Natalus mexicanus Miller, 1902

Tejedor, Adrian, 2011, Systematics Of Funnel-Eared Bats (Chiroptera: Natalidae), Bulletin of the American Museum of Natural History 2011 (353), pp. 1-140 : 60-68

Natalus mexicanus Miller, 1902

Figure 28

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 I 2 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 M 2 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. None- theless, 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).

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 17u and 27u 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 , Arti- beus 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 22u– 26u 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 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) report- ed 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 12u 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.