New species of Histiotus (Chiroptera: Vespertilionidae) from northeastern Brazil Author Feijó, Anderson Author Rocha, Patrício Adriano Da Author Althoff, Sergio Luiz text Zootaxa 2015 4048 3 412 427 journal article 10.11646/zootaxa.4048.3.4 e331e96c-02dd-426c-bca7-1b1741c977cd 1175-5326 232044 4314B6FF-6909-45C0-B3A4-29DBAD328770 Histiotus diaphanopterus , new species Transparent-winged Big-eared Bat Figures 1–2 , 5–8 Holotype . Adult female preserved as dry skin, skull and postcranial skeleton deposited in the Mammal collection of the Universidade Federal da Paraíba ( UFPB 9490, figures 1–2). This specimen was collected on 13 September 2012 by A. Feijó and P.A. Rocha (field number AF 509). The external and cranial measurements of the holotype are presented in table 1. FIGURE 1. Dorsal and ventral view of the holotype (UFPB 9490) of Histiotus diaphanopterus . Scale bar = 2 cm. Type locality. Boqueirão da Onça ( 09°52’48.9” S , 41°4’15.2” W ), in the village of São Pedro do Lago, located in the municipality of Sento Sé, state of Bahia, Brazil . The holotype was collected in a mist-net set in the understory over a seasonal watercourse ( Fig. 3 ). This area is a complex of hills and valleys covered by 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. Paratypes . Seven adults specimens preserved in alcohol with cleaned skulls (males UFPB 9496, UPFB 9494, UPFB 9499; females UPFB 9500, UPFB 9497, UPFB 9495, UPFB 9498), one adult preserved as a dry skin and skull ( UPFB 9492), and two as dry skins, with skull and postcranial skeleton ( UPFB 9496, UPFB 9493) collected in the type locality. Two additional paratypes ( UFPB 6014, UFPB 6015) were collected by M. Beltrão and M.P.A. Fracasso on 3 September 2009 and 22 November 2009 at the Fazenda Almas Private Natural Heritage Reserve, in the municipality of São José dos Cordeiros, Paraíba, Brazil ( 7°28’15” S , 36°53’51”W ). See table 1 for the external and cranial measurements. FIGURE 2. Skull and mandible of the Histiotus diaphanopterus holotype (UFPB 9490). FIGURE 3. Left: View of one of the valleys of Boqueirão da Onça , Sento Sé, Bahia (type locality of H . diaphanopterus ) during the rainy season. Right: Site of the capture of the H . diaphanopterus holotype. Additional specimens. Three other specimens of Histiotus diaphanopterus are known, including an adult male ( MPEG 6306) fluid preserved, collected by R. Piccinini on 21 september 1971 at Faculdade Veterinária do Ceará, Fortaleza, Ceará state, Brazil ; an adult female ( MNK 3714) preserved as a dry skin (skull missing), collected by Muñoz on January 1996 at Pampagrande, Florida, department of Santa Cruz, Bolivia ; and a female ( FMNH 26466) preserved as a stuffed skin collected in Tranqueira, Maranhão state, Brazil , on 9 September 1925 . Distribution. Histiotus diaphanopterus is known from five localities arranged in a northeast-southwest diagonal across South America that includes the Caatinga and Cerrado stricto sensu of Brazil and the Chaco of Bolivia ( Fig. 4 ). The distance between the outermost localities is approximately 3160 km . Four of these sites are located in northeastern Brazil (in the states of Ceará, Paraíba, Bahia, and Maranhão) with the fifth in the center of Bolivia (Appendix). The climate of all these regions is highly seasonal, with two well-defined seasons, a long dry season and a short rainy season. The vegetation is characterized by grasslands, savannas, open woodlands, and xeric thorn forest ( Pennington et al. 2000 ). Etymology. The name diaphanopterus is derived from the Latin word diaphanum (transparent/translucent) + Greek word pteron (wing). It refers to the transparent wings that are characteristic of this new species ( Fig. 5 ). Diagnosis. Histiotus diaphanopterus is distinguished from all other South American genera of Vespertilionidae by its great enlarged ears, which extend well beyond the muzzle ( Fig. 6 ), and by the welldeveloped postorbital process of the jugal bone ( Fig. 2 ). It can be distinguished from other Histiotus by its pale transparent wings and a translucent and triangular-shaped ears with a prominent lobe in the inner border, connected by a high band (~ 4 mm ) across the forehead; its general golden-brownish body color and by the presence of wellmarked bicolored hairs of the dorsum (see table 2). FIGURE 4. Localities recorded for Histiotus diaphanopterus in relation to the principal types of vegetation found in South America and main rivers (dotted lines). 1. Boqueirão da Onça , Sento Sé, Bahia, Brazil (type locality); 2. Fazenda Almas Private Natural Heritage Reserve, São José dos Cordeiros, Paraíba, Brazil; 3. Fortaleza, Ceará, Brazil; 4. Tranqueira, Maranhão, Brazil; 5. Pampagrande, Florida, Santa Cruz, Bolivia. FIGURE 5. Ventral and dorsal view of Histiotus diaphanopterus . Note the pale transparent wings. Description . Histiotus diaphanopterus is a medium sized bat (ToL: 100.6–114.8 mm ; FL: 41.8–47.2 mm ; weight: 8–11 mm ). Face is pale and mostly naked, with sparse hair in the border of the mouth and some long vibrissae on the chin and above the nose. Dorsal fur is soft, long (~ 9 mm mid-dorsally) and brownish-golden in color. Each dorsal hair has a well-defined bicolor pattern, with the base (2/3 or 1/2) dark brownish, and the distal portion brownish-golden or yellowish. The ventral fur is long, with a dark brownish base (2/3 or 1/2) and white distal portion. The legs and forearms are naked. The lower lip has a triangular-shaped pad, similar to that found in other vespertilionids. The ears are translucent, very well developed (EL: 28.8–33.1), and reach well beyond the nostril when laid forward. They are also connected by a high (~ 4 mm ) band across the forehead. The outer border of the ear is slightly convex, whereas the inner border is straight, resulting in the distinct triangular shape. There is also a marked lobe in the basal third of the inner border, surrounded by sparse hairs. The base of the ear has silky, slightly yellowish fur. The tragus is triangular and broad, with a height slightly less than half of the ear length. Ridges are present in the mid-outer region of the ear. The wings are naked, transparent and pale, and inserted at the base of the outer toe. The calcar (CL: 17.2–23.3) is well developed and possesses a small keel. The first phalanx of the third metacarpal is slightly larger than the second phalanx, the first phalanx of the fourth metacarpal is slightly shorter than the second phalanx, and the first phalanx of the fifth metacarpal is larger than the second. The tail (TaL: 46.6–55.3) is long and protrudes slightly beyond the uropatagium ( Figs. 5–6 ). TABLE 1. Body and cranial measurements (in mm) of known specimens of Histiotus diaphanopterus . *Holotype; †Paratype.

Measurement UPFB 9490* Sex Female	UPFB 9491† Male	UPFB 9492† Female	UPFB 9493† Female	UPFB 9494† Male	UPFB 9495† Female	UPFB 9496† Male	UPFB 9497† Female	UPFB 9498† Female	UPFB 9499† Male	UPFB 9500† Female	UFPB 6015† Female	UFPB 6014† Female	MNK 3714 Female
Weight 10 ToL 104.6	8.5 100.6	9.5 111.8	9 111	8 108.3	– 105	8 104	11 114.8	10 103.6	8 105.5	8.5 106.6	10.5 113	9 104	9 –
HBL 53.2	52.6	56.5	60	54.8	58.8	52	60.2	52.4	53.3	56.2	–	52.9	60
TaL 51.4 HFL 10.1	48 10	55.3 7.9	51 9.3	53.5 8	46.2 10.9	52 8.1	54.6 8.4	51.2 10.5	52.2 9.3	50.4 10.1	43 8	52 7.6	57 8
EL 31.4	33.1	32.1	30.4	30.3	31.4	28.8	31.7	29.9	30.9	30.6	29.3	28.2	27
LLE 11.6	11.2	–	9.8	11.7	12.6	10.1	11.8	10.9	10.3	11	–	–	–
HSE 4 FL 44.9	– 44.6	– 45.4	– 46.8	3.9 43.9	4.5 44.7	– 41.8	4.4 47.2	3.4 45.3	3.8 44.4	– 45.7	– 46.6	– 45.3	– 46
TrL 13.5	12.9	13.5	13.8	13.3	13	13.2	13.2	13	14.1	13.5	14.7	13.1	–
CL 17.7	18.9	17.2	17.2	23.3	17.5	17.9	17.7	20.3	17.8	20.1	–	–	–
EB 21.3 GLS 18.63	21.3 18.08	18.12	21.7 18.31	22.8 17.8	20.8 17.9	18.5 17.67	20.5 18.3	20.1 –	21.4 17.5	20.4 17.5	– 18	– –	– –
CI 17.13	16.79	17.01	17.11	16.44	16.95	16.34	17.1	16.9	16.3	16.3	16.6	–	–
PC 4.05 ZB 10.65	4.05 10	4.06 10.29	3.87 10.34	4 10.04	3.73 9.9	3.86 10.06	4 10.26	3.9 9.9	4.1 10.1	3.85 10	4.25 10.41	– –	– –
BB 7.85	8.05	7.73	7.64	7.64	7.48	7.68	7.84	7.7	7.6	7.46	8	–	–
MB 6.96	7.04	6.95	6.86	6.6	6.9	6.62	7.1	6.9	6.4	6.55	7.22	–	–
HPP 2.05 PL 7.64	1.76 7.61	2.01 7.65	2 7.7	1.96 7.22	1.9 7.55	1.76 7.26	1.82 7.56	2.02 7.6	2.4 7.1	1.9 7.4	2.38 8.33	– –	– –
MT 6.21	5.84	6.1	6.27	5.9	6.05	5.82	6.08	5.8	5.8	5.75	5.93	–	–
PB 3.61 BMM 6.89	3.33 6.23	3.26 6.4	3.31 6.18	3.36 6.3	2.96 6.22	3.28 6.32	3.16 6.62	3.1 6.4	3 6.1	3.42 6.18	3.09 6.46	– –	– –
BC 5.2	4.81	4.92	–	4.6	4.67	4.73	5.14	4.7	4.8	4.68	4.78	–	–
ML 12.7	12.3	12.35	12.55	11.85	12.54	11.72	12.36	12.7	12	12.05	12.57	–	–
LMT 6.63	5.95	6.4	6.18	6.16	6.35	6.31	6.57	6.2	6.1	6.23	6.39	–	–
HM 4.46	3.85	4.2	4.2	4.16	4.36	4.08	4.32	4.1	4	4.04	4.2	–	–

TABLE 3. External and cranial measurements (in mm) of Histiotus species. All measurements are given as the mean ± standard deviation, minimum–maximum (N).

Measurements Histiotus diaphanopterus	Histiotus velatus	Histiotus montanus	Histiotus humboldti
ToL 107.4±4.36; 100.6–114.8 (12)	111.4±5.94; 100.0–124.0 (25)	115.0±5.06; 107.0–127.0 (26)	107.7±2.56; 103.2–112 (13)
TaL 50.7±3.51; 43.0–55.3 (12)	52.7±3.1; 46.0–60.00 (25)	53.4±3.16; 48.0–60.0 (28)	52.4±1.94; 48–56 (13)
HFL 9.1±1.17; 7.9–10.9 (10)	9.5±1.30; 6.0–11.0 (25)	10.1±1.10; 7.0–12.0 (28)	8.8±0.39; 8–9.3 (13)
EL 30.8±1.21; 28.8–33.1 (12)	28.2±2.89; 24.0–33.5 (25)	34.3±3.80; 25.5–40.0 (28)	29.6±0.61; 28.2–30.2 (13)
FL 45.1±1.46; 41.8–47.2 (12)	46.6±1.77; 42.6–49.5 (30)	49.1±2.55; 44.0–53.0 (21)	45.3±0.81; 43.7–46.7 (13)
TrL 13.3±0.36; 12.9–14.1 (11)	14.4±1.39; 12.0–17.0 (22)	15.9±1.81; 11.0–19.0 (27)	–
W 9.1±1.08; 8.0–11.0 (11)	10.5±1.55; 8.0–13.5 (25)	11.3±1.35; 8.9–14.5 (24)	10.8±0.68; 10–12 (13)
GLS 17.9±0.36; 17.5–18.6 (10)	18.1±0.51; 17.1–19.2 (45)	17.9±0.67; 17.0–19.9 (18)	17.1±0.27; 16.6–17.5 (11)
CI 16.7±0.33; 16.3–17.1 (11)	17.0±0.48; 15.9–18.3 (46)	16.8±0.41; 16.0–17.6 (17)	15.8±0.22; 15.4–16.1 (11)
PC 3.9±0.14; 3.7–4.2 (11)	4.1±0.21; 3.6–4.6 (49)	4.4±0.16; 4.1–4.8 (20)	4.0±0.19; 3.7–4.3 (11)
ZB 10.1±0.23; 9.9–10.6 (11)	10.3±0.29; 9.8–11.0 (35)	10.9±0.21; 10.5–11.3 (17)	9.6±0.22; 9.3–9.9 (9)
BB 7.7±0.19; 7.4–8.0 (11)	8.1±0.28; 7.6–8.9 (48)	8.3±0.23; 7.9–8.7 (19)	7.7±0.20; 7.3–7.9 (11)
MB 6.8±0.26; 6.4–7.2 (11)	7.6±0.87; 6.4–9.1 (35)	8.5±0.78; 6.8–9.4 (16)	7.0±0.24; 6.6–7.4 (11)
HPP 2.0±0.22; 1.7–2.4 (11)	1.9±0.17; 1.4–2.1 (32)	1.8±0.13; 1.6–2.0 (16)	1.7±0.13; 1.4–1.9 (11)
PL 7.5±0.32; 7.1–8.3 (11)	7.3±0.36; 6.7–8.2 (38)	6.7±0.33; 6.2–7.4 (20)	8.3±0.13; 8.2–8.5 (5)
MT 5.9±0.15; 5.7–6.2 (11)	6.1±0.23; 5.7–6.7 (49)	6.2±0.21; 5.9–6.6 (20)	5.6±0.11; 5.4–5.7 (11)
PB 3.2±0.19; 2.9–3.6 (11)	3.4±0.16; 3.1–3.7 (48)	3.6±0.19; 3.3–4.1 (20)	3.2±0.10; 3.1–3.4 (11)
BMM 6.3±0.22; 6.1–6.8 (11)	6.6±0.29; 6.1–7.9 (48)	6.9±0.22; 6.5–7.3 (19)	6.2±0.22; 6.0–6.6 (11)
BC 4.8±0.19; 4.6–5.2 (11)	5.0±0.21; 4.6–5.5 (49)	4.6±0.23; 4.3–5.1 (20)	4.6±0.09; 4.5–4.8 (10)
ML 12.2±0.34; 11.7–12.7 (11)	12.6±0.37; 11.9–13.6 (48)	12.4±0.39; 11.5–13.4 (20)	11.8±0.21; 11.5–12.2 (11)
LMT 6.3±0.20; 5.9–6.6 (11)	6.5±0.21; 6.0–7.0 (48)	6.6±0.27; 6.3–7.1 (20)	6.1±0.11; 5.9–6.2 (11)
HM 4.1±0.17; 3.8–4.4 (11)	4.1±0.21; 3.7–4.6 (48)	4.1±0.23; 3.7–4.6 (20)	3.9±0.09; 3.8–4.0 (10)

FIGURE 6. Live individuals of Histiotus diaphanopterus showing the diagnostic traits. 1. high band across the forehead; 2. prominent lobe in the inner border of ear; 3. long, triangular tragus; 4. triangular shape of the pale ear; 5. wings attached to the base of the outer toe; 6. ear ridges. The skull has a wide and well-developed braincase, making up approximately two-thirds of the total length of skull. The rostrum slopes slightly upward to the braincase, with a noticeable groove in the medial portion. The sagittal crest is weakly developed. The anterior palatal emargination is semicircular, as deep as it is wide. The basisphenoid region lacks pits. The zygomatic arches converge sharply towards the front and present a welldeveloped, triangular and directed upward post-orbital process in the medial portion of the jugal. In lateral view, the arches have a convex dorsal outline. The palate is concave and extends well beyond the last upper molar. Auditory bullae are well developed, wider than the space between them. The mandible presents an elongated body with a straight ventral profile. The coronoid process is triangular and well developed. The condyloid process is rounded and slightly above the toothrow. The articular process is long, robust, directed backwards, extending beyond the condyloid process. The dental formula is I 2 /3 C 1/1 P 1/2 M 3/3, with a total of 32 teeth. The inner upper incisors are spatulate and separated from one other by a large gap. The outer upper incisors are diminutive, triangular-shaped, and located close to the inner incisors, but separated from the canine by a gap slightly smaller than the diameter of the incisor. The lower incisors are trifid and aligned in a semicircular orientation. The single upper premolar is well-developed and about half of the size of the canine. The first lower premolar is small, and measures about one-third the size of p2. The upper and lower molars are W-shaped, and M3 is half the size of the other molars. Comparison. Histiotus diaphanopterus can be easily distinguished of all other species of the genus by a unique combination of external characters. The general body color of H. diaphanopterus is golden brownish, with well-defined bicolor hairs on the dorsum, whereas H. velatus , H. montanus , H. laephotis , H. alienus , H. humboldti and H. magellanicus have an unicolor or a subtle bicolor pattern of the dorsal hair ( Fig. 7 ). A distinctive triangular ear shape with a prominent rounded lobe in the inner border is present only in H. velatus and H. diaphanopterus , all other species have an oval shape ( Fig. 8 ). H. diaphanopterus , together with H. laephotis , has a pale and transparent wing, where all other species have a darker color. All differences among the Histiotus species are summarized in table 2. The skulls of H. diaphanopterus and H. velatus , the only species that have a triangular ear, are very similar, as observed in the genus as a whole. The external and cranial measurements of H. diaphanopterus overlap with those of H. velatus , except for the total length of the body and tail, and a number of other parameters (e.g. skull length, braincase breadth, mastoid breadth, breadth across M3–M3, mandible length: see table 3), in which H. diaphanopterus is smaller in size than H. velatus . Multivariate analyses. The results of the PCA indicate that the first and second principal components account for 64.92% of the total variation found in the specimens. In this analysis, H. diaphanopterus is clearly separated from H. montanus on the first and second axes, and from the H. humboldti mainly on the first axis, albeit with some slight overlap with H. velatus , despite their distinct grouping ( Fig. 9 ). The measurements most related to the variation in the first axis were zygomatic breadth, breadth across M3–M3, mandibular toothrow length, whereas the second axis was associated with palate length, breadth across canines and greatest length of the skull ( Table 4 ). The discriminant function classified correctly all H. humboldti , H. montanus and H. diaphanopterus specimens, while 10% of H. velatus (N = 2) were classified as the new species. These results indicate that H. diaphanopterus can be differentiated from the other species of the genus in a multivariate space. TABLE 4. Loadings of the first and second principal components (PC) of the 15 cranial measurements of the H. humboldti , H. montanus , H. velatus and H. diaphanopterus .

Measurements	PC 1	PC 2
ZB	0.3293	-0.1417
BMM	0.3236	-0.03965
LMT	0.3196	0.003748
MT	0.319	0.08901
ML	0.3036	0.2538
CI	0.2808	0.2715
BB	0.28	-0.1669
PB	0.2732	-0.2431
PC	0.2629	-0.3257
GLS	0.2247	0.31
HM	0.1973	0.2564
MB	0.1954	-0.3221
PL	-0.1676	0.4005
BC	0.1631	0.4004
HPP	0.08624	0.2301

Remarks. Handley & Gardner (2008) reported Histiotus velatus from Caatinga ( Piccinini 1974—MPEG 6306 ) and from Cerrado (FMNH 26466) of Brazil , but after a reexamination of the specimens by us it clearly show that both belong to Histiotus diaphanopterus . Acosta and Venegas (2006) identified the specimen of H. diaphanopterus from Bolivia ( MNK 3714) as H. macrotus . They described this specimen as having pale wings and ears, yellowish-brown dorsum, and hair tips lighter than the bases. Together with the marked triangular shape of the ear and the well developed lobe, these features define the specimen as H. diaphanopterus . Natural history. Species of the genus Histiotus are typically associated with the subtropical and Andean regions of South America ( Handley & Gardner 2008 ), where they may display a remarkable tolerance of low temperatures ( Eisenberg & Redford 1992 ), although they are also found in savanna and forest habitats. Histiotus diaphanopterus appears to be the only species of Histiotus endemic of tropical areas of xeric vegetation and scrublands (Caatinga, Cerrado and Chaco). In Boqueirão da Onça (the type locality), all the specimens were captured in mist-nets set over a seasonal watercourse within a steep valley surrounded by rocky outcrops and cliffs, where the species may roost in crevices, as reported for other species of Histiotus ( Handley & Gardner 2008 ; Carvalho et al . 2013 ). By contrast, the two specimens from Paraíba were captured in the roof an abandoned house, reflecting the synanthropic habits already reported for this genus ( Peracchi 1968 ; Miranda et al. 2006 , Pacheco et. al. 2010 ). None of the nine adult female of H. diaphanopterus collected in the Caatinga were reproductively active. As all these specimens were collected during the dry season (May, August, September and November), the evidence suggests a seasonal monestry reproductive pattern, characterized by a single peak in pregnancy followed by a lactation peak, with birth occurring in the mid to late rainy season ( Willig 1985 ), coinciding with the surge in the availability of insects ( Iannuzzi et al. 2007 ; Vasconcellos et al. 2010 ). Although there is no specific information on the diet of H. diaphanopterus , the data available on the genus indicate an insectivorous diet with a preference for the orders Lepidoptera and Coleoptera, and less frequently, Trichoptera and Diptera ( Zanon & Reis 2007 ; Gimenez 2010 ; Bracamonte 2013 ).