Pseudoromicia principis, Juste & Torrent & Méndez-Rodríguez & Howard & García-Mudarra & Nogueras & Ibáñez, 2023

Juste, Javier, Torrent, Laura, Méndez-Rodríguez, Aline, Howard, Kelli, García-Mudarra, Juan Luis, Nogueras, Jesús & Ibáñez, Carlos, 2023, A new Pipistrelle bat from the oceanic Island of Príncipe (Western Central Africa), Journal of Mammalogy 104 (2), pp. 361-371 : 6-9

Pseudoromicia principis , new species

Príncipe’s Pipistrelle

Figs. 3–6

Pipistrellus sp. : Juste and Ibáñez 1994:841.

Pipistrellus (N.) sp. : Juste and Ibáñez 1994:841 Pseudoromicia sp. : Rainho et al. 2022.

Holotype.— Female ( EBD 17475M , field number: B6718), stuffed preserved specimen with skull and skeleton removed), mist-netted near Papagaio River in Santo António, Príncipe Island, at sea level on 26th March 1988 by JJ and CI . External measurements (in mm except for weight in g) are: W: 3.8; FA: 32.2; HF: 6; TIB: 11.9; EAR: 8.4. Skull measurements are: GSL: 12.8; CBL: 11.9; CCL: 11.44; PL: 4.5; GBW: 5.9; ZW: —; POB: 3.4; CM 3: 4.1; IM 3: 4.8; SPM: 3.4; M 3 M 3: 5.4; C1-C 1: 3.8; MAND: 9; CM 3: 4.8; IM 3: 5.5. Tissue from the holotype has not been sequenced.

Type locality.— Santo António city, Príncipe Island ( Fig. 1 ), República Democrática de São Tomé e Príncipe (1.635°N, 7.419°W), at sea level .

Paratypes.— A subadult male ( EBD 17358M ) from Santo António, Príncipe Island, preserved in ethanol (70%) with skull and baculum extracted and captured on 20th March 1988 by JJ and CI. Two adult females ( EBD 29604M , EBD 29605M ) captured at the “ Roça Bela Vista ” over the Papagaio River , 3 km apart from Santo António on the 3rd November 1992. One pregnant female ( EBD 29606M ) and one male ( EBD 29607M ) captured on the 12th November 1992 in a small lagoon near the bank of the Papagaio River in the city of Santo António. These last four specimens were preserved in ethanol (70%) with skull extracted and tissue samples preserved separately. The Cytb sequences of three of them are deposited in GenBank with accession numbers: MW287571 , MW287572 , and MW287573 .

Description.— Pseudoromicia principis sp. nov. is a small pipistrelle-like bat ( Fig. 3 ) with tail fully enclosed in interfemoral membrane; forearm length 30.5–32.3 mm (n = 6); greatest skull length 12.3–12.9 mm (n = 6), and length of the upper tooth row ranging from 4.2 to 4.4 mm (n = 6; Tables 3 and 4 ). The ears are rounded, with a relatively small tragus (less than 40% length of the ear). The tragus has a short and straight anterior margin, and a posterior margin that has a sharp angle, giving the general appearance of a parallelogram diagonally truncated, but pointed at the anterior corner ( Fig. 6e ). The posterior edge of the tragus decreases gently at a slope of 260° as it moves toward the exterior of the ear, with a notch at the middle of its margin ( Fig. 6e ). An antitragus is absent. The skull is small, with a short rostrum and rounded braincase.

The pelage is dense, and the texture is very soft, being 6–7 mm long at its longest. Dorsally, the pelage of P. principis sp. nov. is unicolored and a dense dark chocolate brown. The ventral pelage is bicolored: chocolate brown at the base and cream at the tips. The pelage does not extend onto the wings or interfemoral membrane. The ears and tragus are also chocolate brown, as is the skin around the mouth, whereas the skin around the eyes is paler ( Fig. 3 ). The dorsal pelage and wing membrane are chocolate brown, as are the hairless areas covering the tail, femur, tibia, fibula, ankle, hind foot, forearm, and fingers. The external nose (rhinarium) is broad, and has a shape similar to the rhinarium described for Nycticeinops Hutterer et al. (2019) , in which “Pars supranarica” and “Pars internarica,” based on Ade (1998) terminology, cover most of the “Pars supralabialis.” However, the fenestrae of the rhinarium of P. principis sp. nov. are larger and more centered than in Nycticeinops ( Figs. 6c and 6d ).

The cranium of P. principis sp. nov. is small and robust ( Fig. 4 ). The rostrum is low, short, and broad and the braincase is broad and high. The rostrum and braincase are united by a moderate concave curve. The sagittal and lambdoid crests are absent; thus, there is no occipital helmet. The zygomatic arches are wide and delicate. The supraorbital crests are minimally developed and the postorbital process is absent. The auditory bullae are moderate in size. The palate is short and broad. The anterior palatal emargination is deep and wide and forms a U-like shape. The superior incisors displace the “U” curve slightly inward. The dental formula is as follows: I 2/3, C 1/1, P 1/2, M 3/3, total 32. The upper inner incisors are bicuspid and pointed, and the outer incisors show an accessory cusp at the posterior base of the tooth ( Fig. 6b ). The height of the upper outer pair of incisors is 45–70% of the height of the inner pair. The lower incisors are trilobed and rounded ( Fig. 6a ). The mean maximum height of the upper canine is 1.4 mm, and the inferior is 1.0 mm (Supplementary Data SD2). The mean maximum width of the upper premolar is 0.6 mm and the lower is 0.9 mm. Upper premolars are aligned in the tooth row and are in contact with the canines and the molars ( Fig. 4 ). Both the maxillary and mandibular molars are well developed. The third molar is massive and myotodont. The distance between the mesostyle to mesocone of the third molar is 55–79% of the distance between the parastyle and the paracone.

The baculum shows the same general morphological pattern as the bacula described for P. rendalli ( Hill and Harrison 1987) and P. brunnea and P. roseveari ( Monadjem et al. 2013) but differs in having a wide base connected through a long shaft to an expanded and lobed, plate-like structure ( Figs. 5 and 6 ). These similarities support a close phylogenetic relationship between these species and P. principis sp. nov. However, in the new species, the base (0.85 mm) shows two distinct basal lobes. The shaft is very long (1.8 mm), slender, and slightly curved at the tip. It is shelf-like (0.5 mm), and flattens and broadens with two characteristic circular bulges ( Figs. 5 and 6 ).

Echolocation.— Despite intense sampling efforts across Principe Island during recent years, no other vespertilionid bat has been captured or recorded on the island ( Juste et al. 1994; Rainho et al. 2022) nor can any echolocation calls could be confused with those of P. principis sp. nov. This fact together with the fact that many calls were recorded from pipistrelle-like bats that were seen flying at dusk make us confident that all analyzed calls correspond to the new species. The echolocation calls of P. principis sp. nov. show the typical pipistrelle-like call structure ( Fig. 7 ). The first part is characterized by a steep downward frequency modulation (FM), followed by a quasi-constant frequency (QCF) component ( Kalko and Schnitzler 1993). The relative importance of each component varies depending mainly on the surrounding environment (e.g., Kazial et al. 2001). As a result, pipistrelles typically show wide individual variation in shape and structure between calls. Figure 7 illustrates examples of three calls with different combinations of the FM and QCF elements. The mean ± SD and range of the analyzed sequences of calls (N = 40) are as follows: Start Frequency, 55.47 ± 8.43 (44.75–74.05) kHz; End Frequency, 44.71 ± 1.44 (41.92–47.83) kHz; Maximum Energy Frequency or Peak Frequency, 45.69 ± 1.26 (43.9–48.3) kHz; Duration, 5.82 ± 1.39 (5.32–9.41) ms; Inter-pulse interval, 90.55 ± 8.89 (72–114.7) ms. As expected, the Peak Frequency value found is similar to the value (45 kHz) of the Palearctic Pipistrellus pipistrellus , which is approximately the same size ( Van Cakenbergue and Happold 2013), and higher than the values reported for the larger pipistrelles Laephotis kirinyaga (43.9 kHz) and P. nyanza (40.4 kHz). These comparisons must be considered tentative because the last values were obtained from bats flying in a cage instead of from free-flying bats ( Monadjem et al. 2021a).

Distribution.— The new species is endemic to the 128 sq km area of the island of Príncipe, in the Gulf of Guinea (Western Central Africa). This island lies just north of the Equator. As an oceanic island, it has never been in contact with the mainland, from which it is separated by a distance of 220 km ( Fig. 1 ). Pseudoromicia principis sp. nov. is known from several localities, mainly from the northern half of the island ( Juste et al. 1994; Rainho et al. 2022), suggesting that it is common across the lowlands of the northern half of Príncipe Island. The original forest of this part of the island was transformed into cocoa plantations and orchards, with few houses and other human constructions, none of which appear to negatively affect the population of P. principis sp. nov. On the other hand, it is possible that the current distribution pattern on the island is the result of biased sampling, since the forested southern half is much less accessible. Thus, the species could be abundant in this part of the island as well ( Rainho et al. 2022).

Etymology.— The epithet “principis” is derived from the Latin princeps and refers to Príncipe Island (Gulf of Guinea, Western Central Africa) from where the bat is native and endemic. As a vernacular name we propose “Príncipe’s Pipistrelle.”

Diagnosis.— A small pipistrelle-like bat (forearm length 30.5–32.3 mm) with a long baculum with unique flattened tip with three circular bulges. Dark brown pelage with uncolored dorsal hair places the species in the genus Pseudoromicia . Dark chocolate brown pigmentation of hairless parts of the body and membranes (including wings) distinguishes this species from all the members of the translucent white-winged group of species of Pseudoromicia . This is the smallest bat so far described within the genus. It has a tiny moderately inflated skull (12.3– 12.9 mm) with dimensions that do not overlap those of any other species of Pseudoromicia ( Tables 3 and 4 ).

Comparisons.— The skull (size and shape), dentition, baculum (shape and length), pelage coloration, and forearm length distinguish P. principis sp. nov. from all other African pipistrelle-like bats. Its moderately inflated skull in lateral profile differs from the flattened skull of Laephotis and the highly inflated skull in Afronycteris ( Van Cakenbergue and Happold 2013) . It is also distinguished from Afronycteris by the absence of P 1. The dorsal unicolor fur contrasts with the bicolor (or even tricolor) pattern of the fur characteristics of the genus Neoromicia ( Monadjem et al. 2021a) . The wide and centered openings (fenestrae) of the external nose distinguish the new species from Nycticeinops ( Fig. 7 ), as well as the absence of a secondary cuspid in its upper outer incisor (I 2) and the different shape of the baculum. In fact, the shape of the baculum in the new species—with its curved, long, and slender shaft—indicates that it belongs to the genus Pseudoromicia , as confirmed by molecular evidence. The wing membranes and pelage are both chocolate brown, indicating it is part of the dark-winged group of Pseudoromicia , in contrast to the translucent white-winged species, including P. tenuipinnis , which, though similar in size, has a much smaller baculum with a distinct flattened tip ( Monadjem et al. 2021a). There are three known dark-winged species within Pseudoromicia . Two of them, P. roseveari and P. kityoi , can be differentiated from P. principis sp. nov. by the smaller size of the new species (forearm more than 5 mm smaller in P. principis sp. nov.; Tables 3 and 4 ). Pseudoromicia principis sp. nov. more closely resembles the remaining dark-winged species, P. brunnea , since both are relatively similar in size, and show chocolate brown ventral and dorsal pelage. However, the tips of the ventral pelage have a distinct light creamy tinge in the new species. Additionally, P. brunnea is consistently larger in all body, cranial, and dental measurements ( Tables 3 and 4 ). The main differences are to be found in the dentition: P. brunnea shows unicuspid upper incisors with the outer incisor very small ( Fahr 2013), whereas the incisors in P. principis sp. nov. are bicuspid with the outer one relatively large with its tip reaching over the height of the cingulum of the inner ( Fig. 7 ). The bacula are also different, as the shaft is shorter and more curved in P. brunnea ( Fig. 6 ). Finally, the molecular analyses show that the two species differ by 9.9% in their Cytb sequences and that they are not considered to be sister clades ( Fig. 2 ).

Figures

Fig. 3.—Portrait of Pseudoromicia principis sp. nov. showing a typical pipistrelle-like appearance. Pelage is chocolate brown dorsally and ventrally although tips of the ventral pelage present a distinct light creamy tinge. Photograph by Jorge Palmeirim.

Fig. 4.—Skull and mandible of the holotype of Pseudoromicia principis sp. nov. (EBD 17475M) in dorsal, ventral, lateral, front and back views as well as mandible top view. Photographs by Joxerra Aihartza.

Fig. 5.—(A) Dorsal; (B) lateral; (C) ventral; (D) apical (above), and basal (bellow) views of the baculum of the paratype Pseudoromicia principis sp. nov. (EBD 17358M). Photographs by Laura Torrent.

Fig. 6.—(A) Detail of the upper incisors (top left) and drawings of the (a) lower incisors and (b) upper incisors (bottom) of the holotype of Pseudoromicia principis sp. nov. (EBD 17475M). Photograph by Joxerra Aihartza and drawings by Joaquín López-Rojas. (B) Details of the rhinarium of (c) the holotype of P.principis sp.nov.(EBD 17475M) and of (d) Nycticeinops happoldorum (ZFMK-MAM-2009.0029), from Hutterer et al. (2019). Photograph by Laura Torrent.(C) Drawing of the tragi of: (e) P. principis sp. nov. (EBD 17358M, paratype); (f) P. brunnea from Van Cakenberghe and Happold (2013) and (g) P. brunnea (DM13229) from Monadjem et al. (2013) and (D) dorsal and ventral views (from left to right) of bacula of: (h) P. principis sp. nov. (EBD 17358M, paratype); (i) P. rendalli from Hill and Harrison (1987); and (j) P. brunnea (DM13229) from Monadjem et al. (2013). Drawings of P. principis sp. nov. baculum by Joaquín López-Rojas.

Fig. 1.—Map of Príncipe Island and distances to the mainland and other islands in the Gulf of Guinea (Bioko and São Tomé).

Fig. 7.—Selected echolocation calls of Pseudoromicia principis sp. nov. with three examples (A, B, C) of calls showing decreasing frequency modulation (FM) and increasing quasi-constant frequency (QCF) elements. Calls were directly recorded from free-flying bats at dusk in Santo António city and surroundings.

Fig. 2.—Bayesian phylogenetic reconstruction based on the mitochondrial gene cytochrome b (Cytb). Values above branches represent Bayesian posterior probabilities and values below branches are bootstrap values of maximum likelihood (support values <50 are not shown). The right column presents sequences GenBank accession numbers. The sequence JQ956446 is listed in GenBank as Pseudoromicia tenuipinnis but it was probably misidentified. See Table 1 for a complete list of the specimens used and main text for details of the molecular analyses.

Tables

Table 3.—Descriptive statistics (mean ± SD, minimum and maximum values, and number of measured specimens) at six external measurements recorded for Pseudoromicia principis sp. nov. and other members of the black-winged group of the genus Pseudoromicia. Pseudoromicia tenuipinnis is also included for comparisons. See text for definitions of the variables. Measurements for P. brunnea, P. kityoi, P. roseveari, and P. tenuipinnis after Monadjem et al. (2021a).

External variable	P. principis sp. nov.	P. brunnea	P. kityoi	P. roseveari	P. tenuipinnis
FA	31.42 ± 0.74 (30.5–32.3)	34.6 ± 1.06 (32.8–36.7)	37.5 (37–38)	36.5 ± 1.54 (32.6–38.0)	29.4 ± 1.18
	N = 6	N = 15	N = 2	N = 10	(28.1–32.0)
					N = 6
W	4.36 ± 0.38 (3.8–4.8)	6.0 ± 1.04 (4.8–9.4)	7.95 (7.9–8.0)	6.5 ± 0.50 (6.0–7.0)	4.0 ± 0.29 (3.5–4.4)
	N = 5	N = 15	N = 2	N = 10	N = 6
HBL	71.56 ± 4.33 (64.5–75)	84.8 ± 3.14 (80–89)	88.5 (88–89)	87.3 ± 2.95 (83–93)	74.2 ± 2.17 (72–77)
	N = 5	N = 15	N = 2	N = 10	N = 5
TL	34.3 ± 3.23 (30–37.5)	35.9 ± 1.55 (33–38)	35.0 (34–36)	39.7 ± 2.65 (34–44)	29.2 ± 0.82 (28–30)
	N = 5	N = 15	N = 2	N = 9	N = 5
EAR	7.62 ± 0.93 (6.5–8.7)	12.4 ± 0.83 (11–14)	10.0 (10– 10)	12.9 ± 0.64 (12–14)	12.7 ± 0.91 (12–14)
	N = 6	N = 15	N = 2	N = 8	N = 7
HF	5.88 ± 0.38 (5.4–6.5)	7.79 ± 0.97 (7–10)	9.5 (9–10)	9.9 ± 1.10 (8–11)	6.5 ± 0.80 (5–7)
	N = 6	N = 14	N = 2	N = 10	N = 7

Table 4.—Descriptive statistics (mean ± SD, minimum and maximum values, and number of measured specimens) at eight cranial measurements recorded for Pseudoromicia principis sp. nov. and the other members of the black-winged group of the genus Pseudoromicia. The small P. tenuipinnis is also included for comparisons. See text for definitions of the variables. Measurements for P. brunnea, P. kityoi, P. roseveari, and P. tenuipinnis after Monadjem et al. (2021a).

Skull variable	P. principis sp. nov.	P. brunnea	P. kityoi	P. roseveari	P. tenuipinnis
GLS	12.68 ± 0.24 (12.3–12.9)	13.73 ± 0.35 (13.10–14.24)	14.84 (14.7–14.99)	14.13 ± 0.45 (13.4–14.5)	12.43 ± 0.28 (12.00–12.78)
	N = 6	N = 15	N = 2	N = 10	N = 10
ZW	7.2–	8.68 ± 0.49 (7.70–9.61)	9.6 (9.54–9.63)	8.85 ± 0.5 (8.00–9.50)	7.48 ± 0.5 (6.8–8.19)
	N = 1	N = 14	N = 2	N = 9	N = 9
POB	3.33 ± 0.05 (3.3–3.4)	3.92 ± 0.23 (3.60–4.45)	3.95 (3.91–3.99)	3.80 ± 0.19 (3.50–4.09)	3.79 ± 0.2 (3.47–4.25)
	N = 6	N = 15	N = 2	N = 10	N = 9
GBW	6.12 ± 0.26 (5.8–6.5)	7.50 ± 0.24 (6.65–7.69)	7.59 (7.51–7.67)	7.31 ± 0.35 (6.87–7.40)	6.51 ± 0.13 (6.40–6.81)
	N = 6	N = 15	N = 2	N = 10	N = 10
MAND	8.93 ± 0.21 (8.6–9.2)	10.06 ± 0.32 (9.40–10.66)	10.98 (10.76–11.2)	10.4 ± 0.3 (9.8–10.7)	8.77 ± 0.38 (8.2–9.33)
	N = 6	N = 14	N = 2	N = 9	N = 10
CM3	4.23 ± 0.1 (4.1–4.3)	4.86 ± 0.13 (4.60–5.07)	5.16 (5.12–5.20)	5.03 ± 0.2 (4.80–5.30)	4.23 ± 0.14 (3.90–4.35)
	N = 6	N = 15	N = 2	N = 10	N = 10
C1C1	3.78 ± 0.15 (3.7–4.0)	4.22 ± 0.24 (3.63–4.63)	4.67 (4.61–4.74)	4.34 ± 0.25 (3.8–4.7)	3.81 ± 0.29 (3.3–4.14)
	N = 6	N = 15	N = 2	N = 10	N = 9
M3M3	5.15 ± 0.19 (4.9–5.4)	5.86 ± 0.26, (5.50–6.55)	6.19 (6.09–6.1)	6.00 ± 0.25 (5.5–6.3)	5.03 ± 0.18 (4.70–5.29)
	N = 6	N = 15	N = 2	N = 10	N = 9
CM3	4.78 ± 0.29 (4.4–5.3)	5.30 ± 0.33 (4.80–5.86)	5.61 (5.59–5.63)	5.25 ± 0.32 (5.0–5.97)	4.63 ± 0.23 (4.4–5.24)
	N = 6	N = 15	N = 2	N = 9	N = 10