Natalus espiritosantensis ( Ruschi, 1951 )

Tejedor, Adrian, 2011, Systematics Of Funnel-Eared Bats (Chiroptera: Natalidae), Bulletin of the American Museum of Natural History 2011 (353), pp. 1-140 : 39-46

Natalus espiritosantensis ( Ruschi, 1951)

Figure 19

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).

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 Ama- zon 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.

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 I 1 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).

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 (22u C and 94 % humidity, Cueva en Santiago de Chiquitos, Bolivia, locality 26; 25u 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, Itaete´, 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, Itaete´, 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.

Tables

TABLE 11 Summary of measurements a of Natalus espiritosantensis

		Females					Males
	N	Mean	(Min.–Max.)	SD	N	Mean	(Min–Max.)	SD
Weight	3	6.0	(6.0–6.0)	0.0	2		(6.0–6.0)
Forearm length	17	38.6	(37.2–40.4)	0.9	20	39.3	(37.0–42.1)	1.2
Length of tibia, dry	5	19.5	(18.6–20.1)	0.6	7	20.9	(19.4–22.8)	1.1
Length of tibia	8	21.3	(20.1–23.8)	1.4	9	21.9	(20.7–23.1)	0.9
Length of 3rd metacarpal	9	37.7	(35.1–39.6)	1.3	8	37.6	(35.8–39.1)	1.3
Length of 5th metacarpal	9	37.0	(35.3–39.1)	1.3	8	37.2	(34.7–38.5)	1.3
Length of ear	12	14.4	(12.0–15.9)	1.2	15	14.3	(12.0–15.7)	1.2
Length of penis		–	– –	–	6	4.5	(3.6–5.3)	0.6
Length of natalid organ		–	– –	–	6	7.2	(5.4–8.7)	1.4
Greatest skull length*	18	16.3	(15.9–17.0)	0.3	18	16.7	(16.2–17.0)	0.3
Zygomatic breadth*	17	8.5	(8.1–9.0)	0.2	18	8.7	(8.4–8.8)	0.1
Braincase breadth*	17	8.1	(7.9–8.3)	0.1	15	8.4	(8.0–8.6)	0.2
Breadth across molars*	18	5.5	(5.2–5.7)	0.1	18	5.6	(5.4–5.8)	0.1
Breadth across canines*	18	3.8	(3.5–4.0)	0.1	17	3.9	(3.6–4.2)	0.1
Maxillary tooth row*	18	6.6	(6.5–6.9)	0.1	16	6.8	(6.5–7.0)	0.1
Mandibular tooth row*	10	7.0	(6.8–7.3)	0.1	11	7.3	(7.1–7.5)	0.1
Postorbital breadth	18	3.2	(3.0–3.3)	0.1	16	3.2	(3.1–3.5)	0.1
Depth of braincase*	8	6.6	(6.4–6.8)	0.1	11	6.8	(6.5–7.1)	0.2

a Descriptive statistics of measurements for each sex. N 5 sample size; SD 5 standard deviation. Weight is given in g; all other measurements are given in mm. See text for description of measurement methods. Measurements significantly different between sexes (P, 0.05) are followed by an asterisk (*).