled as Nyctiellus lepidus when Gervais (1856) transferred V. lepidus to the genus Nyctiellus .

Vespertilio barbatus Gundlach, 1840: 356 . Holotype unknown. Synonymized with N. lepidus by Gundlach in Peters (1861).

Nyctiellus lepidus: Gervais, 1856: 84 . New combination.

Vespertilio (Nyctiellus) lepidus: Gundlach in Peters, 1861: 150. New combination.

Vespertilio (Natalus) lepidus: Gundlach, 1867: 252 . New combination.

Natalus lepidus: Dobson, 1878: 344 . New combination.

Natalus (Natalus) lepidus: Miller and Rehn, 1901: 274 . New combination.

Natalus (Nyctiellus) lepidus Dalquest, 1950: 443 . New combination.

HOLOTYPE: Holotype by monotypy, MNHN A.621, skin in alcohol with skull removed (skull lost), collected in Cuba (specific locality, date, and collector unknown). Skin in good condition, but highly bleached from long immersion in alcohol .

DISTRIBUTION: Cuba (including the Isle of Pines ) and the Bahamas (Eleuthera, Cat, Great and Little Exuma, and Long; also, as a fossil, in Andros and New Providence; fig. 11) .

DIAGNOSIS: Same as for genus.

DESCRIPTION: Very small size (forearm length 26.6–31.0 mm; greatest skull length 12.5–14.0 mm; weight 2–3 g); muzzle broad and dorsoventrally flattened; nostrils nearly circular, opening ventrolaterally on a round- ed skin pad on margin of upper lip; upper lip thin; lower lip thickened and indented in ventral margin, with numerous transversal grooves; natalid organ low, rather square shaped (with nearly parallel lateral margins) and never reaches forehead; ears relatively short (10.0– 13.6 mm); ear pinna relatively narrow with rounded tip; 7 or more ear ridges along lateral margin of distal pinna; ventral region of ear pinna moderately expanded but funnellike; medial ear margin rigid, with longitudinal fold along ventral face; tragus short, wedge shaped, and contorted into funnellike structure; tibia (12.3– 14.0 mm) shorter than half the length of the forearm; calcar long and thin, occupying less than half the length of the free edge of uropatagium; free margin of uropatagium naked, lacking fringe of hairs; wings relatively long and narrow, with 3rd metacarpal (23.8–26.6 mm) longer than 5th metacarpal (21.2–23.8 mm); pelage dense and lax; hairs long (4–6 mm); pelage color from grayish brown to reddish or orange brown; hairs bicolored, with tips darker than bases; contrast between tips and bases of hairs more marked dorsally than ventrally; dense mustachelike hair tufts along lateral margins of upper lip and on dorsum of muzzle; mustache along lateral margins of upper lip formed by dense, tough, parallel, and ventrally curved hairs; portion of mustache on dorsum of muzzle denser than that along upper lip; dorsum of natalid organ with a tuft of hairs; skull long with slight rostral flexion; rostrum broad and deep, with marked sulcus between nasals; slight palatal emargination; maxillaries swollen; braincase low, with well-developed sagittal crest; maxillary branch of zygomatic arch deeper than twice the height of crowns of last molars; pterygoids convergent; palate extending caudally to half the length of pterygoids; basisphenoid pit deep with steep sides; medial ridge along basisphenoid absent; ectotympanic large, covering most of the periotic; I2 inflected medially; reduced first premolars; molar cusps relatively thin and long; lower molars with talonid broader than trigonid; spinous process of humerus much higher than capitulum; thorax relatively long and narrow; ribs expanded craniocaudally; vertebrae C7 and T1 fused and fused to ribs; vertebrae T12–L4 fused entirely without vestige of sutures; vertebrae L5 and L6 free; caudal vertebrae 8 and 9 longer than distance from ischium to iliac crest of sacrum.

COMPARISONS: Nyctiellus lepidus is the smallest species in the family Natalidae and one of the smallest bats in the world (notably small bats include Crasseonycteris thonglongyai , 1.7–2.0 g; and Pipistrellus nanulus , 2.5 g; Hill and Smith, 1981). Among natalids, it is approached in body weight only by two species of Chilonatalus ( C. micropus , and C. macer ), but these have a forearm longer than 32.0 mm and in Nyctiellus the forearm is shorter than 31.0 mm. Nyctiellus lepidus can also be distinguished by its absolutely and relatively shorter tibia, which is shorter than half the length of its forearm. In all other genera of Natalidae the tibia is always longer than half the length of the forearm.

Externally, N. lepidus can be readily distinguished from all other natalids by its relatively narrow distal third of the ear pinna and by the naked free edge of the uropatagium. In all other natalids, the distal third of the ear pinna is wide (forming part of the funnel-shaped pinna that is typical of natalids) and there is a fringe of hairs along the free margin of the uropatagium. In addition, N. lepidus differs from species of Chilonatalus (the only natalids that could be confused with Nyctiellus because of their small size) by the lack of dermal outgrowths on the dorsum of rostrum and on the chin. In all species of Chilonatalus , the face shows distinctive dermal outgrowths.

The skull of Nyctiellus is well differentiated from that of all other natalids. Its braincase is not markedly inflated and shows a very high sagittal crest that is as high along its rostral half as it is along its caudal half. All other natalids have inflated or globular braincases and a much lower sagittal crest that is more prominent in its rostral half. In N. lepidus , the rostral branch of the zygomatic arch is relatively robust, being deeper (wider) than the height of the last molar. In all other natalids, on the other hand, the rostral base of the zygomatic arch is thin, being shallower (narrower) than the height of the last molar. In N. lepidus , the emargination between the two palatal branches of the premaxillary is narrow and the inner incisors (I1) almost touch each other along the midline, whereas in all other natalids the emargination is wider and the inner incisors are widely separated. Nyctiellus lepidus is also distinguishable from the remaining species of the family by its undivided basisphenoid pit, a structure always bisected by a longitudinal ridge in all

other natalids. In addition, the ectotympanic of N. lepidus is very large, almost covering the entire periotic, whereas in all other natalids the ectotympanic is smaller and a large portion of the periotic is visible.

Dentally, N. lepidus is easily distinguishable from all other natalids by the marked reduction in the first premolar both of the upper and lower dentition. In all other natalids the first premolar is of similar size to the remaining premolars.

VARIATION: Females have larger and longer wings than males (i.e., a longer forearm, P, 0.05, and a longer 3rd metacarpal, P, 0.05). Females from Cuba have longer skulls than males ( Silva-Taboada, 1979).

Average forearm length in male Nyctiellus lepidus from the Bahamas was smaller than those from Cuba (P, 0.05; fig. 12), but the Bahamian males had broader and deeper skulls (larger mean of braincase breadth, postorbital breadth, and braincase depth; P, 0.05; fig. 12) and longer maxillary tooth row (P, 0.05; fig. 12). N. lepidus does not differ in size throughout Cuba and the Isle of Pines ( Silva-Taboada, 1979), nor among islands of the Bahamas (within the sample analyzed here).

NATURAL HISTORY AND CONSERVATION: Nyctiellus lepidus is known from 63 localities (36 are day roosts), including one represented by bone remains only (fig. 11). Almost all known roost sites are caves except for one disused hotel cistern near Ferry, Exuma, Bahamas, which used to be permanently occupied by a colony of this species until its restoration in 2004 (K. Murray, in litt.). Caves occupied by N. lepidus vary widely in size (e.g., large, Cueva del Jagüey, Cuba, locality 155, with 1700 m of linear extension, Silva-Taboada, 1974; small, Cueva del Calabazar, Cuba, locality 142, less than 10 m, Tejedor et al., 2005a). N. lepidus selects caves or cave chambers that have high relative humidity ( Silva-Taboada, 1979) where it is often found roosting in areas of low ceiling and near bodies of water. It is occasionally found in hot caves (temperature range 25u– 40u C, sensu Silva-Taboada, 1977), but more commonly roosts in caves with temperatures toward the low end of that range (Silva- Taboada, 1979). It has been found coexisting with 15 other bat species in the same cave ( Artibeus jamaicensis , Brachyphylla nana , Chilonatalus macer , Eptesicus fuscus , Erophylla sezekorni , Macrotus waterhousii , Mormoops blainvillei , Monophyllus redmani , Noctilio leporinus , Nyctinomops macrotis , Phyllonycteris poeyi , Pteronotus macleayi , Pteronotus parnellii , Pteronotus quadridens , and Tadarida brasiliensis ; Silva-Taboada, 1979), but seems to prefer caves or cave areas not occupied by groups of other species. Nonetheless, in Cueva del Calabazar, Pinar del Río, Cuba, it has been observed roosting in close association with Chilonatalus macer ( Tejedor et al., 2005a) . Within roosting groups, individuals hang widely spaced and are generally quiet, allowing human observers to approach closely (Silva- Taboada, 1979).

Nyctiellus lepidus is found from xeric (858 mm annual precipitation, Long Is., the Bahamas, locality 514) to mesic habitats (1763 mm annual precipitation, Guanayara, Cuba; locality 163) including scrub, semideciduous, and evergreen forest vegetations. In altitude, it ranges from sea level to 422 m.

Nyctiellus lepidus feeds on insects. Common food items in Cuba include leafhoppers ( Cicadellidae and Fulgoridae ), flies ( Muscidae ), termites ( Nasutitermes sp. ) plus moths (Lepidoptera) and hymenopterans (Silva- Taboada, 1979). In a 1969 study of food volume consumption by this species in Cueva Grande de Caguanes (locality 151), Cuba, females were able to carry up to near 30 % of their body weight in terms of stomach contents, versus 22 % in males. Also, females increased food consumption in summer (July) by 34 % relative to winter (December), whereas this increase was only 8.9 % for males. On average, young adults consumed less food (about 15 % of body weight) than did older adults (about 21 %, Silva-Taboada, 1979).

Nyctiellus lepidus has a single annual estrus, and bears one pup per litter. In Cuba, where copulation may take place during winter (December to February), pregnant females have been found between March and July, and lactation extends from July to September, peaking in the latter month. Nonreproducing adult females are found throughout the year and subadults from both sexes are found from July to September ( Silva-Taboada, 1979).

From July to September both sexes roost separately, with females gathering in large maternity colonies in the deepest parts of caves. Male-only groups form in more external areas of the caves or in neighboring caves where maternity colonies are not found. Nonreproductive females occasionally may be found within such groups of males. Allen and Sanborn (1937) noted that N. lepidus might also segregate sexually in July in the Bahamas. During foraging flights, females carry their pups, which average more than 35 % the weight of their mothers.

Nyctiellus lepidus is an abundant species, and it is represented by at least 674 specimens in museum collections. Most specimens have been taken at only a few localities: Sheep Hill Cave, Cat, Bahamas (locality 501) ; Miller’s Cave , Long, Bahamas (locality 512) ; Cueva de Las Tres Dolinas , Cuba (locality 149). Observed fluctuations in the size of colonies may be related to sexual segregation during the reproductive season .

Natural predators of the species are unknown. It is parasitized by trematodes ( Ochoterenatrema pricei , Limatulum solitarium , Urotrema scabridum ), nematodes ( Tricholeiperia sp. Physocephalus sp. , Biacantha silvai), mites (Mesoperigliscurus nyctiellinus, Ornithodoros natalinus , Eutrombicula angulis- cuta, Eutrombicula lipovskyana ), and streblids ( Trichobius wenzeli ; Milán and Stekol’nikov, 2004; Silva-Taboada, 1979).

Nightly, there are two foraging periods. The first begins around sunset (28 min to +11 min) and extends for up to 45 minutes, the second is shorter and ends around sunrise (28 min to +5 min). Males begin and end their foraging bouts before females, especially lactating ones, which carry their young in flight. Such short foraging bouts are associated with a massive exodus and return to the caves and probably with very small home ranges. Mark-recapture trials performed during foraging periods indicated that individuals were unable to return to their cave if released at distances greater than 2 km from the roost ( Silva-Taboada, 1979). Nyctiellus lepidus flies very erratically and low within vegetation or over open pasture.

The body temperature of Nyctiellus lepidus has been observed to increase from 33.5u C to 35.2u C in association with a seasonal increase in ambient temperature from 24.7 (March) to 27.4 (May). This species is susceptible to rapid dehydration outside the roost, and has the highest rate of water loss from patagia among Cuban bats (other species of natalids were not examined; Silva-Taboada, 1979).

This species has been listed as least concern by the IUCN (2010) Its ability to form large colonies in very small caves or cavelike habitats and to forage over open pasture and secondary scrub suggest that it is a resilient species, unlikely to be threatened as long as its roost sites are left undisturbed.