Artibeus fraterculus (Chiroptera: Phyllostomidae) Author Salas, Jaime A Universidad de Guayaquil, Facultad de Ciencias Naturales, Carrera de Biología, Departamento de Zoología, Av. Raúl Gómez Lince s / n y Av. Juan Tanca Marengo, Guayaquil 090112, Ecuador jaime.salasz@ug.edu.ec Author Loaiza S, Christian R Instituto de Ciencias Biológicas “ Antonio Raimondi ”, Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Lima 14, Perú christian.loaiza@unmsm.edu.pe Author Pacheco, Víctor Departamento de Mastozoología, Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Av. Arenales 1256, Jesús María, Lima 14, Perú vpachecot@unmsm.edu.pe text Mammalian Species 2018 2018-08-24 50 962 67 73 http://dx.doi.org/10.1093/mspecies/sey008 journal article 7811 10.1093/mspecies/sey008 4199ae88-c3fe-4d20-a401-957a516d0b83 1545-1410 4573529 419FC5AD-80BC-495E-8B1E-FA7AA973F5D9 Artibeus fraterculus Anthony, 1924 Fraternal Fruit-eating Bat Artibeus fraterculus Anthony, 1924:5 . Type locality “Portovelo, del Oro, Ecuador ; altitude 2000 ft. ” A [ rtibeus ]. j [ amaicensis ]. fraterculus : Hershkovitz, 1949:447 . Name combination. Artibeus jamaicensis fraterculus : Cabrera, 1958:88 . Name combination. Artibeus ( Artibeus ) fraterculus : Marques-Aguiar, 1994:26 . Name combination. CONTEXT AND CONTENT. Order Chiroptera , subor-der Yangochiroptera, family Phyllostomidae , subfamily Stenodermatinae , tribe Stenodermatini . Artibeus fraterculus is the most common species of Artibeus throughout its geographical range; no subspecies are recognized ( Larsen et al. 2007 ; Marques-Aguiar 2008; Redondo et al. 2008 ). Fig. 1. —An adult male Artibeus fraterculus from Bosque Protector Cerro Blanco, Guayas, Ecuador. Photograph by Jaime A. Salas. NOMENCLATURE NOTES. Artibeus fraterculus was considered a subspecies of A. jamaicensis ( Hershkovitz 1949 ; Ortiz de la Puente 1951 ; Cabrera 1958 ; Jones and Carter 1976), but Koopman (1978) accorded specific status to the form based on morphological data. Subsequent reviews by Honacki et al. (1982) , Koopman (1993) , and Simmons (2005) have all treated it as a valid species. The generic name Artibeus is compounded from the Greek words: arti , straight, exactly fitted; and bao , to walk ( Palmer 1904 ). Latin derivation of fraterculus , comes from frater (brother) and culus (diminutive suffix = little brother), which refers to A . fraterculus being the smallest in the group of the large Artibeus ( Tirira 2004 ) . Common names in Spanish are murciélago frutero fraternal or murciélago frutero del suroccidente ( Tirira 2004 ); in English, the names are western artibeus or fraternal fruit-eating bat (Marques-Aguiar 1994; Simmons 2005 ). DIAGNOSIS Artibeus fraterculus can be distinguished from others species of Artibeus that occur in its geographic range by differences in coloration, facial stripe features, and size. Its dorsum is dark gray to grayish brown and overall size is smaller (length of forearm, 52–59 mm ; length of skull, 26 mm ) than Anderson’s fruiteating bat A. aequatorialis Andersen, 1906 , which has a dark gray to blackish gray dorsum (length of forearm, 57–68 mm ; length of skull, 30 mm ), and the great fruit-eating bat A. lituratus (Olfers, 1818) which has a brown, cinnamon brown, or yellowish gray dorsum (length of forearm, 65–78 mm ; length of skull, 31 mm ). Facial lines in A. fraterculus are faint and barely visible, and in some specimens the lower stripes are scarcely perceptible or inconspicuous ( Fig. 1 ), whereas in A. aequatorialis all facial lines are clearly visible and thin, and in A. lituratus they are very prominent or conspicuous. It also varies from the flatfaced fruit-eating bat A. planirostris (Spix, 1823) , which exhibits conspicuous facial lines and grayish dorsum with bases of hairs pale, length of forearm 62–73 mm , and the length of the skull, 30.5 mm ( Ortiz de la Puente 1951 ; Albuja 1999 ; Ortega and Castro-Arellano 2001; Hollis 2005 ; Tirira 2007 ; MarquesAguiar 2008 ). GENERAL CHARACTERS Artibeus fraterculus is the smallest species in the group of large Artibeus ( Patten 1971 ; Owen 1987 ; Marques-Aguiar 2008), similar to A. aequatorialis , but much smaller in overall size ( Koopman 1978 ). The head is large with a relatively long rostrum (rostral index ≥ 0.29); the nose leaf is large and well developed, longer than wide (ratio of about 1.57), more or less elliptical, with a longitudinal rhomboidal keel. The horseshoe of nose leaf is free. The lower lip has about 15 rounded papillae; ears, nose leaf, forearm, tibia, metacarpals, and phalanges are pale brown, contrasting with dark blackish patagium. The tragus varies from gray to dark gray, with a pointed projection on inner margin near tip ( Fig. 1 ). The propatagium extends up to joint of the 1st phalanx of the thumb, patagium extends to near the base of the toes; feet and uropatagium are dark brown. The wing membrane is blackish gray; interfemoral membrane is broad (≥ 10.0 mm); uropatagium with a central notch, slightly hairy and fringed medially; tail absent ( Ortiz de la Puente 1951 ; Patten 1971 ; Marques-Aguiar 1994; Albuja 1999 ; Tirira 1999 ). Artibeus fraterculus , the palest of the South American Artibeus , presents a dichromatic appearance, occurring in both grayish brown and yellowish brown color phases. The pelage is soft and velvety; dorsal pelage is dark gray to grayish brown; fur on the back (mid-dorsum) is short (≤ 8.0 mm). The ventral pelage is pale, with the tips of individual hairs appearing sil-very gray giving it a frosted appearance; base of both dorsal and ventral surfaces of forearm is hairy ( Anthony 1924 ; MarquesAguiar 1994, Albuja 1999 ; Marques-Aguiar 2008). Ranges (mm or g, sexes combined) for standard morphological features and mass of 122 specimens from Ecuador and Peru were: total length, 64–76; length of ear, 15–21; length of nose leaf, 11–14; length of forearm, 52–59; length of hind foot, 12–16; body mass, 30–55 ( Anthony 1924 ; Hershkovitz 1949 ; Ortiz de la Puente 1951 ; Patten 1971 ; Albuja 1999 ; Tirira 2007 ; Salas 2010 ). The skull of A. fraterculus is short with a low sagittal crest; anterior portion of skull is depressed, the palatal is wide, and the brain case is enlarged ( Fig. 2 ). The preorbital process is poorly developed, postorbital process and interorbital ridges moderately developed, supraorbital ridges converge posteriorly, and the postorbital constriction is immediately behind postorbital process. The zygomatic arch is well ossified and subparallel and the paraoccipital process moderately developed; mesopterygoid fossa not constricted posteriorly on basicranium; anterior shape of mesopterygoid fossa U-shaped resulting in curved lateral borders; condylar process not prominent, projecting slightly from ramus; angular process narrow. The nasals are planar; the teeth are large, with a broad occlusal area, and molars are well developed ( Ortiz de la Puente 1951 ; Patten 1971 ; Marques- Aguiar 1994). Means, SD s, and ranges (mm) of cranial and dental measurements for 11 males and 16 females (in parentheses) collected from different localities in Ecuador ( Larsen et al. 2010 ) were: greatest skull length, 26.78 ± 0.50, 25.80–27.65 (26.56 ± 0.32, 26.13–27.21); condyloincisive length, 23.59 ± 0.65, 22.16– 24.71 (23.45 ± 0.39, 22.65–24.17); height of skull, 11.92 ± 0.40, 11.40–12.57 (11.82 ± 0.34, 11.29–12.45); mastoid breadth, 14.50 ± 0.30, 13.95–14.84 (14.33 ± 0.38, 13.44–14.88); greatest width of braincase, 13.15 ± 0.27, 12.67–13.48 (13.06 ± 0.19, 12.79–13.39); breadth of zygomatic arch, 16.27 ± 0.35, 15.55– 16.88 (16.09 ± 0.26, 15.54–16.46); width of postorbital constriction, 6.61 ± 0.23, 6.27–6.96 (6.58 ± 0.17, 6.21–6.81); breadth across upper canines, 7.48 ± 0.21, 7.06–7.73 (7.37 ± 0.16, 7.09–7.71); breadth across outer edges of 2nd upper molars, 11.88 ± 0.33, 11.30–12.26 (11.81 ± 0.28, 11.35–12.34); palatal length, 12.43 ± 0.52, 11.50–13.21 (12.27 ± 0.30, 11.60– 12.86); length of maxillary toothrow, 9.30 ± 0.32, 8.61–9.59 (9.26 ± 0.22, 8.80–9.66); mandible length, 16.88 ± 0.53, 15.67–17.57 (16.87 ± 0.25, 16.42–17.42); length of mandibular toothrow, 10.39 ± 0.32, 9.75–10.91 (10.25 ± 0.22, 9.95– 10.65); and breadth across lower canines, 4.32 ± 0.21, 4.07–4.63 (4.30 ± 0.16, 4.07–4.71). Fig. 3. —Geographic distribution of Artibeus fraterculus redrawn by Christian Loaiza from Marques-Aguiar (2008). Fig. 2. —Dorsal, ventral, and lateral views of the skull and lateral view of mandible of an adult male of Artibeus fraterculus (MUSM [Museo de Historia Natural San Marcos] 24623) from Coina, Otuzco, La Libertad, Peru. Greatest length of skull is 26.5 mm. Photographs by Víctor Pacheco. DISTRIBUTION Artibeus fraterculus occurs only in Ecuador and Peru ( Fig. 3 ; Albuja 1999 , 2002 ; Pacheco 2002 ; Simmons 2005 ; Marques-Aguiar 2008 ). In Ecuador , it inhabits the central and southern coast, and the southwestern foothills of the Andes ( Tirira 2007 ), from sea level to about 1,600 m in elevation and occupies mangroves, desert scrubland, and deciduous and semideciduous forests, where it can be very common (Parker and Carr 1992; Albuja 1999 , 2002 ; Albuja and Muñoz 2000; Tirira 2001 ; Boada and Román 2005; Salas 2008 , 2010 ; Tirira 2012; Pinto et al. 2013 ; Salas et al. 2014 ). It can also occur in some wet areas but it is less abundant in these areas (Albuja and Mena 2004; Tirira 2008 ; McDonough et al. 2011 ; Pinto et al. 2013 ). Loaiza (2010) reported an unusual record in humid montane scrub near 2,064 m in Loja ( Ecuador ). In Peru , it has been recorded west of the Andes in the departments of Tumbes , Piura , Lambayeque , and Ica ( Tuttle 1970 ; Thomas and Thomas 1977 ; Koopman 1978 ; Velázquez 1992; Pacheco et al. 2007 ) and also reported in arid and isolated arid portions of the Amazon basin, in the departments of Cajamarca and Amazonas (East of the Antes), where A. fraterculus extends through the Huancabamba depression ( Ortiz de la Puente 1951 ; Patten 1971 ; Koopman 1978 ), at 2,145 m , which forms both a biogeographic connection between the lowland forests of the Pacific coast and the Amazon basin ( Weigend 2002 ). A . fraterculus occurs in the Ecuador Arid, Sechura Desert, Tumbes-Piura, and Western Ecuador biogeographic provinces, in both Ecuador and northwestern Peru , an area collectively known as the Tumbesian Center of endemism ( Morrone 2001 ; Loaiza 2013 ). No fossils are known. FORM AND FUNCTION The dental formula for Artibeus fraterculus is: i 2/2, c 1/1, p 2/2, m 2/3, total 30 ( Anthony 1924 ; Patten 1971 ; Albuja 1999 ; Marques-Aguiar 2008). M2 is moderately close to M1 and posterior edge of M1 is straight ( Patten 1971 ). The shape of M1 is almost triangular in occlusal view, and the hypocone of M1 is well developed, a character unique to A. fraterculus . Maxillary toothrows converge anteriorly (V-shaped); crowns of I1 bilobed and not pointed; lingual cusp of P4 moderately to well developed; metacone and metaconule of M2 not separated as distinct lobes from rest of tooth (Marques-Aguiar 1994, 2008). The configuration of the cranium in A. fraterculus , including the wide palate, short rostrum, deep dentary, enlarged brain case, and well-developed molars, is very close to congeners such as the Jamaican fruit bat A. jamaicensis , A. lituratus , and the dark fruiteating bat A. obscurus , and reflects an adaptive response to consumption of hard fruits such as figs ( Kalko et al. 1996 ; Nogueira et al. 2009 ; Marchán-Rivadeneira et al. 2010). Parameters (in KHz) of a search-phase frequency-modulated (FM) echolocation call taken from an individual in Rumi Wilco in Vilcabamba ( Loja , Ecuador ) on 9 August 2013 included: a starting frequency of 95.76 (89.45–103.99), ending frequency of 62.28 (59.18–67.96), frequency of maximum energy 74.39 (67.92–84.09); duration 1.61 ms; and exhibited 3 harmonics (Pinto and Boada 2015). ONTOGENY AND REPRODUCTION Artibeus fraterculus exhibits seasonal bimodal polyestrous, with parturition occurring during both the dry and wet seasons, with peaks in February and May ( Graham 1989 ; Mena and Williams de Castro 2002; Marques-Aguiar 2008). Based on Ecuadorian material housed in the National Museum of Natural History (USMNH), Marques-Aguiar (2008) reported pregnant females in October and November and lactating females in July and November. Salas (2010) captured 2 males with testes descended and 1 female with nipples developed in the dry season ( September 2007 ) in mangroves and dry tropical forest; there are records of 4 pregnant females during the wet season ( April 2014 ) in semideciduous forest in Guayas Province , Ecuador (W. Guillén, in litt.). ECOLOGY Artibeus fraterculus inhabits natural roosts such as hollow trees, shrubs, caves, termite mounds, and artificial structures including bridges, churches, houses, gardens, and mines ( Albuja 1999 ; Tirira 2007 ; Carrera et al. 2010 ; Pinto et al. 2013 ). Individuals have been reported to occur in clusters ranging from 9 individuals in a termite nest ( Carrera et al. 2010 ) to 709 individuals in an active coal mine ( Pinto et al. 2013 ). A . fraterculus is present in forests, disturbed habitats, and crop and urban areas ( Ortiz de la Puente 1951 ; Albuja 1999 ; Mena and Williams de Castro 2002; Albuja and Mena 2004; Salas 2008 ; Carrera et al. 2010 ; Pinto et al. 2013 ; Salas et al. 2014 ). Artibeus fraterculus is a generalist frugivore, its diet is varied and includes Mangifera indica (Anacardiaceae) , Brosimum alicastrum , Ficus eximia , F. guianensis , F. maxima , F . obtusifolia (Moraceae) , Muntingia calabura (Muntingiaceae) , Psidium guajava , Syzygium jambos (Myrtaceae) , Eriobotrya japonica (Rosaceae) , Acnistus arborescens , Solanum crinitipes (Solanaceae) , Styrax subargentea (Styracaceae) , Cecropia obtusifolia , Cecropia polystachya (Urticaceae—Loaiza 2010; Novoa et al. 2011 ; Pinto et al. 2013 ). Novoa et al. (2011) reported insect remains in feces at Parque Nacional Cerros de Amotape (Tumbes-Peru), and Albuja (1999) also mentioned that this species feeds on insects, but detailed information is not available. Ectoparasites recorded from A. fraterculus include streblid bat flies ( Streblidae ): Aspidoptera phyllostomatis , Megistopoda aranea , Metelasmus pseudopterus , Speiseria ambigua , Strebla guajiro , Trichobius joblingi ( Stamper 2012 ) , and the mite ( Spinturnicidae ) Periglischrus iheringi (Mendoza-Uribe and Chávez Chorocco 2003) . Endoparasites include Trypanosoma cruzi (Order Kinetoplastida ), with high infection levels (90.1%) reported in individuals collected in Bella María Chica ( Loja province—Pinto et al. 2015). Only the barn owl ( Tyto alba ) has been reported as a predator of A. fraterculus (Thomas and Thomas 1977 ; Moreno 2010 ), but potential predators would include other owls (spectacled owl Pulsatrix perspicillata , Peruvian pygmy owl Glaucidium peruvianum , Peruvian screech owl Megascops roburatus , black-and-white owl Strix nigrolineata , mottled owl S. virgata ), and the bat falcon ( Falco rufigularis —Ridgely and Greenfield 2006; J. Sócola, in litt.). The false vampire bat Vampyrum spectrum given its known predation on fig-eating bats is a possible predator of A . fraterculus (Navarro and Wilson 1982; Kalko et al. 1996 ). Artibeus fraterculus occurs sympatrically with A. aequatorialis and A. lituratus throughout most of its distribution ( Larsen et al. 2010 ), but how resources are partitioned is unknown. It has been captured in association with other species of bats including: A. lituratus , A. aequatorialis , silky short-tailed bat Carollia brevicauda , hairy big-eyed bat Chiroderma villosum , woolly false vampire bat Chrotopterus auritus , common vampire bat Desmodus rotundus , vevelty fruit-eating bat Enchistenes hartii , harmless serotine Eptesicus innoxius , Wilson’s bonneted bat Eumops wilsoni , common long-tongued bat Glossophaga soricina , southern red bat Lasiurus blossevillii , little big-eared bat Micronycteris megalotis , common mastiff bat Molossus molossus , black myotis Myotis nigricans , pale-faced bat Phylloderma stenops , greater spear-nosed bat Phyllostomus hastatus , Matapalo broad-nosed bat Platyrrhinus matapalensis , Baker’s yellow-shouldered bat Sturnira bakeri , and common tent-making bat Uroderma bilobatum , in several localities of mangroves, dry forest, semideciduous forest, and scrubs ( Albuja 1999 ; Boada and Román 2005; Pacheco et al. 2007 ; Salas 2008 , 2010 ; Carrera et al. 2010 ; Novoa et al. 2011 ; Tirira et al. 2012 ; Pinto et al. 2013 ; Salas et al. 2014 ). The geographic distribution of A . fraterculus coincides with other endemic bat species such as molossids (Cabrera’s free-tailed bat Cabreramops aequatorianus and Blunt-eared bat Tomopeas ravus ); phyllostomids (western nectar bat Lonchophylla hesperia and Long-snouted Bat Platalina genovensium ), vespertilionids (Ecuadorian little yellow bat Rhogeessa velilla ), and furipterid (Smoky bat Amorphochilus schnablii — Gardner 2008 ; Pinto et al. 2013 ); all these bat species occur in the Tumbesian Center of endemism ( Loaiza 2013 ). GENETICS Both male and female Artibeus fraterculus have a diploid number (2n) of 30 chromosomes (Lavrenchenko and Dmitriev1994), which is identical to the pygmy fruit-eating bat Artibeus phaeotis (= Dermanura phaeotis Miller, 1902 — Baker et al. 1982 ; Timm 1985 ), whereas several other species of Artibeus ( A. lituratus , A. jamaicensis , and A. planirostris ) exhibit sexual variation in diploid number with females having a 2n = 30 (XX) and males a 2n = 31 (XY1Y2— Baker et al. 1982 ). The divergence of A. fraterculus was about 2.3 million years ago, following the closure of the Panamanian land bridge (ca. 3–4 million years ago). The uplifting of the Andes Mountains played an important role in the diversification of South American species of Artibeus and A. fraterculus is regarded as representative of a historical connection between Middle America and the Western Andean Slope ( Patterson et al. 1992 ; Larsen et al. 2013 ). Sequence variation of 2 mitochondrial genes (ATPase 8 and ATPase 6) was examined among 3 populations ( Patterson et al. 1992 ). Sequence divergence between populations from the west and east of the Andes (Marañón Valley) was very low (<1%), suggesting that A. fraterculus is capable of dispersing across theAndes. Although A. fraterculus has consistently been included in the A. jamaicensis complex ( Hershkovitz 1949 ; Ortiz de la Puente 1951 ; Cabrera 1958 ), Patten (1971) found greater affinities with the hairy fruit-eating bat Artibeus hirsutus Andersen, 1906 and the Honduran fruit-eating bat Artibeus inopinatus Davis and Carter, 1964 , based on analyses of morphological and morphometric data. A cladistic analysis by Owen (1987) , using 22 discrete-state external, cranial, mandibular, and dental characters resulted in an unresolved polytomy of A. fraterculus , A. hirsutus , and A. inopinatus . Hoofer et al. (2008) , based on mtDNA data, documented a well-supported sister relationship between A. hirsutus and a clade composed of A. fraterculus and A. inopinatus . This is consistent with phylogenetic analyses based on cytochrome- b mitochondrial gene ( Lim et al. 2004 ; Guerrero et al. 2008 ; Redondo et al. 2008 ) which place A. fraterculus as sister species of either A. hirsutus or A. inopinatus . These latter 2 taxa are distributed in xeric regions along the western and southern coasts of Middle America and thus A. fraterculus represents a South American radiation of this lineage that is isolated, both geographically and ecologically. CONSERVATION Artibeus fraterculus is the most common bat species in many localities of southwestern Ecuador and north-central Peru ( Tuttle 1970 ; Koopman 1978 ; Parker and Carr 1992; Velásquez 1992 ; Albuja 1999 ; Albuja and Muñoz 2000; Tirira 2001 ; Boada and Román 2005; Pacheco et al. 2007 , 2009 ; Marques-Aguiar 2008; Salas 2008 ; Carrera et al. 2010 ; Loaiza 2010 ; Tirira 2012; Salas et al. 2014 ; Au Hing and Salas 2016), and apparently has no major threats ( Carrera et al. 2011 ). In Ecuador , it has been recorded in many protected areas such as Bosque Protector Cerro Blanco, Estación Científica Pedro Franco Dávila, Área Nacional de Recreación Isla Santay, Reserva Ecológica Manglares Churute, Reserva de Producción de Fauna Manglares El Salado, Área Provincial de Productividad y Conservación El Retiro de Pucón, Ramsar Wetland Manglares Don Goyo, and Jardín Botánico de Guayaquil (Parker and Carr 1992; Albuja 1999 ; Salas 2007 , 2008 , 2010 ; Carrera et al. 2010 ; Salas et al. 2014 ), Parque Nacional Machalilla (Albuja and Muñoz 2000), Bosque Petrificado de Puyango y Reserva Ecológica Arenillas ( Carrera et al. 2010 ), Reserva Yunguilla (unpublished data), Reserva Natural Tumbezia - La Ceiba (Loja) ( Tirira 2001 ), and Reserva Laipuna; in Peru at Parque Nacional Cerros de Amotape ( Tumbes ) ( Pacheco et al. 2007 ; Novoa et al. 2011 ). Currently, this species is listed on the International Union for Conservation of Nature and Natural Resources Red List of Threatened Species as “Least Concern” because of its wide distribution, presumed large population, and because it is unlikely to be declining at nearly the rate required to qualify for listing in a threatened category (Molinari and Aguirre 2015). Although Ecuador also listed it as “Least Concern” ( Carrera et al. 2011 ), one recent survey determined concentrations of lead (Pb) in several urban bat species, in Guayaquil (Guayas-Ecuador), and have found high values in A. fraterculus , from soft tissue such as lungs, heart, liver, pancreas, and kidneys ( X ± SD ) (5.7 ± 1.96 mg /kg), and single individual presented an extraordinarily high value of 128,52 mg/kg in bone tissue ( Baquerizo 2016 ), so the concentration of heavy metals should be considered as a new threat for this species.