HOW DO WE IDENTIFY MICRONYCTERIS (SCHIZONYCETRIS) SANBORNI SIMMONS, 1996 (CHIROPTERA, PHYLLOSTOMIDAE) RELIABLY AND WHERE WE CAN FIND THIS SPECIES IN BRAZIL?

Abstracts

Micronycteris is divided into four subgenera, Micronycteris, Leuconycteris, Xenoctenes, and Schizonycteris. The latter includes Micronycteris (Schizonycteris) minuta, Micronycteris (S.) schmidtorum, Micronycteris (S.) sanborni and Micronycteris (S.) yatesi. Little is known of the biology of M. (S.) sanborni, which is widely distributed in the dry forests of South America, but is known from only few sites. The scarcity of records of M. sanborni appears to be at least partly related to the difficulty of differentiating this species from the other members of the subgenus Schizonycteris. The present study identifies the key traits that distinguish this species from other Schizonycteris, reviews the geographic distribution of the species, and presents some notes on breeding patterns. Six new localities are presented for M. sanborni, and are analyzed together with those available in the literature, providing new insights into ecological and zoogeographic patterns. A number of the diagnostic features established by Simmons (1996) in the description of M. sanborni proved to have little taxonomic value, especially for the differentiation of M. minuta and M. yatesi, which it closely resembles. The primary external difference is the pure white color of the ventral pelage and the proportion of the white base (2/3-4/5) of the dorsal hair in M. sanborni, in contrast with dirty white or pale gray and a much shorter white base of the dorsal hair in the other species. A number of cranial traits are also important. The distributional data now indicate that M. sanborni occurs mainly in mesic and open areas, including disturbed habitats, in the Caatinga scrublands and the Cerrado savannas of northeastern Brazil, especially in areas with rocky outcrops. Micronycteris sanborni appears to be monoestrous, with births coinciding with the rainy season.

Schizonycteris; Intraspecific variation; Dry forest; Brazil; Chiroptera.

Micronycteris está dividido em quatro subgêneros, Micronycteris, Leuconycteris, Xenoctenes e Schizonycteris. Este último inclui Micronycteris (Schizonycteris) minuta, Micronycteris (S.) schmidtorum, Micronycteris (S.) sanborni e Micronycteris (S.) yatesi. Atualmente pouco se sabe sobre a biologia de M. (S.) sanborni, a qual é amplamente distribuída pelas florestas secas da América do Sul, apesar de ser conhecida de apenas poucas localidades. A escassez de registros de M. sanborni parece está parcialmente relacionado a dificuldade de diferenciar esta espécie de outros membros do subgênero Schizonycteris. Dessa forma, o presente estudo visa identificar as características diagnósticas que distingue esta espécie dos outros Schizonycteris, revisar a distribuição geográfica dessa espécie e apresentar comentários sobre o seu padrão reprodutivo. Seis novas localidades são apresentadas aqui para M. sanborni e, juntas com as outras disponíveis na literatura, foram analisadas fornecendo novas abordagens sobre o padrão ecológico e zoogeográfico dessa espécie. Várias características diagnósticas estabelecidas por Simmones (1996) na descrição de M. sanborni mostraram-se de pouco valor taxonômico, especialmente para a diferenciação entre M. minuta e M. yatesi, das quais mais se assemelha. As principais diferenças externas são a coloração branco pura do ventre e a proporção da base branca (2/3-4/5) do pelo dorsal em M. sanborni, em contraste com a coloração branco sujo ou acinzentado e a base dorsal branca muito mais curta das outras espécies. Outras características cranianas mostraram-se também importantes para a diferenciação. Os dados de distribuição levantados indicam que M. sanborni ocorre principalmente em áreas mésicas e abertas, incluindo ambientes alterados, na Caatinga arbustiva e nas savanas do Cerrado do nordeste do Brasil, especialmente em áreas com afloramentos rochosos. Micronycteris sanborni parece ser monoéstrico, com os nascimentos coincidindo com a estação chuvosa.

Schizonycteris; Variação intraespecífica; Floresta Seca; Brasil; Chiroptera.

INTRODUCTION

The bats of the genus Micronycteris Gray, 1866 are found in a variety of habitats, including rainforests, dry forests and savannas, as well as anthropogenic environments such as orchards, pastures, and plantations (Bernard & Fenton, 2002; Nunes et al., 2005; Peracchi et al., 2011; Reid, 1997). Porter et al., (2007), based on molecular data, classify Micronycteris in four subgenera - Micronycteris, Leuconycteris, Xenoctenes and Schizonycteris. The latter includes Micronycteris (Schizonycteris) minuta (Gervais), Micronycteris (S.) schmidtorum Sanborn, Micronycteris (S.) sanborni Simmons and the recently described Micronycteris (S.) yatesi Siles & Brooks.

Micronycteris sanborni is endemic to Brazil, found in mesic habitats within the Cerrado savanna and Brazilian Caatinga scrub (Simmons, 1996). Little is known of the biology of the species, which is classified as "Data Deficient" by Tavares & Aguirre (2008). In fact, while M. sanborni appears to have a relatively ample geographic range, it is known from only eight sites in Brazil (Cunha et al., 2009; Feijó et al., 2010; Gregorin et al., 2008; Gregorin et al., 2011; López-Baucells et al., 2013; Santos et al., 2010; Simmons, 1996). It is possible, however, that the scarcity of records of M. saborni is at least partly related to the difficulty of differentiating this species from the other members of the subgenus Schizonycteris (López-Baucells et al., 2013; Porter et al., 2007; Santos et al., 2010; Siles et al., 2013; Simmons, 1996).

According to Porter et al. (2007), the members of the subgenus Schizonycteris share a number of diagnostic morphological features which distinguishes it from the other members of the subgenus, such as a moderate to high interauricular membrane with a moderate to deep midline notch, dividing the membrane into two triangular flaps; small size (weight < 9 g, forearm < 38 mm); ventral fur white or pale gray or buff, lighter in color than dorsal fur; and non-hypsodont lower incisors, with crown height no more than twice crown width. On the other hand, there is a clear need for the establishment of more reliable criteria for the discrimination of the different species of the subgenus Schizonycteris (Santos et al., 2010; Siles et al., 2013), including the understanding of intraspecific variation.

The present study reviews the morphological and morphometric characters of M. sanborni described by Simmons (1996) and identifies the key qualitative characteristics that distinguish this species from the others of the subgenus Schizonycteris, including new diagnostic traits. The geographic distribution and habitat preference of the species are also revised, based on new localities from the Brazilian Caatinga scrublands. Information on reproductive patterns is also provided.

MATERIALS AND METHODS

Specimens examined

Forty-eight specimens of M. sanborni from six new localities in the Caatinga scrublands of the northeastern Brazil were analyzed in the present study. Three of the localities (described below) were surveyed by the authors in 2012 and 2013, rendering 26 of the specimens analyzed. These specimens were deposited in the mammal collection of the Federal University of Paraiba (UFPB), where the other 22 specimens were found.

Locality 1: municipality of Paripiranga, Brazilian state of Bahia (10°41'S, 37°51'W). In April 2012, five adult specimens, four males (UFPB 6532, 6535, 6543, 6673) and a female (UFPB 6536) were captured at two sites, both anthropogenic open areas adjacent to artificial ponds. Paripiranga is dominated by agricultural landscapes, with cassava and maize plantations, and pastures, interspersed with fragments of shrubby Caatinga, mainly along watercourses. There are numerous caves in this municipality.

Locality 2: Boqueirão da Onça (09°52'30.4"S, 41°6'1.8"W), in the municipality of Sento Sé, Bahia, Brazil. In May and August 2012, two adult males and one female (UFPB 6676, 6793, 6794) were collected in a mist-net set in the understory over a seasonal watercourse. This area is a complex of hills and valleys covered in arboreal Caatinga (sensu Mares et al., 1981), characterized by large deciduous trees of 10-12 m in height that form a continuous canopy during the rainy season (December-April). The vegetation is denser and more humid in the valleys, even during the dry season. This area is characterized by the presence of caves.

Locality 3: Aiuaba Ecological Station (ESEC Aiuaba) (06°36'33"S, 40°7'23.45"W) in the municipality of Aiuaba, state of Ceará, Brazil. Eighteen specimens - seven females and 11 males - were captured between August 2012 and December 2013 in a mist-net adjacent to a small pond in an open, disturbed area near banana and corn plantations. Ten of the specimens were collected and deposited at UFPB (UFPB 8838, 8842, 8846, 8847, 8856, 8860, 8863, 8876, 8877, 8878). This protected area encompasses shrub Caatinga habitats with some taller vegetation along the river margins. The surrounding area is essentially agricultural, with plantations of maize, banana, and cassava, as well as cattle ranches and goat farms. A number of caves are located within the region.

The additional 22 specimens of M. sanborni obtained from the UFPB collection included three from Loreto, Maranhão state (UFPB 5656, 5789, 5790), 18 from Tamanduá Farm, Patos, Paraiba state (UFPB 3245, 5312-5328) and one from Uruçui, Piaui state (UFPB 5788). The specimen reported by Feijó et al. (2010) from São José dos Cordeiros, Paraiba, was also examined. Four specimens of Micronycteris minuta (UFPB 7, 6682, 6608, 8695) were also analyzed qualitatively.

Morphological features

We evaluated the diagnostic features listed by Simmons (1996) for the differentiation of M. sanborni from the other species of the genus Micronycteris: (1) pure white ventral fur that extends anteriorly onto throat and chin; (2) dorsal hairs bicolored, brown with white bases, white base comprises 2/3-4/5 of each hair; (3) high band of skin present between ears, deeply notched in middle; (4) length of calcar approximately the same length as the foot; (5) fur on the uropatagium forms a small, roughly triangular patch whose apex is directed toward the tip of the tail; (6) white hairs on the inside of the pinnae; (7) the leading edge of the pinna covered with short dense fur; (8) gap present between outer upper incisor and canine; (9) P³ smaller than P⁴ in both height and anteroposterior length; (10) P⁴ with an unusually large posterolingual cingulum; (11) gap present between posterior edge of cingulum of M² hypocone and anterolingual edge of M³; (12) height of P₂ less than or equal to its length; (13) P₃ tiny, much smaller than P₂ and P₄, and (14) coronoid process low, upper margin of the ascending ramus with shallow slope. We also verified other characteristics that distinguish M. sanborni from the other species of the subgenus Schizonycteris: (i) dorsal profile of the skull; (ii) anterior portion of the zygomatic arch; (iii) ventral profile of the vertical ramus of the mandible, and (iv) the articular process. The skulls were photographed under a Leica M205C stereomicroscope with an attached DFC295 camera.

Quantitative features

Fourteen cranial and eight body measurements were taken from the specimens using digital calipers (0.01 mm precision) following the criteria described by Simmons (1996) and Vizotto & Taddei (1973), except for the diastemas, which were measured between the external margins of the adjacent cingulae. These measurements were compared with those available in the literature for the other species of the subgenus Schizonycteris.

Geographic database

The records collected in the present study were assessed together with those available in the literature on M. sanborni in an attempt to define ecological and zoogeographic patterns. For each record, whenever available, data were collected on the characteristics of the habitat, collecting site, type of vegetation, season, and the number of specimens collected.

RESULTS AND DISCUSSION

Qualitative data

The specimens analyzed in this study all presented characteristics 1, 2, 3, 7, 9, 12, 13 and 14 without any marked variation. However, the distances between the incisor and canine (trait 8) and M² and M³ (trait 11) varied considerably (Table 1). The distance between the incisor and canine varied between an almost imperceptible 0.02 mm to a maximum of 0.18 mm (Fig. 1A-C), while those between M² and M³ ranged from 0.13 mm to 0.21 mm. In contrast with the findings of (Simmons 1996; Fig. 2), considerable variation was observed in the development of the posterolingual cingulum of the P⁴ (trait 10) and the gap between the P³ and P⁴, and traits 5 and 6 were absent or inconspicuous.

Table 1
Morphometric data for the species of the subgenus Schizonycteris. All measurements are mean ± standard deviations (minimum-maximum) N.

Parameter			Micronycteris sanborni				Micronycteris yatesi	Micronycteris minuta	Micronycteris schimdtorum
	Paripiranga, Bahia	Boqueirão da Onça, Bahia	ESEC Aiuaba, Ceará	Paraiba (Feijó et al. 2010)	Simmons (1996)	Total Range (Min-Max; N)	Siles et al. (2013)	Simmons (1996)	Simmons (1996)
Sex	4 males, 1 female	2 males, 1 female	11 males, 7 females	1 female	2 males, 4 females	38 males,14 females	2 males, 1 female	29 males, 38 females	16 males, 9 females
Body mass	5.7 ± 0.71 (4.7-6.6) 5	5.1 ± 0.28 (5-5.5) 3	5.8 ± 0.5 (4-6) 18	7.5	6.3 (5.5-8) 6	4-8;33	-	7.3 (6.5-8.5) 11	6.2 (5-7.4) 8
Total length	54 ± 1.12 (52.9-55.8) 5	51 ± 2.43 (48.4-53.2) 3	54.7 ± 2.7 (50.3-61) 18	55.8	57.5 (55.5-65) 6	48.4-65.0; 33	54.7 ± 5.8 (48.5-60.8) 3	59.9 (55-69) 28	61.1 (54.5-67) 21
Head and Body length	40.6 ± 1.87 (37.4-42.2) 5	40.1 ± 1.95 (38.1-42) 3	44.5 ± 2 (42.1-49) 18	-	-	37.4-49; 26	45.8 ± 4.7 (41.5-50.9) 3	-	-
Tail length	13.4 ± 2.93 (11.1-18.4) 5	10.9 ± 0.51 (10.3-11.2) 3	10.1 ± 1.8 (7.2-14.8) 18	12.7	12.5 (12-14) 6	10.3-18.4; 33	8.9 ± 1.9 (7-10.8) 3	11.2 (9-14) 28	13.1 (11-17) 21
Hind foot length	9.1 ± 0.73 (8-9.9) 5	8.4 ± 0.45 (8-8.9) 3	9.8 ± 0.7 (8-11.2) 18	9.6	8.7 (8-9) 6	8-11.2; 33	11.1 ± 0.7 (10.3-11.7) 3	11.8 (9-13) 35	9.7 (8-11) 24
Ear length	21.9 ± 0.70 (21.1-22.9) 5	20.7 ± 0.73 (19.9-21.3) 3	19.9 ± 1.4 (14.9-21.7) 18	17.4	20.2 (19-21) 6	14.9-22.9; 33	16.4 ± 1.5 (15.5-18.2) 3	21.1 (19.5-23) 23	19.2 (16-21) 17
Forearm length	34.2 ± 0.43 (33.7-34.6) 5	32.6 ± 0.8 (31.8-33.4) 3	34.6 ± 1.1 (32.6-37.4) 18	33.6	33.6 (32-34) 6	31.8-37.4; 33	35.9 ± 1.1 (34.5-36.7) 3	35.4 (33-36.8) 33	35.3 (33-37.8) 25
Tragus length	5.8 ± 0.53 (5.1-6.4) 5	6.3 ± 0.78 (5.4-6.8) 3	5 ± 0.4 (4.3-6) 17	-	-	4.3-6.8; 25	-	-	-
Calcar length	8.2 ± 1.1 (6.6-9.1) 5	8.5 ± 0.51 (8.1-9.1) 3	8.6 ± 0.8 (7.1-10.6) 18	-	-	6.6-10.6;	26 9.9 ± 0.5 (9.4-10.5) 3	-	-
Greatest length of skull	17.49 ± 0.30 (16.9-17.7) 5	16.75 ± 0.07 (16.7-16.8) 2	16.4	17.3	-	16.4-17.9; 9	17.8 ± 0.1 (17.6-17.9) 3	-	-
Condyloincisive length	15.46 ± 0.40 (14.8-15.9) 5	14.9 ± 0.28 (14.7-15.1) 2	15,1	15.4	15.16 (14.9-15.3)6	14.7-15.9; 15	15.8 ± 0.1 (15.7-15.9) 3	16.64 (15.62-17.54) 39	17.56 (16-34-18.32) 23
Mastoid breadth	7.93 ± 0.24 (7.5-8.0) 5	7.3 ± 1.31 (6.5-8.1) 2	6,5	8.2	-	6.5-8.4; 9	8.1 ± 0.3 (7.8-8.4) 3	-	-
Zygomatic breadth	8.05 ± 0.19 (7.8-8.2) 5	7.75 ± 0.21 (7.6-7.9) 2	7,6	8.2	8.02 (7.8-8.1)5	7.6-8.2; 9	8.1;1	8.54 (8.02-9) 26	9.36 (8.72-9.87) 23
Breadth of braincase	7.37 ± 0.12 (7.2-7.5) 5	7.15 ± 0.21 (7-7.3) 2	7	7.2	7.41 (7.3-7.4)6	7-7.5; 15	7.4 ± 0.03 (7.4-7.5) 3	7.59 (7.23-8.04) 40	7.88 (7.42-8.24) 22
Postorbital constriction	4.07 ± 0.08 (4-4.1) 5	3.9 ± 0.14 (5.2-5.4) 2	3,8	4	-	3.8-5.4; 9	3.9 ± 0.07 (3.9-4) 3	4.12 (3.84-4.37) 43	4.12 (3.98-4.29) 23
Breadth across upper canines	2.82 ± 0.07 (2.7-2.9) 5	2.75 ± 0.07 (2.7-2.8) 2	2,7	2.7	-	2.7-3.9; 9	-		-
Breadth across upper molars	5.24 ± 0.10 (5.1-5.4) 5	5.3 ± 0.14 (5.2-5.4) 2	5,45	5.2	-	5.1-5.7; 9	5.6 ± 0.5 (5.3-6.3) 3		-
Length of maxillary toothrow	6.02 ± 0.23 (5.6-6.3) 5	5.8 ± 0 (5.8-5.8) 2	5,8	6.1	5.76 (5.6-5.9)6	5.6-6.3; 15	6.2 ± 0.02 (6.2-6.2) 3	6.65 (6.37-6.94)45	7.51 (7.1-7.97) 23
Length of mandible	10.56 ± 0.23 (10.1-10.6) 5	10.55 ± 0.35 (10.3-10.8) 2	10,3	10.7	-	10.1-10.9; 9	-		-
Length of mandibular toothrow	6.50 ± 0.21 (6.1-6.6) 5	6.4 ± 0 (6.4-6.4) 2	6,4	6.4	-	6.1-6.7; 9	-		-
I2-C Diastema	0,11 ± 0,06 (0,07-0,18) 3	0,027	-	-	-	0.027-0.187;4	-		-
P3-P4 Diastema	0,10 ± 0,08 (0,04-0,16) 2	-	0,062	-	-	0.042-0.165;3	-		-
M2-M3 Diastema	0,16 ± 0,08 (0,13-0,19) 3	0,21	0,19	-	-	0.13-0.21;5	-		-

Figure 1
Oblique frontal view of the upper dentition in M. sanborni (A: UFPB 6793; B: UFPB 6795; C: UFPB 6536) and M. minuta (D: UFPB 8695). Note the variation in the gap between the outer upper incisor and the canine (white arrow)

Figure 2
Occlusal view of the upper dentition of M. sanborni (upper: UFPB 6536; middle: UFPB 6734; lower: UFPB 6793). The insets to the right highlight differences in the spacing of p³ and p⁴ and the variation in the development of the posterolingual cingulum of p⁴ (white arrow)

The key differences among the species of the subgenera Schizonycteris are summarized in Table 2. While M. schmidtorum is easily distinguished from M. sanborni (see Table 2), its external and cranial morphology is very similar to that of Micronycteris minuta and Micronycteris yatesi.

Table 2
Comparison of diagnostic traits in the species of the subgenus Schizonycteris. Information obtained from *Simmons (1996) and from †Siles et al. (2013).

Subgenus Schizonycteris				Trait
Species	Length of calcar relative to the foot	Color of the ventral fur	Proportion of White base Dorsal Hair	Skin between ears	Leading edge of the pinna	Gap between upper incisor and canine	P3 in relation to P4
Micronycteris sanborni	Similar or Shorter	Pure white	2/3-4/5	High, deep notch	Covered with short fur (< 3 mm)	Absent or Present	Very short
Micronycteris minuta	Shorter or Similar	Dirty white; Pale gray	1/4-1/2	High, deep notch	Covered with short fur (< 3 mm)	Absent or Present	Slightly shorter
Micronycteris schmidtorum*	Longer	Dirty white;	Pale gray	-	Shallow notch	Covered with longer fur (> 5 mm)	Absent Similar
Micronycteris yatesi†	Shorter or Similar	Throat and sternal region white and abdominal area pale buff	1/2-1/3	High, deep notch	Covered with short or longer fur (3.5-5.5)	Present	Very short
Subgenus Schizonycteris				Trait
Species	Distance between P 3 and P 4	P 3 in relation to P 2 and P 4	Height coronoid process in relation to condyloid	Dorsal profile of Skull	Anterior portion of the zygomatic	Articular process	Palatine Bone
Micronycteris sanborni	Short or absent	Thin and Much smaller	Close	Smooth	Narrow	Triangular	Longer, convergent, extends until M1 and M2
Micronycteris minuta	Short or Absent	Slightly shorter	Far	Steep	High	Square	Longer, convergent, extends until M1 and M2
Micronycteris schmidtorum*	Absent	Slightly shorter	Far	Steep	High	Square	Longer, convergent, extends until M1 and M2
Micronycteris yatesi†	-	Much smaller	Close	Smooth	-	Triangular	Shorter, parallel, extends until M2 and M

(Simmons 1996: 10) states that "the calcar is approximately the same length as the hind foot in sanborni" (trait 4), but provided no measurements. In the present study, the difference recorded between the measurement of the foot and the calcar ranged from 0.1 mm to 1.3 mm (Table 1). In addition, a specimen of M. minuta (UFPB 6608) from the Atlantic Forest presents a difference of 0.4 mm between the length of the foot and calcar, which weakens the hypothesis that this trait is useful for the differentiation of the two species. However, the pure white ventral fur found in M. sanborni (Fig. 3A) and the proportion (2/3-4/5) of the white base of the dorsal hair (Fig. 3B) were consistent characters. These two traits can be used to reliably distinguish this species from both M. minuta, characterized by dirty white or pale gray ventral fur and the much shorter white base (1/4 or 1/2) of the dorsal hair (Simmons, 1996) and M. yatesi, which has a pale buff abdomen and an even shorter dorsal hair white base (1/3-1/2) (Siles et al. 2013).

Figure 3
Differences in fur color between M. sanborni e M. minuta. A: Pale gray ventral fur of Micronycteris minuta and pure white ventral fur of Micronycteris sanborni. B: Short white basal dorsal hair in M. minuta and long white basal dorsal hair in M. sanborni

Simmons (1996) concludes that the gap between the canine and the adjacent incisor is unique to M. sanborni. As noted above, however, there is considerable variation in this characteristic, and some specimens of M. minuta (e.g., UFPB 8695) present a small degree of separation between the outer incisor and canine (Fig. 1D). Overall, the teeth of M. sanborni are less robust than those of M. minuta, so traits 9 and 13 are useful to distinguish these two species (Fig. 4). Furthermore, the height of the coronoid process in relation to the condyloid process (trait 14), the smooth dorsal profile of the skull (i), the narrow anterior portion of the zygomatic arch (ii), the smooth curve of the ventral profile of the vertical ramus of the mandible (iii), and the triangular and less well-developed articular process (iv), are also all valuable parameters for the recognition of M. sanborni (Fig. 4). The palatine bone in M. sanborni (as in M. minuta and M. schmidtorum) is longer, narrower and extends anteriorly to approximately between M¹ and M², while in M. yatesi, it is short and parallel and extends anteriorly until M² and M³ (Siles et al., 2013).

Figure 4
Diagnostic cranial traits for the differentiation of M. minuta (UFPB 8695) and M. sanborni (A, B, C: UFPB 6543, D and E: UFPB 6535). White arrow: A = P³; B = anterior portion of the zygomatic arch; C = Dorsal profile of skull; D = p₃; E = articular process. See Table 2.

Quantitative data

The original description of M. sanborni was based on the analysis of only six specimens (Simmons, 1996). As the present study includes a greater number of specimens, it is possible to redefine the morphometric parameters for the species (Table 1). Overall, M. sanborni presents the smallest dimensions in comparison with the other species, followed by M. yatesi, M. minuta, and M. schmidtorum. External measurements overlapped considerably among M. sanborni, M. yatesi, and M. minuta. On the other hand, the cranial measurements of M. sanborni overlapped only discreetly with those of M. yatesi. These findings corroborate those of Siles et al. (2013). The length of the maxillary toothrow, the breadth of the braincase, the condyle-incisive length and the greatest length of the skull are the most important parameters for the differentiation of these species.

Geographic distribution and habitat preferences

A total of 14 localities (Table 3, Fig. 5) are known for M. sanborni. Most sites are arranged in a northeast-southwest diagonal across Brazil, corresponding to the scrub and savanna biomes (Caatinga and Cerrado) located between the Amazon and Atlantic Forest biomes (see Mares et al., 1985; Sampaio, 1995).

Table 3
Localities for Micronycteris sanborni. The code numbers refer to the points shown in Fig. 5. N = number of specimens

Reference	Locality	Code	N	Biome	Season	Features of the study site
López-Baucells et al. (2013)	Biological Dynamics Forest Fragmentation Project in Manaus, Amazonas	1	1	Amazon Forest	Dry	Lowland terra firme forest
Cunha et al. (2009)	Buraco das Araras Private Reserve, Mato Grosso	2	1	Cerrado	Rainy	Shrubs and trees (3-8 m) near a permanent lake
Gregorin et al. (2011)	Serra Geral do Tocantins Ecological Station, Tocantins	3	1	Cerrado	Rainy	Rocky, open savanna adjacent to rocky outcrops
Nogueira (1998)	Jaíba, Minas Gerais	4	4	Caatinga	-	Mistnets placed near Limestone outcrops
Gregorin et al. (2008)	Serra das Confusões National Park, Piaui	5	2	Caatinga	Dry	Low scrub with some larger trees in valleys, near rocky outcrops and a watercourse
Feijó et al. (2010)	Fazenda Almas Private Reserve, Paraíba	6	1	Caatinga	Dry	Shrubs and trees (3-8 m), near a reservoir
Simmons (1996)	Chapada do Araripe, Ceará	7	2	Caatinga	-	Small canyon with mesic vegetation (trees 12-17 m height with closed canopy), adjacent to a reservoir
Simmons (1996)	Exu, Pernambuco	8	4	Caatinga	-	Small cloud forest with large evergreen trees (10-12 m) and granite outcrops
This study	Boqueirão da Onça, Bahia	9	3	Caatinga	Dry	Shrubs and trees (3-8 m) on the banks of a watercourse in a humid valley
This study	Paripiranga, Bahia	10	5	Caatinga	Dry	Agricultural matrix with trees and shrubs (3-8 m) on hillsides and riverbanks
This study	Aiuaba Ecological Station, Ceará	11	18	Caatinga	Dry/ Rainy	Low scrub on the banks of a watercourse, adjacent to banana, cashew and maize plantations
This study	Tamandua Farm, Santa Terezinha, Patos, Paraiba	12	1	Caatinga	Dry	Unknown
This study	Buritizal Farm,Uruçui, Piaui	13	1	Cerrado	Rainy	Unknown
This study	Barra do Sonhém Farm, Loreto, Maranhão	14	1	Cerrado	-	Unknown

Figure 5
Recorded localities for Micronycteris sanborni in relation to Brazilian biomes. Circles: previous records; Triangles: new records. The sites are numbered as in Table 3. "?" refers to a doubtful records

Cunha et al. (2009) and Santos et al. (2010) reported the occurrence of M. sanborni in the Buraco das Araras Nature Reserve in Mato Grosso do Sul state, and López-Baucells et al. (2013) recorded the species in the Biological Dynamics Forest Fragmentation Project in Manaus, Amazonas state, Brazil. Both these records represent extreme outliers in the geographic distribution of the species (Fig. 5), and in fact, both studies describe a beige or dirty white ventral coloration, which is distinct from the pure white coloration described by Simmons (1996), and confirmed in all the specimens analyzed in the present study. Based on this evidence, Siles et al. (2013) have already speculated that the specimen reported by Santos et al. (2010) may in fact be Micronycteris yatesi. In addition to the contradictory coloration and the fact that it represents an extreme outlier, the record from Manaus is also inconsistent with the available evidence on the ecology of the species, i.e., its preference for dry habitats. Unfortunately, López-Baucells et al. (2013) do not collect the specimen for further confirmation. Nogueira et al. (2014) also do not recognize this record due to the absence of voucher material. Furthermore, as suggested by Siles et al. (2013), individuals previously reported as M. minuta or M. schimdtorum from the Caatinga and Cerrado biomes should also be re-assessed, given the potential ecological differences among species.

Simmons (1996: 17) concluded that M. sanborni preferentially uses denser and more humid habitats within the Cerrado and Caatinga, a conclusion reinforced by Nogueira et al. (2007). However, the results of the present study indicate that the species also occurs in open areas of the Caatinga, including disturbed habitats (Table 3), as well as open areas of the Cerrado (Gregorin et al., 2011), although this may reflect seasonal factors, in particular the distribution of the rains in the semiarid Caatinga, which tend to be restricted to a three or four-month period (Prado, 2003). During the dry season, many bodies of water dry up, with the few permanent sites becoming focal points in the distribution of a wide range of fauna, including insects (Vasconcellos et al., 2010). In the present study, most of the M. sanborni specimens were collected during the dry season and all were close to bodies of water (Table 3), which may reflect a seasonal ranging pattern related to insect foraging. Nevertheless, these observations indicate that the species occurs in mesic and open habitats, whether preferentially or not, including degraded environments, and that a similar pattern may be observed in the Cerrado savannas.

Nogueira et al., (2007) identified M. sanborni as a cave-dwelling species. However the lack of records of this species from surveys of caves (Gregorin & Mendes, 1999; P.A. Rocha, pers. obs.), including those within the areas surveyed in the present study, does not support this conclusion. The available evidence (Table 3) indicates a possible preference for rocky outcrops and cliffs, where the species may roost in crevices.

Reproduction patterns

Based on the two pregnant M. sanborni specimens captured in December and another non-pregnant female collected in April, (Simmons 1996: 18) concluded that "many [M. sanborni] give birth in the rainy season and wean their young around the beginning of the following dry season". The 18 M. sanborni specimens (11 male and seven female) collected at ESEC Aiuaba - the largest series available from a single locality - also reinforce this reproductive pattern. Three of the females captured in December (rainy season) were at an advanced stage of gestation, and one collected in April (early dry season) was lactating. The three other females, captured in August and September (dry season) presented no signs of reproductive activity. These findings indicate that the species is monoestrous, which is typical of the gleaning animalivore bats of the subfamily Phyllostominae (Durant et al., 2013), with births coinciding with the rainy season, when insects are more abundant (Vasconcellos et al., 2010).

CONCLUSION

The M. sanborni specimens analyzed in the present study provided important new insights into the taxonomy, distribution, and biology of the species. In particular, a number of the traits on which the original description of the species was based were found to be highly variable, and thus of reduced value for taxonomic diagnosis, in particular with regard to the morphologically similar M. minuta. Therefore, a careful re-evaluation of the specimens of the subgenus Schizonycteris reported previously is strongly recommend, taking into account the diagnostic traits reported here, especially for the specimens from the Caatinga and Cerrado biomes. Micronycteris sanborni appears to prefer mesic, arid and disturbed habitats within the dry polygon of tropical South America, in particular those associated with rocky outcrops. The results of this study also indicate that this species may be captured relatively more easily by setting mist-nets over bodies of water, especially during the dry season, when feeding resources become scarce. This may be confirmed by further research in the dry forest and savanna ecosystems of central and northeastern Brazil. The species also appears to be monoestrous, with births coinciding with the rainy season.

ACKNOWLEDGMENTS

We would like to thank CAPES/REUNI for conceding graduate stipends to PAR and AF, and CNPq for a research grant to AF (project number 551993/2011-1) and to SFF (project number 303994/2011-8). We are also grateful to Jefferson Mikalauskas, Pedro Dantas and Willy Leal for the helping in the field, Hannah Larissa Nunes, Rumening Barbosa Vasconcelos and Pedro Cordeiro Estrela for authorizing the analysis of collection specimens and Carol Nunes Liberal for taking the photographs.

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Publication Dates

• Publication in this collection
  2015

History

• Accepted
  08 Apr 2015