Myotis armiensis, Carrion-Bonilla & Cook, 2020

Carrion-Bonilla, Carlos Alberto & Cook, Joseph Anthony, 2020, A new bat species of the genus Myotis with comments on the phylogenetic placement of M. keaysi and M. pilosatibialis, Therya 11 (3), pp. 508-532 : 515-520

Myotis armiensis , species novum

Armien’s Myotis , Myotis de Armién

Figure 7 , 8 , and 9 ; Tables 5 and 6

Myotiskeaysipilosatibialis, LaVal, 1973 , part

Myotiskeaysipilosatibialis, Hernandez-Meza et al. 2005 , part.

Myotiskeaysipilosatibialis, Wilson, 2008 , part.

Myotis nigricans, Larsen et al. 2012a , part.

Myotis riparius, Larsen et al. 2012b , part.

Myotis keaysi, Chaverri et al. 2016 , part.

Myotis cf. pilosatibialis, Moratelli et al. 2016 , part.

Myotis cf. pilosatibialis, Moratelli et al. 2017 , part.

Holotype and type locality. Voucher MSB 262089 ; adult male; preserved as skin, skull and skeleton ( Figures 8 and 9 ) at the Museum of Southwestern Biology ( MSB), University of New Mexico collected on 20 March 2012 by Joseph A. Cook and collaborators (Tropical Biology Class 2012 and Instituto Conmemorativo Gorgas de Estudios de la Salud) at La Amistad International Park Ranger Station (8° 89 ′ N, -82° 61 ′ W, elevation 2, 214 m), Bugaba District, Chiriquí Province, Panamá. Tissues deposited at the same museum (NK 209314, LN2 preservation), with additional tissues at Instituto Gorgas, Panama City (-80°C preservation). The specimen is well preserved. The measurement for the forearm (44 mm) recorded on the specimen tag is incorrect and should be FA = 39 mm as now recorded in the Arctos Museum Database.

Paratypes. Nineteen additional specimens were collected from Chiriquí Province, Panamá and Cordillera Oriental ( Ecuador ). Two specimens were designated as paratypes based on genetic identification, (partial cytochrome b), morphometrics and qualitative data: skin of one adult female ( MSB 262085 ), collected by Joseph A. Cook and collaborators, 20 March 2012 ; skin and skull of one female, adult (TTU 85060) collected by Robert J. Baker and collaborators (Sowell Expedition-Ecuador, 2001), 24 July 2001 .

Six paratypes identified solely by genetic identification (partial cytochrome b) were collected at Bugaba District, Chiriquí Province, Panamá [one adult male ( MSB 262237 ) collected by Joseph A. Cook and collaborators, 20 March 2012)], Jurutungo, Río Sereno , Renacimiento District, Chiriquí Province, Panamá [sex unknown ( MSB 262788 ), collected by Gorgas Institute field researchers, 6 May 2011], Santa Clara , Renacimiento District, Chiriquí Province, Panamá [one female, age unknown ( TTU 39146 ), collected by Robert J. Baker, 19 January 1983], Cabañas del Aliso, Cosanga, Napo Province, Ecuador [one female, age adult, (QCAZ 17245) collected by Carlos A. Carrión Bonilla, 13 December 2017), Yantzaza, Campo Minero Fruta del Norte , Zamora Chinchipe, Ecuador [male, adult ( QCAZ 12461 ), collected by Paula Iturralde, 3 March 2011]. Another specimen from Ojo de Agua , 2 km Nof Santa Clara, Renacimiento District, Chiriquí Province, Panamá ( ROM 104302 ), collected by Burton Lim and Eamon O’Toole, on 8 March 1995 was identified based on barcode cytochrome c oxidase subunit I.

Ten paratypes identified with morphometric analysis of craniometric measurement analysis and qualitative morphological of skins and skulls were collected from La Amistad International Park Ranger Station , Bugaba District, Chiriquí Province, Panamá [(two females, adults ( MSB 262217 -18, only skins were studied, no skulls available) collected by Joseph A. Cook and collaborators, 20 March 2012)]; Cerro Punta, Casa Tiley , Tierras Altas District, Chiriquí Province, Panamá [female, adult ( USNM 323599 , by Handley, C. and Greenwell, F.M., 6 March, 1962)]; El Volcán 2 min S. W, Tierras Altas District, Chiriquí Province, Panamá [two females, adults, ( USNM 331942 , USNM 331943 , by Tyson E, collected 21 March 1962)]; Cuesta de Piedra , Tierras Altas District Chiriquí Province, Panamá [female, adult ( USNM 331953 , by Tyson E, 28 March 1962)]; 36 km, north of Concepción , Bugaba District, Chiriquí Province, Panamá [five females, adults ( TCWC 12655 -59, by Patten, D.R., 8 June 1964) ]. We did not include any specimens from Costa Rica in the type series, because the Chaverri et al. (2016) study was unvouchered, and therefore morphological confirmation is not possible.

Distribution. Myotis armiensis sp. n. is known from the premontane and montane forest of Chiriquí Province, Panamá, extending its distribution into La Amistad International Park in Panamá ( Las Nubes Rangers Station ) and Costa Rica ( Valle del Silencio ). Elevation in Panamá and Costa Rica varies from 975 m to 2,500 m: Concepción (≈ 8°.51 ′ N, -82°.62 ′ W, 2,011m), Cerro Punta (8°.88 ′ N, -82°.73 ′ W, 1,280 m), Cuesta de la Piedra (8°.88 ′ N, -82°.73 ′ W, 975 m), El Volcán (8°.88 ′ N, -82°.73 ′ W, 1,280 m), Parque Internacional la Amistad Ranger Station : (8°.89 ′ N, -82°.61 W, 2, 214 m), Jurutungo, Río Sereno (8°.9 ′ N, -82°.73 W, 2,219 m), Santa Clara (≈ 8°.83 ′ N, -82°.75 ′ W, ≈ 1,178 m), Ojo de Agua, Santa Clara (8° 42 ′ N, -82°.45 W, 1,500 m), Valle del Silencio, Costa Rica (9° 11 ′ N, -82°.96 W, 2,500 m). In Ecuador, M. armiensis sp. n. is known from Cordillera Oriental. Elevation in Ecuador varies from 1,200 m to 2,249 m: Yantzaza, Campo Minero Fruta del Norte , Zamora Chinchipe (-3°.75 ′ S, -78°.53 ′ W, 1, 200 m), Colonia Azuay, Tungurahua Province, Ecuador (-1°.34 ′ S, -78.20°, 1,660 m), Cabañas el Aliso, Sector Las Caucheras, Quijos, Napo Province (-3°.75 ′ S, -78°.53 ′ W, 2,249 m). See Figure 10 for species distribution in Costa Rica, Panamá and Ecuador.

Etimology. Myotisarmiensis honors Dr. Blas Armién in recognition of his outstanding contributions to research in zoonotic emergent diseases, public health, and mammalogy in Panamá. Over two decades, he has supported the systematic development of holistic museum collections, including associated cryogenic biorepositories and parasites. This infrastructure (>11,000 specimens) is now the basis for new insights into temporal and spatial aspects of the biology of Panama’s mammals and associated parasites and pathogens.

Diagnosis. Due to the dearth of availability of substantial specimen material and despite the lack of a single morphologicalcharacter that consistentlydistinguishes M. armiensis from the rest of Neotropical congeners, Myotisarmiensis can be distinguished by a combination of the following morphological traits: pelage is short andwoolly, dorsal and ventral fur bicolored; insertion of the plagiopatagium occurs on the foot at the level of the base of toes by a wide membrane; lack or relatively low presence of fur on dorsal surface of tibia, foot and plagiopatagium, and border of the uropatagium without a fringe; skull is moderately large; forehead is steeply sloping; rostrum is long; lambdoidal crest is present and high; sagittal crest present, with height from low to medium; occipital crest is absent; occipital region flattened and the shape of the braincase is globular.

Myotis armiensis can be readily distinguished from Myotis congeners from Central and South America based on gene trees [partial sequence of cytochrome- b (~710 pb) and partial cytochrome c oxidase subunit I (~ 657 pb)] and species tree phylogenetic analysis of one exon: recombination activating gene II (RAG2), and 3 intron regions: protein kinase C, iota (PRKCI), signal transducer and activator of transcription 5A (STAT5A), and thyrotropin (THY). Finally, molecular synapomorphies in mitochondrial and intron genes regions sequences support the species level recognition of M. armiensis sp. n. compared to other species in the New World Myotis radiation (Appendix VI– X). These served as diagnostic characters for the species.

Description. Amedium to large species of Myotis (FA 36.3–39.4 mm, n = 13 and weight 4.5-5.6 gr, n = 10); other measurements ( Tables 5 and 6 ), with external size larger than M. pilosatibialis str ., M. sp. (Quintana Roo, México) and smaller than M. oxyotus gardneri , and M. keaysi str . Ears are brown in color, comparatively small to medium-sized (EL 11–14 mm). Dorsal and ventral fur is woolly and short (LDF 5.3 -7.4 mm, LVH 4.5-8.3 mm). Dorsal pelage is bicolor, with brownto darkbrownatthebaseandfrombrownto Mummy Brown at the tips. Ventral pelage is bicolor, with Buckthorn Brown to buff at the tips and dark brown to black at the base. Abdomen is bicolor, from Buckthorn Brown to black with buff tips. Sides and wing color are dark brown or Cinnamon Brown to Mummy Brown. Uropatagium and plagiopatagium are Mummy Brown or Cinnamon Brown. Insertion of the plagiopatagium occurs at the foot at the level of the base of toes by a wide membrane. The uropatagium lacks fringinghairs along the trailing edge. Fur presence on tibia, foot and plagiopatagium, with fur extending across a quarteror lessthan this atthe baseof thedorsal andventral side of uropatagium. Skull and mandible are medium-size (GLS 13.0 –14.0 mm, MAL 8.3–10.3). The dental formula is: 2/3, 1/1, 3/3, 3/3 = 38. Inthe holotype, the second upper premolar (p3) is aligned and visible in lateral view. Rostrum is long and frontals are steeply sloping; lambdoidal crest is well developed and occipital region is flattened.

Comparisons. In comparison with species in the ruber group, M. armiensis sp. n. differs from simus and riparius by having a less contrasting dorsaland ventral coloration (dorsal fur with dark brown to Mummy Brown and ventral fur with Buckthorn Brown to dark brown), with more contrasting (Orange-Brown or Chocolate) in simus , (golden -yellow) in midastactus, (ventral hairs with dark brown based and yellowish tips/reddish-brown or cinnamon brown dorsal color) in riparius , (Bister Brown color of dorsal hairs at tips and buff to orange of ventral color at tips) in pilosatibialis [type material]. M. armiensis sp. n. can be distinguished from keaysi by having shorter woolly hair on dorsal and ventral side, with longer woolly hair, larger proportion of fur on dorsal and ventral side of the uropatagium, and furrier tibia in keaysi . It differs from simus by having the plagiopatagium attached broadly to the side of the foot at the level of the toes; with a narrow band of membrane (<1.5 mm) attached to foot or ankles and with extremely short and woolly fur in simus . M. armiensis sp. n. shares the flattened occipital region and a moderate to high sagittal crest with members of the ruber group. It can be distinguished from M. ruber by presence of woolly hair, with silky pelage in ruber . Cranial index of M. armiensis sp. n. is only larger that M. pilosatibialis str . but smaller than other congeners inthe rubergroup (CRI: armiensis = 47.0–53.7, pilosatibialis = 45.8–49.1, keaysi = 49.7–53.9; simus = 73.0–88.1; ruber = 78.4–85.0; riparius = 64.6–76.1), reflecting a narrower skull configuration.

Myotisarmiensis sp. n. differs from the albescens group ( albescens , handleyi , nesopolus , nigricans , oxyotus oxyotus , oxyotus gardneri, izecksohni, lavali and levis ) by having short woolly hair. It only shares the woolly hair trait with chiloensis . In addition, it can be distinguished from albescens group by the presence of a moderate sagittal crest [absent in albescens , very low or absent in oxyotus , absent in nigricans or very low, absent in lavali , very low in chiloensis ]. Myotisarmiensis sp. n. differs from levis and albescens by the absence of fringe of hairs along the edge of the uropatagium. Occipital region is flattened in M. armiensis sp. n. [rounded in albescens , oxyotus , lavali , nigricans ]. The cranial index for albescens group is larger than M. armiensis sp. n, having the narrowest skull configuration in comparison with this species group.

Reproductive data. One pregnant female with one embryo (MSB 262085) collected by Joseph A. Cook and collaborators at Las Nubes Ranger Station, La Amistad International Park, 20 March 2012. Another female (USNM 323599) with embryo (crown-rump = 3 mm) collected at Cerro Punta, Casa Tiley, Chiriquí Province, collected by Greenwell, F. M, 6 March 1962. In Ecuador, one pregnant female (TTU 85060) with embryo (crown-rump = 3 mm) collected by Robert J. Baker and collaborators (Sowell-Expedition, 2001) at Colonia Azuay, Tungurahua Province, 24 July , 2001.

Habitat and ecological notes. Las Nubes Ranger Station, thetype locality for this new species, is part of a natural corridor (401, 000 ha) of relatively undisturbed montane habitats of the eastern Talamanca Mountains that rise between the Pacific and Caribbean coastlines of Panamá and Costa Rica ( Morrone 2017). At La Amistad International Park, Las Nubes Ranger Station, M. armiensis sp. n. was foundto occur sympatrically with Desmodus rotundus , Anoura geoffroyi , Sturnira cf. burtonlimi , Sturnira mordax , Enchistenes hartii ( Phyllostomidae ), and Tadarida brasiliensis ( Molossidae ). All captures in 2011, 2012 were with ground mist nets located on the edge of secondary growth forest near Las Nubes Rangers Station. Specimens were collected at a clearing on the edge of the forest (Cerro Punta, Casa Tiley) and in montane forest near a lake shore and moist montane secondary growth forest (2 miles S. W of El Volcán). We did not record any other species of Myotis living in sympatry at La Amistad International Park, but based on historic samples, the nominal subspecies M. oxyotus gardneri was found in sympatry with the new species at Cerro Punta and El Volcán.

At Valle del Silencio Costa Rica, M. armiensis sp. n. was found with Sturnira burtonlimi , Dermanura tolteca , Hylonycterisunderwoodi , Anouracultrata ( Phyllostomidae ), and Lasiurus blossevillii , Myotis cf. nigricans , and M. oxyotusgardneri ( Vespertilionidae ). The vegetation there was characterized by the presence of oak trees ( Quercus spp ) and bamboo ( Chusquea spp .), although some sites at Valle del Silencio were dominated by swampy bogs ( Chaverri et al. 2016).

In Ecuador, M. armiensis sp. n. is known from premontane and montane cloud forest of Cordillera Oriental. These forestscorrespond to Evergreen Lower Montane Forest and Cloud Montane Forest (Bosque Siempreverde Montano Bajo and Bosque de Neblina Montano; Valencia et al. 1999). Onespecimen of M. armiensis sp. n. was netted across a trail leading to secondary growth forest in Cabañas del Aliso, Cosanga, Quijos Valle, Napo Province in December, 2017. Other species captured in sympatry at that location were: Sturnira bogotensis , Carollia brevicauda ( Phyllostomidae ), Tadarida brasiliensis ( Molossidae ), and M. oxyotus oxyotus and Histiotus montanus ( Vespertilionidae ). The vegetation there was characterized by the presence of epiphytes (moss, ferns, orchids, bromeliads), bamboo ( Chusquea spp .), and pepper plants ( Piper spp . and Peperomia spp .). Another specimen of M. armiensis sp. n. was captured in Colonia Azuay, Tungurahua Province at the north side of the Río Pastaza. This locality is bisected by the Río Topo, a tributary of the Pastaza river and comprises secondary forest and fruitorchards ( Haynie et al. 2006). Other bat species captured in sympatry atthat locationwere: Anoura caudifer , Artibeus lituratus , Carollia perspicillata , and Sturnira erythromus . ( Phyllostomidae ).

Remarks. It was not possible to examine a set of fluid preserved specimens (n = 43) collected at La Amistad International Park Ranger Station, Bugaba District, Chiriquí Province, collected in 2018 by Joseph A. Cook and collaborators (Tropical Biology Class 2018 and Gorgas Institute field workers). Those specimens, until recently housed at the Gorgas Institute in Panama, may represent M. armiensis sp. n., but confirmation will require further molecular and morphological analysis (MSB 262086 –88, MSB 262219– 262224, 268090–93, MSB 327505–327516, MSB 327520, MSB 327522 –327527, MSB 327575–578, MSB 327601–602, MSB 327649–50, MSB 327700, MSB 327703, MSB 327705, MSB 327709, MSB 327712, MSB 327956).

Based on this report and other museum collections records, the diversity of Myotis comprises at least six species in Panamá: M. albescens , M. oxyotusgardneri , M. riparius , M. pilosatibialis , M. nigricans s.l., and M. armiensis sp. n. In Ecuador, the recognition of this newly identified lineage, increases the diversity to eight species of Myotis : M. albescens , M. riparius , M. simus , M. oxyotus oxyotus , M. diminutus , M. keaysi , M. nigricans s.l., and M. armiensis sp. n. In Costa Rica, Myotis diversity increases to seven species: M. elegans , M. riparius , M. albescens , M. pilosatibialis , M. nigricans s.l., M. oxyotus . gardneri and now M. armiensis sp. n.

Nomenclatural statement. — Alife science identifier (LSID) number was obtained for new species described herein: urn:lsid:zoobank.org:pub:9EB39E62-C9AC-41C0-AE76-9C5325608BEE .

Conservation. Myotisarmiensis sp. n. is restricted to higher and cooler mountain forest of Panamá, Costa Rica and Cordillera Oriental ( Ecuador). These habitats are susceptible to the effects of climate change, in addition to ongoinghabitat destruction. This report aims to contribute to efforts to study these environments and more narrowly add to our understanding of species limits of this elusive group of bats.

Figures

Figure 7. Adult female of Myotis armiensis sp.n. (QCAZ 17245) captured at Cabañas del Aliso,Cosanga,Napo Province,Ecuador. Photographed by Carlos Carrión Bonilla.

Figure 8. Dorsal (A) and ventral view (B) of the cranium,dorsal view of the mandible (C),and lateral view of the cranium (D) and mandible of the holotype of M. armiensis sp. n. (MSB 262089). Scale bar = 5 mm. Photograph taken by John Korbin (Sandia National Laboratory-New Mexico,USA).

Figure 9. Dorsal and ventral views of the skins of the holotype of M. armiensis sp.n. (MSB 262089),M.pilosatibialis str.(TCWC 24101,paratype), and M.keaysi str.(MSB 70381). Scale bar = 10 mm.

Figure 10. Map of part of Central and South America showing localities examined for M. armiensis, with triangle (type locality) and distribution in Costa Rica, Panamá, and Ecuador with circles. See Appendix I for localities of examined in Panamá and Ecuador.

Tables

Table 5. Selected measurements (mm) and body weight (g) of the holotype (MSB

Characters	MSB 262089 ♂	Paratypes
Body mass	5	5 (4.5–5.6) n = 9
HB	90	85 (77–92) n = 11
Tail	38	39 (32–48) n = 12
Foot	8	8 (7–10) n = 12
Ear	13	14 (11–14) n = 12
LDF	6.4	6.1 (5.3–7.4) n = 9
LVF	7.2	6.2 (4.5–7.4) n = 9
FA	37.1	38.1 (36.3–39.4) n = 12
3MC	34	34.3 (32.9–35.9) n = 12
GLS	13.3	13.5 (13.0–14.0) n = 9
CCL	12.2	12.1 (11.7–12.5) n = 9
CBL	12.3	12.8 (12.5–13.0) n = 9
CIL	11.9	12.8 (12.2–13.2) n = 9
BAL	12.1	11.6 (11.3–11.9) n = 9
ZB	7.9	8.6 (8.0–8.8) n = 7
MAB	6.6	7.1 (6.6–7.4) n = 9
BCB	7.3	6.8 (6.2–7.2) n = 9
IOB	4.4	4.6 (4.2–4.8) n = 9
POB	4.2	3.5 (3.2–3.7) n = 9
BAC	3.6	3.7 (3.4–4.0) n = 9
BAM	5.4	5.6 (5.3–6.0) n = 9
MTL	5.2	5.2 (5.0–5.4) n = 9
M1–3	2.7	2.9 (2.5–3.0) n = 9
MAL	9.5	9.6 (8.9–10.3) n = 9
MAN	5.7	5.5 (5.3–5.7) n = 9