Specimens and Measurements

For this study I examined 3234 specimens of Natalus (including all 20 holotypes in the family). These specimens are housed in 26 museums, all of which are listed (including abbreviations) in appendix 1.

Morphological terminology follows Giannini et al. (2006) for the cranium, Smith (1972) and Morgan and Czaplewski (2003) for the postcranium, Freeman (1998) for the dentition, and Ridgway (1912) for pelage coloration. A total of 1137 specimens were measured for this study, of which eight were juveniles or young adults. Additional measurements were taken from Pedersen et al. (2003), López-González et al. (1998), Taddei and Uieda (2001), Silva-Taboada (1979), and Goodwin (1959). Length of forearm and length of tibia were measured from study skins, fluid-preserved specimens, and fresh specimens, whereas ear length was measured exclusively from fluid-preserved and fresh specimens. Given that measurements of length of tibia taken from fluid-preserved specimens have been found to be significantly larger on average than those taken from dry skins (Tejedor, 2005), means of length of tibia taken by those two measures are reported separately. Lineal measurements were taken with dial and digital calipers and are given in millimeters. Measurements of weight were taken from specimen tags and are given in grams. Lineal measurements are defined as follows:

Forearm length: Distance from the elbow to the distal end of the forearm including carpals, taken with the wing at least partially folded.

Ear length: Maximum distance between the ventral point of attachment of the pinna and the tip of the pinna.

Length of tibia: Distance from the proximal end of the tibia to the posterior base of the calcar (in dry specimens), and distance from the knee to the ankle with both knee and ankle bent to an angle of at least 90° (in fluid-preserved specimens).

Length of 3rd metacarpal: Distance from wrist to distal end of 3rd metacarpal, taken with the wing folded.

Length of 5th metacarpal: Distance from wrist to distal end of 5th metacarpal, taken with the wing folded.

Length of penis: Maximum distance from the caudal base to the tip of the penis, without stretching.

Length of natalid organ: Maximum distance from the rostral margin to the caudal margin of the natalid organ (in Nyctiellus and Chilonatalus) or from the dorsal point of flexion between rostrum and forehead to the caudal margin of the natalid organ (in Natalus), taken externally.

Greatest skull length: Maximum distance between the anteriormost point of the skull, including the incisors, and the posteriormost point of the occiput.

Zygomatic breadth: Greatest distance across the external margins of the zygomatic processes.

Braincase breadth: Greatest breadth of the globular part of the braincase, taken perpendicular to the skull's longitudinal axis.

Postorbital breadth: Least breadth across the postorbital constriction.

Breadth across molars: Greatest distance between the labial edges of the upper molar series.

Breadth across canines: Greatest distance between the labial edges of the cingula of the upper canines.

Maxillary toothrow length: Greatest crown length of the maxillary tooth row, measured from the anteriormost edge of the canine to the posteriormost edge of M3.

Mandibular toothrow length: Greatest crown length of the mandibular tooth row, measured from the anteriormost edge of the canine to the posteriormost edge of m3.

Mental length: Least distance from the mental foramen to the ventral margin of the dentary between the angular process and the condyle (used only for Natalus primus, a species for which numerous fossil specimens had incomplete mandibular tooth rows).

Depth of braincase: Distance between the basioccipito-palatal plane and the dorsalmost edge of the sagittal crest.

Cranial measurements (except mental length) are illustrated in figure 1.

Fig. 1.

Cranial dimensions measured in this study: A, postorbital breadth; B, zygomatic breadth; C, braincase breadth; D, breadth across canines; E, breadth across molars; F, maxillary toothrow length; G, greatest skull length; H, depth of skull; I, mandibular toothrow length.

In addition, to graphically represent interspecific variation in cranial shape, several indices were calculated: (1) relative breadth across canines  =  breadth across canines/greatest skull length; (2) relative breadth across molars  =  breadth across molars/maxillary toothrow length; (3) relative maxillary toothrow length  =  maxillary toothrow length/ greatest skull length; (4) relative breadth of postorbital constriction  =  postorbital breadth/zygomatic breadth.

Ecomorphological Analyses

Ecomorphological traits were inferred from a combination of measurement data and field observations. Measurements of forearm length, length of tibia, and 3rd and 5th metacarpals were used as descriptors of flight surface shape. In all natalids, the uropatagium is roughly wedge shaped and its free margin extends from near the ankle to the tip of the tail; therefore, its extension depends mostly on the length of the legs and tail. For this reason, the length of the tibia was used as an indicator of the size of the uropatagium. Two indices were calculated to represent shape of flight surfaces: (1) shape of the wing tip ( =  length of 5th metacarpal/length of 3rd metacarpal) and (2) relative size of the uropatagium ( =  length of tibia/forearm length). In addition, two indices were calculated to represent relative size of organs related (or potentially related) to reproduction in males: (1) relative length of the penis ( =  length of penis/forearm length) and (2) relative length of the natalid organ ( =  length of natalid organ/forearm length). Forearm length was used to define three body size classes: (1) large (mean forearm length 43.5–49 mm), including Natalus major, Natalus jamaicensis, and Natalus primus; (2) medium (mean forearm length of 37–39 mm), including the remaining species of Natalus; and (3) small (mean forearm length of 29–34 mm), including Nyctiellus and Chilonatalus. Because of the outlying position of Natalus primus relative to other Natalus with respect to several ecomorphological traits, a distinction is made between N. primus and the remaining species of Natalus, which are hereinafter treated as the “Natalus stramineus group.” Similarly, a distinction is made between Chilonatalus micropus and a Chilonatalus “tumidifrons group” ( =  C. tumidifrons + C. macer).

In figures, tables, and plates, species are abbreviated as follows: Cma, Chilonatalus macer; Cmi, Chilonatalus micropus; Ctu, Chilonatalus tumidifrons; Nes, Natalus espiritosantensis; Nja, Natalus jamaicensis; Nla, Natalus lanatus; Nma, Natalus major; Nme, Natalus mexicanus; Npr, Natalus primus; Ntu, Natalus tumidirostris; and Nst, Natalus stramineus.

Statistical Analyses

I used two-way ANOVAs to detect overall differences among species and populations (geographic subsets within a given species) and between sexes, as well as interaction effects between populations/species and sex. Where interaction effects were not found, one-way MANOVAs (performed over all variables simultaneously) were used to detect sexual differences within species. I also used one-way MANOVAs (performed over all variables simultaneously) to detect differences between two populations of one species within a single sex when only one sex was well represented and sexual differences in that species had been detected with previous ANOVAs. In species where simultaneous one-way MANOVAs were impractical due to unequal distribution of missing measurements, one-way ANOVAs were performed separately for each variable. Post hoc comparisons (Tukey tests for unequal sample sizes) tested for pairwise differences among species or populations. The significance level was set to P  =  0.05 for the Tukey tests and the one-way MANOVAs in which tests were performed simultaneously over the sampling units. The significance level was set to P  =  0.01 for all the two-way ANOVAs and the one-way ANOVAs in which multiple separate tests were performed over the same sampling units. I used canonical analyses to detect differences in body dimensions among species and among geographical samples within each species. All analyses were performed using STATISTICA 5.5 (StatSoft, Inc., 1995).

Type Genus

Natalus Gray, 1838.

Geographic Distribution

New World, from northern Mexico (Sonora and Baja California in the west and Tamaulipas in the east), through Central America (including several adjacent continental and oceanic islands), the West Indies (Greater and Lesser Antilles and the Bahamas), northern South America (northern Colombia, through Venezuela, and the Guianas, plus offshore Caribbean islands), eastern and central Brazil, to southern Brazil (São Paulo), eastern Bolivia and northeastern Paraguay; generally restricted to tropical environments (ranging from semiarid to wet) rich in caves, and below 2500 m (fig. 2; pls. 1–3).

Fig. 2.

Distribution of the family Natalidae. Solid dots indicate collection localities of extant specimens; open dots indicate collection localities of bone remains (e.g., fossils and subfossils) only. The distribution of Natalidae spans the intertropics of the New World, being notably absent from the western Amazon basin, Puerto Rico, and the southern Lesser Antilles. Natalids are more common in the northern Neotropics. Light gray shading shows land above 600 m.

Diagnosis

Natalid organ present in males; funnel-shaped ears lacking a ridge or flap between lateral and ventral regions of pinna; ear ridges vestigial; lachrymal fossa present; long infraorbital canal, extending from P2 to M2; styliform process on rostral margin of ectotympanic; presence of cingular labial cusp on p4; lingual talonid crest of m3 straight; presence of protocone on P4; lack of upper molar ectocingulum; manubrium of sternum expanded laterally into platelike structure; long caudal vertebrae.

Description

Funnel-eared bats range in size from the very small Nyctiellus lepidus (2–3 g, forearm length 26.6–31.0 mm), one of the world's smallest bats, to the medium-sized Natalus primus (6.0–12.6 g, forearm length 46.1–51.2 mm). Funnel-eared bats are characterized by slender bodies, long extremities and tail, and wide wing membranes. The tail is usually longer than the head and body combined, and is entirely enclosed in an extensive, triangular or wedge-shaped uropatagium. The wing membranes are thin and translucent. The plagiopatagium inserts either at the ankle or at the tibia. The calcar is long and in most species extends along most of the free edge of the uropatagium. The body pelage is long, from lax to woolly, and ranges widely in coloration from pale buff to rich chestnut brown. Usually, ventral hairs are monocolored and dorsal hairs are bicolored with darker tips and lighter bases, with the exception of N. lanatus, in which both ventral and dorsal hairs have darker bases and lighter tips. The muzzle is long, slender, and dorsoventrally flattened. Natalids have a relatively simple facial anatomy, lacking, with the exception of the genus Chilonatalus, the dermal folds and excrescences typical of other tropical bat families (pl. 4). The dense pelage along the lateral margins of the upper lips gives these bats the appearance of having thick mustaches. The mustache hairs are curved ventrally and may direct airflow toward the mouth and ear, as has been suggested for the bat family Mormoopidae (Smith, 1972). The nostrils are usually oval shaped, ventrolaterally oriented, and open at the end of a dorsally prominent longitudinal nasal ridge at the margin of the upper lip. The lower lip is thickened and bears paired central pads incised by numerous diagonal grooves with the appearance of primate dermatoglyphs.

Males have a unique organ called the natalid organ on the dorsal surface of the muzzle. This organ is generally visible externally as a swollen mass, which can be as large as half the skull length in the genus Chilonatalus (pl. 5). The natalid organ secretes a translucent greenish, viscous liquid that may function in communication.

The ears are medium to large in size, with the pinna square shaped and expanded laterally to various degrees, in most species having the appearance of a funnel with a pointed apex. The ventral surface of the ears is relatively smooth; the typical ear ridges of bats are extremely reduced in size and restricted to a narrow area near the lateral margin of the distal pinna (pl. 5). The hair follicles on the ventral surface of the ear are relatively conspicuous. There is no cartilaginous ridge or flap between the lateral and ventral regions of the ear pinna. The tragus is small and twisted with a lanceolate tip. The eyes are very small, partly surrounded by the bases of the ears, and are partially hidden by the profuse facial pelage.

The skull is long and delicate, with a long, narrow, and dorsoventrally flattened rostrum (pls. 6–14). The braincase varies from moderately inflated to globular and is usually sharply elevated above the rostrum. The premaxilla is expanded dorsally and caudally to various degrees. The palatal branches of the premaxilla are fused along the ventral midline, leaving two small foramina and a slight rostral emargination. The infraorbital canal extends from P2 to M2, and opens caudally in a depression termed the lachrymal fossa (Morgan and Czaplewski, 2003). The ectotympanic is expanded rostrally into a styliform process. The condyloid and coronoid processes of the mandible are at nearly the same level above the alveolar plane. The angular process is long and has a dorsally or anterodorsally curved tip (pl. 15). The dental formula is 2/3, 1/1, 3/3, 3/3  =  38. There is a small gap between i3 and the lower canine. There is an accessory cusp on the labial cingulum of p4 of various degrees of development. The lingual talonid crest of m3 is straight. A protocone is present in P4 and the mesostyle of the upper molar series is elongated rostrocaudally forming an accessory crest termed a mesostylar crest (Morgan and Czaplewski, 2003; pl. 16).

The humerus is characterized by a distal articular surface displaced laterally relative to the longitudinal axis of the humerus, a broad, triangular-shaped epitrochlea, and tuberosities of similar size (pl. 17). The axial skeleton has various degrees of fusion between its constituting bones. The vertebrae C7 to T1 up to C7 to T6 are fused among them and with the ribs. The vertebrae from last thoracic to antepenultimate or penultimate lumbar are fused into a continuous, laterally compressed column with no evidence of sutures between elements. The sternum is expanded laterally into a platelike structure. The ribs are greatly expanded craniocaudally or fused entirely among them and with the sternum into a rigid thoracic bell-shaped structure (pl. 18). The tail vertebrae are greatly elongated.

Fig. 3.

Dorsal view of the left half of the uropatagium of two natalids: A, Nyctiellus lepidus, showing naked free margin of uropatagium; and B, Chilonatalus macer, showing fringe of hairs on free margin of uropatagium. Scale bar  =  20 mm.

Fig. 4.

Schematic lateral view of the heads of two natalids: A, Chilonatalus micropus, showing dermal outgrowths on the muzzle; and B, Natalus tumidirostris, showing lack of dermal outgrowths on the muzzle.

Fig. 5.

Schematic dorsal view of the heads of three natalids: A, Chilonatalus macer, showing large, elliptical natalid organ and straight lateral and medial margins of ear; B, Chilonatalus micropus, showing small, hemispherical natalid organ, straight medial margin of ear, and concave lateral margin of ear; and C, Natalus tumidirostris, showing wedge-shaped natalid organ and concave medial and lateral margin of ear.

Fig. 6.

Medial view of the feet in two species of Natalus: A, Natalus lanatus, showing ungual tufts; and B, Natalus mexicanus, showing no ungual tufts.

Fig. 7.

Dorsal view of the postorbital region and base of the rostrum in two species of Natalus: A, Natalus jamaicensis, showing parallel sides of postorbital region and concave maxilla; B, Natalus major, showing sides of postorbital region diverging anteriorly and convex maxilla.

Fig. 8.

Ventral view of the posterior palate in two species of Natalus: A–B, Natalus tumidirostris, showing caudal margin of palate (a) always rostral to sphenorbital fissure (b); and C, Natalus espiritosantensis, showing caudal margin of palate caudal to sphenorbital fissure.

Fig. 9.

Ventral view of the rostral end of the skull in two species of Natalus: A, Natalus mexicanus, showing I1 located rostral to I2; and B, Natalus stramineus, showing I1 at level with I2.

SPECIES ACCOUNTS

Genus Nyctiellus Gervais, 1856

Nyctiellus Gervais, 1856: 84.Type species Vespertilio lepidus Gervais, 1837, by monotypy.

Natalus Dobson, 1878: 344. Part, not Natalus Gray, 1838.

Natalus (Nyctiellus): Dalquest, 1950: 443. Name combination.

Diagnosis

Very small size; tibia shorter than half the length of the forearm; calcar occupying less than half the length of the free edge of uropatagium; free margin of uropatagium naked, lacking fringe of hairs; distal third of ear pinna relatively narrow, with seven or more ear ridges; ear tip rounded; funnellike form restricted to lateral and basal portions of ear pinna; free edge of uropatagium lacking fringe of hairs; natalid organ low, rather square shaped (with nearly parallel lateral margins) never reaching forehead; broad, deep rostrum; swollen maxilla; low braincase; slight cranial flexion, anterior portion of zygomatic arches wider (deeper) than twice the height of last molars; slight palatal emargination; basisphenoid pit deep and lacking longitudinal septum; ectotympanic large, covering most of the periotic; I2 inflected medially; reduced first premolars; molars cusps relatively thin and long, talonid broader than trigonid in lower molars; spinous process of humerus much higher than capitulum. A comparison of diagnostic characters between Nyctiellus, and other natalid genera is summarized in table 3.

TABLE 3

Summary of diagnostic characters of four genera of Natalidae

Etymology

From the latinized diminutive of nyx, Greek for “night.”

Contents

N. lepidus (type species) (Gervais, 1837).

Nyctiellus lepidus (Gervais, 1837)

Figure 10

Fig. 10.

Skull and mandible of Nyctiellus lepidus (AMNH 167133, male, Little Exuma, Bahamas). Scale bar  =  10 mm.

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).

Fig. 11.

Geographic distribution of Nyctiellus lepidus (squares), Chilonatalus macer (upright triangles), C. micropus (circles), and C. tumidifrons (upside down triangles). Open symbols indicate localities represented by bone remains only. Names of localities are listed in appendix 1. Gray shading on land indicates relief, with darknes increasing with altitude.

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 rounded 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).

Fig. 12.

Geographic variation of Nyctiellus lepidus. Cuba (N  =  17) includes specimens from La Habana, Isla de la Juventud, and Granma. The Bahamas (N  =  37) include specimens from Cat, Eleuthera, Little Exuma, Long. All specimens are male. Specimens from Cuba have slightly longer forearms but have narrower skulls and smaller rostra (Tukey, P < 0.05). Symbols: black dots, means; vertical gray bars, two standard deviations around the mean; vertical black line, two standard errors around the mean.

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 25°–40° 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 anguliscuta, 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 (−8 min to +11 min) and extends for up to 45 minutes, the second is shorter and ends around sunrise (−8 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 33.5° C to 35.2° 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.

Genus Primonatalus Morgan and Czaplewski, 2003

Primonatalus Morgan and Czaplewski, 2003: 733. Type species Primontalaus prattae Morgan and Czaplewski, 2003 by original designation.

Diagnosis

Small size; distinct mandibular angle present; ventral margin of mandible nearly straight between p4 and mandibular angle; coronoid process slightly higher than condyloid, dorsally to alveolar plane of dentary; rostral margin of ascending ramus of mandible forming angle of about 70° with alveolar plane of dentary; pointed projection on margin of dentary between angular process and condyloid sometimes present; angular process spatulated with prominent medial projection; anterior rim of orbit nearly perpendicular to alveolar plane of maxilla; maxillary branch of zygomatic arch thin, nearly as deep as crown height of M2; p3 with labial cingulum distinctly indented between roots; occlusal outline of P4 with anterior indentation; mesostylar crests of M1 and M2 long and broadly curved (crescent shaped); mesostylar crest present on M3; capitulum of humerus large and bulbous; spinous process short and separated from capitulum by small notch. A comparison of diagnostic characters between Primonatalus, and other natalid genera is summarized in table 3.

Etymology

From primus, Latin for “first,” and natalus, type genus of the family Natalidae. The name indicates that it is the earliest known member of Natalidae.

Contents

P. prattae (type species) Morgan and Czaplewski, 2003.

Primonatalus prattae Morgan and Czaplewski, 2003

Figure 13

Fig. 13.

A, Holotype of Primonatalus prattae, UF 10864, right dentary, image inverted. B, Right: dorsolateral view of right ascendant ramus of mandible with mandibular angle, UF 121145. Left: caudal view of right ascendant ramus of mandible with mandibular angle, UF 121145. C, Reconstruction of the skull and mandible of Primonatalus prattae. Specimens (a) UF 108638; (b) UF 108647 (not shown entirely); (c) UF 108642 (not shown entirely); (d) UF 108641 (holotype; right dentary, image inverted); (e) UF 121145 (not shown entirely; right mandibular angle, image inverted); (f) UF 121136 (right P4, image inverted); (g) UF 121139 (right M3, image inverted). Skull contour is conjectural. Scale bars  =  5 mm.

Holotype

UF 108641, partial right dentary with m1–3, collected by A.E. Pratt in Thomas Farm, 12 km northeast of Bell, Gilchrist County, Florida (maped by Morgan and Czaplewski, 2003). Age of fossil deposit: early Miocene (early Hemingfordian North American land mammal age).

Paratypes

UF 121145, ascending ramus of right dentary (fig. 13); UF 108647, edentulous partial left dentary with symphysis and alveoli for i1–p4; UF 108642, partial left dentary with p3 and alveoli for p2 and p4; UF 121136, right P4; UF108638, partial left maxilla with M1–2; UF 121139, right M3; UF 121141, periotic; UF 108650, distal half of left humerus.

Distribution

Known only from the type locality.

Diagnosis

Same as for genus.

Description

Small size (maximum width of distal humerus 2.8–2.9 mm, N  =  4); distinct mandibular angle present and closer to level of coronoid than to level of condyloid; ventral margin of mandible almost straight between p4 and mandibular angle; coronoid process slightly higher than condyloid above alveolar plane of dentary; rostral margin of ascending ramus of dentary forming angle of about 70° with alveolar plane of dentary; rounded projection on margin of dentary between angular process and condyloid sometimes present; angular process spatulated with prominent medial rounded projection; anterior rim of orbit nearly perpendicular to alveolar plane of maxilla; maxillary branch of zygomatic arc thin, nearly as deep as crown height of M2; maxilla apparently not inflated; i1 and i2 separated from i3 by small gap; occlusal outline of p3 long and constricted at level of cusp; p3 with labial cingulum distinctly indented between roots of tooth; mesostylar crests on M1 and M2 long and broadly curved; mesostylar crest present on M3 and longer along postparacrista; cingular cusp of P4 apparently short and broad; occlusal outline of P4 with anterolingual indentation; molars cusps relatively broad; spinous process of humerus much higher than capitulum; capitulum of humerus large and bulbous; spinous process short and trilobed, separated from capitulum by small notch.

Comparisons

Primonatalus prattae is known from a few fragmentary specimens, many of which are the only specimens known of their type. Therefore, for most characters, the morphological variation within this species cannot be evaluated at present. Nonetheless, the material at hand allows for distinguishing P. prattae unambiguously from other species of Natalidae, using a combination of unique and shared characters.

The only currently known diagnostic character unique to Primonatalus prattae is the apophysis of the angular process, which is characterized by a rounded medial projection that makes it broader than the shaft. In all other natalids, except Nyctiellus lepidus, the apophysis of the angular process is about as wide as the shaft and lacks a medial projection. The angular process of Nyctiellus lepidus is similar to that of P. prattae, but the medial projection in N. lepidus (which is absent in some individuals) is smaller than that of P. prattae and pointed. The lower dentition of P. prattae also differs from that of Nyctiellus. In P. prattae, the labial cingulum of p3 is indented between the roots of the tooth, whereas in Nyctiellus this cingulum is straight. Also, in P. prattae, the lower molar hypoconids diminish progressively in size from m1 to m3, whereas in Nyctiellus all hypoconids are of similar size. Finally, P. prattae differs from Nyctiellus in its broadly curved mesostylar crests of M2 and M3 (nearly straight in Nyctiellus), and its thin base of the zygomatic arch (thicker than 3/2 the height of the last molar in Nyctiellus, in lateral view).

The coronoid process of the holotype of P. prattae is slightly higher than the condyloid process above the alveolar plane of the dentary, a character it shares only with Natalus primus (although this character is polymorphic in the latter). All other species of Natalidae have a coronoid process that is slightly lower than or as high as the condyloid above the alveolar plane of the dentary. On the other hand, P. prattae differs from all species of the genus Natalus in that the base of its dentary bone ventral to molars is nearly straight (markedly curved in the genus Natalus). Also, it is distinguished from most species of Natalus in the presence of a mesostylar crest in M3, a feature absent in most representatives of Natalus (excluding N. primus). Finally, a large, bulbous capitulum and a short, triangular spinous process on the humerus distinguish P. prattae from the genera Chilonatalus and Nyctiellus, which have a smaller, somewhat cylindrical capitulum and a long and hooked spinous process. The size of the humerus, however, is most similar to that of the genus Chilonatalus (table 10).

Note

The characters that associate P. prattae with each of the three extant genera of Natalidae are all seen on separate specimens. The angular process is most similar to that of Nyctiellus, the dentary and lower and upper dentition are most similar to those of Chilonatalus, and the distal humerus is most similar to that of Natalus. This opens the question of whether Primonatalus is a chimera. The evidence, however, suggests otherwise. All natalid fossils from Thomas Farm were recovered from a single 3 m thick section of sediments of uniform taphonomy, indicating a similar age and origin of the fossils. Also, the size relationship among all Primonatalus specimens is similar to that among corresponding anatomical elements of extant natalid genera. Assuming similar body proportions between the Thomas Farm natalid fossils and extant natalids, it is reasonable to hypothesize that all fossils assigned to Primonatalus belong to a single taxon.

Genus Chilonatalus Miller, 1898

Natalus: Dobson, 1880: 443. Part, not Natalus Gray, 1838.

Natalus (Chilonatalus) Miller, 1898: 326. Type species Natalus micropus Dobson, 1880 by original designation.

Chilonatalus: Miller, 1903: 119. First use as a genus.

Diagnosis

Dermal outgrowths on dorsum of rostrum and on chin, producing in profile a double-lipped aspect; ears large, without ear ridges; mustached formed by parallel hairs forming a compact row; plagiopatagium attaching at midtibia; rostrum long and slender, braincase globular and delicate, mandibular symphysis with long posteroventral projection; shaft of angular process long, slender, dorsally curved with a markedly hooked tip; labial cingular cusp of p4 long and pointed; ribs fused into a rigid thoracic bell. A comparison of diagnostic characters between Chilonatalus, and other natalid genera is summarized in table 3.

Etymology

combination of the names of the genera Natalus and Chilonycteris ( =  Pteronotus), given by Miller (1898) in reference to the Pteronotus-like dermal outgrowths on the muzzle of this genus.

Contents

C. macer Miller, 1914; C. micropus (type species) Dobson, 1880; C. tumidifrons Miller, 1906.

Chilonatalus macer Miller, 1914

Figure 14

Fig. 14.

Holotype of Chilonatalus macer (USNM 113724, female, Baracoa, Cuba). Scale bar  =  5 mm.

Chilonatalus micropus: Miller, 1904: 340. Not Natalus (Chilonatalus) micropus Miller, 1898.

Chilonatalus macer Miller, 1914: 225. Type locality Baracoa, Guantánamo, Cuba.

Natalus (Chilonatalus) macer: Dalquest, 1950: 443. New combination.

Natalus micropus macer: Viña Bayés and Deas Díaz, 1970: 7. New combination.

Holotype

USNM 113724, adult female, skin in alcohol with skull removed, collected by W. Palmer on 6 February 1902, “in a cave” (identified by Silva-Taboada, 1979, as Cueva de la Majana), Baracoa, Cuba. The skin has the tail membrane and both hind legs disconnected from the body. The skull is complete but has been apparently slightly compressed transversally, so that the zygomatic arches are asymmetrically buckled.

Distribution

Cuba, Isle of Pines, Grand Cayman (fossil only); fig. 11.

Diagnosis

Forearm short (32.1–33.8 mm); tibia long (18.2–20.25 mm); penis short (1.5–1.9 mm); natalid organ long (2.35–7.7 mm); greatest skull length (13.8–14.5 mm); least postorbital breadth relatively narrow; lateral margin of ear straight; attachment of wing to tibia on the proximal half of the tibia (at about 1/3 of its length, measured from the knee); in lateral view, braincase uninflated and rising from rostrum as a gently curving slope dorsal to orbit; ridge between basisphenoid furrows wide; caudal margin of ascending ramus of mandible forming a straight angle with alveolar plane of dentary; lateral sides of basisphenoid pits nearly parallel; p2 not crowded; fusion between original elements of thoracic cage seamless ventrally. A comparison of diagnostic characters between C. macer, and other species of Chilonatalus is summarized in table 4.

TABLE 4

Diagnostic characters of species of the genus Chilonatalus

Description

Small size (forearm length 32.1–33.8 mm; greatest skull length 14.2–14.9 mm; weight 2–4 g); muzzle long and dorsoventrally flattened; nostrils elliptical, opening ventrolaterally at the end of tubelike projections on margin of upper lip; upper lip slightly thickened; lower lip markedly thickened and constricted in dorsal and ventral margin, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; high dermal tubercle on dorsum of rostrum caudal to nostrils; tubercles of ramal vibrissae coalesced into transversal ridge ventral to lower lip; natalid organ very large (up to 1/2 of greatest length of skull), elliptical, and reaching crown of head; ears relatively long (12.7–16.4 mm); ear pinna very wide and funnel shaped; pinna with moderately pointed tip; lateral and medial margins of pinna straight; three very small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus markedly short, lanceolate, and twisted into helixlike structure; tibia (18.2–20.3 mm) longer than half the length of the forearm; calcar very long and thin, occupying about 2/3 of the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively long and wide, with 3rd metacarpal (30.3–32.4 mm) longer than 5th metacarpal (27.9–30.5 mm); wings attach to tibia at proximal third of distance between knee and ankle; pelage dense and lax; hairs long (5–8 mm, dorsally; 3–7 mm, ventrally); pelage color from light brown to orange brown, lighter dorsally; hairs bicolored, with tips darker than bases; dense mustachelike hair tufts along lateral margins of upper lip; mustache formed by dense, tough, parallel, and ventrally curved hairs; natalid organ nearly naked; skull long and narrow with moderate rostral flexion; rostrum long and narrow, with marked sulcus between nasals; moderate palatal emargination; maxilla convex dorsal to molars; braincase greatly inflated, rising gently from rostrum; sagittal crest moderately developed; postorbital constriction relatively wide (42%–44% of zygomatic breadth); maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids convergent; palate extending caudally to half the length of pterygoids; basisphenoid pit deep and steep sided; longitudinal medial ridge on basisphenoid present; ectotympanic large, covering about half of the periotic; upper incisors long and pointed; occlusal profile of premolars long; upper premolars of similar size and not crowded; mesostylar crests on M1 and M2 long and broadly curved, mesostylar crest present on M3; cingular cusp of p4 long and pointed; molars cusps relatively broad; spinous process of humerus much higher than capitulum; thorax relatively short and wide; all ribs fused among each other and with sternum forming a single bell-shaped structure; vertebrae C7 to T7 fused among themselves and to ribs; vertebrae T11–L5 fused entirely without vestige of sutures; vertebrae L6 free; caudal vertebrae 4–7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

Chilonatalus macer is easily distinguishable from species of the genus Natalus and from Nyctiellus lepidus by generic-level diagnostic characters: presence of dermal outgrowths on dorsum of rostrum and on chin, producing a double-lipped aspect; presence of three ear ridges; mandibular symphysis with long posteroventral projection; shaft of angular process curved dorsally and with a markedly hooked tip; and labial cingular cusp of p4 long and pointed. In the genera Natalus and Nyctiellus, the face lacks dermal outgrows, the ear shows ridges in various numbers, the mandibular symphysis shows a short (or absent) posteroventral projection, the mandibular angle may be pointed (Nyctiellus) or blunt (Natalus); and the labial cingular cusp of p4 is short or very little developed.

From the other two species of Chilonatalus, C. macer can be separated using a combination of external and cranial characters. Externally, Chilonatalus macer differs from C. micropus in its straight lateral margin of the ear, the attachment of the wing on the proximal half of the tibia, a short penis (1.5–1.9 mm), a long tibia (18.2–20.25 mm), and a large, elliptical natalid organ (length of natalid organ 2.35–7.7 mm). Chilonatalus micropus, in contrast, is characterized by a concave lateral ear margin, a wing attaching to the tibia on its distal half, a long penis (3.6–6.5 mm), a short tibia (14.7–17.95 mm), and a small, hemispherical natalid organ (length of natalid organ 3.3–3.7 mm). Cranially, C. macer and C. micropus can be separated by the dorsal flexion point of the skull (with a well-defined angle in C. micropus and a gently curving slope in C. macer), the angle formed by the caudal margin of the ascending ramus of mandible with the alveolar plane of the dentary (straight in C. macer and about 70° in C. micropus), the lateral sides of the basisphenoid pits (nearly parallel in C. macer and widely diverging caudally in C. micropus), and by the fusion of the ribs with sternum (seamless in C. macer and retaining sutures in C. micropus).

Chilonatalus macer does not differ appreciably from Chilonatalus tumidifrons in external characters. The easiest way to separate both species is by skull size (greatest skull length 13.8–14.5 mm in C. macer and 15.15–15.95 mm in C. tumidifrons. Also, the two species differ in the relative width of the postorbital constriction (42%–44% of zygomatic breadth in C. macer and 38%–41% in C. tumidifrons), in the degree of crowding of P2 (not crowded in C. macer and crowded in C. tumidifrons), and in the relative width of the ridge between basioccipital furrows (narrow in C. macer and wide in C. tumidifrons).

Variation

In a sample of 12 males and 18 females the only measurement that showed sexual dimorphism in size was the length of the humerus (Silva-Taboada, 1974). The species shows no geographic variation between western and eastern Cuba or between Cuba and the Isle of Pines.

Natural History and Conservation

Chilonatalus macer is known from 33 localities (including two represented by bone remains only), of which 22 are day roosts, and 19 are caves. On three occasions it has been found roosting solitarily in highly unusual conditions: (1) inside a house for drying tobacco; (2) inside a camping tent, and (3) on a sugarcane sappling. These occurrences suggest that occasionally some individuals are unable to return to their permanent roosts before sunrise.

Chilonatalus macer roosts in warm and humid caves (six of these have been hot caves) but it has also been found solitarily in cooler and drier caves. These bats generally form groups of 30–50 individuals in protected areas of low ceilings, keeping a wide distance between individuals, which usually hang from a single foot. This species has been found coexisting in the same caves with 13 other bat species (Artibeus jamaicensis, Brachyphylla nana, Eptesicus fuscus, Erophylla sezekorni, Macrotus waterhousii, Mormoops blainvillei, Monophyllus redmani, Natalus primus, Nyctiellus lepidus, Phyllonycteris poeyi, Pteronotus macleayi, Pteronotus parnellii, and Pteronotus quadridens), but usually roosts separated from them (Silva-Taboada, 1979). Nonetheless, C. macer has been found in close association with other species on two occasions: (1) apparently solitarily, within a colony of Pteronotus quadridens (Cueva del los Majáes, Tejedor et al., 2005a); and (2) in a small group contiguous with a large colony of Nyctiellus lepidus (Cueva del Calabazar, Tejedor et al., 2005a).

Chilonatalus macer is commonly found in mesic habitats having up to 2521 mm of annual precipitation (Baracoa, Cuba; locality 152), but is occasionally found in xeric environments (e.g., Cueva de los Masones, locality 154; annual precipitation of 834 mm). It has been found from sea level up to 230 m (Cueva del Indio; locality 106).

Very little is known of the food habits of C. macer. In Cuba it has been found to feed mostly on moths (Lepidoptera) and occasionally on spiders. It can carry in its stomach up to 28.6% of its body weight (Silva-Taboada, 1979).

The reproductive pattern of C. macer is largely unknown. Two pregnant females found in May carried embryos measuring 10 mm in crown-rump length. Of two females taken in August, one was lactating and another postlactating. Reproductively inactive females have been found in January, March, and December (Silva-Taboada, 1979). In May, in Cueva La Barca, Pinar del Rio, Cuba, sexes have been found forming separate groups, with females roosting deep in a hot area of the cave and males occupying a cooler area near a small entrance, suggesting a pattern of sexual segregation similar to that of N. lepidus.

Chilonatalus macer is represented by at least 123 specimens in museum collections, most of which were collected at Cueva No. 2 Punta del Este, and Cueva del Promontorio, both in Isla de la Juventud, Cuba. Colonies are relatively small, containing from a few dozen to a few hundred bats.

Natural predators are not known. Chilonatalus macer is parasitized by the streblid Trichobius frequens (Silva-Taboada, 1979).

The foraging exodus of C. macer has been recorded to begin 14 min after sunset and to last for over 30 min. Individuals returning to their roosts have been taken late at night (23:00 hr) indicating that these bats were active for long periods throughout the night (Silva-Taboada, 1979). This species has an amazingly maneuverable flight. It is able to fly without hovering within reduced spaces (0.125 m³) and is easily distinguishable inside caves by its rather rectilinear flight path and its very slow and shallow wing beat. Such slow, maneuverable flight, coupled with a small size, may enable this bat to forage in denser vegetation than most other Neotropical bats. It dehydrates and dies very rapidly if taken out of their caves during daytime.

It is is listed in IUCN's Red List of Threatened Species (IUCN, 2010) as near threatened under Chilonatalus micropus. With the recognition of this taxon as a Cuban endemic different from Chilonatalus micropus, the study of its population status merits attention to accurately evaluate its conservation needs. Given its habit of aggregating in relatively small numbers in isolated and sparsely distributed colonies, its future IUCN category may increase in threat level.

Chilonatalus micropus (Dobson, 1880)

Figure 15

Fig. 15.

Holotype of Chilonatalus micropus (BMNH 80.12.14.1, “environs of Kingston,” Jamaica). Scale bar  =  5 mm.

Natalus micropus Dobson, 1880: 443. Type locality “Environs of Kingston, Jamaica.”

Natalus (Chilonatalus) brevimanus: Miller, 1898: 328. Type locality “Old Providence island, Caribbean Sea,” Colombia.

Chilonatalus micropus: Miller, 1907: 185. New combination.

Chilonatalus brevimanus: Miller, 1907: 185. New combination.

Natalus micropus brevimanus: Varona, 1974: 31. New combination.

Natalus micropus micropus: Varona, 1974: 32. Name combination.

Holotype

Holotype by monotypy, BMNH 80.12.14.1 collected in the “Environs of Kingston, Jamaica.” Skull in good condition.

Distribution

Hispaniola (Dominican Republic), Jamaica, San Andrés and Providencia islands (Colombia); fig. 11.

Diagnosis

Forearm long (30.7–35.1 mm); tibia relatively short (14.7–17.95 mm); penis long (3.6–6.5 mm), natalid organ hemispherical and small (3.3–3.7 mm); least postorbital breadth relatively wide; lateral margin of ear deeply notched; wing attaches at the distal half of tibia (at about 2/3 of its length, measured from the knee); dorsal point of flexion between rostrum and braincase forming a well-defined angle dorsal to orbit; braincase globular and rising abruptly from rostrum; ridge between basisphenoid furrows wide, caudal margin of ascending ramus of mandible forming an angle smaller than 70° with alveolar plane of dentary; p2 not crowded; fusion between original elements of thoracic cage complete but with visible suture lines. A comparison of diagnostic characters between C. micropus, and other species of Chilonatalus is summarized in table 4.

Description

Small size (forearm length 30.7–35.1 mm; greatest skull length 13.5–14.7 mm; weight 2.6 g); muzzle long and dorsoventrally flattened; nostrils elliptical, opening ventrolaterally at the end of short, tubelike projections on margin of upper lip; upper lip slightly thickened; lower lip markedly thickened and constricted in dorsal and ventral margin, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; low dermal tubercle on dorsum of rostrum caudal to nostrils; tubercles of ramal vibrissae coalesced into transversal ridge ventral to lower lip; natalid organ small and hemispherical, located at intersection between rostrum and braincase; ears relatively long (13.0–16.4 mm); ear pinna very wide and funnel shaped; pinna with moderately pointed tip; medial margin of pinna straight; lateral margin of pinna concave; three very small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus markedly short, lanceolate, and twisted into helixlike structure; tibia (14.7–17.9 mm) slightly shorter than half the length of the forearm; calcar very long and thin, occupying about 2/3 of the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively long and wide, with 3rd metacarpal (25.5–33.5 mm) longer than 5th metacarpal (23.7–30.2 mm); wings attach to tibia at about 2/3 the distance from knee to ankle; pelage dense and lax; hairs long (4–7 mm, dorsally; 3–6 mm, ventrally); pelage color from light grayish brown to yellowish or reddish brown, lighter dorsally; hairs bicolored, with tips darker than bases; dense mustachelike hair tufts along lateral margins of upper lip; mustache formed by dense, tough, parallel, and ventrally curved hairs; natalid organ nearly naked; skull long and narrow with moderate rostral flexion; rostrum long and narrow, with marked sulcus between nasals; moderate palatal emargination; maxilla concave dorsal to molars; braincase extremely inflated (globular), rising abruptly from rostrum; sagittal crest poorly developed; postorbital constriction relatively wide (41%–45% of zygomatic breadth); maxillary branch of zygomatic arch thin, as deep as the height of crowns of last molars; pterygoids convergent; palate extending caudally to half the length of pterygoids; basisphenoid pit deep and steep sided; longitudinal medial ridge on basisphenoid present; ectotympanic medium sized, covering about half of the periotic; upper incisors long and pointed; I1 similar in length to I2; occlusal profile of premolars long; upper premolars of similar size and not crowded; mesostylar crests on M1 and M2 long and broadly curved, mesostylar crest present on M3; cingular cusp of p4 long and pointed; molar cusps relatively broad; spinous process of humerus much higher than capitulum; thorax relatively short and wide; all ribs fused among each other and with sternum forming a single bell-shaped structure with sutures remaining among original elements; vertebrae C7 to T3 fused among themselves and to ribs; vertebrae T11–L5 fused entirely without vestige of sutures; vertebrae L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

From species of the genera Natalus and Nyctiellus, Chilonatalus micropus can be distinguished on the basis of generic characters (see comparisons under account of Chilonatalus macer). From other species of Chilonatalus (i.e., C. tumidifrons and C. macer), C. micropus can be distinguished by several external and osteological characters. Externally, in C. micropus, the distal fourth of the ear is narrower than in the remaining species of Chilonatalus, leaving a concavity in the lateral margin of the pinna, which is absent in C. macer and C. tumidirostris. Also, the dermal tubercle above the nostrils is relatively low in C. micropus, whereas it is high and prominent in C. tumidifrons and C. macer. In C. micropus, the plagiopatagium attaches to the distal half of the tibia whereas in the other two species of Chilonatalus it attaches to the proximal half of the tibia. In addition, males of C. micropus have a relatively long penis (3.6–6.7 mm) and a small, hemispherical natalid organ, whereas males of C. tumidifrons and C. macer have a relatively short penis (penis length less than 2.5 mm) and a very large, elliptical natalid organ that in full development extends from the rostral tubercle to the crown.

Cranially, C. micropus is characterized by a globular braincase, which rises in a sharp angle from the rostrum. In C. macer and C. tumidifrons the braincase is relatively not as greatly inflated and rises from the rostrum in a gentler, sloping curve. Also, in C. micropus the caudal margin of the ascending ramus of the mandible is more concave and the shaft of the mandibular angle is thinner. In C. tumidifrons and C. macer the dorsal margin of the mandibular angle is deeper, rendering the caudal margin of the ascending ramus of the dentary less concave than in C. micropus.

In addition to the discrete characters mentioned above, C. micropus can be distinguished from C. tumidifrons on the basis of skull size alone (greatest skull length 13.5–14.7 mm in C. micropus and 15.15–15.95 mm in C. tumidifrons).

Variation

In C. micropus, females are larger than males in length of the forearm and 3rd and 5th metacarpals (Tukey, P < 0.05; table 8). Ottenwalder and Genoways (1982) showed that males are larger than females in depth of braincase and braincase breadth (the latter only true for Jamaican populations).

The inflation of the braincase decreases westward, with animals from Hispaniola having the most globular braincase within both the species and the family Natalidae (mean braincase breadth also follows this trend yet the differences were not statistically significant; P > 0.01; fig. 16). The depth of the rostrum, on the other hand, appears to decrease eastward with animals from Hispaniola having the most dorsoventrally flattened and slender rostra. Individuals from Jamaica were the largest in most external dimensions, with the exception of ear length (P < 0.01; fig. 16). In a larger sample, Ottenwalder and Genoways (1982) found the specimens from Old Providence to be the smallest (on average) in greatest skull length, breadth of braincase (males only) and maxillary tooth row (males only).

Fig. 16.

Geographic variation of Chilonatalus micropus. SAP: San Andrés and Providencia islands, Colombia (12 females, 24 males); Jam: Jamaica (19 females, 29 males); Hisp: Hispaniola (2 females, 4 males). Mean braincase breadth of the sample from Hispaniola was larger but the difference was not statistically significant. The sample from Jamaica was larger in most external dimensions (Tukey, P < 0.05), most notably in length of 5th metacarpal, length of penis, and length of natalid organ. Symbols: black dots, means; vertical gray bars, two standard deviations around the mean; vertical black line, two standard errors around the mean.

Natural History and Conservation

Species known from 21 localities of which eight have been day roosts, all of them caves. All caves known to harbor C. micropus are warm and humid, and at least five of these (Windsor, Oxford, Monarva, Los Patos, St. Clair) are medium-sized to large caves with hot sections (Fincham, 1997). In St. Clair cave, C. micropus was found in the warmest areas, where the air was saturated with water vapor and had high concentrations of hydrogen sulfide (Goodwin, 1970). It seems to favor protected areas inside caves such as high recesses (Osburn, 1865), wall chambers (Goodwin, 1970), or the underside of low ledges (Kerridge and Baker 1978), where it has been found roosting in loose clusters. Genoways et al. (2005), however, observed C. micropus roosting out in the main passageway of St. Clair Cave. It coexists in caves with nine other bats species (Artibeus jamaicensis, Erophylla sezekorni, Monophyllus redmani, Mormoops blainvillei, Natalus jamaicensis, Phyllonycteris aphylla, Pteronotus macleayi, Pteronotus parnellii, and Pteronotus quadridens). Osburn (1865; fide Genoways et al., 2005) observed C. micropus roosting separately from other species, but Goodwin (1970) found it in a mixed colony with Natalus jamaicensis, although he assumed the two species were segregated within the colony. When disturbed within caves, it retreats, flying near walls at about 1 m above the floor (Kerridge and Baker, 1978).

Chilonatalus micropus occurs most commonly in mesic environments receiving up to 2899 mm in annual precipitation (Port Antonio, Jamaica; locality 247), from sea level to 400 m in elevation (Mahogany Hall Cave, Jamaica; locality 244). Its food habits are unknown, but as for other representatives of Natalidae, C. micropus is most certainly insectivorous. The reproductive pattern is also little known. Samples of females taken in mid-July have contained 2.6% (Genoways et al., 2005) to 90% (Kerridge and Baker, 1978) lactating individuals. Fourteen females taken on 29 July seemed to be reproductively inactive (Genoways et al., 2005), suggesting that lactation may end during this month in Jamaica.

Chilonatalus micropus is represented by 335 museum specimens, with the largest samples having been taken in St. Clair cave (Jamaica), Cueva los Patos (Dominican Republic), and Old Providence Island. It is moderately gregarious at roosts, forming groups from 10–20 (Genoways et al., 2005) to several hundred individuals (Goodwin, 1970, Kerridge and Baker, 1978).

Nothing has been published on the activity patterns of C. micropus. In the Dominican Republic, one individual was netted at 20:00 hr apparently coming out of the upper entrance of Cueva los Patos, Barahona, 1.5 hours after the end of the exodus of six other bat species. A second individual was netted at 23:00, flying over a creek in Arroyo Chico, Samaná, Dominican Republic, indicating that the species is active until late at night.

Chilonatalus micropus flies very slowly and does not entangle in mistnets when caught in them. In an ecomorphological study, Obrist et al. (1993) predicted, based on dimensions of the ear pinna, that the echolocation calls of C. micropus probably consist of two harmonics in the 40–80 kHz range.

Chilonatalus micropus is listed in IUCN's Red List of Endangered Species (IUCN, 2010) as near threatened, but this classification included the Cuban C. macer, which seems to be a more common species. Yu and Dobson (2000) considered it “very rare,” yet their conclusion was based on distribution and population data from Kerridge and Baker (1978), which stated that it was restricted to Jamaica. Chilonatalus micropus nonetheless appears to be more vulnerable than its current IUCN status indicates. The geographic range of this species is fragmented across four islands, two of which (San Andrés and Providencia) are very small, isolated, and with dense human populations. The only large population C. micropus in Jamaica is known from St. Clair Cave, where a resident population of feral cats is reported to feed on the cave's bats (McFarlane, 1986). On Hispaniola, where farmers traditionally engage in large-scale extraction of bat guano from caves, the only known roost site is Cueva Los Patos No. 2, a cave in the immediate vicinity of a small town. With such a limited known distribution and potential threats, the population status of this species warrants investigation to accurately assess its conservation needs.

Chilonatalus tumidifrons Miller, 1903

Figure 17

Fig. 17.

Holotype of Chilonatalus tumidifrons (USNM 122024, male, San Salvador, the Bahamas). Scale bar  =  5 mm.

Chilonatalus tumidifrons Miller, 1903. Type locality “Watling Island” [ =  San Salvador Island], Bahamas.

Natalus (Chilonatalus) tumidifrons: Dalquest, 1950: 443. New combination.

Natalus micropus tumidifrons: Varona, 1974: 32. New combination.

Natalus tumidifrons: Ottenwalder and Genoways, 1982: 32. New combination.

Holotype

USNM 122024, adult male, skin in alcohol with skull removed, collected by J.H. Riley on 12 July 1903 in a cave near Sandy Point (locality 524 in appendix 1), San Salvador Island, the Bahamas. Skin and skull in good condition.

Distribution

The Bahamas (Abaco, Andros, and San Salvador; also, as a fossil, in New Providence, Cat and Great Exuma); fig. 11.

Diagnosis

Forearm short (31.7–36.0 mm) relative to skull length; length of tibia (17.8–20.05 mm); penis short (1.1–2.25 mm); natalid organ long (3.6–7.25 mm); skull long (15.15–15.95 mm) relative to forearm length; least postorbital breadth relatively narrow; lateral margin of ear straight; attachment of wing to tibia on the proximal half of the tibia (at about 1/3 of its length, measured from the knee); in lateral view, braincase rises from rostrum as a softly curving slope dorsal to orbit; ridge between basisphenoid furrows wide; caudal margin of ascending ramus of mandible forming a straight angle with alveolar plane of dentary; lateral sides of basisphenoid pits nearly parallel; p2 crowded; seamless fusion of ribs to sternum. A comparison of diagnostic characters between C. tumidifrons, and other species of Chilonatalus is summarized in table 4.

Description

Small size (forearm length 31.7–36.0 mm; greatest skull length 15.0–16.0 mm; weight 3–3.5 g); muzzle long and dorsoventrally flattened; nostrils elliptical, opening ventrolaterally at the end of tubelike projections on margin of upper lip; upper lip slightly thickened; lower lip markedly thickened and constricted on dorsal and ventral margin, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; high dermal tubercle on dorsum of rostrum caudal to nostrils; tubercles of ramal vibrissae coalesced into transversal ridge ventral to lower lip; natalid organ very large (up to 1/2 of greatest length of skull), spindle shaped, reaching crown of head; ears relatively long (14.7–17.2 mm); ear pinna very wide and funnel shaped; pinna with moderately pointed tip; lateral and medial margins of pinna straight; three very small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus markedly short, lanceolate, and twisted into helixlike structure; tibia (17.8–20.1 mm) longer than half the length of the forearm; calcar very long and thin, occupying about 2/3 of the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively long and wide, with 3rd metacarpal (30.3–32.4 mm) longer than 5th metacarpal (27.9–30.5 mm); wings attach to tibia at proximal third of distance between knee and ankle; pelage dense and lax; hairs long (5–9 mm, dorsally; 4–7 mm, ventrally); pelage color from light brown to orange brown, lighter dorsally; hairs bicolored, with tips darker than bases; dense mustachelike hair tufts along lateral margins of upper lip; mustache formed by dense, tough, parallel, and ventrally curved hairs; natalid organ nearly naked; skull long and narrow with moderate rostral flexion; rostrum long and narrow, with marked sulcus between nasals; moderate palatal emargination; maxilla convex dorsal to molars; braincase greatly inflated, rising gently from rostrum; sagittal crest moderately developed; postorbital constriction relatively narrow (38%–41% of zygomatic breadth); maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids convergent; palate extending caudally to half the length of pterygoids; basisphenoid pit deep and steep sided; longitudinal medial ridge on basisphenoid present; ectotympanic large, covering about half of the periotic; upper incisors long and pointed; occlusal profile of premolars long; upper premolars of similar size and crowded; mesostylar crests on M1 and M2 long and broadly curved, mesostylar crest present on M3; cingular cusp of p4 long and pointed; molars cusps relatively broad; spinous process of humerus much higher than capitulum; thorax relatively short and wide; all ribs fused together and with sternum forming a single bell-shaped structure; vertebrae C7 to T7 fused together and to ribs; vertebrae T11–L5 fused entirely without vestige of sutures; vertebrae L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

From species of the genera Natalus and Nyctiellus, Chilonatalus tumidifrons can be distinguished on the basis of generic level characters (for generic-level comparison between Chilonatalus and Natalus and Nyctiellus see account of C. macer). From Chilonatalus micropus, and Chilonatalus macer, C. tumidifrons can be distinguished using a combination of external and internal characters.

Externally, Chilonatalus tumidifrons differs from C. micropus in its straight lateral margin of the ear, the attachment of the wing on the proximal half of the tibia, a short penis (1.1–2.25 mm), a long tibia (17.8–20.05 mm), and a large, elliptical natalid organ (length of natalid organ 3.6–8.5 mm). Chilonatalus micropus, in contrast, is characterized by a deeply notched (concave) lateral ear margin, a wing attaching to the tibia on its distal half, a long penis (3.6–6.5 mm), a short tibia (14.7–17.95), and a small, hemispherical natalid organ (length of natalid organ 3.3–3.7). Cranially, C. tumidifrons and C. micropus can be separated by the dorsal flexion point of the skull (with a well-defined angle in C. micropus and a gently curving slope in C. tumidifrons), the angle formed by the caudal margin of the ascending ramus of mandible with the alveolar plane of the dentary (straight in C. tumidifrons and about 70° in C. micropus), the lateral sides of the basisphenoid pits (nearly parallel in C. tumidifrons and caudally divergent in C. micropus), and by the fusion of the ribs with sternum (without vestige of sutures in C. tumidifrons and retaining sutures in C. micropus).

Chilonatalus tumidifrons does not differ appreciably from Chilonatalus macer in external characters. The skull of Chilonatalus tumidifrons (greatest skull length 15.15–15.95 mm), however, is absolutely and proportionately (relative to forearm length) larger than that of C. macer (13.8–14.7 mm). Also, the two species differ in the relative width of the postorbital constriction (38%–41% of zygomatic breadth in C. tumidirostris and 42%–44% in C. macer), in the degree of crowding of P2 (crowded in C. tumidifrons and not crowded in C. macer), and in the relative width of the ridge between basicranial furrows (narrow in C. tumidifrons and wide in C. macer).

Variation

No significant sexual variation has been detected in the samples available of C. tumidifrons (Ottenwalder and Genoways, 1982). Specimens from Abaco had significantly deeper braincases (on average) than those from San Salvador (P < 0.001; fig. 18).

Fig. 18.

Morphometric variation among two island populations of Chilonatalus tumidifrons. Islands: Aba  =  Abaco (1 female, 19 males); Sal  =  San Salvador (12 females, 20 males). On average, males from Abaco had significantly deeper braincases than males from San Salvador (Tukey, P < 0.05). Symbols: black dots, means; vertical gray bars, two standard deviations around the mean; vertical black line, two standard errors around the mean.

Natural History and Conservation

Chilonatalus tumidifrons is known from 20 localities (including 8 represented by bone remains only) of which eight are caves, this species' only known roost type. It has been found in caves both large and small where it often roosts above water, but also in drier areas. Individuals hang regularly spaced, and generally from a single foot (Miller, 1905). It has been found in caves with two other bat species (Erophylla sezekorni and Macrotus waterhousii; Andersen, 1994; Hall et al., 1998). When found sharing caves with Erophylla, C. tumidifrons occupies low areas often under shelves or ledges (Hall et al., 1998). Roost-site temperatures at one cave (locality 520) ranged from 22.8° to 24.2° C and in a second cave (locality 522) from 23.6 to 23.9° C. Roosting groups have been observed to switch roosting caves set on average 1 km apart, apparently on a daily basis. A colony of about 300 individuals in Abaco was observed to have abandoned a cave entirely, coinciding with the occupation of that cave by 100–200 Erophylla (Allen, 1905).

Chilonatalus tumidifrons is associated with deciduous forest habitats of moderate precipitation (1021–1288 mm annual precipitation) and occurs near sea level throughout its range. It is presumably insectivorous, but nothing has been published on the diet of this species.

Chilonatalus tumidifrons is known from at least 123 museum specimens. It has been found in groups ranging from less than 10 to over 500 individuals. The population of San Salvador Island could be relatively large given the high abundance of small, unsurveyed caves on the island that may potentially harbor colonies of this species (Hall et al., 1998). In Andros, C. tumidifrons is known from a single cave (Bat Cave) and although only four individuals were taken there, many individuals were observed to swarm out of the cave during a feeding exodus (Andersen, 1994). Chilonatalus tumidifrons has no known predators and reportedly is parasitized by the streblid Trichobious wenzeli (Hall et al., 1998).

The reproduction biology of C. tumidifrons is not known. Colonies apparently formed exclusively by males have been found in July (Allen, 1905), suggesting the sexual segregation pattern that occurs during the period of lactation in other species of the genus. Males have an extremely short penis (1.0–2.3 mm) relative to other natalids, but the possible implications of this trait in the reproduction and mating system of the species is unknown.

Foraging activity begins around sunset. At Crescent Top Cave (locality 520) emergence has been recorded to extend from 17:33 to 18:05 (January 1996) and from 17:44 to 18:10 (January 1997; Hall et al., 1998). Judging from its limb morphology, the flight of C. tumidifrons must be very slow, having been compared to that of a large moth (Miller, 1905).

Chilonatalus tumidifrons is listed as vulnerable in the IUCN's Red List of Threatened Species (IUCN, 2010). The extremely reduced range of this species, fragmented across three islands, is of concern. On Abaco and Andros this species is known from only two caves in each case. It seems most abundant in San Salvador, but further survey work is needed on that island to estimate its population size and conservation status (Hall et al., 1998).

Genus Natalus Gray, 1838

Natalus Gray, 1838: 496. Type species Natalus stramineus Gray, 1838, by monotypy.

Phodotes Miller, 1906: 85. Type species Natalus tuminidirostris Miller, 1900, by original designation.

Diagnosis

Natalid organ wedge shaped and extending onto crown; plagiopatagium attaching above ankle, calcar extending throughout most of free edge of uropatagium; well-developed fringe of hairs along free edge of uropatagium; sagittal crest moderately high and most pronounced in its anterior half; angular process curved anterodorsally; apophysis of angular process rounded or quadrate; ventral margin of dentary curved ventral to molars; labial cingular cusp of p4 well developed but short; lesser trochanter in proximal view (aligning greater trochanter with shaft of femur) projects beyond head of femur away from axis of greater trochanter; larger axis of head of humerus oriented posteroventrally; lesser tuberosity almost as high as greater tuberosity and higher than head of humerus; head of humerus much larger than greater tuberosity; spinous process of humerus smaller than one half the radius of capitulum; capitulum swollen and wide at its midpoint;. A comparison of diagnostic characters between Natalus, and other natalid genera is summarized in table 3.

Etymology

Gray (1838) did not give reasons for choosing the name Natalus (derived from Latin natalis, “of or relating to birth”), but Goodwin (1959) speculated that it was related to the unknown origin or “birthplace” of the taxon. Other authors have suggested that it derives from the neotenic aspect of the bat, as in the newborn (e.g., Gómez-Laverde, 1986).

Contents

Natalus espiritosantensis (Ruschi), 1951; N. jamaicensis (Goodwin), 1959; N. major Miller, 1902; N. mexicanus Miller, 1902; N. lanatus Tejedor, 2005; N. primus Anthony, 1919; N. stramineus Gray, 1838; N. tumidirostris Miller, 1900.

Natalus espiritosantensis (Ruschi, 1951)

Figure 19

Fig. 19.

Holotype of Natalus espiritosantensis (MBML 1801, male, Espirito Santo Brazil). Scale bar  =  10 mm.

Natalus stramineus: Winge, 1893: 36. Not Natalus stramineus Gray, 1838.

Myotis espiritosantensis Ruschi, 1951: 7. Type locality “Gruta do Rio Itaúnas, no municipio de Conceição da Barra, no E.E. Santo,” Brazil.

Natalus espiritosantensis: Ruschi, 1970: 5. New combination.

Natalus stramineus natalensis: Goodwin, 1959: 5. Type locality Natal, Rio Grande do Norte, Brazil; holotype USNM 242830.

Natalus stramineus espiritosantensis: Pine and Ruschi, 1976: 184. New combination.

Natalus stramineus macrourum: Gardner, 2008: 398. New combination.

Holotype

MBML 1801 male, skin in alcohol with skull extracted, collected by A. Ruschi in April 1953, Gruta Itaúnas (locality 37 in appendix 1), Conceicão da Barra, Espirito Santo, Brazil. The skull is missing the right petrosal, and the right pterygoid process (along with parts of the posterior palate), but is otherwise complete. The skin is in fairly good condition but has the three right metacarpals broken as well as a few perforations in the wing membrane, and is moderately bleached by long immersion in alcohol.

Distribution

South America south of the Amazon River in the countries of Brazil (Bahia, Ceará, Distrito Federal, Espirito Santo, Goiás, Mato Grosso do Sul, Mato Grosso, Minas Gerais, Pará, Piauí, Rio Grande do Norte, São Paulo), Bolivia, and Paraguay (fig. 20).

Fig. 20.

Geographic distribution of Natalus espiritosantensis. Solid circles indicate localities where the species has been collected alive. Open circles indicate localities represented by bone remains only. Names of localities are listed in appendix 1. Gray shading on land indicates relief, with darknes increasing with altitude.

Note

In his recent review of South American natalids, Gardner (2008) assigned this taxon to Natalus stramineus macrourum. His decision stems from the description from Bahia, Brazil, of Spectrellum macrourum Gervais, 1856, and the subsequent allocation of this taxon to Natalus by Dobson (1878). Although the scant diagnostic characters of S. macrourum given by Gervais (1856) are reminiscent of the Natalidae, no specimens or illustrations of this taxon are known at present and Dobson did not argument its allocation to Natalus. In the absence of objective evidence that S. macrourum is indeed a natalid, it is preferable to name all South American Natalus south of the Amazon based on this taxon's oldest known holotype: Myotis espiritosantensis.

Diagnosis

Medium size (forearm length 37.0–42.1 mm); maxillary toothrow length short (6.5–7.0 mm); medial margin of ear pinna deeply concave; lateral margin of ear pinna deeply notched; nostrils small, oval, opening ventrolaterally; ventral pelage monocolored; dorsal pelage bicolored, with hair bases lighter than tips; hair at base of claws short and inconspicuous or long and thin, never forming tufts; premaxilla not inflated, with premaxillary maxillary suture anterior to infraorbital foramen; maxilla convex but not inflated; postorbital region with sides widely diverging rostrally; palate ending caudally at 2/3 of the distance between M3 and tip of pterygoid process; caudal margins of maxillary bones forming an acute angle with longitudinal axis of skull; basisphenoid pit shallow; caudal margin of ascending ramus of dentary perpendicular to alveolar margin of dentary; I1 not visible in lateral view, being obscured by I2; mesostylar crest of M3 absent. A comparison of diagnostic characters between N. espiritosantensis, and other species of Natalus is summarized in table 5.TABLE 6TABLE 7TABLE 9

TABLE 5

Diagnostic characters of species of the genus Natalus

TABLE 6

Summary of measurements^a of Nyctiellus lepidus

TABLE 7

Summary of measurements^a of Chilonatalus macer

TABLE 8

Summary of measurements^a of Chilonatalus micropus

TABLE 9

Summary of measurements^a of Chilonatalus tumidifrons

TABLE 10

Range of diameter of distal humerus in fossil and extant Natalidae

Description

Medium sized (forearm length 37.0–42.1 mm; greatest skull length 15.9–17.0 mm; weight 6 g); muzzle long and dorsoventrally flattened; nostrils elliptical, opening anteroventrally on shallow depression on margin of upper lip; upper lip thickened; lower lip markedly thickened and constricted along dorsal and ventral margin, with numerous transverse grooves; small, smooth central pad on dorsal margin of lower lip; natalid organ medium sized and wedge shaped, extending from caudal base of rostrum to crown of head; ears medium sized (12.0–15.9 mm); ear pinna funnel shaped but distally thin; pinna with markedly pointed tip; medial and lateral margins of pinna deeply concave; five to six small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus short, lanceolate, and twisted into helixlike structure; tibia (20.1–23.8 mm) slightly longer than half the length of the forearm; calcar long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively broad, with 3rd metacarpal (35.1–39.6 mm) slightly longer than 5th metacarpal (34.7–39.1 mm); wings attach to tibia above ankle; pelage dense and lax; hairs long (8 mm, dorsally; 7 mm, ventrally); pelage usually darker dorsally than ventrally; pelage color from pale buff ventrally and light brown dorsally to bright yellowish brown both ventrally and dorsally (pl. 1); dorsal hairs bicolored, with tips darker than bases; ventral hairs usually monocolored; dense mustachelike hair tufts along lateral margins of upper lip and on dorsum of muzzle; mustache formed by dense, lax, irregularly arranged, and ventrally curved hairs; natalid organ covered with thin hairs; skull long and relatively broad with moderate rostral flexion; rostrum wide and short, with sulcus between nasals almost imperceptible; moderate rostral palatal emargination; maxilla convex above molars; braincase inflated, rising abruptly from rostrum; sagittal crest moderately developed; postorbital constriction wide; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids nearly parallel; palate extending caudally to more than half the distance between bases and tips of pterygoids; basisphenoid pit shallow; longitudinal medial ridge on basisphenoid present; ectotympanic small, covering less than half of periotic; upper incisors short and peglike; I2 obscuring I1 in lateral view; occlusal profile of premolars long; upper premolars of similar size; mesostylar crests on M1 and M2 short and straight, mesostylar crest absent on M3; cingular cusp of p4 medium sized and broad; molars cusps relatively broad; spinous process of humerus about as high as capitulum; thorax relatively short and wide; ribs markedly expanded craniocaudally and extensively in contact with one another; vertebrae C7 to T1 fused to each other and to ribs; vertebrae T12–L4 fused entirely without vestige of sutures; vertebrae L5 and L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

Natalus espiritosantensis is a medium sized Natalus. Its forearm is smaller than those of the three greater Antillean species (N. primus, N. major, and N. jamaicensis) and larger on average than those of N. mexicanus and N. lanatus. It lacks external and cranial diagnostic features and must therefore be identified by a combination of characters and by geographic distribution. Externally, it is one of three species (the other two being N. mexicanus and N. stramineus) that combine a concave medial margin of the ear with small, elliptical, and ventrolaterally pointing nostrils. All greater Antillean Natalus and N. lanatus have a straight medial margin of the ear and can thus be distinguished from N. espiritosantensis by this trait alone.

Craniodentally, N. espiritosantensis can be distinguished from Natalus jamaicensis by the sides of its postorbital region, which are nearly parallel in N. jamaicensis and diverge anteriorly in N. espiritosantensis, in dorsal view. From N. lanatus, N. espiritosantensis differs in that the caudal margin of the palatal branches of the maxillae, in ventral view, form an acute angle with the midline of the skull, whereas in N. lanatus they form a nearly straight angle. N. espiritosantensis is distinguished from N. primus by its shallow basisphenoid pits, which are deep in N. primus. From Natalus tumidirostris, N. espiritosantensis differs in its convex yet uninflated maxilla (markedly inflated in N. tumidirostris) and in the caudal extension of the palate that reaches 2/3 of the distance between the caudal edge of M3 and the tip of the pterygoids (the palate ends caudally before reaching the sphenorbital fissure in N. tumidirostris). From Natalus major it differs in its smaller skull (greatest skull length is larger than 17.0 mm in N. major and smaller than 17.0 mm in N. espiritosantensis) and from N. mexicanus and N. stramineus in having a shorter and broader rostrum (breadth across molars ranges from 80%–85% of the length of the tooth row in N. espiritosantensis, and from 72%–81% in N. mexicanus and N. stramineus).

Variation

On average, males of Natalus espiritosantensis are larger than females in seven cranial dimensions (table 11), but females have longer mandibular tooth rows. Despite its vast geographic distribution, Natalus espiritosantensis is the least variable of the continental species of Natalus. Except for the smaller size (not statistically significant; one-way ANOVA, P > 0.01; fig. 21A) of individuals from northeast Brazil (Ceará, Rio Grande do Norte), no morphometric differences were apparent in the sample available for this species (fig. 21B).

Fig. 21.

A, Plot of means (black dots), two standard deviations around the mean (gray bars), and two standard errors of the mean (vertical black lines) of greatest skull length of Natalus espiritosantensis from five geographic areas: (A) Bolivia (5 females, 6 males); (B) SW Brazil [Mato Grosso do Sul], Paraguay (4 females, 6 males); (C) SE Brazil (Espirito Santo, Goiás, Minas Gerais, São Paulo; 7 females, 7 males); (D) NE Brazil (Ceará, Bahia, Rio Grande do Norte; 4 females, 2 males); (E) N Brazil (Pará; 2 males). Although the observed mean greatest skull length of males from NE Brazil was smaller, the difference was not statistically significant (MANOVA, P > 0.01). B, Plot of canonical scores for 6 cranial measurements of N. espiritosantensis from five geographic areas (same as above). Variable loadings are listed in table 12. The lack of morphometric separation between distant geographic units of N. espiritosantensis is congruent with the morphological homogeneity of the species (see text).

TABLE 11

Summary of measurements^a of Natalus espiritosantensis

Natural History and Conservation

This species is known from 36 localities (in 3 of these represented by bone remains only), of which 17 are caves. It has been captured in mistnets in 5 localities (3 in Ceará, Brazil, and 2 in Noel Kempff Mercado National Park, Bolivia). It roosts in caves opening both in sandstone and in limestone. The caves where N. espiritosantensis has been found are humid but not hot (22° C and 94% humidity, Cueva en Santiago de Chiquitos, Bolivia, locality 26; 25° C and 94% humidity, Cueva Concepcioncita, Bolivia, locality 27) and usually contain open bodies of water. It has been found coexisting in caves with 22 other bat species (Anoura geoffroyi, Anoura caudifer, Artibeus planirostris, Carollia perspicillata, Chrotopterus auritus, Desmodus rotundus, Diphylla ecaudata, Glossophaga soricina, Lionycteris spurrelli, Lonchorhina aurita, Lonchophylla mordax, Macrophyllum macrophyllum, Micronycteris megalotis, Micronycteris aff. minuta, Phylloderma stenops, Pteronotus gymnonotus, Pteronotus parnellii, P. personatus, Pteropteryx macrotis, Pteropteryx kappleri, Tonatia saurophila, Tonatia bidens; Gregorin and Mendes, 1999; Pine and Ruschi, 1976; Taddei and Uieda, 2001; Trajano and Gimenez, 1998; Trajano and Moreira, 1991). On one occasion N. espiritosantensis was found roosting solitarily at the edge of a compact cluster of Carollia perspicillata (Rodrigo Lopes Ferreira, in litt.).

Natalus espiritosantensis occurs from xeric habitats (e.g., caatinga, Itaeté, Brazil, 772 mm annual precipitation; locality 29) to moist habitats (Amazonian forest, Aripuaná, Brazil, 2119 mm annual precipitation; locality 50) and from sea level to middle elevations (1000 m, Brasilia, Brazil; locality 36). Nothing is known of the diet of this species.

Natalus espiritosantensis is the species of natalid with the widest geographic distribution, but is apparently rare over much of its large range. It is known from 73 museum specimens, most of which have been collected at two localities: Mato Grosso do Sul (Paranaiba, Rio Verde), and Poço Encantado, Itaeté, Bahia, both in Brazil. Colony sizes seem comparatively small, ranging from 5–10 individuals to about 50. It was one of the most common bats in two caves (Olhos D'agua, locality 45; Trajano and Gimenez, 1998; and in Caverna Planaltina, locality 53; Trajano and Moreira, 1991). Of two collections obtained in Paranaiba, Mato Grosso do Sul, Brazil, one taken in summer (28 January 1979) contained both males and females, whereas a second collection taken in early spring (3 November 79) was composed only of males, suggesting temporal sexual segregation.

Nothing is known of reproductive patterns in N. espiritosantensis. Apparently pregnant females (with greatly swollen abdomens) have been taken in Mato Grosso do Sul, Brazil, in summer (28 January 1979) and in late winter (7 September 1993).

Natalus espiritosantensis is not listed in IUCN's Red List of Threatened Species (IUCN, 2010). It is an infrequently encountered species, and may be threatened by the practice of extermination of cave bat colonies that is widespread in Brazil. Large karst areas of southeast Brazil seem to have already suffered massive declines in populations of cave bat species. The vast geographic range of this species suggest that remote populations will escape intense human disturbance, but if bat extermination campaigns continue in the densely populated rural areas of Brazil, this bat may become extinct over a large part of its range.

Natalus jamaicensis (Goodwin, 1959)

Figure 22

Fig. 22.

Holotype of Natalus jamaicensis (AMNH 182000, male, Jamaica). Scale bar  =  10 mm. Photo: Mariko Kageyama, AMNH (see appendix for institutional abbreviations).

Natalus major jamaicensis Goodwin, 1959: 9. Type locality “St. Clair, St. Catherine Parish, Jamaica, British West Indies.”

Natalus stramineus jamaicensis: Linares, 1971: 83. New combination.

Natalus major: Morgan, 1989: 686. Part, not Natalus major Miller, 1902.

Natalus jamaicensis: Dávalos, 2005: 95. New combination.

Holotype

AMNH 182000, adult male, skull and skin in fluid, collected by C.B. Lewis in St. Clair Cave (locality 250 in appendix 1), St. Catherine Parish, Jamaica on 5 March 1954. The skull is complete and the skin is in good condition.

Distribution

Jamaica, known to be extant at the type locality only (fig. 23).

Fig. 23.

Geographic distribution of Natalus jamaicensis (upside down triangles), N. major (squares), N. primus (circles), and N. stramineus (upright triangles). Open symbols indicate localities represented by bone remains only. Names of localities are listed in appendix 1. Gray shading on land indicates relief, with darknes increasing with altitude.

Diagnosis

A large representative of Natalus with a long forearm (44.1–44.8 mm) relative to its skull length (17.4–18.1 mm); medial margin of ear pinna straight; lateral margin of ear pinna deeply notched; nostrils small, oval, opening ventrolaterally; ventral pelage monocolored; dorsal pelage bicolored with hair bases lighter than tips; hair at base of claws short and inconspicuous or long and thin, never forming tufts; premaxilla not inflated, with maxilloincisive suture anterior to infraorbital foramen; maxilla above molars concave; palate ending caudally at 2/3 the distance between M3 and tip of pterygoid process; caudal margins of maxilla in ventral view forming an acute angle with longitudinal axis of skull; basisphenoid pit shallow; postorbital region narrow, with sides nearly parallel, in dorsal view; braincase rising abruptly from rostrum, with an angle greater than 60° between dorsal plane of rostrum and frontal plane of forehead; braincase rounded in dorsal profile, with breadth almost as great as length; postorbital constriction, its sides almost parallel; caudal margin of ascending ramus of mandible perpendicular to alveolar margin of dentary; I1 not visible in lateral view, being obscured by I2; mesostylar crest of M3 absent. A comparison of diagnostic characters between N. jamaicensis and other species of Natalus is summarized in table 5.

Description

Size large (forearm length 44.0–47.0 mm; greatest skull length 17.2–18.1 mm; weight 5.9–7.3 g); muzzle long and dorsoventrally flattened; nostrils elliptical, opening ventrolaterally on shallow depression on margin of upper lip; upper lip thickened; lower lip markedly thickened and constricted along dorsal and ventral margin, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; natalid organ medium size and elliptical, extending from caudal base of rostrum to crown of head; ears relatively long (15.3–19.1mm); ear pinna funnel shaped; pinna with markedly pointed tip; medial margin of pinna straight; lateral margin of pinna deeply concave; five to six small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus short, lanceolate, and twisted into helixlike structure; tibia (24.3–25.7 mm) slightly longer than half the length of the forearm; calcar long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively broad, with 3rd metacarpal (40.8–42.8 mm) slightly longer than 5th metacarpal (39.9–41.4 mm); wings attach to tibia above ankle; pelage dense and lax; hairs long (9–11 mm, dorsally; 6–7 mm, ventrally); pelage usually darker dorsally than ventrally; dorsal hairs bicolored, with tips darker than bases; ventral hairs usually slightly bicolored and rarely monocolored; pelage color from buff with tips sepia or ochraceous (tawny olive; pl. 1); ventral hair bases are buff with tips pinkish buff; dense mustachelike hair tufts along lateral margins of upper lip and on dorsum of muzzle; mustache formed by dense, lax, irregularly arranged, and ventrally curved hairs; natalid organ covered with thin hairs; skull long and relatively slender with moderate rostral flexion; rostrum long and slender, with sulcus between nasals short, shallow, and confined to point of flexion between rostrum and braincase; moderate rostral palatal emargination; maxilla concave dorsal to molars; braincase greatly inflated (globular), rising abruptly from rostrum; braincase in dorsal view nearly circular; sagittal crest well developed; postorbital constriction narrow, its sides nearly parallel; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids nearly parallel; palate extending caudally to more than half the distance between bases and tips of pterygoids; basisphenoid pit shallow; longitudinal medial ridge on basisphenoid present; ectotympanic small, covering less than half of periotic; upper incisors short and peglike; I2 obscuring I1 in lateral view; upper premolars slightly increasing in size from P2 to P4 and crowded; mesostylar crests on M1 and M2 short and straight, mesostylar crest absent on M3; cingular cusp of p4 medium sized and broad; molars cusps relatively broad; spinous process of humerus about as high as capitulum; thorax relatively short and wide; ribs markedly expanded craniocaudally and extensively in contact with one another; vertebrae C7 to T1 fused among themselves and to ribs; vertebrae T12–L4 fused entirely without vestige of sutures, forming a laterally compressed column; lumbar column relatively short and concave ventrally; vertebrae L5 and L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

The large body size (forearm length 44.0–47.0 mm) of Natalus jamaicensis readily separates this species from the continental and Lesser Antillean species of the genus Natalus (Natalus stramineus, forearm 36.9–41.9 mm; Natalus tumidirostris, forearm 35.0–42.0 mm; Natalus mexicanus, forearm 34.0–40.6 mm; and Natalus lanatus, forearm 35.4–38.6 mm), and from species of the genera Nyctiellus and Chilonatalus. Natalus jamaicensis is best distinguished from other greater Antillean Natalus (N. primus and N. major) by discrete cranial or external characters.

Cranially, N. jamaicensis is a very distinctive species. Its skull shows several modifications concomitant with its high degree of cranial flexion. First, in N. jamaicensis the frontal plane of the braincase raises very steeply from the rostrum, in an angle greater than 60°, a condition that is unique among species of the genus Natalus. Second, the braincase of N. jamaicensis is markedly inflated and almost as wide as long, and as a result has an almost circular profile in dorsal view. In all other species of Natalus the braincase is longer than wider and thus appears oval shaped. Third, the postorbital constriction of the skull of N. jamaicensis is proportionally narrower than in all other species of Natalus, with sides almost parallel in dorsal view, while in all other species of Natalus the sides of the postorbital constriction markedly diverge anteriorly. In addition, the rostrum of N. jamaicensis is flattened dorsally to a greater degree than in other species of Natalus, and shows a marked reduction of the sulcus between nasal bones, and a concave shape of the maxilla in the area dorsal to the molars. The concave maxilla is a readily observed character and is sufficient to diagnose N. jamaicensis because all other species of Natalus have markedly convex to markedly inflated maxillary bones.

Natalus jamaicensis is less well differentiated in external morphology, and no discrete external character has been found to distinguish it from N. major. It differs in its straight medial ear margin from most continental species of the genus (except N. lanatus), which have slightly to deeply concave medial ear margins. From N. lanatus it can be distinguished by the lack of hair tufts at the base of claws, which are present in N. lanatus. From Natalus primus, N. jamaicensis can be distinguished by its concave lateral margin of the ear pinna, which is straight in N. primus.

Variation

Secondary sexual dimorphism in Natalus jamaicensis was detected in two cranial measurements: breadth across canines and mandibular tooth row (table 12).TABLE 13

TABLE 12

Loadings of the first two canonical axes of two canonical variates analyses (CVA) performed with 5 geographic samples of Natalus espiritosantensis

TABLE 13

Summary of measurements^a of Natalus jamaicensis

Natural History and Conservation

Natalus jamaicensis is known from just two localities, in only one of which (St. Clair Cave, St. Catherine) it is represented by an extant population. From the second locality, Wallingford Cave, St. Elizabeth, it is known by a single subfossil mandible. In St. Clair Cave, N. jamaicensis has been found at the entrance of a hot passage (Hoyt and Baker, 1980) through which runs a permanent stream and in a protected lateral recess 3.7 m above the floor of the hot passage (Goodwin, 1970). The bats usually hang from one foot and keep a distance between individuals of about 10 cm (Goodwin, 1970). A total of nine other bat species are found in St. Clair: Artibeus jamaicensis, Chilonatalus micropus, Erophylla sezekorni, Monophyllus redmani, Mormoops blainvillei, Phyllonycteris aphylla, Pteronotus macleayi, Pteronotus parnellii, and Pteronotus quadridens (Hoyt and Baker, 1980). Goodwin (1970) found N. jamaicensis in close association with Chilonatalus micropus but forming separate groups. Similarly, Hoyt and Baker (1980) noticed that these two species were spatially segregated with N. jamaicensis occupying the first 50 m of the hot passage and being replaced in deeper areas by a larger colony of C. micropus. St. Clair cave is located in an area of semideciduous forest (1472 mm annual precipitation) at 100 m above sea level.

In spite of occurring in a single cave, it has been extensively collected, being represented by at least 78 museum specimens. The size of St. Clair's colony appears to be very small. Observers have usually found it to be much less numerous than that of C. micropus (Hoy and Baker, 1980; Genoways et al., 2005). The only numeric estimate is that of Goodwin (1970) who reports only about 50 bats of this species in St. Clair. A total of 25 females taken in July and December did not show signs of reproductive activity (Goodwin, 1970).

Nothing is known of the diet and nocturnal activity of N. jamaicensis. As in other natalids this bat probably forages with slow flight in cluttered habitats. Its flight has been described as fluttery and mothlike (Goodwin, 1970). Natalus jamaicensis dehydrates very rapidly when taken outside the caves where they roost (Hoyt and Baker, 1980).

Natalus jamaicensis may be the most critically endangered species of all natalids and one of the world's mammals in greatest risk of extinction. Traditionally treated as Natalus stramineus, it was listed as critically endangered by the IUCN's (IUCN, 2010) until 2008. It was considered the rarest of Jamaican bats by Goodwin (1970) and McFarlane (1986) yet,alarmingly, it has been intensively collected, apparently being more common in museum collections than in the wild (see above). This species' only known roost site, St. Clair Cave, receives no form of official protection (Dávalos and Eriksson, 2003), and is thus open to unregulated human visitation. St. Clair Cave, in addition, has resident populations of feral domestic cats that feed on the bats (species not specified) and rats of the cave (McFarlane, 1997). A brief mistnet survey of St. Clair in December 2001 by Dávalos and Eriksson (2003) failed to detect this species. Immediate efforts are needed to understand this species' conservation requirements and to formulate a plan for its protection.

Natalus lanatus Tejedor, 2005

Figure 24

Fig. 24.

Holotype of Natalus lanatus (KU 39628, female, Nayarit, Mexico). Scale bar  =  10 mm.

Natalus stramineus saturatus: Hall and Dalquest, 1963: 242. Part; specimen from Fortín, Veracruz, Mexico.

Natalus stramineus mexicanus: Anderson, 1972: 241. Part; two specimens from two localities in Chihuahua, Mexico.

Natalus stramineus: Rodríguez-Herrera, 2004: 125. Not Natalus stramineus Gray, 1838.

Natalus lanatus Tejedor, 2005: 1110. Type locality “6 miles SSE of Las Varas, Nayarit, Mexico.”

Holotype

KU 39628, adult female, skin and skull, collected by J.R. Alcorn on 1 November 1950 (original field number JRA 13312) 6 miles SSE of Las Varas (locality 357 in appendix 1), Nayarit, Mexico. The skin is well preserved and the skull is complete.

Paratypes

include an adult female (KU 39621) and an adult male (KU 39620), also collected by JRA at the same locality and date as the holotype.

Distribution

Mexico (Chihuahua, Durango, Guerrero, Jalisco, Nayarit, Sinaloa, and Veracruz) and Costa Rica (fig. 25).

Fig. 25.

Geographic distribution of Natalus lanatus (open triangles) and N. mexicanus (solid circles). Names of localities are listed in appendix 1. Some localities of N. mexicanus obtained from museum catalogues or the literature, especially those of the Mexico Basin and Veracruz highlands, may actually represent Natalus lanatus (see text). Gray shading on land indicates relief, with darknes increasing with altitude.

Diagnosis

A small species of funnel-eared bat (forearm length 16.0–19.2 mm); legs considerably shorter than forearm; medial margin of ear straight; lateral margin of ear deeply notched; 0–1 folds on lateral margin of ear; nostrils small, opening ventrolaterally; bicolored ventral fur and bicolored or tricolored dorsal hairs; dorsal and ventral hairs always darker at the base than at the tips; pelage dense, woolly, and dull, grayish to ochraceous; ventral surface and more than half of dorsal surface of pinna profusely covered with hairs; legs and feet conspicuously hairy with tufts of long hairs projecting from bases of claws; rostrum shallow in lateral view; premaxilla not inflated; maxilloincisive suture anterior to infraorbital foramen; maxilla dorsal to molars convex, not inflated; sides of postorbital region in dorsal view widely diverging rostrally; palate between pterygoids ending caudally 2/3 of the distance between M3 and tip of pterygoid; posterior margins of maxilla almost perpendicular to longitudinal axis of skull, in ventral view; basisphenoid pit shallow; caudal margin of ascending ramus of mandible perpendicular to alveolar margin of dentary; I1 visible in lateral view, not obscured by I2; mesostylar crest on M3 absent. A comparison of diagnostic characters between N. lanatus, and other species of Natalus is summarized in table 5.

Description

Size small (forearm length 35.4–38.6 mm; greatest skull length 15.0–16.4 mm; weight 5.0–6.5 g); muzzle long and not particularly flattened dorsoventrally; nostrils narrowly elliptical, opening ventrolaterally to ventrally on very shallow depression on margin of upper lip; upper lip thickened; lower lip markedly thickened and constricted along dorsal and ventral margin; natalid organ medium size, elliptical and swollen, extending from caudal base of rostrum to crown of head; ears relatively short (12.0–15.6 mm); ear pinna funnel shaped and broad; pinna with moderately pointed tip; medial margin of pinna straight; lateral margin of pinna moderately concave; three to no small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus short, lanceolate, and twisted into helixlike structure; tibia (16.0–19.2 mm) shorter than half the length of the forearm; calcar long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with fringe of thin hairs; wings broad and relatively short, with 3rd metacarpal (31.2–33.9 mm) shorter than 5th metacarpal (33.2–35.5 mm); wings attach to tibia above ankle; pelage dense and woolly; hairs long (8–9 mm, dorsally; 7–8 mm, ventrally); pelage darker dorsally than ventrally; dorsal pelage color from gray (mouse gray) to ochraceous (tawny olive) (pl. 1); dorsal hairs bicolored or tricolored, with dark bases, light middle parts, and medium-dark tips; ventral pelage from gray to ochraceous but hairs markedly bicolored, with bases darker than tips; dense mustachelike hair tufts along lateral margins of upper lip and on dorsum of muzzle; mustache formed by dense, lax, irregularly arranged, and ventrally curved hairs; natalid organ covered with long hairs; ventral face of ears covered with sparse wooly hairs; feet with marked ungual hair tufts at base of claws and fine covering of short erect hairs along tibia; skull long and relatively broad with moderate rostral flexion; rostrum conical, with wide base and tapering tip, with sulcus between nasals almost imperceptible; moderate rostral palatal emargination; maxilla convex above molars; braincase inflated, and elongated; sagittal crest well developed; postorbital constriction wide; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; caudal margin of palatal branch of maxilla nearly perpendicular to longitudinal axis of skull; pterygoids nearly parallel; palate extending caudally to more than half the distance between bases and tips of pterygoids; basisphenoid pit shallow; longitudinal medial ridge on basisphenoid present; ectotympanic small, covering less than half of periotic; upper incisors long and pointed; I1 visible in lateral view, not being obscured by I2; occlusal profile of premolars long; upper premolars of similar size; mesostylar crests on M1 and M2 short and straight, mesostylar crest absent on M3; cingular cusp of p4 medium sized and broad; molar cusps relatively broad.

Comparisons

Natalus lanatus can be readily distinguished from all other known species of Natalus by its bicolored ventral pelage. The contrast among color bands in ventral pelage may be less noticeable in some individuals, but hair bases are always darker than tips. In all other species of Natalus, the ventral fur is monocolored (with the exception of Natalus jamaicensis, which has slightly lighter ventral hair tips, but the contrast in banding pattern is much less than in N. lanatus). Natalus lanatus can also be distinguished by its often tricolored dorsal hairs, which are always darker at the base than at the tips. In all other species of Natalidae the light and dark banding pattern of dorsal hairs, when present, is reversed, with the tips always darker than the bases. Natalus lanatus is also distinguishable from all other species in the genus by its hairier legs and feet, with conspicuous ungual tufts (fig. 6). In all other species of Natalus the legs are more sparsely haired and the tips of the toes usually lack long hairs (in cases where long hairs are present at the base of claws, they do not form the dense tufts characteristic of N. lanatus). In some individuals of N. lanatus, however, the hair tufts at the base of claws may be thin, approaching the condition of the most thickly furred feet of other species of Natalus. Therefore, this character must be used in combination with ventral pelage and cranial characters for an accurate diagnosis of N. lanatus.

In addition to the characters mentioned above, Natalus lanatus differs from the sympatric Natalus mexicanus by its dense, woolly, dull, and often darker pelage, which does not show marked differences in overall darkness throughout the dorsum. The pelage of N. mexicanus is silkier and lax, and when grayish (as in juveniles and young adults), it shows a distinctive patch of dark-tipped hairs posterior to shoulders. From N. mexicanus, N. lanatus is also distinguishable by ear characters (only useful with fluid-preserved and fresh specimens). In N. lanatus the medial margin of the pinna is straight to slightly convex, and the apex of the pinna is relatively broad (the angle formed between the medial and lateral margins of the apex of the pinna in N. lanatus is about 90°). In N. mexicanus, the medial margin of the pinna is slightly concave, forming an angle smaller than 90° with the lateral margin of the pinna, giving the apex a more acutely pointed appearance. The ventral surface of the pinna in N. lanatus is also more densely haired and correspondingly shows a much denser packing of hair follicles than the pinna of N. mexicanus. With regard to body dimensions, the length of the tibia in N. lanatus averages almost 3 mm less than in N. mexicanus, and its overall leg length is considerably smaller than the forearm length. In N. mexicanus, the leg is about as long as or slightly longer than the forearm. Cranially, N. lanatus shows a longer and more anteriorly inflated braincase, and a better-developed sagittal crest than N. mexicanus. In addition, the skull of N. lanatus is slightly but significantly wider than that of N. mexicanus, as reflected by greater averages for zygomatic breadth, breadth across molars, and postorbital breadth. Conversely, the maxillary tooth row of N. lanatus is slightly shorter than that of N. mexicanus.

Variation

Males of Natalus lanatus have a slightly but significantly larger mean breadth across canines than females (table 14). Bats from the eastern versant of the Mexican highlands (Veracruz) have significantly longer forearms than bats from the western versant (Durango, Jalisco, Nayarit), and have wider skulls (zygomatic breadth, postorbital breadth, P < 0.05; fig. 26). A specimen of N. lanatus from Costa Rica (Río Savegre) is reported to be unusually large relative to N. mexicanus from that country, implying a larger size than in N. lanatus from Mexico (B. Rodríguez, personal commun.).

Fig. 26.

Sexual and geographic variation in four cranial dimensions of Natalus lanatus from the Atlantic and Pacific versants of the Mexican highlands. Geographic areas: A  =  Atlantic (Veracruz; 8 males, 5 females); P  =  Pacific (Chihuahua, Durango, Jalisco, Nayarit; 18 males, 19 females). Symbols: black dots, means; vertical gray bars, two standard deviations around the mean; vertical black line, two standard errors around the mean. Females have narrower breadths across canines in both geographic areas (MANOVA, P < 0.05) whereas individuals (regardless of sex) from the Atlantic versant have longer forearms and wider skulls than individuals from the Pacific versant (Tukey, P < 0.05).

TABLE 14

Summary of measurements^a of Natalus lanatus

Natural History and Conservation

Natalus lanatus is known from 16 localities in Mexico and two in Costa Rica (B. Rodríguez and R.K. LaVal, personal commun.; fig. 25). In five of these localities it has been collected in a roost, of which four have been mines and one a cave. In at least three occasions it has been collected in mistnets (localities 70, 79, and 298). With further inspection of museum collections the number of collection localities of this species in Mexico and Central America will likely increase significantly. One specimen mistnetted in Río Macho, Costa Rica reported as N. stramineus, probably represents N. lanatus (see below).

At its roosts, Natalus lanatus has been found coexisting with Balantiopteryx plicata, Carollia perspicillata, Desmodus rotundus, Glossophaga sp., Macrotus sp., Myotis thysanodes, Natalus mexicanus, and Pteronotus parnellii. Large caves or mines are not known from some of the locations where it has been mistnetted (e.g., Rio Savegre, Monte Verde), suggesting that it may often use relatively small cavities as roosts.

The collection localities of Natalus lanatus differ considerably in climatic regimes, ranging from dry mountain subtropical habitats with marked seasonal variations in temperature and precipitation (e.g., La Bufa, Chihuahua; Anderson, 1972), through the zone of transition between pine/oak and tropical deciduous forests (Durango, C. López-González, field notes), to continuously moist montane tropical forest (Orizaba, Veracruz; Hall and Dalquest, 1963). Most of the localities for which geographic coordinates are known with certainty correspond to middle elevations, ranging from 500 to 2000 m. The record from Río Macho, Costa Rica, a wet mountain forest habitat (1300 melevation, 2700 mm annual precipitation) without known caves, most likely corresponds to N. lanatus than to N. mexicanus, given that the latter species has been collected in Costa Rica exclusively in lowland areas with abundant caves.

Natalus lanatus is represented by at least 70 museum specimens. Given that it has been described only recently, many Mexican specimens of N. lanatus identified as N. stramineus ( =  N. mexicanus) probably remain in museum collections. This species may be less gregarious than other species of Natalidae. Although it has been collected in moderately large numbers at some localities (e.g., near Tuxpan, Veracruz, locality 445 in appendix 1; and in Ameca, Jalisco, locality 320), over half of the collection localities of this species are represented by a single museum specimen (appendix 1). In addition, it has been collected roosting solitarily in a cave occupied by a colony of Carollia perspicillata (Hall and Dalquest, 1963).

Nothing is known of the diet or activity patterns of Natalus lanatus, although it is possible that specimens of this taxon may have served as a basis for natural history accounts of Natalus mexicanus (e.g., Villa-R., 1966). As a representative of the genus Natalus, however, the new species is probably similar in its ecology to other species of the genus (e.g., Natalus primus, Tejedor et al., 2005b; and Natalus tumidirostris, Linares, 1998) in being a slow-flying insectivore that forages through low vegetation. The differences in morphology between N. lanatus and N. mexicanus (see section titled Ecomorphological Diversity), however, may reflect some ecological divergence between these two taxa, as it has been found for other closely related bat species (e.g., Pipistrellus, Barlow et al., 1997). Ecological studies of N. lanatus, with a focus on understanding its interaction with its sympatric close relative N. mexicanus, are highly needed.

Natalus lanatus is listed as least concern in the IUCN's Red List of Threatened Species (IUCN, 2010), but certainly more data is needed from this poorly known species before accurate conservation assessments can be undertaken.

Natalus major Miller, 1902

Figure 27

Fig. 27.

Holotype of Natalus major (USNM 101395, male, Hispaniola [Dominican Republic]). Scale bar  =  10 mm.

Natalus major Miller, 1902: 398. Type locality “near Savaneta, Santo Domingo,” Dominican Republic.

Natalus stramineus major: Linares, 1971: 83. New combination.

Holotype

USNM 101395, adult male skull and skin in fluid, collected by W.M. Gabb between 1869 and 1871 “near Savaneta (locality 195 in appendix 1), Dominican Republic.” The skull is complete (fig. 27) and the skin is in good condition.

Distribution

Hispaniola, including the Dominican Republic and Haiti (fig. 23).

Diagnosis

Forearm long (41.1–45.0), skull long relative to forearm, breadth across canines large (3.9–4.5), maxillary tooth row (7.5–8.0); medial ear margin straight; lateral ear margin deeply notched; nostrils small, opening ventrolaterally; ventral hairs monocolored; dorsal hairs bicolored, hair bases lighter than tips; hair at base of claws short and inconspicuous or long and thin, never forming tufts; maxilla dorsal to molars convex, not inflated; postorbital region with sides widely diverging rostrally; point of flexion between rostrum and braincase dorsal to the anterior edge of orbit; palate ending caudally 2/3 of the distance between M3 and tip of pterygoid; caudal margins of palatine wing of maxilla forming an acute angle with longitudinal axis of skull; basisphenoid pits shallow; caudal margin of ascending ramus of mandible perpendicular to alveolar plane of lower molars; I1 not visible in lateral view, obscured by I2; mesostylar crest on M3 absent. A comparison of diagnostic characters between N. major, and other species of Natalus is summarized in table 5.

Description

A large natalid (forearm length 41.1–45.0 mm; greatest skull length 17.0–18.1 mm; weight 5.5–10.0 g); muzzle long and dorsoventrally flattened; nostrils elliptical, opening anteroventrally on shallow depression on margin of upper lip; upper lip thickened; lower lip markedly thickened and constricted along dorsal and ventral margin, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; natalid organ medium size and elliptical, extending from caudal base of rostrum to crown of head; ears medium sized (13.0–18.9 mm); ear pinna funnel shaped with pointed tip; medial margin of pinna straight; lateral margin of pinna deeply concave; five to six small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus short, lanceolate, and twisted into helixlike structure; tibia (23.2–25.4 mm) slightly longer than half the length of the forearm; calcar long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings wide, with 3rd metacarpal (40.3–42.7 mm) slightly longer than 5th metacarpal (38.3–41.2 mm); wings attach to tibia above ankle; pelage dense and lax; hairs long (7 mm, dorsally and ventrally); pelage usually darker dorsally than ventrally; dorsal hairs bicolored, with tips darker than bases; ventral hairs monocolored; dorsal hair bases buff to drab with tips sepia to fuscous brown (pl. 1); ventral hairs creamy buff; dense mustachelike hair tufts along lateral margins of upper lip and across muzzle; mustache formed by dense, lax, irregularly arranged, and ventrally curved hairs; natalid organ covered with thin hairs; skull long and relatively broad with moderate rostral flexion; rostrum short and broad, with moderate sulcus between nasals; moderate rostral palatal emargination; maxilla convex dorsal to molars; braincase greatly inflated, rising gently from rostrum; braincase elliptical in dorsal view; sagittal crest well developed; postorbital constriction wide, its sides diverging rostrally; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids nearly parallel; palate extending caudally to more than half the distance between bases and tips of pterygoids; basisphenoid pit shallow; longitudinal medial ridge on basisphenoid present; ectotympanic small, covering less than half of periotic; upper incisors short and peglike; I2 obscuring I1 in lateral view; upper premolars slightly increasing in size from P2 to P4 and crowded; mesostylar crests on M1 and M2 short and straight, mesostylar crest absent on M3; cingular cusp of p4 medium sized and broad; molars cusps relatively broad; spinous process of humerus about as high as capitulum; thorax relatively short and wide; ribs markedly expanded craniocaudally and extensively in contact with one another; vertebrae C7 to T1 fused and fused to ribs; vertebrae T12–L4 fused into a laterally compressed column without vestige of sutures; lumbar column relatively long and not particularly concave ventrally; vertebrae L5 and L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

Unique morphological features are not apparent in Natalus major. It, therefore, must be distinguished from other species of Natalidae by a combination of shared diagnostic characters. From species of the genera Chilonatalus and Nyctiellus, Natalus major is distinguished by its large size (forearm length > 41.1 mm) and by generic-level characters (table 3).

Natalus major can be easily distinguished from continental and Lesser Antillean species of Natalus on the basis of its larger forearm length and its straight medial ear margin. Natalus mexicanus has a slightly concave medial ear margin and its forearm is shorter than 40.0 mm. Only very large individuals of N. stramineus, N. tumidirostris, and N. espiritosantensis reach the forearm length of the smallest individuals of N. major, yet in the first three species, the medial ear margin is concave. Natalus lanatus, on the other hand, has a straight medial ear margin, but its forearm is shorter than 38.0 mm.

From Natalus primus, N. major can be distinguished by size, ear, and cranial characters. Relative to N. major, N. primus has a larger forearm (more than 46.0 mm; the forearm is shorter than 45.0 mm in N. major), has a straight lateral ear margin (concave or notched in N. major), and is characterized by deep basisphenoid pits (shallow in N. major), the presence of a mesostylar crest on M3 (absent in N. major), and an elongated premaxillary region (reflected in a laterally visible gap between I2 and the upper canine and a rostrally projecting I1; in N. major neither the gap between I2 and the upper canine, and I1 are visible in lateral view).

Of all natalids, Natalus major is most similar to Natalus jamaicensis in size and external characters, but can be easily distinguished by its wide postorbital region with sides widely diverging anteriorly, whereas the postorbital region in N. jamaicensis is narrow and with sides nearly parallel. The maxilla of N. major is convex dorsal to the molars, whereas that of N. jamaicensis is concave. Also, the braincase of N. major is oval in dorsal profile (with length greater than the greatest breadth) and does not rise abruptly from the rostrum (in an angle smaller than 55°), whereas that of N. jamaicensis is nearly circular in dorsal profile (with length similar to greatest breadth) and rises abruptly from the rostrum in an angle greater than 60°.

Variation

On average, males of Natalus major are significantly larger than females in length of tibia (Tukey; P < 0.05) and breadth across canines (Tukey; P  =  0.05; table 15). Geographic variation is not apparent in this species. Most individuals have been collected in neighboring localities of the northwest of Hispaniola and other localities on the island are represented by only one or a few individuals.TABLE 16

TABLE 15

Summary of measurements^a of Natalus major

TABLE 16

Summary of measurements^a of Natalus mexicanus

Young adults with silky, grayish pelage have smaller zygomatic breadths even though the remaining cranial dimensions are similar to that of full adults. A specimen from Haiti (KU 150721), which Timm and Genoways (2003) speculated could belong to a separate subspecies because of its smaller dimensions and coloration, appears to be a young adult.

Natural History

Natalus major is known from 30 localities (including two represented by fossil remains only) of which at least 10 have been roost sites, nine of them caves and one a large hollow tree (Timm and Genoways, 2003). The caves where N. major has been found range from small to very large, are always humid, and often contain hot chambers and bodies of water. Most of these caves have a phreatic origin, with wide chambers and constricted entrances, but some are also fluvial caves characterized by linear passages. One was a sea cave with its floor partially inundated by the tide. N. major roosts in loose groups of less than 10 to more than 50 individuals, occupying areas of low ceilings (including solution cavities) or cave walls. Individuals hang from one or both feet, without body contact with the substrate or among themselves, and keeping a distance between individuals of about 10 cm (pl. 19-A). Occasionally, pairs of individuals are found hanging back to back. Natalus major can coexist at roosts with 10 other bat species (Artibeus jamaicensis, Brachyphylla nana, Chilonatalus micropus, Erophylla bombifrons, Macrotus waterhousii, Monophyllus redmani, Mormoops blainvillei, Phyllonycteris poeyi, Pteronotus quadridens, and Pteronotus parnellii), but it has never been found in multispecies groups. It usually tolerates disturbance for long periods and can occasionally be caught by hand while roosting, but this happens only when a colony has not been disturbed for a long time. On second and third visits to a cave the bats are usually alert and the groups move to alternative roosting sites within the cave at the slightest disturbance (e.g., the beam of a flashlight). When retreating from disturbance, the bats fly close to the floor and walls of the caves (pl. 9-B).

Natalus major is found from semiarid lowlands of thorn scrub (Pepillo Salcedo, Dominican Republic, 883 mm annual precipitation; locality 187) to degraded wet forest (Camp Perrin, Haiti, 2841 mm annual precipitation) and from sea level to about 1000 m (locality 182). Little is known of the diet or reproduction in this species. Young adults have been found in late October, indicating that parturition and lactation probably take place from July to September, as in Natalus mexicanus. Natalus major is the most common of Greater Antillean Natalus, being represented by 105 museum specimens, most of which have been captured in the northeast of the Dominican Republic. Roosting colonies may reach a few hundred individuals.

Natalus major begins its foraging activity shortly after sunset. One individual was mistnetted at 15∶39, at least 4 km away from any known cave where the species roosted. A second individual was mistnetted well after dark entering a cave not used by the species as a day roost, suggesting that night roosts may be used at least occasionally. It has a very slow and maneuverable flight and dehydrates quickly if taken outside the cave during daytime.

Natalus major is listed asnear threatened in IUCN's Red list of Threatened Species (IUCN, 2010). Yu and Dobson (2000) considered this species “very rare,” yet their conclusion was based on distribution and ecological data from Hoyt and Baker (1980), who listed the type localities of N. major major and N. major jamcensis as the only localities of N. major (sensu lato), and based their natural history account on N. jamaicensis. Even though it is represented by relatively few specimens compared to continental species (e.g., N. tumidirostris and N. mexicanus), it seems ubiquitous throughout Hispaniola (particularly in the moist northeast) and is one of the most frequently encountered bats in the island's caves. Given that a significant proportion of the many caves that may remain unsurveyed in Hispaniola's protected karstic areas (e.g., Parque Nacional Jaragua and Parque Nacional los Haitises) probably harbor this species, N. major may be more accurately regarded as of least concern for conservation. Nonetheless, considering that this species is restricted to Hispaniola, adequate population assessments should be undertaken to evaluate its potential conservation needs.

Natalus mexicanus Miller, 1902

Figure 28

Fig. 28.

Holotype of Natalus mexicanus (USNM 96496, Baja California Sur, Mexico). Scale bar  =  10 mm.

Natalus mexicanus Miller, 1902: 399. Type locality “Santa Anita, lower California, Mexico.”

Natalus mexicanus saturatus: Dalquest and Hall, 1949: 153. Type locality “3 kilometers east of San Andres Tuxtla, 1000 feet elevation, Veracruz, Mexico.”

Natalus stramineus mexicanus: Goodwin, 1959: 6. Part, new combination.

Natalus stramineus saturatus: Goodwin, 1959: 7. Part, new combination.

Natalus saturatus: Dávalos, 2005: 100. New combination.

Holotype

USNM 96496, adult female, skin in alcohol with skull extracted, collected by J.F. Abbot in August 1897, at Santa Anita (locality 266 in appendix 1), Baja California Sur, Mexico. The skin is in good condition. The skull has the braincase caved in and cracked on its left side but otherwise is in good condition.

Distribution

Southern North America and Central America in the countries of Mexico (Baja California Sur, Campeche, Chiapas, Chihuahua, Colima, Distrito Federal, Durango, Guerrero, Hidalgo, Jalisco, Mexico, Michoacán, Morelos, Nayarit, Nuevo León, Oaxaca, Puebla, Quintana Roo, San Luis Potosí, Sinaloa, Sonora, Tabasco, Tamaulipas, Veracruz, Yucatán, Zacatecas), Guatemala, Belize, Honduras, El Salvador, Nicaragua, Costa Rica, and Panama, including several offshore continental or oceanic islands (María Magdalena and Cozumel, Mexico; Coiba, Panama; San Andrés and Old Providence, Colombia); fig. 25.

Diagnosis

Size small (forearm length 34.0–40.6 mm); medial margin of ear slightly concave; lateral margin of ear deeply notched; premaxilla not inflated with maxilloincisive suture rostral to infraorbital foramen; maxilla convex but not inflated dorsal to molars; palate ending caudally about 2/3 of the distance between the caudal margin of M3 and the tip of the pterygoid process; ventral hairs monocolored; dorsal hairs monocolored or bicolored with bases lighter than tips; toes lacking conspicuous tufts of hair at base of claws; caudal margins of the maxillary bones forming an acute angle with midline of skull; basisphenoid pit double and shallow; postorbital region with sides widely diverging rostrally, in dorsal view; caudal margin of ascending ramus of dentary perpendicular to alveolar plane of dentary; I1 slightly projected rostrally and visible in lateral view, not being obscured by I2; mesostylar crest of M3 absent. A comparison of diagnostic characters between N. mexicanus, and other species of Natalus is summarized in table 5.

Description

Small to medium natalid (forearm length 34.0–40.6 mm; greatest skull length 14.9–16.8 mm; weight 3.5–8.0 g); muzzle long and dorsoventrally flattened; nostrils elliptical; opening ventrolaterally, sometimes at the end of tubelike projections, on shallow depression on margin of upper lip; upper lip thickened; lower lip markedly thickened and constricted along dorsal and ventral margin, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; natalid organ medium size and elliptical, extending from caudal base of rostrum to crown of head; ears medium sized (12.0–17.0 mm); ear pinna funnel shaped but distally thin, with markedly pointed tip, medial margin slightly concave, and lateral margin deeply concave; five to six small ear ridges along lateral margin of distal pinna; ventral region of pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus short, lanceolate, and twisted into helixlike structure; tibia (18.7–22.3 mm) slightly longer than half the length of the forearm; calcar long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively broad, with 3rd metacarpal (33.4–37.3 mm) similar in size to 5th metacarpal (33.1–37.2 mm); wings attach to tibia above ankle; pelage dense and lax; hairs long (8 mm, dorsally; 7 mm, ventrally); pelage usually darker dorsally than ventrally; pelage color from almost white ventrally and very light yellow brown dorsally to bright orange brown and chestnut brown both ventrally and dorsally (pl. 1); dorsal hairs bicolored, with tips darker than bases; ventral hairs usually monocolored; dense mustachelike hair tufts along lateral margins of upper lip and on dorsum of muzzle; mustache formed by dense, lax, irregularly arranged, and ventrally curved hairs; natalid organ covered with thin hairs; skull long and narrow with moderate rostral flexion; rostrum narrow, with shallow sulcus between nasals; maxilla dorsal to molars; braincase inflated, rising gently from rostrum; sagittal crest moderately developed; postorbital constriction narrow; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; caudal margin of palatal branch of maxilla forming an acute angle with longitudinal axis of skull; pterygoids nearly parallel; palate extending caudally to half the distance between bases and tips of pterygoids; basisphenoid pit shallow; longitudinal medial ridge on basisphenoid present; ectotympanic small, covering less than half of periotic; upper incisors short and peglike; I1 visible in lateral view, not being obscured by I2; occlusal profile of premolars long; upper premolars slightly increasing in size from P2 to P4; mesostylar crests on M1 and M2 short and straight, mesostylar crest absent on M3; cingular cusp of p4 medium sized and broad; molars cusps relatively broad; spinous process of humerus about as high as capitulum; thorax relatively short and wide; ribs markedly expanded craniocaudally and extensively in contact with one another; vertebrae C7 to T1 fused among themselves and to ribs; vertebrae T12–L4 fused entirely without vestige of sutures; vertebrae L5 and L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

Natalus mexicanus is one of the two smallest species in the genus Natalus, the other being N. lanatus. Its forearm is shorter than those of all insular (N. primus, N. major, N. jamaicensis, and N. stramineus) and South American (N. tumidirostris and N. espiritosantensis) representatives of the genus. The only distinct diagnostic external character of N. mexicanus is the shape of the medial margin of the ear, which is slightly concave, and seems intermediate in shape between the straight medial margin of N. lanatus, N. primus, N. major, and N. jamaicensis, and the markedly concave medial margin of N. tumidirostris, N. espiritosantensis, and N. stramineus. In addition, most N. mexicanus can be distinguished from N. tumidirostris by the large and nearly circular nostrils in this species versus small and elliptical nostrils in N. mexicanus. This trait, however, can be variable in N. tumidirostris (see Comparisons under the account of that species) and should thus be used in combination with other traits for a confident diagnosis of N. mexicanus. For a comparison of external morphology between N. mexicanus and its sympatric species N. lanatus, see Comparison under the account of the latter species.

Craniodentally, N. mexicanus is diagnosed by a combination of characters; therefore, identification must be done by elimination of species with which it may be confused. From the greater Antillean species N. mexicanus can be distinguished by forearm length (less than 40.6 mm in N. mexicanus, greater than 41.1 mm in Greater Antillean species). From N. stramineus it is distinguished by the position of its first incisors. In N. mexicanus, I1 is rostral to I2 in ventral view and in N. stramineus I1 is at the level of I2, so that it is not visible in lateral view. From N. tumidirostris it differs in its convex yet uninflated premaxilla (markedly inflated in N. tumidirostris) and in the caudal extension of the palate, which reaches 2/3 of the distance between the caudal edge of M3 and the tip of the pterygoids (the palate ands caudally at M3 or M2 in N. tumidirostris). Relative to N. espiritosantensis, N. mexicanus has a more slender skull and a longer tooth row, yet there are overlaps in measurements, therefore an appropriate differentiation of both species should be based also on external characters and geographic distribution. From Natalus lanatus, its sympatric species, N. mexicanus is distinguished by a deeper and less tapering rostrum in lateral view, more robust dentition, especially incisors and canines, caudal margins of maxillary bones, in ventral view, forming an acute angle with midline of skull, less globular braincase, and smaller sphenorbital fissure.

Variation

Males of N. mexicanus are slightly, yet significantly, larger than females in eight external and cranial measurements (table 15).

Size variation in N. mexicanus is due mostly to variation within populations rather than to variation among populations. Nonetheless, individuals from eastern Mexico (Tamaulipas to Chiapas) and Central America (Guatemala, Colombia [San Andrés and Providencia], and Panama) average larger in forearm length (fig. 29A) than individuals from western Mexico (Jalisco to Sonora and Baja California). This trend, however, is not uniform, because individuals from the Yucatan average smallest and those from the Isthmus of Tehuantepec average largest in most measurements. Differences in body proportions are slight, but specimens from Panama are notable in having a relatively shorter and wider rostrum (Fig. 29.fig. 29).

Fig. 29.

A, Plot of means (black dots), two standard deviations around the mean (gray bars), and two standard errors of the mean (vertical black lines) of forearm length of Natalus mexicanus from 10 geographic areas: A  =  N Peninsular Mexico (Baja California Sur; 16 males, 18 females; B  =  NW Mexico (Chihuahua, Sonora; 11 males, 12 females); C  =  W Mexico (Durango, Jalisco, Nayarit, Sinaloa; 29 males, 32 females); D  =  South Central Mexico (Guerrero, Morelos, Puebla; 8 males, 7 females); E  =  NE Mexico (Tamaulipas; 6 males, 11 females); F  =  Isthmic Mexico (Veracruz, Oaxaca; 30 males, 22 females); G  =  N Central America (Chiapas, Guatemala; 12 males, 6 females); H  =  Yucatan (Belize, Campeche, Guatemala [Petén], Quintana Roo, Yucatán; 30 males, 18 females); I  =  San Andrés and Providencia Isl., Colombia (3 males, 4 females); J  =  Southern Central America (Panama; 16 males, 9 females). Individuals from Isthmic Mexico, San Andrés and Providencia, and S Central America are significantly larger than those from the Yucatan, and W and NW Mexico (one-way ANOVA, P < 0.01).

Fig. 29

(continued). B, Plot of canonical scores for seven cranial measurements of N. mexicanus from nine geographic areas (same as above, San Andrés and Providencia not included). Variable loadings are listed in table 17. Three most divergent groups are distinguished: (1) individuals from the Yucatan characterized by overall small skulls; (2) individuals from Isthmic Mexico, characterized by large skulls and long rostra; and (3) individuals from Panama, characterized by large skulls and short rostra.

Natalus mexicanus exhibits the widest color variation of any natalid, but most is individual rather than geographic. Some individuals from the Isthmus of Tehuantepec (Los Tuxtlas, Veracruz, and Tehuantepec, Oaxaca) have the darkest pelage of any natalid, being rich chestnut brown dorsally, and slightly lighter ventrally. Some individuals from Baja California, conversely, are extremely pale, being pale buff dorsally and almost pure white ventrally. Most populations, however, exhibit color variants that range from buff to bright orange brown and yellow, and it is likely that the apparent lack of color variants within any one population is mostly due to small sample size.

Natural History and Conservation

N. mexicanus is known from 253 localities, in 85 of which this species has been taken at roost sites (63 are reported as caves, 21 as mines, two were hollow trees, and one was a drainage pipe under a road [Moreno, 1996]). Some reported localities for this species are represented by specimens not examined in this work; therefore may include misidentified specimens of Natalus lanatus.

Natalus mexicanus roosts in caves ranging from very large in linear extension (e.g., more than 10 km in linear extension, Gruta de Cacahuamilpa, Guerrero), to very small (e.g., less than 10 m, Cueva Chica, Baja California). Several individuals collected in Progreso, Guatemala, were taken from behind an overhanging rock where they roosted under full daylight together with a group of Glossophaga sp. (Goodwin, 1934). N. mexicanus is generally found in warm and humid caves, but avoids the warmest portions of such refuges; in a cave in Veracruz Hall and Dalquest (1963) observed it roosting in a relatively cool area at the entrance of a hot passage occupied by large colonies of Pteronotus personatus and Pteronotus davyi. Temperatures measured in N. mexicanus roosts have ranged between 17° and 27° C (Ávila-Flores and Medellín, 2004; Mitchell, 1965; personal obs.). The relative humidity of roost sites has been reported to range from 74% to 99% (Ávila-Flores and Medellín, 2004; Mitchell, 1965, McNab, 1969). On one occasion, I found the relative humidity of a roost as low as 54% (deep end of Cueva Chica, Baja California), but the bats caught there might have been displaced from a more sheltered (and perhaps more humid) location where the largest colony was found, due to disturbance created by human visitors. George G. Goodwin (personal commun. in Mitchell, 1965; as N. stramineus saturatus) mentioned that two groups of three to five individuals of N. mexicanus had been found in San Antonio, Oaxaca, roosting during the day in hollow trees in a limestone/karst area with thorn scrub vegetation.

Natalus mexicanus has been found coexisting in caves with 32 other bat species (Artibeus hirsutus, Artibeus jamaicensis, Artibeus lituratus, Balantiopteryx io, Balantiopteryx plicata, Carollia brevicauda, Choeronycteris mexicana, Desmodus rotundus, Diaemus youngi, Diphylla ecaudata, Glossophaga soricina, Glyphonycteris sylvestris, Leptonycteris nivalis, Leptonycteris yerbabuenae, Lonchorhina aurita, Macrotus californicus, Macrotus waterhousii, Micronycteris megalotis, Mimon cozumelae, Mormoops megalophylla, Myotis peninsularis, Myotis thysanodes, Myotis velifer, Myotis keaysi, Myotis nigricans, Plecotus townsendi, Pteronotus davyi, Pteronotus gymnonotus, Pteronotus parnellii, Pteronotus personatus, Pteropteryx macrotis, Tadarida brasiliensis; Arita, 1997). Still, it generally roosts separated from other species (Mitchell, 1965). While roosting, N. mexicanus hangs in loose aggregations from the walls of caves and tunnels and less frequently from ceilings, keeping a regular distance (of about 10 cm) between individuals (Mitchell, 1965). In the roost, individuals can be extremely quiet, allowing themselves to be hand-caught, or can fly away at the least indication of human presence (Hall and Dalquest, 1963; Mitchell, 1965). It has been found in caves on a variety of rock types, including limestone, volcanic rock, and loose sandstone. Groups of N. mexicanus appear to move between alternative caves. Hall and Dalquest (1963) noted that the number of individuals in a “lava cave” near San Andres Tuxtla, Mexico, changed on a daily basis, reaching a low of two bats on 2 January 1948, and a high of about 300 on 10 January 1948. Also, the population in Mina Armolillo, Sonora, decreased from about 1000 bats during November 1963–April 1964 to about 200 bats during June–July. During the later period, individuals banded in February in Mina Armolillo were found roosting in Mina Yeger (about 3 km south of Mina Armolillo), which never harbored N. mexicanus from August to March, and in Mina La Aduana (less than 1 km apart from Mina Yeger), which harbored a permanent colony of N. mexicanus that increased in size from June to July 1964. The emigration from Mina Armolillo coincided with late pregnancy, and lactation of N. mexicanus and with a marked increase in numbers of Leptonycteris sp. (identified as L. nivalis in the original account) and Glossophaga soricina in that mine (Mitchell, 1965).

Using niche models based on collection localities of the state of Michoacán, Wang et al. (2003) predicted that N. mexicanus would be found in tropical deciduous and semideciduous forests characterized by a 22°–26° C mean annual temperature and 800–1500 mm annual precipitation. In the rest of its range, however, the habitats of this species vary from desert scrub (Pescadero, Baja California, Mexico, 156 mm annual precipitation; locality 265) to degraded rain forest (Teapa, Tabasco, Mexico, above 3800 mm annual precipitation; locality 426). Also, it occurs in a wide variety of altitudes, ranging from sea level to 2300 m (Tlalpan, Mexico; locality 294). It is possible, however, that some of the high elevation localities of N. mexicanus may actually represent records of N. lanatus.

Although it is surely insectivorous, nothing is known of the diet of N. mexicanus. The reproductive pattern of a colony of N. mexicanus inhabiting Mina Armolillo, Sonora, was studied by Mitchell (1965) between 1964 and 1965. His study showed that N. mexicanus is monoestrous and bears a single pup per year. The gestation period was found to be very long, with copula and fertilization probably taking place during December or early January (when the males are at the height of spermatogenesis and the females begin to show implantation) and parturition around late July. In males, from June to October the testes were barely visible even upon dissection. Beginning in October, the testes increased in size from about 1.5 mm in length to slightly over 2.0 mm by the end of January, with a corresponding increase in seminal sperm counts.

All pregnant females examined by Mitchell (1965) between January and August always carried a single embryo exclusively in the left horn of the uterus. Between January and April the embryo showed little growth, although both anterior and posterior limb buds were well formed by the end of this period. The weight of the embryos increased from 0.01 g in early April to 0.3 g in late May, by which time the limbs (forearm  =  5 mm) and wing membranes were well formed. From this point on, the weight and forearm length of the embryos underwent an exponential increase, which ended about 20 days after birth for weight and 40 days after birth for forearm length. At birth, which took place between 12–20 July, newborns weighed 1.45–1.75 g and their forearms measured 11.0–16.0 mm. The fastest growth took place immediately after birth until weights leveled off at 2.8–4.4 g (about a 145% increase from birth weight) and forearm lengths at 34–35 mm (about a 185% increase from forearm length at birth). The end of the growth spurt in forearm length coincided with the onset of flight, which took place around late August. After the onset of flight, the weight of the young increased slowly but steadily until the observations ended on 26 February, by which time the bats had reached 5.7–6.2 g, nearly equalling the weight of the adults (5.7–6.6 g). During this period, forearm length increased more slowly than weight, but also attaining a range (35–38 mm) near that of adults (36–39 mm).

The N. mexicanus of Mina Armolillo were born naked and with eyes closed. Lightly haired young with eyes open were not seen until 7 August, about two weeks after birth. By 24 August, when the young were first observed to fly actively, their pelage had grown longer and was deep (or darkish) mouse gray on the tips and smoke gray basally. By 27 November, the pelage had grown even longer and was lighter in overall color, with hair tips drab and hair bases pale smoke gray. Two months later (26 February), body hairs of the subadults were still drab at the tips but had become even lighter basally (light grayish olive).

In Mina Armolillo, on 20 July, about 50 newborn N. mexicanus were found in a cluster on the wall, about 1 m from the floor and much closer to the entrance (about 18 m) than the areas where adults roosted (40–75 m away from the entrance). Three or four adult females, which were nursing their young within the cluster, flew away carrying the newborn bats with them when the cluster was approached by human observers. The cluster was formed by mixed haired and naked young, evidently of different ages. When the most advanced young were able to fly, they left the cluster and hung separately in its vicinity. These young still nursed, but some began to consume insects. Neither sex of N. mexicanus seems sexually mature in the first year.

Natalus mexicanus is the natalid most common in collections, being represented by at least 2491 museum specimens. The number of specimens per locality is more evenly distributed relative to that of other species. Colony sizes of N. mexicaus can be moderately large (e.g., about 1000 individuals, Mina Armolillo, Sonora), but are generally formed by only a few hundred bats (Alvarez, 1963; Hall and Dalquest, 1963), and some bats are occasionally found roosting solitarily (Cueva de Agua Caliente, Izabal).

The lyre snake Trimorphodon biscutatus has been reported to prey on N. mexicanus in Chamela (Sánchez-Hernández and Ramirez-Bautista, 1992). The fungus Histoplasma capsulatum was isolated from internal organs of two out of five Natalus from Morelos (Taylor et al., 1999). Lunaschi (2002) reported the trematode Ochoterenatrema labda (Digenea: Lecithodendriidae) as a parasite of this species.

Nocturnal emergence begins at about 30 min after sunset (Reid, 1997). Mitchell observed the N. mexicanus of Mina Armolillo begin their foraging 10–15 min before total darkness, with emergence lasting about 10 min. On 27 January 1964 only one bat remained in the mine immediately after the colony's emergence. The bats began returning to the cave 2 hours after emergence and continued entering and leaving the cave for the remainder of the night. Before emergence, most individuals were hanging near the entrance of the mine in a restless state, and when disturbed some flew out of the mine and hung in the vegetation outside until it became dark (Mitchell, 1965). During their foraging activity, N. mexicanus visits sources of drinking water (e.g., a swimming pool near Mina Armolillo; Mitchell, 1965).

The flight of N. mexicanus is slow and very maneuverable. Only a few bats were caught in two nets set over a swimming pool in Alamos, Sonora, even though many bats were observed drinking water from the pool (Mitchell, 1965). Even when some bats hit the net, they rarely became entangled and were able to fly off.

The echolocation calls of N. mexicanus have been described as very weak (low intensity) and hard to detect unless the bat is <0.5 m from the microphone. The search calls consist of short (about 2 ms) FM sweeps with most energy in the second harmonic at 100–130 kHz, but with occasional emphasis on the fundamental frequency. They are emitted at short and variable intervals and with a low duty cycle (Rydell et al., 2002). Miller (2004) stated that current echolocation call detection techniques are unsuited for detecting the low-intensity calls of N. mexicanus during foraging.

Natalus mexicanus is very susceptible to dehydration. Bats taken from the humid interior of Mina Armolillo (84% relative humidity) to the exterior (65% relative humidity) died within an hour, even though sheltered from the sun (Mitchell, 1965). Shaldach (in Nowak 1994) reported torpid N. mexicanus (indentified as N. stramineus) in a cave in Tamaulipas, in an oak forest area, with an outside temperature of 12° C.

Natalus mexicanus is listed as least concern in the IUCN Red List of Threatened Species (IUCN, 2010) ”]. Even though its separation from Natalus stramineus implies a marked range reduction for N. mexicanus, its abundance and large number of known localities indicate that its current IUCN status is correct.

Natalus primus Anthony, 1919

Figures 30, 31

Fig. 30.

Holotype of Natalus primus (AMNH 41009, fossil right dentary, image inverted). Scale bar  =  10 mm. Photo: Mariko Kageyama, AMNH (see appendix for institutional abbreviations).

Fig. 31.

Skull and mandible of Natalus primus (dorsal and lateral views plus mandible: AT 1, Pinar del Río, Cuba; ventral view: AT2, Pinar del Río, Cuba). Scale bar  =  5 mm.

Natalus primus Anthony, 1919: 642. Type locality “Daiquirí,” Santiago de Cuba, Cuba.

Natalus major primus: Goodwin, 1959: 10. New combination.

Natalus stramineus primus Varona, 1974: 33. New combination.

Natalus major: Tejedor et al., 2004: 153. Not Natalus major Miller, 1902.

Holotype

AMNH 41009, a fossil right dentary (fig. 30), collected by H.E. Anthony in 1917, Cueva de Los Indios (locality 28 in the appendix), Daiquirí, Santiago de Cuba, Cuba. The holotype is missing the coronoid process plus the incisors, canine, and first premolar, and is stained dark brown. (A second right dentary, designated by Anthony as a topotype, is in the vial with the holotype. It is complete, but lacks almost all teeth except p4 and m1).

Distribution

Cuba, Isle of Pines, the Bahamas (Abaco, Andros, New Providence, and Eleuthera), and Grand Cayman. There is only one locality (Cueva La Barca, Cuba; Tejedor et al., 2004) where live N. primus has been found and 14 localities where the species is represented by fossils (fig. 23).

Diagnosis

Largest living species in the genus Natalus (forearm length 46.1–51.2 mm, greatest skull length 18.1–19.9 mm); rostrum long; point of flexion between rostrum and braincase slightly caudal to rostral edge of orbit; medial and lateral ear margin straight; nostrils small, opening ventrolaterally; ventral hairs monocolored; dorsal hairs bicolored, hair bases lighter than tips; hairs at base of claws short and inconspicuous or long and thin, never forming tufts; premaxilla not inflated; maxilloincisive suture anterior to infraorbital foramen; maxilla dorsal to molars convex, not inflated; postorbital region with sides widely diverging rostrally; caudal margin of palate at 1/2 of the distance between M3 and tip of pterygoid; caudal margin of maxilla behind M3 nearly at right angle to longitudinal axis of skull; basisphenoid pits deep and steep sided; caudal margin of dentary forming a 70° angle with alveolar margin of lower molars; I1 visible in lateral view, not obscured by I2; mesostylar crest present on M3. Diagnostic characters contrasting N. primus with other species of Natalus are summarized in table 5.

Description

Size large (forearm length 46.1–51.2 mm; greatest skull length 18.1–19.9 mm; weight 6–12.6 g); muzzle very long and dorsoventrally flattened; nostrils elliptical, opening ventrolaterally at the end of short tubelike projections on shallow depression on margin of upper lip; upper and lower lips markedly thickened; lower lip markedly constricted at midline, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; ears long (20.2–21.2 mm); ear pinna very wide and funnel shaped, with moderately pointed tip; lateral and medial margins of pinna straight; four very small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus markedly short, lanceolate, and twisted into helixlike structure; tibia (25.4–29.1 mm) longer than half the length of the forearm; calcar very long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively long and wide, with 3rd metacarpal (43.2–49.0 mm) much longer than 5th metacarpal (40.0–44.8 mm); wings attach to tibia above ankle; pelage dense and lax; hairs long (8–9 mm) both dorsally and ventrally; hairs bicolored, with tips darker than bases; pelage color from drab with fuscous tips to buff with tips sepia; dense mustachelike hair tufts along lateral margins of upper lip; mustache formed by dense, lax, irregular, and ventrally curved hairs; skull long and narrow with moderate rostral flexion; rostrum long and narrow, with marked sulcus between nasals; moderate rostral palatal emargination; maxilla convex dorsal to molars; braincase greatly inflated, rising gently from rostrum; sagittal crest moderately developed; postorbital constriction narrow relative to skull length; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids slightly convergent; palate extending caudally to half the length of pterygoids; basisphenoid pit deep and steep sided; longitudinal medial ridge on basisphenoid present; ectotympanic large, covering about half of the periotic; upper incisors long, pointed, and slightly hooked; premolars markedly long in occlusal profile; upper premolars of similar size and not crowded; mesostylar crests on M1 and M2 long and broadly curved, mesostylar crest present on M3; cingular cusp of p4 short and broad; molars cusps relatively broad; spinous process of humerus about as high capitulum; thorax relatively short and wide; ribs greatly expanded craniocaudally with extensive contact among themselves; vertebrae C7 to T1 fused among themselves and to ribs; vertebrae T12–L4 fused entirely without vestige of sutures; vertebrae L5 and L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

Natalus primus is the largest of all extant Natalus, and overlaps only in range of forearm length with N. jamaicensis. N. primus can, therefore, be distinguished by size alone from most species in the family Natalidae, including those of the genera Chilonatalus and Nyctiellus. In addition to overall body size, N. primus differs from the genera Chilonatalus and Nyctiellus in generic level characters (table 3).

Externally, N. primus is unique within the genus Natalus in having a straight lateral ear margin, which gives the ear pinna a rather square shape with a broad tip. In all other Natalus, the lateral ear margin is concave or notched and the ear tip is much more pointed.

Cranially, Natalus primus is unlike any other species of Natalus in that its basisphenoid pits are very deep and steep sided (as in the genus Chilonatalus), while in the remaining species of the genus the basisphenoid pits are shallow. Also, in N. primus, the rostrum appears proportionately longer, relative to skull length, than in all other species of Natalus. This overall greater length of the rostrum in N. primus is the result of (1) the rostral elongation of the premaxilla, with an anterior projection of the incisors, and (2) the position of the dorsal point of flexion of the skull, which, in lateral view, lies caudal to the anterior edge of the orbit. In all other species of Natalus, the premaxilla is not markedly elongated, so that the incisors are at or near the level of the canines, and the dorsal point of flexion of the skull, in lateral view, lies dorsal to the anterior edge of the orbit. Finally, in N. primus, the posterior edge of the ascending ramus of the mandible forms an angle of about 70° with the alveolar plane of the lower molars, and usually shows a small rounded projection between the base of the angular process and the condyloid process. In all other species of Natalus, the caudal margin of the ascending ramus of the mandible is nearly perpendicular to the alveolar plane of the lower molars and the rounded process between the base of the angular process and the condyloid process is always absent.

Variation

On average, males of N. primus are heavier and have a longer tibia and a larger skull than females (Tukey; P < 0.05).

Tejedor et al. (2004) reported that the extant population from Cueva La Barca was significantly smaller in four cranial dimensions than a fossil sample (attributed to late Pleistocene; Silva-Taboada, 1974) from Central Cuba, but could not distinguish whether the difference was due to chronological or geographic variation. Comparison with fossil material (also attributed to late Pleistocene; Morgan, 1989, 1994) from the Bahamas and the Cayman islands indicates significant geographic differences among the three island groups (table 17, fig. 32). The N. primus from the Bahamas are largest, with little overlap in range of mental length with the sample of fossils from Cuba, and no overlap with the extant sample. The sample from Grand Cayman is the smallest and does not overlap in range with any of the Cuban samples, which are of intermediate size. In addition, the caudal margin of one dentary from Grand Cayman does not form an angle of about 70° with the alveolar plane of the dentary, a diagnostic trait of N. primus, but is rather perpendicular to the alveolar plane of the mandible. These differences suggest that N. primus as recognized here may represent a complex of allopatric species rather than a single widespread taxon. Future fossil finds in the Bahamas and Cayman Islands should help test this hypothesis.TABLE 18TABLE 19

Fig. 32.

Morphological variation among extant and fossil populations of Natalus primus. Populations: A  =  Abaco; B  =  Eleuthera; C  =  Cuba (extant); D  =  Cuba (fossil, topotype of N. primus); E, F  =  Grand Cayman.

TABLE 17

Loadings of the first two canonical axes of two canonical variates analyses (CVA) performed with 9 geographic samples of Natalus mexicanus

TABLE 18

Summary of measurements^a of Natalus primus

TABLE 19

Variation in mental length among extant and extinct populations of Natalus primus

Natural History and Conservation

Natalus primus is known from 22 localities but is known in the flesh from only one: Cueva La Barca (locality 130 in the appendix), Pinar del Río, Cuba, a large cave comprising several warm and humid chambers (including a hot chamber) and one permanent pond. In Cueva La Barca, N. primus occupies rather well-ventilated areas of the warm chambers, roosting almost exclusively along the east walls, which are more sinuous than the west walls and are farther from entrances. Roosting groups contain a few dozen to a few hundred bats. Individual bats hang from one or both feet without ventral contact with the substrate and regularly spaced from each other, keeping a distance between themselves of about 10 cm. The roosting groups scatter on the lower parts of walls, at about 1 m from the floor, and occasionally on the low roofs of wall niches. Specific roosting spots were regularly occupied by similarly sized groups of N. primus in all visits to the cave, indicating that seasonal migrations out of Cueva La Barca are unlikely.

Ten other bats (Phyllonycteris poeyi, Pteronotus quadridens, Pteronotus macleayi, Pteronotus parnellii, Mormoops blainvillei, Brachyphylla nana, Erophylla sezekorni, Monophyllus redmani, Artibeus jamaicensis, and Chilonatalus macer) roost together with Natalus primus in Cueva La Barca, yet none were ever observed in mixed groups. Groups of N. primus sometimes roost adjacent to groups of M. blainvillei (which also appear to favor the cave's walls as roosting areas). Captive N. primus individuals are aggressive and frequently attack bats of other species, even of larger size, if confined together in a small enclosure.

In general, individuals of N. primus remain active while roosting during the day, taking flight at the slightest sign of disturbance (human steps, distant glare from a flashlight), but usually some individuals allow the extreme close proximity of the observer for a few seconds. If disturbance (e.g., artificial illumination) persists for some minutes, all bats move to alternative roosting areas of the same chambers, joining the groups that may already be present there. When moving to other areas inside the cave, the bats invariably fly extremely close to the walls and about 1 m from the floor, forming a highly distinctive, continuous stream of bats along the wall. No N. primus was ever captured with a butterfly net more than 2 m away from any cave wall. Cueva la Barca is located in an area of nearly undisturbed semideciduous forest of moderate precipitation (1402 mm), near sea level.

Analysis of stomach contents obtained at dawn on 23 July 1993 revealed that the bats had consumed insects belonging to eight orders. The most commonly represented groups were: Lepidoptera, Orthoptera (Gryllidae), and Coleoptera. The remaining orders (represented by single cases) were Hymenoptera (Formicidae), Neuroptera, Diptera, Homoptera, and Hemiptera.

The reproductive activity of N. primus is largely unknown. Three females collected on 1 May 1992 were pregnant, each holding a single large embryo. At midday, on 17 April 1993, most N. primus groups were observed to have abandoned their usual roosting areas in Cueva La Barca and moved to the entrance of the hot chamber. Most of the N. primus groups observed in this unusual location were composed of what appeared to be copulating pairs, which were much more easily approached by humans than isolated bats. The long period of pregnancy reported for other species of Natalidae (e.g., Nyctiellus, Silva-Taboada, 1979; Natalus mexicanus, Mitchell, 1965), however, indicates that such pairing between individuals of N. primus may represent a behavior other than copulation.

With 58 museum specimens, N. primus is relatively well represented in collections despite being known from a single extant colony. On July 1993, visual estimates indicated that a few thousand Natalus primus inhabited Cueva La Barca. Observations made as recently as August 2001 suggest that this bat remains common in the cave (F. Balseiro, personal commun.). It may be an occasional prey of owls, as suggested by fossil remains of this species found in an early Holocene deposit accumulated at least partially through the feeding activity of the barn owl (Tyto alba; Jimenez-Vázquez et al., 2005).

The flight of Natalus primus is extremely slow and highly maneuverable. Several individuals released during the day in the forest outside the cave entrance showed a greater tendency and ability to fly through highly cluttered understory vegetation than most other species (except Chilonatalus macer) present in Cueva La Barca. Given the slow flight of this bat and its high rate of dehydration outside the cave (as judged by the rapid increase in brittleness of patagia of handled animals) it is probable that its foraging range is relatively small. On two occasions (April and July 1993) the species was not seen inside the cave between 22:00 and 24:00 hr and animals collected early in the morning on 23 July 1993 had full stomachs indicating that foraging may extend until daybreak. The permanent pool of Cueva La Barca might serve as source of drinking water for N. primus. The echolocation calls of N. primus are unknown, but it produces weak and high-pitched audible sounds when held in the hand.

Natalus primus is a critically endangered bat (IUCN 2006). The only known extant population of N. primus (i.e., that of Cueva La Barca) appears to be a relict of what was a widespread species that ranged throughout most of Cuba, the Bahamas, and the Cayman Islands. This dramatic reduction in range appears to have begun in the late Pleistocene and to have extended into the late Holocene (Silva-Taboada, 1974, Tejedor et al., 2004), suggesting a population decline that may have continued until the present. Cueva La Barca is thus far protected from human disturbance by its remoteness in Guanahacabibes Peninsula, but it may soon become more accessible as Cuba opens its remote areas to tourism (Díaz-Brisquet and Pérez-López, 2000). Although 1992 estimates indicated a relatively large population of Natalus primus (Tejedor et al., 2004), its current population trend is unknown and should be evaluated to adequately formulate conservation plans for this species.

Natalus stramineus Gray, 1838

Figure 33

Fig. 33.

Holotype of Natalus stramineus (BMNH 70.2324, male, collection locality unknown).

Natalus stramineus Gray, 1838: 496. Original description based on unspecified material of unknown geographic origin deposited at the BMNH. Handley and Gardner (1990) deduced that this taxon's description must have been based on the specimen numbered BMNH 70.2324.

Natalus dominicensis Shamel, 1926: 67. Subjective synonym. Original description based on material (USNM 113605) from the island of Dominica.

Holotype

Holotype by monotypy, BMNH 70.2324, adult male in alcohol with skull removed; collector and collection locality unknown. The skull lacks parts of the left temporal but is otherwise complete. The skin is in good condition although both tibiae and 15 finger bones are broken.

Distribution

Islands of the Lesser Antilles north of the St. Lucia Channel: Anguilla, Antigua, Barbuda, Dominica, Guadeloupe, Marie Galante, Martinique, Montserrat, Nevis, Saba, and St. Maarten (skeletal remains only; fig. 23).

Note

The name Natalus stramineus has been historically applied to populations of the genus Natalus from virtually the entire Neotropics. The original description of Natalus stramineus (Gray, 1838), however, gives no indication of the geographic origin of the holotype, leading to widespread confusion concerning the nomenclature, and geographic and taxonomic limits of species of Natalus. The type locality of N. stramineus was listed as Brazil for about a century (Cabrera, 1957; Carter and Dolan, 1978; Dobson, 1878). Despite claims that the type locality was in the Lesser Antilles (Goodwin, 1959; Handley and Gardner, 1990), opinions that it could actually be in Brazil persisted (Taddei and Uieda, 2001). This conflict was compounded by the fact that N. stramineus was assumed to range throughout South America, and to be sympatric with N. tumidirostris to the north of the Amazon (Dávalos, 2005; Koopman, 1981; Simmons, 2005; Soriano and Ochoa, 1997). Recently, Tejedor (2006), on the basis of the inflated premaxilla of the holotype of N. stramineus, confirmed that the type locality of this species is in the northern Lesser Antilles (although the specific island remains uncertain) and showed that N. tumidirostris is the only taxon that occurs in South America north of the Amazon.

Diagnosis

Medium-sized representative of genus Natalus (forearm length 37.2–40.0 mm, breadth across canines (3.8–4.2 mm) large in relationship to skull length; maxillary tooth row (6.8–7.5 mm) medial margin of ear deeply concave; lateral margin of ear deeply notched, 5–6 folds on lateral margin of ear; nostrils small, opening ventrolaterally; ventral hairs monocolored; dorsal hairs bicolored, hair bases lighter than tips, hair at base of claws short and inconspicuous or long and thin, never forming tufts; premaxilla inflated, with a lateral profile nearly forming a straight angle between rostral plane of premaxilla and dorsal plane of nasals; maxilloincisive suture dorsal to infraorbital foramen, maxilla dorsal to molars convex, not inflated; sides of postorbital region widely diverging rostrally, in dorsal view; palate between pterygoids ending caudally at two thirds of the distance between M3 and tip of pterygoid; posterior margins of maxilla, in ventral view, forming an oblique angle with longitudinal axis of skull; basisphenoid pits shallow; caudal margin of ascending ramus of mandible perpendicular to alveolar margin of dentary; I1 not visible in lateral view, obscured by I2; mesostylar crest on M3 absent. A comparison of diagnostic characters between N. stramineus, and other species of Natalus is summarized in table 5.

Description

Medium-sized natalid (forearm length 36.9–41.9 mm; greatest skull length 15.7–17.5 mm; weight 4.6–5.3 g); muzzle long and dorsoventrally flattened; nostrils elliptical, opening ventrolaterally on shallow depression on margin of upper lip; upper lip thickened; lower lip markedly thickened and constricted along midline, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; natalid organ medium size and elliptical, extending from caudal base of rostrum to crown of head; ears relatively long (14.6–17.5 mm); ear pinna funnel shaped but distally thin; pinna with markedly pointed tip; medial margin of pinna slightly to deeply concave; lateral margins of pinna deeply concave; five to six small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus short, lanceolate, and twisted into helixlike structure; tibia (19.8–23.2 mm) slightly longer than half the length of the forearm; calcar long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively long and pointed, with 3rd metacarpal (33.8–38.1 mm) longer than 5th metacarpal (33.3–37.0 mm); wings attach to tibia above ankle; pelage dense, lax, and slightly woolly; hairs long (8–9 mm, dorsally; 6–7 mm, ventrally); dorsal hairs slightly bicolored, with bases lighter than tips; ventral hairs monocolored; dorsal hairs smoke gray with wood brown tips to amber or orange brown with medium brown tips (pl. 1); ventral hairs pale smoke gray or pinkish buff to light amber-chestnut or orange brown; dense mustachelike hair tufts along lateral margins of upper lip and on dorsum of muzzle; mustache formed by dense, lax, irregularly arranged, and ventrally curved hairs; natalid organ covered with thin hairs; skull long and relatively broad with moderate rostral flexion; rostrum wide and short, with sulcus between nasals shallow; moderate rostral palatal emargination; premaxilla moderately to markedly inflated; maxilloincisive suture slightly to markedly displaced caudally, sometimes dorsal to infraorbital foramen, in lateral view; maxilla convex above molars; braincase moderately inflated, rising gently from rostrum; sagittal crest moderately developed; postorbital constriction wide; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids nearly parallel; palate extending caudally to more than half the distance between bases and tips of pterygoids; basisphenoid pit shallow; longitudinal medial ridge on basisphenoid present; ectotympanic small, covering less than half of periotic; upper incisors short and peglike; I2 obscuring I1 in lateral view; occlusal profile of premolars long; upper premolars of similar size; mesostylar crests on M1 and M2 short and straight, mesostylar crest absent on M3; cingular cusp of p4 medium sized and broad; molars cusps relatively broad; spinous process of humerus about as high as capitulum; thorax relatively short and wide; ribs markedly expanded craniocaudally and extensively in contact with one another; vertebrae C7 to T1 fused among themselves and to ribs; vertebrae T12–L4 fused entirely without vestige of sutures; vertebrae L5 and L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

The inflation of the premaxilla and the associated caudal displacement of the maxilloincisive suture is sufficient to distinguish N. stramineus from other species of Natalus as herein restricted. In most specimens of N. stramineus from the northern Lesser Antilles, the maxilloincisive suture is dorsal to the infraorbital foramen, whereas in specimens from the central Lesser Antilles and in all other species of Natalus this suture is located more anteriorly, at about 1/3 of the distance between the infraorbital foramen and the anteriormost margin of the premaxilla (plates 8, 14; table 1). Also, in specimens with an inflated premaxilla, in lateral view, the anterior and dorsal planes of the premaxilla form a nearly right angle in N. stramineus, whereas in all other Natalus this angle is obtuse, particularly so in N. tumidirostris. Specimens of N. stramineus that lack the inflated premaxilla can be distinguished from other species of Natalus by a combination of characters including size, discrete traits, and cranial proportions.

On the basis of body size alone, Natalus stramineus can be distinguished from the large Greater Antillean species N. primus, N. major, and N. jamaicensis. The observed range of forearm length in N. stramineus (37.2–41.9 mm) overlaps only slightly with that of N. major (41.1–45.0 mm, P < 0.01; table 1), the smallest of the Greater Antillean species. On the other hand, N. stramineus is slightly larger than the North American Natalus lanatus, and the North and Central American N. mexicanus (table 2), but from these species, N. stramineus is more easily distinguished by external and cranial characters. Whereas in N. stramineus the medial ear margin is concave (usually as much as the lateral ear margin), in N. lanatus it is straight. In addition, N. lanatus has shorter legs (length of tibia in fresh or fluid-preserved specimens, 16.2–19.2 mm) than N. stramineus (length of tibia 19.8–21.5 mm, P < 0.01). From N. mexicanus, N. stramineus can be distinguished by its upper incisors, which are at the same level in ventral view, whereas in N. mexicanus the caudal base of I1 is rostral to the caudal base of I2.

Natalus stramineus is most similar in size and external characters to the South American N. tumidirostris and N. espiritosantensis. From N. tumidirostris, N. stramineus can be separated by its small, oval, and ventrolaterally oriented nostrils (larger, usually circular, and more anteriorly facing in N. tumidirostris) and by a palate extended caudally between the pterygoids (the palate is emarginated in N. tumidirostris). Relative to N. stramineus, N. espiritosantensis has a more robust, shorter rostrum (reflected in its shorter maxillary tooth row, P < 0.01; table 5).

Variation

The sample of Natalus stramineus examined for this study showed significant sexual, geographic, and individual variation. Males were significantly larger than females in two external and four cranial dimensions (MANOVA, P < 0.05; table 20). Canonical variate analyses between four geographic samples (Anguilla, Antigua + Barbuda, Saba + Montserrat, Dominica), using four external and seven cranial dimensions, indicate that the sample from Dominica is morphometrically distinct from that of the remaining islands, in particular with longer 3rd metacarpals (fig. 34A) and narrower breadths across canines (fig. 34B). The three available skins from Anguilla are grayish brown (smoke gray at base and wood brown at tips, with an overall drab appearance), whereas those from the remainder of the range have a reddish amber brown to tawny olive brown pelage.

Fig. 34.

Canonical variates analyses (CVA) scores for external (A) and cranial (B) measurements of populations of Natalus stramineus from 6 Lesser Antillean islands: (•) Antigua + Barbuda, females; (▪) Antigua + Barbuda, males; (⧫) Anguilla, males; (•) Montserrat + Saba, females; (▪) Montserrat + Saba, males; (○) Guadeloupe, females; (□) Guadeloupe, males. Axes are scaled relative to their eigenvalues. The first canonical axes can be interpreted as a measure of the length of the 3rd metacarpal (A) and of breadth across canines (B; table 21).

TABLE 20

Summary of measurements^a of Natalus stramineus

TABLE 21

Loadings of the first two canonical axes of two canonical variates analyses (CVA) performed with 4 geographic samples of Natalus stramineus

The morphology of the rostrum showed both geographic and individual variation. The inflation of the premaxilla that characterizes the holotype of N. stramineus was present in all specimens from Anguilla, Barbuda, and Antigua, and in one female from Saba and another from Montserrat. Two adult females and one adult male from Saba, however, lacked this trait, being indistinguishable, at least cranially, from specimens from Guadeloupe and Dominica.

Natural History and Conservation

Natalus stramineus is known from 35 localities (including three represented only by bone remains), 15 of which have been caves. It is found both in the volcanic inner-arc islands (Saba, Nevis, Montserrat, Dominica, and Martinique) and in the limestone outer-arc islands (Anguilla, St. Maarten, Barbuda, Antigua, Guadeloupe (Grande-Terre), Marie Galante; Baker et al., 1978; Genoways et al., 2001; Pedersen et al., 2003, in press). In Dominica, in addition, it has been taken in a brick tunnel (Genoways et al., 2001). On Nevis, it has been found in a small, humid cave (3 m wide by 6 m high) that is not permanently occupied throughout the year (Pedersen et al., 2003). In Dominica, it has been found coexisting with several thousand Pteronotus davyi in a narrow cave opening on a sandy cliff (Genoways et al., 2001).

Natalus stramineus occurs from sea level to middle elevations and in habitats ranging from relatively dry (e.g., Barbuda, 925 mm annual precipitation; locality 7) to rain forest (e.g., Sylvania, Dominica, 3232 mm; locality 171) and from sea level to 473 m (locality 171).

Although its diet has never been studied, N. stramineus is surely insectivorous, as are other representatives of Natalidae (e.g., Nyctiellus lepidus, Silva-Taboada, 1979; Natalus primus, Tejedor et al., 2004).

It is known from 114 museum specimens, most of which are from the islands of Dominica (77), Barbuda (12), and Saba (8), where it seems to be a common bat. The records from Marie Galante, and Martinique, the last of which is known from a mention in A. Schwartz's research notes (Timm and Genoways, 2003), are based on a single specimen each.

Little is known of reproductive activity in N. stramineus but it may be concentrated earlier in the year than in other species of Natalus from the West Indies. Females taken in April in Dominica included lactating, nonpregnant, and pregnant individuals, yet a sample from July was composed entirely of nonreproductive females (Genoways et al., 2001). N. stramineus is parasitized by the streblid Trichobius caecus (Genoways et al., 2001).

In an ecomorphological study, Jennings et al. (2004) stated that N. stramineus stramineus can fly very slowly in clutter and that it hunts by slow hawking and/or by gleaning. They found that N. stramineus produced multiharmonic FM echolocation calls with most energy in the second harmonic. The greatest energy of the fundamental frequency was centered around 60 kHz, and that of the second harmonic at 90–100 kHz. The duty cycle was intermediate (Jennings et al., 2004).

Natalus stramineus is listed as least concern in the current global red list of threatened species (IUCN, 2010) However, its small, naturally fragmented geographic range, and its apparent requirement for humid caves, point to a limited availability of suitable habitat and therefore to a vulnerable status. The species seems, nonetheless, locally common in at least four islands (Antigua, Barbuda, Dominica and Saba; Genoways et al., 2001; S.C. Pedersen, personal commun.), and future surveys may increase the number of islands where it is known to occur. On Nevis, it has been encountered less frequently, with the single specimen in museum collections from that island having been killed accidentally by a ceiling fan (Pedersen et al., 2003). In Martinique, it is also known from a single individual (Timm and Genoways, 2003), and in St. Maarten, it has been recorded exclusively from a skull and partial skeleton found in a cave (Genoways et al., 2007). In Montserrat, an island where bat populations have been severely affected by recent volcanic eruptions (Pedersen, 2003), the only known population of N. stramineus occurs in Aymers Ghaut (S.C. Pedersen, in litt.), one of the island's valleys most vulnerable to devastating pyroclastic flows and lahars (Baker, 1985). If N. stramineus does not occur in other, undiscovered sites on Montserrat, its long-term survival on that island seems highly uncertain.

Natalus tumidirostris Miller, 1900

Figure 35

Fig. 35.

Holotype of Natalus tumidirostris (USNM 102106, male, Curaçao). Scale bar  =  10 mm.

Natalus tumidirostris Miller, 1900: 160. Type locality “Hatto, Curaçao, Netherlands Antilles.”

Phodotes tumidirostris: Miller, 1906: 85. New combination.

Phodotes tumidirostris continentis Thomas, 1910: 513. Type locality “San Esteban, Carabobo, Venezuela”; holotype, BMNH 5.11/12.25.

Natalus tumidirostris tumidirostris (part): Goodwin, 1959: 11. New combination.

Natalus tumidirostris continentis (part): Goodwin, 1959: 11. New combination.

Natalus tumidirostris haymani: Goodwin, 1959: 12. Type locality “Mt. Tamana, Trinidad, Trinidad and Tobago”; holotype, AMNH 176590.

Natalus stramineus tronchonii: Linares, 1971: 81. Type locality “Cueva de los Gavilanes, Rio Guasare, Zulia, Venezuela”; holotype, MBUCV 1578.

Natalus stramineus: Linares, 1998: 515. Not Natalus stramineus Gray, 1838.

Holotype

USNM 102106, adult male, skin in alcohol with skull removed, collected by L.J. Guthrie on 5 January 1900, in Hatto [ = Hato] (locality 467 in appendix 1), Curacao, Netherlands Antilles. Both the skin and skull are in good condition but the skin color has faded due to long immersion in alcohol.

Distribution

Mainland South America north of the Amazon River in the countries of Colombia, Venezuela, Guyana, Suriname, and French Guiana, and also on the islands of Trinidad, Tobago, Margarita, Curaçao, and Bonaire. Although to date it has not been reported from Brazil it very likely occurs there given that three collection localities (two in Guyana and one in Suriname) lie less than 15 km from the border with that country (fig. 36).

Fig. 36.

Geographic distribution of Natalus tumidirostris. Solid circles indicate localities where the species has been collected alive. Open symbols indicate localities represented by bone remains only. Names of localities are listed in appendix 1. Gray shading on land indicates relief, with darknes increasing with altitude.

Diagnosis

Size medium (forearm length 35.0–42.0mm), medial margin of ear pinna deeply concave; lateral margin of ear pinna deeply notched; nostrils usually large, opening anteriorly; maxilla above molars convex and markedly inflated; palate ending caudally always rostral to optic canal; ventral pelage monocolored; dorsal pelage monocolored or, if bicolored, hair bases lighter than tips; hair at base of claws short and inconspicuous or long and thin, never forming tufts; caudal margins of maxilla in ventral view forming an acute angle with longitudinal axis of skull; basisphenoid pit shallow; postorbital region with sides widely diverging rostrally, in dorsal view; caudal margin of ascending ramus of mandible perpendicular to alveolar margin of dentary; I1 not visible in lateral view, being obscured by I2; mesostylar crest of M3 absent. A comparison of diagnostic characters between N. tumidirostris, and other species of Natalus is summarized in table 5.

Description

Size medium (forearm length 35.0–42.0 mm; greatest skull length 15.5–17.3 mm; weight 4.3–8.9 g); muzzle long and dorsoventrally flattened; nostrils often wide and nearly circular, rarely elliptical; opening anteriorly on shallow depression on margin of upper lip; upper lip thickened; lower lip markedly thickened and constricted along dorsal and ventral margin, with numerous transversal grooves; small, smooth central pad on dorsal margin of lower lip; natalid organ medium size and elliptical, extending from caudal base of rostrum to crown of head; ears medium sized (13.0–16.4 mm); ear pinna funnel shaped but distally thin; pinna with markedly pointed tip; medial and lateral margins of pinna deeply concave; five to six small ear ridges along lateral margin of distal pinna; ventral region of ear pinna greatly expanded, covering the eye and tragus in lateral view; medial ear margin thin and flexible; tragus short, lanceolate, and twisted into helixlike structure; tibia (18.9–22.4 mm) slightly longer than half the length of the forearm; calcar very long and thin, occupying about half the length of the free edge of uropatagium; free margin of uropatagium with sparse fringe of thin hairs; wings relatively broad, with 3rd metacarpal (33.7–38.7 mm) slightly longer than 5th metacarpal (30.4–38.3 mm); wings attach to tibia above ankle; pelage dense and lax; hairs long (7–9 mm, dorsally; 6–7 mm, ventrally); pelage usually darker dorsally than ventrally; pelage color from almost white ventrally and very light brown dorsally to bright orange brown both ventrally and dorsally (pl. 1); dorsal hairs bicolored, with tips darker than bases; ventral hairs usually monocolored; dense mustachelike hair tufts along lateral margins of upper lip and across muzzle; mustache formed by dense, lax, irregularly arranged, and ventrally curved hairs; natalid organ covered with thin hairs; skull long and relatively broad with moderate rostral flexion; rostrum wide, with sulcus between nasals almost imperceptible; moderate rostral palatal emargination; maxilla inflated, obscuring molars in dorsal view; braincase inflated, rising abruptly from rostrum; sagittal crest moderately developed; postorbital constriction wide; maxillary branch of zygomatic arch thin, less deep than twice the height of crowns of last molars; pterygoids nearly parallel; palate extending caudally to level of M2 or M3; basisphenoid pit shallow; longitudinal medial ridge on basisphenoid present; ectotympanic small, covering less than half of periotic; upper incisors short and peglike; I2 obscuring I1 in lateral view; occlusal profile of premolars long; upper premolars of similar size; mesostylar crests on M1 and M2 short and straight, mesostylar crest absent on M3; cingular cusp of p4 medium sized and broad; molars cusps relatively broad; spinous process of humerus about as high as capitulum; thorax relatively short and wide; ribs markedly expanded craniocaudally and extensively in contact with one another; vertebrae C7 to T1 fused among themselves and to ribs; vertebrae T12–L4 fused entirely without vestige of sutures; vertebrae L5 and L6 free; caudal vertebrae 4 to 7 longer than distance from ischium to iliac crest of sacrum.

Comparisons

Fenestration of the palate is more extensive in N. tumidirostris than in any other species of Natalus. All palatal fenestrae, the interpterygoid and the intermolar, are very large and can coalesce with each other in various ways creating three main patterns: (1) all fenestrae separate, caudal edge of palate nearly at level with the caudal margin of M3 (common in individuals from Colombia); (2) intermolar fenestrae coalesced and separate from interpterygoid fenestrae, caudal edge of palate nearly at level with caudal margin of M3 (common in individuals from Sierra de Perijá); (3) all fenestrae coalesced forming deep palatal emarginations that reach caudal margin of M1 (common in individuals from the center and east of the species' range). Occasionally, the degree of coalescence of the fenestrae is not symmetrical within a single individual, creating a combination of any two of the patterns mentioned above. In N. tumidirostris, thus, the caudal edge of the palate lies at the caudal margin of M1 or M3 whereas in all other species of Natalus the caudal margin of the palate lies at 1/2–2/3 of the way between the caudal margin of M3 and the tip of the pterygoid processes. Also, in all other species of Natalus, the intermolar palatal fenestrae, if present, are usually small and only rarely coalesce.

In Natalus tumidirostris, the maxillae are conspicuously inflated (although less so in individuals from Colombia and western Venezuela) and in dorsal aspect may hide the molars from view. In all other Natalus the labial margins of the molars are visible in dorsal view. In most specimens of N. tumidirostris, in lateral aspect, the rostral surface of the premaxilla forms a shallow (obtuse) angle with the dorsal surface of the nasals, whereas in all other species of Natalus this angle is less obtuse (even straight, in N. stramineus). Also in lateral view, the dorsal surface of the nasals of N. tumidirostris is more parallel with the alveolar margin of the maxilla than in other species of Natalus, making the rostrum of this species appear relatively deeper anteriorly. In all other species of Natalus, especially in N. lanatus and N. primus, the rostrum tapers anteriorly more markedly.

Externally, Natalus tumidirostris can be distinguished from N. mexicanus, N. lanatus, N. primus, N. major, and N. jamaicensis by its concave medial margin of the ear. In N. tumidirostris, the medial margin of the ear pinna is almost as concave as the lateral margin, so that the ear tip appears acutely pointed. In the remaining aforementioned species, the medial margin of the ear pinna is straight to very slightly concave, so that the ear tip appears less acutely pointed. In most cases, N. tumidirostris can be distinguished from other species of the genus by the shape and size of its nostrils. The nostrils of N. tumidirostris tend to be as large as the external nasal septum, circular, and forwardly oriented. The nostrils of other species of Natalus are always smaller than the external nasal septum, elliptical, and usually oriented ventrolaterally. In some individuals of N. tumidirostris (as is common in Sierra de Perijá and on the island of Trinidad), however, these traits are less noticeable and the nostrils are similar in shape as in other species of the genus; thus, the shape of the nostrils should be used in combination with other traits, especially cranial ones, for a confident diagnosis of N. tumidirostris.

Natalus tumidirostris has a longer forearm and skull than N. mexicanus and N. lanatus. It is, however, smaller than the three Greater Antillean species N. primus, N. major, and N. jamaicensis. N. tumidirostris overlaps widely in size with two other species of the genus: N. espiritosantensis and N. stramineus. Nonetheless, its toothrow length is larger than that of N. espiritosantensis. From N. stramineus, N. tumidirostris is best identified on the basis of qualitative characters only.

Variation

Gómez-Laverde (1986) reported that young adults (individuals with fused epiphyses and silky grayish pelage) from Cueva de Macaregua, Colombia, had a mean zygomatic breadth significantly smaller than that of (older) adults with brownish or yellowish pelage.

Pelage color varies widely in Natalus tumidirostris. Some specimens from Cueva Ricardo Zuloaga, state of Miranda, Venezuela, are bright orange brown, whereas most individuals from Paraguaná peninsula are extremely pale, being pale buff dorsally and pale cream to white ventrally. The palest individuals from Paraguaná, in addition, show an extreme lack of skin melanin, having entirely light pink faces and ears. Several color variants are usually present in a single population, and it seems that the apparent lack of variants within a population is due primarily to small sample size.

Male Natalus tumidirostris are larger than females in 10 of 14 measurements (P < 0.05; table 22). Females from Colombia, however, had a longer forearm than males from Colombia, offsetting the species-wide sexual difference in this trait (interaction effect P < 0.05).

TABLE 22

Summary of measurements^a of Natalus tumidirostris

Natalus tumidirostris is the most geographically variable of the four continental species of Natalus. Four populations (Perijá, Paraguaná, Curaçao-Bonaire, and Trinidad) showed no overlap in a canonical variate analysis based on one external (forearm length) and seven skull measurements. Specimens from Colombia, the coastal ranges of northern Venezuela, Venezuelan Guiana, and Trinidad are the largest in both external and internal measurements, whereas populations from Perijá, and Curaçao-Bonaire were the smallest. Specimens from Paraguaná were characterized by a relatively short forearm but a relatively large skull (P < 0.05, fig. 37).

Fig. 37.

Plot of canonical scores of forearm length and six cranial variables of Natalus tumidirostris from nine geographic areas: A  =  Colombia; B  =  Perijá (Zulia); C  =  Paraguaná; D  =  Curaçao; E  =  Continental Falcón; F  =  Coastal Cordillera; G  =  Guyana Shield (Bolívar); H  =  Sucre; I  =  Trinidad. Variable loadings are shown in table 23. Four areas contain morphometrically divergent populations: (1) Curaçao, characterized by bats of overall small size; (2) Paraguaná, characterized by bats with short forearms and large skulls; (3) Perijá, Characterized by bats with long forearms and small skulls; and (4) Trinidad, characterized by bats with overall large body size.

TABLE 23

Loadings of the first two canonical axes of two canonical variates analyses (CVA) performed with 9 geographic samples of Natalus tumidirostris

Inflation of the maxilla is less marked in animals from the western part of the range (Colombia, Perijá). Similarly, fenestration of the palate is less extensive in specimens from the western part of their range, especially in animals from Sierra de Perijá (pl. 7).

Note

The population from Perijá was originally described as a subspecies of N. stramineus (N. s. tronchonii) by Linares (1971) mainly on the basis of a supposedly unique pattern of palatal fenestration. Upon examining the skull of the holotype of N. s. tronchonii, I found that it had been incompletely cleaned and that the remaining soft tissue obscured a pattern of palatal fenestration similar to that of specimens of N. tumidirostris from Colombia.

Natural History and Conservation

Natalus tumidirostris is known from 64 localities, including two represented by bone remains only. In 33 of the collection localities it has been found at day roosts, almost all being caves (30) and mines (2), except for a group of three individuals found roosting in a hollow rubber tree near Tamana caves (Goodwin and Greenhall, 1961). Natalus tumidirostris has been found in caves varying from medium (e.g., Cueva Pararille; De Bellard Pietri, 1969) to large size (e.g., Ricardo Zuloaga, De Bellard Pietri, 1969), although it also probably occupies caves of smaller sizes. As in other species of Natalus, N. tumidirostris roosts in caves that are warm and humid, but avoids the warmest areas within the caves. In a study performed in Cueva del Guano and Cueva Piedra Honda (listed as “Cueva Barra Honda”), Paraguaná, Venezuela, N. tumidirostris selected roost sites of about 30° C but moved to warmer (33° C) or cooler (28° C) spots when disturbed (Genoud et al., 1990). Some of the caves inhabited by N. tumidirostris may contain high levels of ammonia (e.g., Cueva Ricardo Zuloaga). Most caves known to harbor N. tumidirostris are formed in limestone. Linares and Löbig-A. (1973) mentioned that N. tumidirostris shifts roosting caves throughout the year.

Roosts of Natalus are unknown in the Guyana Shield (southern Venezuela, the Guianas, and extreme northern Brazil), and all 12 records of the genus from this area correspond to captures with mistnets. In the Guyana shield, however, other cave-dwelling bats (i.e., mormoopids, Lonchorhina) have been found in caves formed by the accumulation of large boulders around the eroding Precambrian granite inselbergs that dominate the Guianan landscape. It is therefore likely that on the Guianan shield Natalus tumidirostris also roosts in these types of caves.

Natalus tumidirostris has been found sharing roosts with 10 other bat species (Pteronotus parnellii, Pteronotus gymnonotus, Pteronotus personatus, Mormoops megalophylla, Leptonycteris curasaoe, Phyllostomus hastatus, Carollia perspicillata, Artibeus jamaicensis, Desmodus rotundus, Myotis keaysi) and roosts in closest association to Carollia perspicillata with which it often forms mixed groups, as in Macaregua (Gómez-Laverde, 1986) and Cueva las Animas. Within roosting groups individuals hang widely spaced and are generally quiet, sometimes allowing themselves to be caught by hand. Occasionally, when large multispecies groups of bats abandon certain areas of a given cave due to the presence of visitors, individuals of N. tumidirostris are the last to leave their roosting spots. Nonetheless, it has been observed to become more alert while roosting when a cave is repeatedly visited by humans (Gómez-Laverde, 1986). It generally roosts in low areas of walls, but it is occasionally found hanging from high (3–5 m) ceilings.

Natalus tumidirostris has been found in habitats ranging from dry cactus scrub (Bonaire, 464 mm annual precipitation; locality 465) to wet forest (Camp Patawa, French Guiana), but most commonly it is found in areas of deciduous to semideciduous forest. It occurs from sea level to middle elevations (e.g., Cueva Macaregua, Colombia, 1400 m; locality 67).

Natalus tumidirostris feeds on insects, and is reported by Linares (1998) to consume mostly Lepidoptera and Diptera. It seems to have a single annual estrus, and bears only one pup per year. The timing of the reproductive activity varies slightly among localities. In northern Venezuela, 13 (65%) out of 20 females collected between 16–30 April 2004 were pregnant. In the only well-known Colombian population, however, birth takes place before late March (Gómez-Laverde, 1986). Throughout lactation, juveniles have been found to aggregate in compact clusters in cave ceilings during the daytime. Gómez-Laverde (1986) described the development during four months of one such groups in Cueva Macaregua, Colombia. In this cave, in late March, hairless neonatal individuals were found aggregated in a compact cluster on the cave ceiling, in association with a few adult females, which flew away after being disturbed. By mid-April, this group had consolidated into a large mass of many juveniles that occupied a 1 × 1.5 m of substrate. By the end of the month, these juveniles had appreciably grown, were already haired, and some were able to fly. In early June, the cluster had disappeared and, in its stead, there were many dispersed, adult-sized, and gray-colored individuals, all capable of full flight. The following year the cluster of juveniles was much reduced in size, reaching a maximum of only about 200 individuals, and was in a different location. It was not determined, however, whether this change reflected an overall smaller number of births or a change in the distribution of the newborns within the cave. In an incident in Macaregua, a piece of cave ceiling fell to the floor with about 10 nonflying pups still clinging to it; in spite of the accidental change in location, the pups continued to be fed, since observations made 15 days after the initial one revealed that they had grown appreciably and were still on the piece of fallen ceiling. A photograph taken in Cueva Ricardo Zuloaga, Venezuela, in an unspecified date, documents a similar cluster-forming behavior of newborn N. tumidirostris (Carreño, 1998). Sex ratios appear widely skewed in some caves (e.g., an all male colony in Cueva del Guano in April, 2004) suggesting a pattern of sexual segregation similar to that of other natalids.

Natalus tumidirostris is an abundant species known from at least 961 museum specimens, 74% of which having been collected in just three localities: Cueva Macaregua, Colombia; Cueva Ricardo Zuloaga, Venezuela; and Tamana Caves, Trinidad. It appears most densely distributed along northernVenezuela. Natural predators are not known, but at least in Cueva del Guano, Paraguaná, they could be occasional victims of giant centipedes (Scolopendra gigantea, which is reported to actively hunt bats in this cave; Molinari et al., 2005). One of the few known specimens from French Guiana, was caught by a domestic cat that brought it into a house (Charles-Dominique et al., 2001). Parasites of this species include Tricholeiperia trinidadensis (Nematoda, Molineidae; Gibbons and Omah-Maharaj, 1991) and the bacterium Borrelia (Marinkelle and Grosse, 1968).

Harp trap surveys in Cueva Macaregua (Cadena, 1974) indicate that nightly foraging begins relatively early at around sunset. The same study reported continuous activity of bats leaving and entering the cave until 22:00, when observations were stopped. Occasionally there was a peak in the number bats leaving the cave about half an hour after sunset.

The flight of Natalus tumidirostris is slow and very maneuverable, as in other species of the genus. If on the ground, N. tumidirostris seems unable to crawl, but can initiate flight vertically with strong downward thrusts of the wings (Riskin et al., 2005).

As in other species of natalids, Natalus tumidirostris dies quickly (in fewer than 20 hr) of starvation and/or dehydration when kept in captivity. Its basal metabolic rate (1.54 ml O₂/ghr) is very low (30% below expected value) relative to that of other Neotropical insectivorous bats of similar body mass. Such a low basal metabolic rate may help this bat reduce its risk of starvation and water loss when roosting in warm caves and when foraging in dry habitats (Genoud et al., 1990). Natalus tumidirostris seems able to survive lower temperatures than other small Neotropical bats due to its relatively low thermal conductance (0.41 ml O₂/ghr °C), which is probably afforded by its long and lax hair (Genoud et al., 1990). The thermoneutral zone of N. tumidirostris was determined to lie between 28° and 35° C, and this bat is able to maintain a stable body temperature of about 32° C within ambient temperature values ranging between 28° and 20° C, falling into torpor when the ambient temperature decreases below 20° C. It seems, however, unable to survive ambient temperatures below 10° C for longer than 2 hours (Genoud et al., 1990).

Natalus tumidirostris is a species of least concern in IUCN's Red List of Threatened Species (IUCN, 20102010). In northern Venezuela it seems a ubiquitous and locally abundant bat and therefore not threatened. Petit (1996) considered it to be threatened in Curaçao, with an islandwide population count of just 50–60 bats. The colony of Hato Cave, the source of the holotype of the species, has disappeared and the cave has been turned into a tourist attraction. Whitout appropriate management, this unique island population might become extinct.

Flight Morphology

The relative size and shape (aerodynamic design) of flight surfaces (wings plus uropatagium) is highly variable among bats and has a profound influence on their ecology. Bats with pointed wing tips and narrow flight surfaces (high aspect ratio, defined as the ratio of the length to the width of a wing) fly fast, have little maneuverability, and exploit food resources in open spaces. Bats with broad wing tips and broad flight surfaces (low aspect ratio) tend to fly more slowly, have high maneuverability, and exploit food resources in cluttered habitats (i.e., within vegetation, McKenzie et al, 1995; Norberg and Rayner, 1987; Norberg, 1998; Stockwell, 2001). The maneuverability and flight speed of bats is significantly influenced by the size of the uropatagium, which represents a caudal extension of the flight membranes that is used in steering and adds aerodynamic drag. Bats with a large uropatagium tend to have higher flight maneuverability and to fly more slowly than bats with a small uropatagium (Lawlor, 1973; Norberg, 1995).

Because of their wide wings and large uropatagia, natalids represent an extreme strategy among bats for slow, maneuverable flight (Jennings et al., 2004; Norberg, 1998). Still, even within Natalidae there is significant variation in two measures of flight-surface design, the shape of the wing tip and the size of the uropatagium. With regard to wing-tip shape, natalids seem to comprise three distinct groups: (1) bats with relatively narrow wing tips (Nyctiellus, Chilonatalus, and Natalus primus); (2) bats with broad wing tips (Natalus lanatus); and (3) bats with wing tips of intermediate width (remaining members of genus Natalus; figs. 38, 39). With regard to size of the uropatagium, natalids also fall into three categories: (1) bats with small uropatagia (Nyctiellus); (2) bats with large uropatagia (Natalus, Chilonatalus tumidifrons, and C. macer); and (3) bats with intermediate-sized uropatagia (Chilonatalus micropus, Natalus lanatus; figs. 38, 39).

Fig. 38.

Plot of wing-tip shape index vs. relative size of the uropatagium in 11 species of Natalidae. Five different ecomorphs are formed by the intersection of these two indices. The genus Natalus is the most diverse in flight morphology, with most species clustering in the intermediate wing tip and large uropatagium ecomorph and two outliers: (1) Natalus primus, which clusters with two species of Chilonatalus, and (2) Natalus lanatus, whose broad wing tip is unique among natalids.

Fig. 39.

Wing outlines of six species of Natalidae: A, Nyctiellus lepidus (modified from Silva-Taboada, 1979); B, Natalus primus; C, Chilonatalus macer (modified from Silva-Taboada, 1979); D, Natalus major; E, Chilonatalus micropus; F, Natalus lanatus. Nyctiellus lepidus has the narrowest wing of all natalids.

Principles of bat-wing aerodynamics predict that natalids with narrow wing tips and small uropatagia will fly faster and with less maneuverability than natalids with broad wings and large uropatagia. Although natural history information that might corroborate these predictions is scant and vague, field observations seem to make a distinction between the flight of most natalids and that of Nyctiellus lepidus. With the exception of Nyctiellus lepidus, the flight of most species of Natalidae has been described as slow, very maneuverable, and even mothlike (Goodwin, 1970; Jennings et al., 2004; Miller, 1905; Tejedor et al., 2004, 2005; the term “agile” given by some authors [e.g., Mitchell, 1965] is understood here to mean maneuverable). The flight of Nyctiellus lepidus, on the other hand, is relatively fast (Silva-Taboada, 1979).

Despite the difficulty of interpreting the flight morphology of natalids in the absence of behavioral data, the differences found among genera and species are notable and suggest the existence of five distinct ecomorphs. Sympatric species normally belong to separate ecomorphs (table 24). In this regard, the outlying position of N. lanatus is remarkable given that its sympatry with N. mexicanus represents the only known case of coexistence of two natalid species of the same genus. In only one case (Chilonatalus macer and Natalus primus) is the same ecomorph shared by two sympatric species.

TABLE 24

Distribution and ecomorphs of Natalidae

TABLE 25

Loadings of the first two canonical axes of a canonical variates analyses (CVA) performed with 4 external variables of Natalidae

TABLE 26

Loadings of the first two canonical axes of a canonical variates analyses (CVA) performed with 7 cranial variables of Natalidae

Molariform Dentition

Among bats, natalids show a particularly marked rostrocaudal elongation of the mesostyle of the upper molars. These modified molar cusps have been termed mesostylar crests by Morgan and Czaplewski (2003: fig. 4; pl. 16). Bat genera from other families, including Thyroptera (Thyropteridae), Furipterus (Furipteridae), and Kerivoula (Vespertilionidae) also show mesostylar crests, usually with a slightly different orientation and a lesser degree of development. Within Natalidae, the development of mesostylar crests is greatest in Primonatalus, Chilonatalus, and Natalus primus. In these taxa, the mesostylar crests are high, long, and broadly curved, occupying more than a third of the labial side of the occlusal surface of the upper molars. In Nyctiellus and the remaining species of the genus Natalus, the mesostylar crests are straight and relatively short (occupying less than 1/3 of the labial side of the occlusal surface of the upper molars). In addition, most members of Natalus (except N. primus) lack a mesostylar crest on M3.

Long, sharp edges on molar crests appear within several predatory mammalian lineages (e.g., carnivorans: Butler, 1946; insectivorans and microchiropterans: Strait, 1993). The dilambdodont tooth of insectivorous bats, bearing multiple shearing crests on the W-shaped ectoloph, is a classic example (Koopman and MacIntyre, 1980). These structures are thought to be optimal for shearing relatively soft food items as opposed to grinding coarser food, and are more highly developed in animals that specialize in eating boneless muscle (Evans and Sanson, 2003) and/or soft-bodied insects (Strait, 1993). Among insectivorous bats, the consumption of soft food items is also directly reflected in the shape of the skull. Bats with short, broad rostra can deliver stronger bites and are thought to specialize on eating hard-shelled insects (e.g., beetles), whereas bats with long, narrow rostra deliver weaker bites and consume soft-bodied insects (e.g., moths; Freeman, 1979).

The mesostylar crests of natalids represent additional shearing crests to the already well-developed dilambdodont teeth of these bats. Also, natalids show the greatest elongation of the rostrum among all insectivorous bats. This combination of traits suggests that natalids select soft food items. Moreover, the variation observed within the family in the development of the mesostylar crests seems to be associated with variation in the elongation of the rostrum.

Two main natalid groups are defined by rostral geometry: (1) bats with longer, narrower rostra (Chilonatalus and Natalus primus); and (2) bats with shorter, wider rostra (Nyctiellus and the remaining species of Natalus; fig. 40). Only species with long, narrow rostra show long and broadly curved mesostylar crests. Although the potential functional association of these two traits seems highly influenced by phylogeny (all species with long rostra and more shearing teeth descend from relatively basal nodes), it does indicate the existence of different natalid ecomorphs with relation to skull shape and molariform dentition. This variation probably reflects significant trophic niche differentiation among natalids.

Fig. 40.

Plot of scores of the second canonical root obtained by canonical variates analysis of seven cranial dimensions from 12 species of Natalidae. CII is an axis of rostrum shape, being most influenced by maxillary tooth row (table 2). Black dots are score means and gray bars represent two standard deviations around the mean. Species toward the positive side of the axis have long, narrow rostra, whereas species toward the negative side have relatively short, broad rostra. Long and broadly curved mesostylar crests occur only in species with long, narrow rostra.

Dietary data that could test this hypothesis is scant but hints at niche partitioning within Natalidae. The most complete dietary study of a natalid, Nyctiellus lepidus (a broad-skulled species) reported a preponderance of insects of medium hardness (Homoptera, Diptera, and Hymenoptera; Silva-Taboada, 1979). By contrast, accounts of the diet of narrow-skulled species mention a marked predominance of moths (Chilonatalus macer; Silva-Taboada, 1979) or moths and small crickets (Natalus primus; Tejedor et al., 2004).

As in the design of flight morphology, the putative ecomorphs of the feeding apparatus are partitioned among sympatric species with the exception of Natalus primus and Chilonatalus macer, which share the long rostrum/long mesostylar crest ecomorph (table 24). A second sympatric species pair, N. mexicanus and N. lanatus, also fall within the same ecomorph.

Body Size

For a small family, Natalidae has a wide variation of body sizes. The largest member of the family, Natalus primus, is five times heavier and has almost twice the forearm length of Nyctiellus lepidus, the smallest natalid and one of the smallest bats in the world. Body sizes in Natalidae have a strong taxonomic component, with medium to large body sizes occurring only in the genus Natalus and small body sizes in Chilonatalus and Nyctiellus.

The distribution of body size in Natalidae appears to be related to sympatry among species (fig. 41). In three of the five natalid faunas with sympatric species there is a wide difference between the largest and smallest member of the assemblage. At present, the fauna of the Bahamas is unique within the West Indies in that it is composed of allopatric taxa (N. lepidus and C. tumidifrons occur on different islands) and lacks a large species. During the last Pleistocene glaciation, however, the fauna of the Bahamas was similar to that of Cuba, having three sympatric species, and including an even larger-bodied representative of Cuba's recent Natalus primus (Morgan, 1989, 2001).

Fig. 41.

Variation of forearm length in Natalidae in relation to geographic distribution. Vertical gray bars represent the observed range of variation per species per region and the horizontal black line represents the median. Large gray rectangles frame populations that occur in sympatry. Sample sizes: Bahamas (Ctu, 53; Nyl, 45); Cuba (Npr, 51; Cma, 20; Nyl 24); Hispaniola (Nma, 34; Cmi, 6); Jamaica (Nja, 21; Cmi, 48); SAP  =  San Andrés and Providencia islands, Colombia (Nme, 7; Cmi, 36); M-CA  =  Mexico–Central America (Nme, 298; Nla, 33); SAN  =  South America N of the Amazon (230); SAS  =  South America S of the Amazon (37); LA  =  lesser Antilles (65). There is no overlap in forearm length neither among genera nor among insular populations that occur in sympatry. Representatives of the composite fauna of San Andrés and Providencia islands (i.e., the West Indian derived C. micropus, and the continental derived N. mexicanus) show the least amount of difference in forearm length among sympatric members of these two genera.

Differences in body size among closely related insular species are traditionally explained by two nonexclusive mechanisms: species assortment and/or character displacement. Species assortment states that only species with divergent morphology can successfully colonize and coexist on an island (Grant and Abbot, 1980), whereas character displacement is defined as the divergence in morphology between species after the onset of sympatry as a result of selection due to competition (Brown and Wilson, 1956). Rigorous demonstration of either mechanism requires proof of competition for resources and a genetic (rather than environmental) base for the observed morphological variation (Schluter, 2000). Nonetheless, preliminary explanations seek support in the pattern of distribution and phylogenetic history of the taxa in question. The characteristic evidence for species assortment is that members of each size class are closest relatives. That for character displacement is that taxa that occur both allopatrically and sympatrically are more divergent between themselves when they occur sympatrically than when they occur allopatrically (Losos, 1990).

Both patterns are present in Natalidae. The consistent generic difference in body size between Natalus (always large) and Chilonatalus (always small) in all islands where small and large natalids are found sympatrically is compatible with species assortment. By contrast, a unidirectional change in body size of the large (Natalus) and small (Chilonatalus micropus) natalids on the islands of Hispaniola, Jamaica, San Andrés, and Providencia, suggests character displacement. In Jamaica, where the largest Natalus (N. jamaicensis) of those islands occurs, C. micropus reaches its maximal body size, whereas in Hispaniola, where the smaller N. major occurs, C. micropus is also smaller (fig. 41). In San Andrés and Providencia, moreover, a member of the Antillean fauna (Chilonatalus) coexists with a medium-sized member of the continental fauna (N. mexicanus). In these two islands, N. mexicanus appears to have reached its largest body size and C. micropus its smallest, in agreement with the predictions of character displacement. Although the size difference between C. micropus and N. mexicanus on San Andrés and Providencia is much smaller than that between C. micropus and greater Antillean Natalus, the lack of differentiation in discrete characters of the insular N. mexicanus relative to that of the mainland (they are recognized as a single species) suggests that interaction between these two taxa is relatively recent and that the difference observed, if due to size divergence, may be only incipient.

Independently of the preponderance of one or the other mechanism in structuring natalid assemblages, two extreme cases, one of exaggerated size difference (between N. primus and C. macer in Cuba) and a second of lack of difference (between N. mexicanus and N. lanatus in Mexico) suggest that competition and the evolution of body size are related in Natalidae. The large difference in forearm size between N. primus and C. macer may be related to the fact that these species share a similar morphospace. Natalus primus is unique in its genus in that it resembles Chilonatalus in its relatively long wing tip, large uropatagium, long rostrum, and high development of mesostylar crests of the upper molars. It is possible that the greater morphological similarity between N. primus and Chilonatalus has forced N. primus to become disproportionately larger to avoid competition. If body size is taken into account as an additional ecomorphological component, the pair N. primus/C. macer splits into clearly distinct groups in both wing shape and skull shape morphospaces (fig. 42 A, B).

Fig. 42.

A, Canonical analysis axis scores for four limb measurements of 12 species of Natalidae. Loading contributions of variables to each axis is shown in table 3. CI is an axis of body size and CII is an axis of wing-tip shape, with bats on the positive side of the axis having more pointed tips. Scores of canonical analyses are shown in table 25.

Fig. 42

(continued). B, Canonical analysis axis scores for seven skull measurements of 12 species of Natalidae. Loading contributions of variables to each axis is shown in table 2. C I is an axis of body size and C II is an axis of rostrum shape, with bats on the negative side of the axis having longer, narrower rostra. Natalus primus, which shares many ecomorphological traits with Chilonatalus, is widely separated from them in ecomorphological space when body size is taken into account. Scores of canonical analyses are shown in table 26.

The pair N. lanatus and N. mexicanus represent an opposite case. These two species are very similar in forearm length but have different flight morphology. Also, even though they both belong to the relatively wide-rostrum/short mesostylar crest ecomorph, they fall in opposite extremes of that ecomorph in the cranial shape ordination (fig. 42B). Separation into different flight and food-processing ecomorphs may thus be sufficient to partition resources between these two species, relaxing competition and the selective pressure to diverge in size. Nonetheless, as suggested before, it is possible that these two species may show some habitat segregation both in altitude and in roost selection, and that competition in this species pair may actually be minimal in nature.

Genital Morphology

The relative length of the penis (length of the penis/forearm length) is markedly variable among natalids. Three classes of penis length relative to body size can be distinguished in Natalidae: (1) penis long (C. micropus); (2) penis intermediate (Natalus and Nyctiellus); and (3) penis short (C. macer and C. tumidifrons; fig. 43). The mean relative penis length of C. tumidifrons (5.4% of forearm length) is more than 10 standard deviations shorter than that of C. micropus (14.6% of forearm length; figs. 43, 44).

Fig. 43.

Distribution of relative penis length in 11 species of Natalidae. Black dots are means and vertical gray bars are two standard deviations around the mean. Most natalids have an intermediate-length penis but the genus Chilonatalus includes species with short or long penises.

Fig. 44.

Ventral view of males of two species of Chilonatalus (left, C. tumidifrons; right, C. micropus) showing longer penis in C. micropus.

Genital morphology has been shown to be associated with mating strategies and with the likelihood that females will mate with multiple males (Hosken and Stockely, 2004). In species with promiscuous females, sperm competition is intense and males are selected for production of large amounts of sperm (i.e., larger testes), for a deeper delivery of the ejaculate (i.e., longer penises), and for prolonged intromissions, all of which will increase the probability of inseminating females (Arnqvist, 1998). Trends like these have been documented in primates (Dixson, 1987; Harcourt et al., 1981; Verrell, 1992), carnivores (Dixson, 1995), birds (Briskie and Montgomery, 1997; Møller, 1988), flies (Hosken and Ward, 2001), and butterflies (Gage, 1994).

The positive association between intensity of sperm competition and testis size found in a wide range of taxa has been confirmed in bats (Hosken, 1997, 1998; Wilkinson and McCracken, 2003). Investigations of the relationship of penis morphology to mating system in bats, however, have been inconclusive. In a study including 163 species of 12 bat families, significant positive correlations were found among relative baculum length, relative testis size, and mating system (Hosken et al., 2001). The relationships did not hold, however, after correction for phylogenetic history. The authors, therefore, speculated that other factors unrelated to sexual selection could influence baculum length, including aspects of female tract morphology and the size of the uropatagium, the last seen as a physical obstacle during copulation.

Natalids are an interesting group in which to explore genital evolution in bats given their significant variation in penis length and relative size of the uropatagium. Comparisons of penis length with length of the tibia (a correlate of size of the uropatagium in Natalidae, see Methods) showed no familywide correlation (fig. 45). Stronger trends, however, were detected within two species groups that differ in the relative size of the natalid organ: (1) bats with large natalid organs, reaching 13%–26% the length of the forearm; and (2) bats with small natalid organs, reaching 6%–16%. Interestingly, across Natalidae, relative penis length does appear to be negatively associated with relative length of the natalid organ (fig. 46).

Fig. 45.

Relationship of penis length with length of the tibia in Natalidae. Familywide, penis length is not correlated with length of the tibia. Natalids, however, cluster into two groups that differ in the relative size of their natalid organ. *Includes four species of Natalus.

Fig. 46.

Plot of relative penis length vs. relative length of the natalid organ in seven species of Natalidae. The relative length of the penis is negatively correlated with the relative length of the natalid organ. *Includes four species of Natalus.

The natalid organ, a unique synapomorphy of Natalidae (Simmons, 1998), is a presumed exocrine gland that is present in the forehead of adult males only (Dalquest, 1950; Goodwin, 1959). The size and shape of the natalid organ varies widely among natalid genera (fig. 47; pl. 5), reaching its maximum development (8.5 mm; 53% of the skull length) in C. tumidifrons. Although the function of the natalid organ is unknown, its exclusive presence in males suggests it has a sexual function. When manipulated, living males of the genus Natalus sometimes secrete a drop of an oily, translucent green liquid through a pore on the anterodorsal surface of the natalid organ. This secretion does not dissolve in alcohol, as individuals with hardened amber-colored droplets are occasionally found among specimens preserved in fluid. It is possible that secretions from the natalid organ function as a social signal in male-female and/or male-male interactions. The apparent negative association of the size of this organ with male genital size strengthens the hypothesis that both penis length and natalid organ are sexually selected in natalids.

Fig. 47.

Distribution of relative size of the natalid organ in 10 species of Natalidae. Two groups of species can be distinguished with relation to relative size of the natalid organ: one, containing species with a relatively large natalid organ and a second containing species with a relatively small natalid organ.

Plate 1.

Top: Inundated cockpit karst covered with evergreen forest; Los Haitises, Hato Mayor, Dominican Republic; habitat of Natalus major. Bottom: Tower karst covered with xerophytic and semideciduous forest on the ridges and evergreen forest in the valleys; Sierra de Viñales, Pinar del Río, Cuba; habitat of Chilonatalus macer.

Plate 2.

Top: Sandstone mesas with savanna (cerrado) on the tops and semideciduous forest at the base; Serranía de Santiago, Santa Cruz, Bolivia; habitat of Natalus espiritosantensis. Bottom: Gullies cut deep into these mesas support a more humid forest.

Plate 3.

Top: Alluvial sediments covered with thorn scrub; Las Cuevas, Baja California Sur, Mexico; habitat of Natalus mexicanus. Bottom: Granite inselbergs covered in sparse xaxicolous vegetation with rainforest at the base; Les Nouragues, French Guiana. Rocks piled at the base of these inselbergs often form caves that may harbor Natalus tumidirostris.

Plate 4.

A, Nyctiellus lepidus, Cueva del Calabazar (locality 142), Pinar del Río, Cuba (illustration A. Tejedor); B, Chilonatalus macer, Cueva del Calabazar (locality 142), Pinar del Río, Cuba (illustration: A. Tejedor); C, Chilonatalus micropus, Arroyo Chico (locality 197), Samaná, Dominican Republic (photo: G. Nuñez/A. Tejedor); D, Natalus major, Cueva de la Laguna Juan García (locality 194), Samaná, Dominican Republic (photo: G. Nuñez/A. Tejedor); E, Natalus mexicanus, Cueva Chica, Las Cuevas (locality 260), Baja California Sur, Mexico (photo: G. Nuñez/A. Tejedor); F, Natalus tumidirostris, Patawa (locality 216), Kaw, French Guiana (photo: Brian W. Keeley).

Plate 5.

Dorsal, frontal, and lateral views (first, second, and third rows, respectively) of the natalid organ (in gray shading) in four species of Natalidae: A, Nyctiellus lepidus; B, Chilonatalus macer; C, Chilonatalus micropus; D, Natalus tumidirostris. Anteroventral view of the maximally extended ear pinna in six bat species with lanceolate ear pinna: E, Saccopteryx bilineata; F, Myotis nigricans; G, Pteronotus pranelli; H, Thyroptera tricolor; I, Furipterus horrens; J, Kerivoula hardwickei; and in five species of Natalidae: K, Nyctiellus lepidus; L, Chilonatalus micropus; M, Natalus primus; N, Natalus major; O, Natalus tumidirostris. Regions of the ear pinna: 1, distal pinna; 2, ear folds; 3, lateral extension of the pinna; 4, basal (ventral) extension of the pinna. Scale bars  =  5 mm.

Plate 6.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: Dorsal view. Specimens: Nyctiellus lepidus: (1) AMNH 167133, male, Little Exuma, Bahamas; (2) AMNH 61169, male, Havana, Cuba; (3) UF 4454, Long, the Bahamas; Chilonatalus micropus: (4) AMNH 216125, male, Samaná, Dominican Republic; (5) USNM 15849, Providencia Isl., Colombia; (6) BMNH 80.12.14.1, holotype, Kingston, Jamaica; Chilonatalus macer: (7) AMNH 186980, male, Isle of Pines, Cuba; (8) USNM 113724, holotype, female, Baracoa, Cuba; (9) AMNH 126161, La Habana, Cuba; Chilonatalus tumidifrons: (10) USNM 122024, male, San Salvador Isl., the Bahamas; (11) USNM 576614, male, Abaco, the Bahamas; (12) UF 24853, male, Abaco, the Bahamas.

Plate 7.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: dorsal views, continued. Specimens: Natalus primus: (13) AMNH AT 1, field number, female, Pinar del Río, Cuba; (14) AMNH AT 2, collector number, female, Pinar del Río, Cuba; Natalus jamaicensis: (15) AMNH 182000, male, St. Catherine, Jamaica; (16) AMNH 246127, male, St. Catherine, Jamaica; Natalus major: (17) USNM 101395, holotype, male, Puerto Plata, Dominican Republic; (18) AMNH 275487, field number, male, Maria Trinidad Sánchez, Dominican republic; (19) AMNH 97589, female, Barahona, Dominican Republic; (20) KU 150721, male, Department du L'Ouest, Haiti; Natalus stramineus: (21) BMNH 70.2324, male; (22) FMNH 47702, female, Montserrat; (23) USNM 544834, male, Anguilla; (24) BMNH 18.4.1.4, Antigua; (25) USNM 113605, holotype of Natalus dominicensis, male, Dominica; (26) USNM 113601, male, Dominica; (27) 18215, Dominica; (28) KU 150727, female, Grande Terre, Guadeloupe.

Plate 8.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: dorsal views, continued. Specimens: Natalus lanatus: (29) KU 39628, male, Nayarit, Mexico; 30) KU 39620, holotype, female, Nayarit, Mexico; (31) KU 82901, male, Veracruz, Mexico; (32) MSB; Natalus mexicanus: (33) USNM 96476, holotype, female, Baja California Sur, Mexico; (34) KU 39677, female, Nayarit, Mexico; (35) KU 23815, male, Veracruz, Mexico; (36) USNM 519080, male, Canal Zone, Panama; Natalus espiritosantensis: (37) USNM 549504, male, Pará, Brazil; (38) USNM 242830, holotype of Natalus stramineus natalensis, Rio Grande do Norte, Brazil; (39) MBML 1801, holotype, Espirito Santo, Brazil; (40) MNK 2072, male, Santa Cruz, Bolivia; Natalus tumidirostris: (41) ROM 45239, male, Sucre, Colombia; (42) AMNH T7, field number, male, Zulia, Venezuela; (43) USNM 102106, holotype, male, Curaçao; (44) female, Kaw, French Guiana.

Plate 9.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: ventral views. For specimen numbers, see plate 6.

Plate 10.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: ventral views, continued. For specimen numbers, see plate 7.

Plate 11.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: ventral views, continued. For specimen numbers, see plate 8.

Plate 12.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: lateral views. For specimen numbers, see plate 6.

Plate 13.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: lateral views, continued. For specimen numbers, see plate 7.

Plate 14.

Geographic and individual variation in skull morphology in 12 extant species of Natalidae: lateral views, continued. For specimen numbers, see plate 8.

Plate 15.

Lateral view of the ascendant ramus of the left dentary of Myotis (A, included for comparison) and seven species of Natalidae: B, Nyctiellus lepidus; C, Chilonatalus micropus; D, Chilonatalus macer; E, Natalus primus; F, Primonatalus prattae; G, Natalus mexicanus; H, Natalus major.

Plate 16.

Left upper molar tooth row in 6 species of Natalidae: A, Nyctiellus lepidus; B, Chilonatalus tumidifrons; C, C. micropus; D, Natalus primus; E, Primonatalus prattae; F, Natalus mexicanus.

Plate 17.

Proximal (two upper rows) and distal (two lower rows) epiphyses of the left humerus (ventral views: 1–9, 19–27; dorsal views: 10–18; 28–36) in 10 species of Natalidae:—1, 10, 19, 28, Nyctiellus lepidus;—2, 11, 20, 29, Chilonatalus micropus;—3, 12, 21, 30, C. macer;—4, 13, 22, 31, Natalus primus;—5, 14, 23, 32, N. major; —6, 15, 24, 33, N. jamaicensis;—7, 16, 25, 34, N. tumidirostris;—8, 17, 26, 35, N. espiritosantensis;—9, 18, N. mexicanus (proximal epiphysis only);—27, 36, Primonatalus prattae (distal epiphysis only).

Plate 18.

Dorsal (top), ventral (middle), and lateral (bottom) views of the axial skeleton of four species of Natalidae: A, E, I, Nyctiellus lepidus; B, F, J, Chilonatalus macer; C, G, K, C. micropus; D, H, L, Natalus tumidirostris.

Plate 19.

Roosting habits of Natalus major. A, Roosting group of females in Cueva de Cristian (locality 185), Hato Mayor, Dominican Republic. Natalids often roost in loose aggregations of uniformily spaced out individuals of a single sex. B, Group of adult females and young adults of both sexes in Cueva de Murciélagos (locality 190), María Trinidad Sanchéz, Dominican Republic. When disturbed, adult bats are the first to fly away to alternative roosting sites within caves.

The presence of opposite evolutionary trends in genital size within Chilonatalus is remarkable, and suggests significant differences in mating system among species of this genus. The long penis of C. micropus might be related to high levels of sperm competition in this species, perhaps entailed by high levels of female promiscuity. Conversely, the extremely short penis of C. tumidifrons and C. macer, together with the extreme development of their natalid organ suggest a different strategy. In these two species sperm competition could be reduced by an influence of this gland in social communication. It is possible that individuals with some extreme quality of the natalid organ or its production may have more exclusive access to females, as may occur among harem-keeping or lekking species with exaggerated secondary sexual dimorphism (Andersson, 1994). These intriguing hypotheses remain to be tested with behavioral data.