Natalus primus Anthony, 1919

Tejedor, Adrian, 2011, Systematics Of Funnel-Eared Bats (Chiroptera: Natalidae), Bulletin of the American Museum of Natural History 2011 (353), pp. 1-140 : 68-73

Natalus primus Anthony, 1919

Figures 30 , 31

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 70u 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 70u 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 70u 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.

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.

a Specimens from Cueva La Barca b Data from Silva-Taboada (1979) c Includes specimens from Abaco, Andros, and

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

Eleuthera

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.

Figures

Fig. 30. Holotype of Natalus primus (AMNH 41009, fossil right dentary, image inverted). Scale bar 5 10 mm. Photo: Mariko Kageyama, AMNH (see appendix for institutional abbreviations).